MODELING THE MIRROR: GRASP LEARNING AND
ACTION RECOGNITION

byErhan Oztop_________________________________________________A Dissertation Presented to the
FACULTY OF THE GRADUATE SCHOOLUNIVERSITY OF SOUTHERN CALIFORNIAIn Partial Fulfillment of theRequirements for the Degree
DOCTOR OF PHILOSOPHY(COMPUTER SCIENCE)

August 2002

Copyright 2002

Erhan Oztop

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DEDICATION

To my Grandmother

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ACKNOWLEDGEMENTS
The time I had at USC during the Ph.D. route was a very enriching period of my life. I had theopportunity to work in an exciting and stimulating research environment, led by Michael Arbib.
I would like to present my deepest gratitude to The Scientific and Technical Research Council ofTurkey (TUBITAK) for providing me the scholarship that made it possible for me to attempt andcomplete the Ph.D. study presented in this thesis. The study would not have been possible if TUBITAK
did not provide support for the very first semester and the final semester at USC.
I would like to thank Michael Arbib for guiding and educating me throughout the my years at
USC. He has been an extraordinary advisor and mentor, whom I owe all the brain theory I learned. I
would also like to present my gratitude to Michael Arbib for providing support via HFSP and USCBP
grants. Without HFSP and USCBP support, this study would not be possible.
Stefan Schaal is a great mentor, who has been a constant support and source of inspiration withnever-ending energy. Besides introducing me to Robotics, he and his colleague, Sethu Vijayakumar
were very influential in maturating the concept of machine learning in my mind.
I also owe a great debt of gratitude to Nina Bradley for being a source positive energy andmentoring me especially in infant motor development. Without her, the thesis would be lacking a major
component.
I am also full of gratitude to my Ph.D. qualification exam comittee members Maja Mataric andChristoph von der Malsburg for their guidance and support.
I am greatly indebted to Giacomo Rizzolatti for enabling me to visit his lab and providing theopportunity to communicate with not only himself but also with Vittorio Gallese and Leonardo Fogassi
who have provided invaluable insights about mirror neurons. In addition, I am very thankful to
Massimo Matelli and Giuseppe Luppino, for the first hand information on the mirror neuron system
connectivity, and to Luciano Fadiga for stimulating discussions. I would also like to thank to Christian
Keysers and Evelyne (Kohler) for not only actively involving me in their recording sessions but alsooffering their sincere friendship.
I am very thankful to Hideo Sakata for giving me the opportunity to visit his lab in Tokyo andinteract with many researchers including Murata-san with whom I had very stimulating discussions.
I am deeply thankful to Mitsuo Kawato, for giving me the opportunity to interact with various
researchers in Japan by having me at ATR during the summer of 2001. My research experience at ATR
was very rewarding; I greatly expanded my knowledge on motor control and motor learning. I would
like to salute the staff at ATR for all their help. I also would like to present my thanks to the friends at
ATR for welcoming me and making me feel at home.
I would like to present my appreciation and thanks to my mentors at Middle East Technical
University in Turkey. I present my sincere thanks to my masters advisor Marifi Guler for introducing
me to neural computation and to Volkan Atalay for introducing me to computer vision, and supporting
my Ph.D. application. Especially, I would like to present my gratitude to Fatos Yarman Vural for her
guidance and support during my Masters study and for preparing me for the Ph.D. work presented in

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this dissertation. Other influential Computer Science professors to whom I am grateful for educating
me are Nese Yalabik, Gokturk Ucoluk and Sinan Neftci.
I would like to present my gratitude to Tosun Terzioglu, Albert Ekip, Turgut Onder and Semih
Koray who were professors of the Mathematics Department at the Middle East Technical University.
They taught me how to think ‘right’ and exposed the beauty of mathematics to me.
Throughout these six years at USC, I had the pleasure to meet several valuable people who
contributed to this dissertation. Firstly, I am very thankful to Aude Billard and Auke Jan Ijspeert for all
their support and scientific interaction and feedback. They have a huge role in helping me get throughthe tough times during my Ph.D. work. In addition, I would like to thank Aude Billard for providingme the computing hardware and helping me have a nice working environment, which was very
essential for the progress of my Ph.D. study. I am thankful to my great friend Sethu Vijayakumar for his
support and stimulating discussions. Jun Nakanishi, Jun Mei Zu, Aaron D’Souza, Jan Peters andKazunori Okada besides being of great support, were always there to discuss issues and helped me
overcome various obstacles. I am deeply thankful to Shrija Kumari for offering not only her smile andfriendship but also her energy to proofread my manuscript. I owe a lot to Jun Mei Zu: she has always
been there as a great friend and has always offered her help and support when I needed it most. I am
indebted to my ex-officemate and a very valuable friend Mihail Bota for his constant support andinteractions for improving the thesis and providing me the psychological support to overcome many
obstacles throughout my Ph.D. years. Finally, I would like to thank Juan Salvador Yahya Marmol forbeing a good friend and sharing my workload during various periods of my Ph.D. I count myself very
lucky to have these great friends and colleagues whom once again I present my gratitude: Thank you
guys!
Not a Hedco Neuroscience inhabitant but a very valuable friend, Lay Khim Ong was always there
for offering her help both psychologically and physically (Hey Khim: thank you for your great editing!).
I would like to thank other great friends who supported me (in spite of my negligence in keeping intouch with them). Kyle Reynolds, Awe Vinijkul, Aye Vinijkul Reynolds, Alper Sen, Ebru Dincel: please
accept my sincere thanks and appreciation.
I owe deep gratitude to my wife Mika Satomi for her patience in dealing with me in difficult times.
She was always there. Her contribution to this thesis is indispensable. I especially celebrate and thankher for the artistic talents and hard work that she generously offered me throughout the Ph.D. study.
I am greatly indebted to Paulina Tagle and Laura Lopez for their support and help over all theseyears. I also would like to thank Laura Lopez and Yolanda Solis for their kind friendship and support.
My gratitude to Luigi Manna, who helped me with the hardware and software issues during the Ph.D.
study.
I would like to thank Laurent Itti for his generous help for improving our lab environment andproviding partial support for my research. Also, I would like to salute his lab members for their support
and friendship. Florence Miau, in particular, had always offered her warm friendship during herinternship at USC.
I would like to present my appreciation to the good things in life particularly, I would like to thankthe ocean for comforting and rejuvenating me during difficult times.
Finally, I am deeply indebted to my family, to whom I owe much more than what can be
expressed. This work would not be possible without the help of my parents. (Anne ve Baba, Evrim ve
Nurdan: Hersey icin cok cok tesekkurler!)

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TABLE OF CONTENTS

DEDICATION ........................................................................................................................... ii
ACKNOWLEDGEMENTS .....................................................................................................iii
LIST OF FIGURES .....................................................................................................................x
1

INTRODUCTION...............................................................................................................12

CHAPTER II: BIOLOGICAL BACKGROUND ............................................................4
2.1

Abbreviations ...............................................................................................................4

2.2

Premotor areas..............................................................................................................4

2.2.1
2.2.2
2.2.3
2.2.4
2.2.5
2.3

The superior temporal sulcus...................................................................................12

2.4

Parietal Areas..............................................................................................................13

2.4.1
2.4.2
2.4.3
2.4.4

3

Area F5...................................................................................................................5
Area F4.................................................................................................................10
Areas F2 and F7 (dorsolateral prefrontal cortex) ...........................................11
Area F1 (the primary motor cortex).................................................................12
Areas F3 (SMA proper), F6 (pre-SMA)............................................................12

The anterior intraparietal area (AIP) ...............................................................13
The caudal intraparietal sulcus (c-IPS)............................................................15
Areas VIP, MIP and LIP ....................................................................................17
Areas 7a and 7b (PG and PF)............................................................................18

2.5

Connectivity and other brain regions......................................................................19

2.6

Mirror neurons in humans........................................................................................23

2.7

Summary .....................................................................................................................25

CHAPTER III: MIRROR NEURON SYSTEM MODEL.............................................26
3.1

The mirror neuron system for grasping and FARS model...................................26

3.2

The hand-state hypothesis ........................................................................................29

3.2.1

Virtual fingers.....................................................................................................29

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3.2.2
3.3

The MNS (mirror neuron system) model ...............................................................31

3.3.1
3.3.2
3.4

Grand schema 1: reach and grasp....................................................................36
Grand schema 2: visual analysis of hand state...............................................38
Grand Schema 3: core mirror circuit................................................................42

Simulation results ......................................................................................................46

3.5.1
3.5.2
3.5.3
3.6

Overall function..................................................................................................33
Schemas explained.............................................................................................33

Schema implementation............................................................................................36

3.4.1
3.4.2
3.4.3
3.5

The hand-state hypothesis ................................................................................30

Non-explicit affordance coding experiments .................................................46
Explicit affordance coding experiments..........................................................50
Justifying the visual analysis of hand state schema ......................................54

Discussion and predictions.......................................................................................56

3.6.1
3.6.2

The hand state hypothesis ................................................................................56
Neurophysiological predictions.......................................................................57

4 CHAPTER IV: MULTILAYER SUPERVISED HEBBIAN LEARNING AND
PROBABILITY CODING................................................................................................................60
4.1

Neural coding .............................................................................................................60

4.2

Operation of the proposed network ........................................................................61

4.3

Testing the proposed architecture ...........................................................................64

4.3.1
4.3.2
4.3.3
4.4
5

Deterministic environment ...............................................................................64
Stochastic environment .....................................................................................66
Combining multiple layers ...............................................................................68

Summary .....................................................................................................................69

CHAPTER V: INFANT GRASP LEARNING ..............................................................71
5.1

Motivation...................................................................................................................71

5.2

Infant reach and grasp...............................................................................................71

5.3

Neural maturation versus interactive learning......................................................74

5.4

Infant Learning to Grasp Model (ILGM) ................................................................75

5.4.1
5.4.2
5.5

Layers of infant learning to grasp model........................................................76
Functional description of ILGM layers ...........................................................77

Joy of grasping............................................................................................................78

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5.5.1
5.5.2
5.6

Learning approach direction with palm orienting behavior................................80

5.6.1
5.6.2
5.7

Simulation results ..............................................................................................85
Conclusions and predictions ............................................................................86

Affordance input matters..........................................................................................87

5.9.1
5.9.2
5.9.3
5.9.4

6

Simulation results ..............................................................................................83
Conclusions and predictions ............................................................................84

Task constraints shape infant grasping...................................................................84

5.8.1
5.8.2
5.9

Simulation results ..............................................................................................80
Conclusions and predictions ............................................................................82

Is infant palm orienting learned or innate? Learning the wrist orientation...........
......................................................................................................................................82

5.7.1
5.7.2
5.8

Mechanical grasp stability ................................................................................78
Implementing the grasp stability .....................................................................79

Simulation results ..............................................................................................88
Comparison of ILGM with Lockman et al. (1984) .........................................88
ILGM kinematics analysis (five months of age).............................................88
ILGM kinematics analysis (nine months of age)............................................89

5.10

Summary and conclusion .....................................................................................91

5.11

Discussion ...............................................................................................................92

CHAPTER VI: NEUROPHYSIOLOGICAL VIEW OF LEARNING TO GRASP......
..............................................................................................................................................93
6.1

Grasp learning circuit and mirror neurons are complementary networks........93

6.2

Introduction to primate grasping ............................................................................94

6.3

Neural correlates of infant reach and grasp ...........................................................95

6.4

Primate grasp development hypotheses.................................................................97

6.4.1
6.4.2
6.5

Affordance-based learning to grasp model (LGM) ...............................................98

6.5.1
6.5.2
6.5.3
6.5.4
6.6

Hypothesis I: two coexistent grasping circuits ..............................................97
Hypothesis II: single grasping circuit..............................................................98

Localizing learning to grasp model in primate cortex ..................................99
What does cerebral cortex know about a grasp? .........................................101
Simulation level description of LGM layers.................................................102
Why LGM is relevant: good model versus bad model ...............................102

Wrist orientation-learning revisited: neural level analysis ................................103

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6.6.1
6.6.2
6.6.3
6.7

Object axis selectivity: neural level analysis.........................................................106

6.7.1
6.7.2
6.8

Neural level analysis........................................................................................107
Conclusions and neurophysiological predictions .......................................108

Object size selectivity...............................................................................................109

6.8.1
6.8.2
6.9

Neural level analysis........................................................................................103
LGM represents a ‘menu’ of grasps in terms of neural activity ................104
Predictions and discussion .............................................................................106

Simulation results ............................................................................................109
Conclusions and neurophysiological predictions .......................................111

Generalization: learning to plan based on object location..................................113

6.9.1
6.9.2

Simulation results ............................................................................................113
Summary and Conclusion ..............................................................................115

7 CHAPTER VII: BIOLOGICALLY REALISTIC F5 VISUAL SERVO CIRCUITS FOR
GRASPING AND EMERGENCE OF MIRROR NEURONS..................................................117
7.1

Motivation.................................................................................................................117

7.2

The link between the mirror neuron system and grasp learning ......................118

7.2.1
7.2.2
7.2.3
7.2.4
7.2.5
7.2.6
7.3

Implementation: F5 manual visual control circuit for 2D arm ..........................123

7.3.1
7.3.2
7.3.3
7.3.4
7.3.5
7.4
8

Two Visual Control Hypotheses ....................................................................119
Mirror neurons in feed-forward control (alternative I) ..............................121
Mirror Neurons in feedback control (alternative II)....................................122
The target of implementation .........................................................................122
The visual servo task .......................................................................................123
The feed-forward model learning..................................................................123

A leaky integrator model for F5 manual visual feedback circuit ..............124
Simulation: visual feedback control with leaky integrators.......................127
Simulation: feedback and lower motor centers............................................128
F5 Feed-forward visual control and mirror neurons ..................................130
Simulation: trajectory planning and controller performance.....................135

Feed-forward unit activity and mirror neurons ..................................................137

CHAPTER VIII: CONCLUSIONS ...............................................................................142
8.1

Mirror neurons .........................................................................................................142

8.2

Grasp learning: infant development......................................................................144

8.3

Grasp learning: monkey neurophysiology...........................................................144

8.4

Grasp learning: neural architecture.......................................................................145

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9

CHAPTER IX: FUTURE WORK ...................................................................................146
9.1

Simultaneous learning in MNS model and LGM ................................................146

9.2

Going beyond grasping: learning the ‘hand state’ ..............................................146

9.3

Tactile feedback for grasping .................................................................................146

9.4

Learning to extract the right affordance ...............................................................147

9.5

More realistic models of the limb and the brain regions ....................................147

9.6

Sensitivity analyses for the simulation parameters.............................................147

10

REFERENCES ..............................................................................................................149

11

APPENDIX ...................................................................................................................164
11.1
11.1.111.1.2
11.2

Mirror neuron system model (MNS).................................................................164
Color segmentation..........................................................................................164
Reach and grasp schema precision grasp planning and execution...........165
Learning to grasp models (ILGM and LGM) ...................................................165

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LIST OF FIGURES
Figure 2.1 Lateral view of macaque brain showing the areas of agranular frontal
cortex and posterior parietal cortex (adapted from Geyer et al. 2000). The naming
conventions: frontal regions, Matelli et al.(1991); parietal regions, Pandya and Seltzer(1982)..........................................................................................................................................................................5
Figure 2.2 A canonical neuron response during grasping of various objects in the dark(left to right and top to bottom: plate, ring, cube, cylinder, cone and sphere. The
rasters and histograms are aligned with object presentation. Small grey bars in eachraster marks onset of key press, go signal, key release, onset of object pulling, releasesignal, and object release, respectively. The peaks in ring and sphere object cases
correspond to the grasping of the object by the monkey (adapted from Murata et al.
1997a).........................................................................................................................................................................6
Figure 2.3 The motor responses of the same neuron shown in Figure 2.2. The motor
preference of the neuron is also carried over to the visual preference (compare thering and sphere histograms of both figures) (adapted from Murata et al. 1997a) ..........................................7
Figure 2.4 Activity of a cell during action observation (left) and action execution(right). There is no activity in presentation of the object during both initialpresentation and bringing the tray towards the monkey. The vertical line over thehistogram indicates the hand-object contact onset. (from Gallese et al., 1996). ..............................................8
Figure 2.5 Visual response of a mirror neuron. A. Precision grasp B. power grasp C.
mimicking of precision grasp. The vertical lines over the histograms indicate thehand-object contact onset. (adapted from Gallese et al., 1996) ..........................................................................9
Figure 2.6 Example of a strictly congruent manipulating mirror neuron: A) The
experimenter retrieved the food from a well in a tray. B) Same action, but performedby the monkey. C) The monkey grasped a small piece of food using a precision grip.
The vertical lines over the histograms indicate the hand-object contact onset (adaptedfrom Gallese et al., 1996). ........................................................................................................................................9
Figure 2.7 The classification of area F5 neurons derived from published literature(Dipellegrino et al. 1992; Gallese 2002; Gallese et al. 1996; Murata et al. 1997a; Murata
et al. 1997b; Rizzolatti et al. 1996a; Rizzolatti and Gallese 2001). All F5 neurons fire in
response to some motor action. In addition, canonical neurons fire for object
presentation while the mirror neurons fire for action observation. The majority ofhand related F5 neurons are purely motor (Gallese 2002)(labelled as Motor Neurons in
the figure)................................................................................................................................................................10xi

Figure 2.8 The macaque parieto-frontal projections from mesial parietal cortex, medial bank of theintraparietal sulcus and the surface of the superior parietal lobule (adapted from
Rizzolatti et al. 1998). Note that the Brodmann’s area 7m corresponds to Pandya and
Seltzer's (1982) area PGm......................................................................................................................................11
Figure 2.9 The intraparietal sulcus opened to show the anatomical location of AIP in
the macaque (adapted from Geyer et al. 2000) ..................................................................................................13
Figure 2.10 An AIP visual-dominant neuron activity under three task conditions:Object manipulation in the light, object manipulation in the dark and object fixation in
the light. The neuron is active during fixation and holding phase when the action is
performed in light condition. However, during grasping in dark the neuron shows noactivity. The fixation of the object alone without grasping also produces a discharge(adapted from Sakata et al. 1997a).......................................................................................................................14
Figure 2.11 Activity the same neuron in Figure 2.10 during fixation of different
objects. The neuron show selectivity for horizontal plate (adapted from Sakata et al.
1997a).......................................................................................................................................................................14
Figure 2.12 An AIP visual-dominant neuron’s axis orientation tuning and object
fixation response is shown. The neuron fires maximally during the fixation of avertical bar or a cylinder. The tuning is demonstrated in the lower half of the figure(adapted from Sakata et al. 1999).........................................................................................................................15
Figure 2.13 Response of an axis-orientation-selective (AOS) neuron in the caudal partof the lateral bank of the intraparietal sulcus (c-IPS) to a luminous bar tilted 45°
forward (left) or 45 backward (right) in the sagittal plane. The monkey views the bar
with binocular vision. The line segment under the histograms mark the fixation startand the period of 1 second. (adapted from Sakata et al. 1999) ........................................................................16
Figure 2.14 The response of the same neuron in Figure 2.13, for monocular visionconditions for the left and right eyes. (adapted from Sakata et al. 1999) .......................................................16
Figure 2.15 Orientation tuning of a surface-orientation selective (SOS) neuron. First
row: Stimuli presented. Middle row: responses of the cell with binocular view. Last
row: responses of the cell with monocular view (adapted from Sakata et al. 1997a)...................................17
Figure 2.16 The reconstructed connectivity of area 7a. The thickness of the arrows
represent the strength of the connection. (adapted from Bota 2001) ..............................................................20
Figure 2.17 The reconstructed connectivity of area 7b. The thickness of the arrows
represent the strength of the connection. (adapted from Bota 2001) ..............................................................21
Figure 2.18 The reconstructed connectivity of area AIP. The thickness of the arrows
represent the strength of the connection. (adapted from Bota 2001) ..............................................................22

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Figure 3.1 Lateral view of the monkey cerebral cortex (IPS, STS and lunate sulcus opened). The
visuomotor stream for hand action is indicated by arrows (adapted from Sakata et al.,1997).........................................................................................................................................................................27
Figure 3.2 AIP extracts the affordances and F5 selects the appropriate grasp from the
AIP ‘menu’. Various biases are sent to F5 by Prefrontal Cortex (PFC) which relies on
the recognition of the object by Inferotemporal Cortex (IT). The dorsal stream through
AIP to F5 is replicated in the MNS model ..........................................................................................................28
Figure 3.3 Each of the 3 grasp types here is defined by specifying two "virtual fingers",
VF1 and VF2, which are groups of fingers or a part of the hand such as the palm
which are brought to bear on either side of an object to grasp it. The specification of
the virtual fingers includes specification of the region on each virtual finger to bebrought in contact with the object. A successful grasp involves the alignment of two"opposition axes": the opposition axis in the hand joining the virtual finger regions to be
opposed to each other, and the opposition axis in the object joining the regions where thevirtual fingers contact the object. (Iberall and Arbib 1990) ..............................................................................29
Figure 3.4 The components of hand state F(t) = (d(t), v(t), a(t), o1(t), o2(t), o3(t), o4(t)).
Note that some of the components are purely hand configuration parameters (namelyv,o3,o4,a) whereas others are parameters relating hand to the object .............................................................31
Figure 3.5 The MNS (Mirror Neuron System) model. (i) Top diagonal: a portion of the
FARS model. Object features are processed by cIPS and AIP to extract grasp
affordances, these are sent on to the canonical neurons of F5 that choose a particulargrasp. (ii) Bottom right. Recognizing the location of the object provides parameters to
the motor programming area F4 which computes the reach. The information about thereach and the grasp is taken by the motor cortex M1 to control the hand and the arm.
(iii) New elements of the MNS model: Bottom left are two schemas, one to recognize
the shape of the hand, and the other to recognize how that hand is moving. (iv) Just to
the right of these is the schema for hand-object spatial relation analysis. It takes
information about object features, the motion of the hand and the location of theobject to infer the relation between hand and object. (v) The center two regions
marked by the gray rectangle form the core mirror circuit. This complex associates thevisually derived input (hand state) with the motor program input from region
F5canonical neurons during the learning process for the mirror neurons. The grandschemas introduced in section 3.2 are illustrated as the following. The “Core Mirror
Circuit” schema is marked by the center grey box; The “Visual Analysis of Hand
State” schema is outlined by solid lines just below it, and the “Reach and Grasp”
schema is outlined by dashed lines. (Solid arrows: established connections; dashedarrows: postulated connections) ..........................................................................................................................32

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Figure 3.6 (a) For purposes of simulation, we aggregate the schemas of the MNS (Mirror Neuron
System) model of Figure 3.5 into three "grand schemas" for Visual Analysis of Hand
State, Reach and Grasp, Core Mirror Circuit. (b) For detailed analysis of the Core
Mirror Circuit, we dispense with simulation of the other two grand schemas and use
other computational means to provide the three key inputs to this grand schema .....................................34
Figure 3.7 (Left) The final state of arm and hand achieved by the reach/grasp
simulator in executing a power grasp on the object shown. (Right) The hand state
trajectory read off from the simulated arm and hand during the movement whoseend-state is shown at left. The hand state components are: d(t), distance to target attime t; v(t), tangential velocity of the wrist; a(t), Index and thumb finger tip aperture;o1(t), cosine of the angle between the object axis and the (index finger tip – thumb tip)
vector; o2(t), cosine of the angle between the object axis and the (index finger knuckle– thumb tip) vector; o3(t), The angle between the thumb and the palm plane; o4(t),The angle between the thumb and the index finger .........................................................................................37
Figure 3.8 Grasps generated by the simulator. (a) A precision grasp. (b) A powergrasp. (c) A side grasp...........................................................................................................................................38
Figure 3.9 (a) Training the color expert, based on colored images of a hand whose
joints are covered with distinctively colored patches. The trained network will be usedin the subsequent phase for segmenting image. (b) A hand image (not from thetraining sample) is fed to the augmented segmentation program. The color decision
during segmentation is done by consulting to the Color Expert. Note that a smoothing
step (not shown) is performed before segmentation ........................................................................................40
Figure 3.10 Illustration of the model matching system. Left: markers located byfeature extraction schema. Middle and Right: initial and final stages of model
matching. After matching is performed a number of parameters for the Hand
configuration are extracted from the matched 3D model ................................................................................41
Figure 3.11 The scaling of an incomplete input to form the full spatial representationof the hand state As an example, only one component of the hand state, the apertureis shown. When the 66 percent of the action is completed, the pre-processing we apply
effectively causes the network to receive the stretched hand state (the dotted curve) as
input as a re-representation of the hand state information accessible to that time
(represented by the solid curve; the dashed curve shows the remaining, unobserved
part of the hand state) ...........................................................................................................................................44
Figure 3.12 The solid curve shows the effective input that the network receives as theaction progresses. At each simulation cycle the scaled curves are sampled (30 sampleseach) to form the spatial input for the network. Towards the end of the action the
networks input gets closer to the final hand state.............................................................................................45

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Figure 3.13 (a) A single grasp trajectory viewed from three different angles to clearly show its 3D
pattern. The wrist trajectory during the grasp is marked by square traces, with the
distance between any two consecutive trace marks traveled in equal time intervals. (b)Left: The input to the network. Each component of the hand state is labelled. (b) Right:
How the network classifies the action as a power grasp: squares: power grasp output;
triangles: precision grasp; circles: side grasp output. Note that the response for
precision and side grasp is almost zero ..............................................................................................................47
Figure 3.14 Power and precision grasp resolution. The conventions used are as in theprevious figure. (a) The curves for power and precision cross towards the end of theaction showing the change of decision of the network. (b) The left shows the initialconfiguration and the right shows the final configuration of the hand .........................................................48
Figure 3.15: (Top) Strong precision grip mirror response for a reaching movementwith a precision pinch. (Bottom) Spatial location perturbation experiment. The mirror
response is greatly reduced when the grasp is not directed at a target object. (Only theprecision grasp related activity is plotted. The other two outputs are negligible.) ......................................48
Figure 3.16 Altered kinematics experiment. Left: The simulator executes the grasp
with bell-shaped velocity profile. Right: The simulator executes the same grasp withconstant velocity. Top row shows the graphical representation of the grasps and thebottom row shows the corresponding output of the network. (Only the precision
grasp related activity is plotted. The other two outputs are negligible.) .......................................................49
Figure 3.17 Grasp and object axes mismatch experiment. Rightmost: the change of theobject from cylinder to a plate (an object axis change of 90 degrees). Leftmost: theoutput of the network before the change (the network turns on the precision grip
mirror neuron). Middle: the output of the network after the object change. (Only theprecision grasp related activity is plotted. The other two outputs are negligible.) ......................................50
Figure 3.18 The plots show the level of mirror responses of the explicit affordancecoding object for an observed precision pinch for four cases (tiny, small, medium, big
objects). The filled circles indicate the precision activity while the empty squares
indicate the power grasp related activity ...........................................................................................................52
Figure 3.19 The solid curve: the precision grasp output, for the non-explicit affordancecase, directed to a tiny object. The dashed curve: the precision grasp output of themodel to the explicit affordance case, for the same object ...............................................................................52

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Figure 3.20: Empty squares indicate the precision grasp related cell activity, while the filled squares
represent the power grasp related cell activity. The grasps show the effect of changing
the object affordance, while keeping a constant hand state trajectory. In each case, thehand-state trajectory provided to the network is appropriate to the medium-sized
object, but the affordance input to the network encodes the size shown. In the case of
the biggest object affordance, the effect is enough to overwhelm the hand state’s
precision bias. .........................................................................................................................................................53
Figure 3.21 The graph is drawn to show the decision switch time versus object size.
The minimum is not at the boundary, that is, the network will detect a precision pinch
quickest with a medium object size. Note that the graph does not include a point for"Biggest object" since there is no resolution point in this case (see the final panel of
Figure 3.19) .............................................................................................................................................................54
Figure 3.22 The precision grasp action used to test our visual system is depicted bysuperimposed frames (not all the frames are shown).......................................................................................54
Figure 3.23 The video sequence used to test the visual system is shown together withthe 3D hand matching result (over each frame). Again not all the frames are shown.................................55
Figure 3.24 The plot shows the output of the MNS model when driven by the visual
recognition system while observing the action depicted in Figure 3.22. It must beemphasized that the training was performed using the synthetic data from the grasp
simulator while testing is performed using the hand state extracted by the visualsystem only. Dashed line: Side grasp related activity; Solid line: Precision grasp
related activity. Power grasp activity is not visible as it coincides with the time axis.................................56
Figure 4.1 The elevated circular region corresponds to the area defined by theequation (x*x+y*y) <0.25. The environment returns +1 as the reward if the action falls
into the circular region, otherwise –1 is returned..............................................................................................64
Figure 4.2 The adaptation of the firing potential of the stochastic units are shown as aseries of evolving 3D maps. (left to right and top to bottom)..........................................................................65
Figure 4.3. The normalized histogram of the actions generated over 60000 samples.
Note that the actions generated captured the environment’s reward distribution (seeFigure 4.1). ..............................................................................................................................................................66
Figure 4.4 The stochastic environment’s double peaked reward distribution (see text
for the explanation)................................................................................................................................................66
Figure 4.5 Some snapshots showing the phases of learning of the layer in thestochastic environment where the reward distribution has two peaks (see Figure 4.4). .............................67
Figure 4.6. The normalized histogram of 60000 data points (actions) generated by thetrained layer in the stochastic environment depicted in Figure 4.4................................................................68

xvi

Figure 5.1 Infant grip configurations can be divided in two categories: power and precision grips.
Infants tend to switch from power grips to precision grips as they grow (adapted from
Butterworth et al. 1997) .........................................................................................................................................73
Figure 5.2 The structure of the Infant Learning to Grasp Model. The individual layers
are trained based on somatosensory feedback ..................................................................................................76
Figure 5.3 Hand Position layer specifies the approach direction of the hand towards
the object. The representation is allocentric (centred on the object). Geometrically the
space around the object can be uniquely specified with the vector (azimuth, elevation,
radius). The Hand Position layer generates the vector by a local population vector
computation. The locus of the local neighbourhood is determined by the probability
distribution represented in the firing potential of Hand Position layer neurons (seeChapter 4, for details)............................................................................................................................................77
Figure 5.4:The grasp stability we used in the simulations is illustrated for ahypothetical precision pinch grip (note that this is a simplified, the actual hand usedin the simulations has five fingers)......................................................................................................................79
Figure 5.5 The trained model’s Hand Position layer is shown as a 3D plot. One
dimension is summed to reduce the 4D map to a 3D map. Intuitively the map says:‘when the object is above the shoulder and in front grasp it from the bottom’ ............................................81
Figure 5.6: The output of the trained model’s target position layer is shown as a 3D
plot. One dimension is summed to reduce the 4D map to a 3D map. The object is on
the left side of the (right handed) arm. Intuitively, the map says ‘when the object is on
the left side grasp it from the right side of the object’ ......................................................................................81
Figure 5.7 The learning evolution of the distribution of the Hand Position layer isshown as a 3D plot. Note that the 1000 neurons shown represent the probability
distribution of approach directions. Initially, the layer is not trained and responds in arandom fashion to the given input. As the learning progresses, the neurons gain
specificity for this object location.........................................................................................................................82
Figure 5.8 ILGM planned and performed a power grasp after learning. Note thesupination (and to a lesser extent extension) of the wrist required to grasp the object
from the bottom side .............................................................................................................................................83
Figure 5.9 Two learned precision grips (left: three fingered; right four fingered) are
shown. Note that the wrist configuration for each case. ILGM learned to combine thewrist location with the correct wrist rotations to secure the object.................................................................83
Figure 5.10 ILGM was able to generate two fingered precision grips. However thesewere less than the three or four finger grips ......................................................................................................84

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Figure 5.11 The cube on the table simulation set up. ILGM interacts with the object with the physicalconstraint that it has to avoid collision with the table ......................................................................................85
Figure 5.12 ILGM learned a ‘menu’ of precision grips with the common property thatthe wrist was placed well above the object. The orientation of the hand and thecontact points on the object showed some variability. Two example precision grips areshown in the figure................................................................................................................................................85
Figure 5.13. ILGM acquired thumb opposing index finger precision grips ..................................................86
Figure 5.14 The three cylinder orientations and grasp attempts by the poor visioncondition. ................................................................................................................................................................87
Figure 5.15 The orientation match of the hand and the cylinder is illustrated. Dashedline with diamonds: 5 months old infants; Solid line with diamonds: 9 months old
infants; Dashed line with circles: ILGM with no affordance; Solid line with circles:
ILGM with affordance (infant data from Lockman et al. (1984)). Right panel illustrates
the object orientation used for the simulation and for the infants in this comparison ................................88
Figure 5.16 The hand orientation and cylinder orientation difference curves forindividual trials. The columns from left to right correspond to horizontal, diagonal
and vertical orientations. The upper row flat class of error curves, lower row non-flatclass for error curves (see text for explanation) .................................................................................................89
Figure 5.17 The hand orientation and cylinder orientation difference curves while
ILGM was executing four types of grasp in the full-vision condition. Left two figures
are two typical error curves for the horizontal cylinder. Note that the two horizontal
case error patterns reflect the two possible grasps: from the bottom and from the top.
The third and fourth are typical error curves for the diagonal and vertical cylinders
respectively .............................................................................................................................................................90
Figure 5.18 The grasps performed after ILGM learned the association between thewrist rotations and the object affordance (orientation) ....................................................................................91
Figure 6.1: The overall MNS model. The grey background rectangle shows the focusof this chapter. In addition to the areas shown, area F2 will be posited as being
involved in grasp planning. .................................................................................................................................94

xviiiFigure 6.2 Left: precision grasp (pad opposition); Middle: Power grasp (palm opposition); Right:
Side grasp (side opposition). Each of the 3 grasp types here is defined by specifying
two ‘virtual fingers’, VF1 and VF2, which are groups of fingers or a part of the handsuch as the palm which are brought to bear on either side of an object to grasp it. The
specification of the virtual fingers includes specification of the region on each virtual
finger to be brought in contact with the object. A successful grasp involves thealignment of two "opposition axes": the opposition axis in the hand joining the virtual
finger regions to be opposed to each other, and the opposition axis in the object joining
the regions where the virtual fingers contact the object (adapted from Iberall andArbib 1990)..............................................................................................................................................................95
Figure 6.3 The two possible organization of learning to grasp circuit are shown.
According to Hypothesis I, two grasping circuits exist; the phylogenetically older one
located in area F1 (hatched background) and the newer one in the premotor cortex(solid background). According to Hypothesis II, F1 is involved in only executing thepremotor cortex instructed movements. LGM is based on the latter hypothesis. The
details of LGM are shown in Figure 6.4. Note that we introduced area F2 forcomplementing the MNS structures. The visual input to area F2 originates from MIP(not shown) and V6a .............................................................................................................................................98
Figure 6.4 The Learning to Grasp Model. F5 is implicated in all grasp relatedparameters. Dashed connections indicate the direct corticospinal projections of
premotor areas. Area F5 works with area F2 and F4 to transform visual affordances
signalled by parietal areas into a grasp plan. The grasp plan is then, relayed toprimary motor cortex (F1) and spinal cord for execution. The tactile feedback of theaction is integrated in the first somatosensory cortex (SI), which mediates theadaptation of the parietal-premotor and inter-premotor connections .........................................................100
Figure 6.5 The top-left shows the Hand Position layer output summed over the radius(approach direction is encoded in spherical coordinates) as a 3D plot. The top-centre
panel shows the sample generated from the Hand Position distribution. Bottom-leftshows the Wrist Rotation layer output summed over the heading axis as a 3D plot.
The bottom-centre panel shows the parameters picked from the Wrist Rotation layer
distribution. Note that Wrist Rotation layer distribution depends on (i.e. represents a
conditional distribution) the sample picked from the Hand Position layer. The
rightmost panel shows the executed grasp ......................................................................................................104
Figure 6.6 Using the same LGM used for Figure 6.5, another grasp plan is generated(left four panels). The resulting grasp is shown on the right. By comparing the grasp
plan shown on the left four panels with of Figure 6.5’s grasp plan we see how theselection of a different approach direction (see the centre-top panels of both figures)changed the Wrist Orientation distribution .....................................................................................................105

xix

Figure 6.7:Two very different grasp generation from the same LGM. Upper panel: Grasping withmaximum wrist extension with some pronation. Lower panel: Grasping withmaximum wrist supination and small wrist extension. Note that the Wrist Layerprobability map is the same since the approach direction was chosen the same (thesmall dots in the right most panels). .................................................................................................................105
Figure 6.8 The grasps performed after LGM learned the association of hand rotations
with the object orientation input (full vision condition). Note that the left panel showsa bottom side grasp. All of the shown grasp configurations satisfied grasp stability
criterion .................................................................................................................................................................107
Figure 6.9 In the poor-vision case, the hand rotation neurons in LGM show the same
response for horizontal (left panel), diagonal (centre panel) and vertical (right panel)
object presentations because of the lack of axis orientation input ................................................................107
Figure 6.10 When LGM has access to axis orientation information the Hand Rotationneurons represent different plans in response to horizontal (left panel), diagonal(centre panel) and vertical (right panel) object presentations .......................................................................108
Figure 6.11 The small object presentation produced two peaks of activity in the Hand
Position layer corresponding to the probability distribution of approach directions.
The right panel shows the executed grasp when the data generation was localized in
the area pointed by the leftmost arrow.............................................................................................................109
Figure 6.12: A large cube was grasped by securing the object between the thumb andthe other fingers (right panel). The Hand Position layer activity is shown on the left
panel. The neuron with largest activity is marked with an arrow................................................................110
Figure 6.13 The largest object presentation and grasping. The Hand Position reflects asingle reach direction as indicated with an arrow ..........................................................................................110
Figure 6.14:The Hand Position layer activity is superimposed to demonstrate that the
maximum activity loci are separated for each object indicating selectivity for object size. ..........................111
Figure 6.15 The trained Learning to Grasp Model executed grasps to objects located atnine different locations in the workspace. The grasp locations were not used in the
training. All of the grasps shown were stable..................................................................................................114
Figure 6.16 The same model used in generating Figure 6.15 was used to generate a
different set of grasps. Again all the grasps were stable. ...............................................................................114

xx

Figure 6.17 The internal mechanisms of representing and generating multiple grasp plans are shown.
Solid arrows (except object encoding) denote learned connections while empty arrows
indicate data generation. The flow of operation starts with the presentation of theobject (the bottom centre) and follows the arrows. At the top-centre, the data
generation can yield multiple approach directions. The two possible approachdirections are shown creating two streams (left column and right column), each ofwhich yields different grasp execution (bottom pictures of left and right column)...................................115
Figure 7.1 The MNS model repartitioned to show the focus of this chapter. The grey
background marks area of interest....................................................................................................................118
Figure 7.2 One alternative visual control structure for manipulation is shown within
the MNS framework. The mirror neurons generate feed-forward commands...........................................119
Figure 7.3 Another alternative visual control structure for manipulation is shownwithin the MNS framework (compare with Figure 7.2). The mirror neurons generate
feedback commands ............................................................................................................................................120
Figure 7.4 The feedback and feed-forward control view of the F5 grasping circuit,alternative I: F5mirror neurons learn to generate feed-forward command. The desired
state is assumed to be available and is converted to a correction motor command by
F5motor-only units using stochastic gradient descent. F5canonical neurons gate thefeed-forward and feedback pairs.......................................................................................................................121
Figure 7.5. The feedback and feed-forward control view of the F5 grasp circuit,alternative II: F5mirror neurons learn to compute the error. The error is thenconverted to a correction motor command by F5motor-only units. F5canonicalgenerates the feed-forward command signal...................................................................................................122
Figure 7.6 The schema level view of the feedback controller. The visual processing
encapsulates the process of extracting an error based on the vision of the hand and theobject. Lower Motor Centers encapsulates the functionality involved in transforming
the motor signal into actual commands sent to muscles................................................................................125
Figure 7.7 The leaky integrator implementation of the feedback circuit that solves theinverse kinematics problem for precision grasping. See text for the explanation ......................................126
Figure 7.8 Three grasping tasks executed by the feedback circuit proposed shown on
the upper half of the figure. The change of arm/hand configuration during theexecution is illustrated by snapshots of the arm/hand. Each hand figure isaccompanied (lower half) by the error plot. The grasp execution is stopped (success)when the sum of finger distances to their target was less than 2mms. ........................................................128
Figure 7.9.The Visual feedback circuit generating desired trajectories for the ‘lower
level motor centre’ (implemented as a PD controller) ....................................................................................129

xxi

Figure 7.10 The slow (2 seconds) (lower half) and fast (0.5 seconds) (upper half) performance of the‘visual feedback servo’ + ‘PD controller’ system is shown. The right hand side graphs
show the tracking error (of the wrist) versus time. In the slow case, the object can be
grasped but in the fast case, it is missed...........................................................................................................130
Figure 7.11 The F5 mirror neurons viewed as the memory based feed-forward
controller. The arrows below the sheet of neurons indicate outputs while the arrows
coming above the sheet indicate inputs............................................................................................................133
Figure 7.12 The arm configurations that were acquired during 6 object grasping
actions are shown. Each of the superimposed configurations is represented by a unit
in the feed-forward layer ....................................................................................................................................134
Figure 7.13 The trajectory generation with feedback and feed-forward control is
illustrated for comparison with Figure 7.8 (feedback-only system). In the lower panel
the error graphs are plotted as error versus iteration. The error is the sum of squared
distances of the fingertips to their targets. The rightmost object was not grasped in the
training (a novel object/location). Thus the system could not make use of the feedforward signal, approximately after iteration 25 and switched to feedback only mode,
resulting in slower positioning of the fingers on the target locations ..........................................................135
Figure 7.14 The feedback, feed-forward and lower level motor servo and the dynamic
arm was simulated all together. Upper half: The grasp lasted 0.5 seconds. Lower half:
the grasp lasted 2 seconds. The fast movement error reduced with a factor of 6 while
the slow movement reduced with a factor of 10 in terms (compare with Figure 7.10)..............................136
Figure 7.15 The top row demonstrates two trajectory-planning examples for grasping
without obstacle. The bottom row demonstrates how new trajectories are formed byintroduction of an obstacle as a local inhibition on the feed-forward controller units ..............................137
Figure 7.16 The feed-forward unit activations for four grasp observations shown asunit versus time. Each graph consists of 157 neurons acquired during the learning
phase (the rows). The columns represent the time..........................................................................................138
Figure 7.17 A mirror neuron recorded during a grasp observation. On the left theraster plots; on the right the histogram. The recording data shown spans 2 seconds. In
addition, the hand start to move approximately at time = 1 second indicated by thevertical bar at the centre of the raster panel (Rizzolatti and Gallese 2001) ..................................................139
Figure 7.18 Top row: Real mirror neuron recording during a precision grasp. Bottom
row: One of the feed-forward controller unit’s responses to vision of a grasping
action. In the left panels, each raster row corresponds to a trial (Poisson spike
generation for the model). The right panels show the histograms. The rasters aligned
according to the contact of the hand with the object ......................................................................................140

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Figure 7.19. The similarity of a real neuron and model unit is demonstrated. Left two panels real
mirror neuron rasters and histogram. Right two panels are the model generated
rasters and histogram. A slow increasing activity is observed in both cases ..............................................140
Figure 7.20 Left: a sharp mirror neuron activity, which could only be replicated with
our simulator by reducing the receptive field. Right: Similar response profile obtained
from one of the feed-forward module units.....................................................................................................141
Figure 7.21 The population activity of feed-forward units with smaller receptive
fields. The feed-forward unit we used to match the real mirror firing profile in Figure
7.20 is marked with an ellipse ............................................................................................................................141

1

1

INTRODUCTION

Imagine two friends chatting over a coffee table. At the instant when one of them wants to get a sipof coffee, he effortlessly reaches and grasps his cup, shaping his hand according to the properties of thecup. If it were a mug, he would reach and grab the handle so as to counteract gravity; if it were a paper
cup, probably he would grasp the cup with his whole hand covering the surface of the cup unless thecoffee is too hot, forcing him to grab the cup from its outer rim. When he starts reaching for the cup, hisfriend easily understands that he wants to drink coffee even before his hand contacts the mug. Probably
the way he reaches and shapes his hand conveys the information that he is not aiming at other objects
on the table. He could possibly even infer that his coffee is hot before he grabs it. The situation for thetwo is reciprocal; they switch roles of being observer and actor as they sip their coffee.
When considered individually each of them is engaged in two tasks -grasping and observing. The
former is a goal directed movement while the latter is a perceptual task. The grasping task requires theintegration of information from a variety of sources (MacKenzie and Iberall 1994). The context andvisual analysis of an object determines the general grasp plan. Proprioceptive (during reach), tactile andkinesthetic information (after contact) are used to guide the hand and arm to complete the grasp. Thus,
the task of grasping involves, at the least, the determination of the following information:
1. How to conform the hand to the object. Based on object properties such as the shape,orientation and size the questions of ‘which side of the object the hand should approach’;‘which fingers should be engaged’, and ’what should the appropriate wrist rotation be’
must be answered.
2. How to control the limbs. According to the physical properties of the environment and thebiomechanics of the limbs, a control mechanism must engage muscles to transport the handand shape it to match the specifications given by (1).
The former is the problem of grasp planning; the latter is the problem of grasp execution, which
involves dynamics, that is, the adjustment of forces that the muscles must exert to achieve the specified
plan. Many other information sources are integrated to refine the reach and grasp plan. For example,
obstacle avoidance, speed, and accuracy requirements affect the reach component while the force
requirements to secure a heavy slippery object or to handle a delicate object affect the grasp component.
The perceptual task, in essence, does not involve determining movement related parameters, as no
movement has to be made. Nevertheless, the observer recognizes the action even before it is complete.
Thus, the observer has to analyze the motion of the hand and its relevance to the target to determine
whether the hand approach and preshape would yield a grasping behavior. It is interesting to note that
there is some similarity in action recognition and action generation in terms of the underlying
computations.
In fact, if one could compare the activity of observer’s brain while he is engaged in grasping versus
while he is observing his peer grasping, one would see that the motor related regions of the observer’s
brain was active in both observation and execution. Thus, one could conclude that the observer’s brain
mirrored the action of his peer by establishing equivalence between the observed action and his grasp
plan.

2

The mechanism I caricaturized above is the focus of this thesis. The execution-observation
matching system as introduced above does exist in monkey. There is strong evidence that human brain
is also endowed with similar mechanism.
To be precise, this thesis investigates the cortical mechanisms involved in:
1. Translation of a visual description of an object into an appropriate grasp plan that is,learning to make motor plans that yield grasps that are appropriate for the target objects
2. Mapping of observed grasp actions into internal motor representations
3. Developmental processes shaping neural circuits to provide the functionality (1)4. Developmental processes of (2), that is learning to recognize observed grasp actions based on
self-executed grasps
The thesis analyzes (human and monkey) behavior and monkey neurophysiology from adevelopmental perspective, and constantly asks the questions: what is the underlying factor that giverise to such mechanisms? How does it shape the basic schemas of newborns into a functional form? The
aim of the thesis is to give answers to these questions via computational models that learn and adapt
starting from minimal bootstrapping behaviors. The models and the hypotheses developed in the thesis
are based on:
1. Human infant motor development studies
2. Human behavioral and neuroimaging studies
3. Monkey neurophysiology and neuroanatomy studies
The thesis also presents significant predictions that can be experimentally tested with the hope thatexperimentalists will be stimulated to conduct the experiments suggested or design new experiments totest the model predictions and further uncover details of the cortical mechanisms of action recognition(mirror neurons), visuomotor learning and motor planning. The results of these experiments thenwould feedback into the modeling presented here, leading to validation (or rejection) and refinementsof the models developed.
The organization of the thesis is as follows:
Chapter II presents the basic biological background with an emphasis on the brain areas that willbe the focus of modeling. ‘Mirror Neurons’ (Dipellegrino et al. 1992; Gallese et al. 1996; Rizzolatti et al.
1996a) of the monkey premotor cortex are introduced in this chapter. The research on locating mirror
neurons in human is also reviewed in Chapter II.
Chapter III develops the Mirror Neuron System (MNS) model based on the hypothesis that selfobservation of grasping movements mediates the adaptation of parietal-premotor and premotorpremotor connections. Using simulation results, the chapter presents predictions on the timing of mirror
neuron responses (and others) and suggests neurophysiological experiments for testing the predictions.
In addition, Chapter III introduces the grand schemas of Visual Analysis and Reach and Grasp. The
simulated 3D arm/hand of the Reach and Grasp schema is used in other chapters to graphically display
the learned grasp actions.
Chapter IV develops a reinforcement learning based neural architecture that is capable ofrepresenting multiple values of a variable in terms of its probability distribution. The probability
distributions are shaped through interaction with the environment so as to reflect the reward
distribution in the environment. Chapter IV shows how layers can be connected to build multilayer
reinforcement networks that are capable of representing conditional probability distributions. The
architecture present in Chapter IV is used by Chapter V and Chapter VI.
Chapter V develops the Infant Learning to Grasp Model (ILGM) based on infant literature. ILGM
is a schema level behavioral model that reproduces many infant behaviors and produces testable

3

hypotheses through simulation results. The notable property is that ILGM starts with a very basic
repertoire of action mimicking neonates and show how a range of grasping categories can emerge via
explorative interaction with the environment.
Chapter VI introduces the neurophysiological Learning to Grasp Model (LGM) as a neural levelinstantiation of ILGM constrained by monkey neurophysiology and neuroanatomy. LGM replicatesexisting premotor cortex findings such as the object selectivity of F5 canonical neurons and yields
testable predictions about the grasp learning circuit in monkeys. This chapter also, poses serious
questions to neurophysiologists on the assessment used to relate neuron firing to behavior. In
particular, Chapter VI argues, by simulation results and examples from literature, that behavior-neuralactivity correlation is not an appropriate measure for investigating brain mechanisms of movement
planning. The chapter suggests an experimental methodology for deciphering the neural substrates of
movement planning suitable for finding the neuron populations that encode the true movement control
variables (parameters).
Chapter VII asks the question, ‘why do the mirror neurons exist?’ The hypothesis of the chapter(introduced in Chapter III) is that mirror neurons evolved initially to provide visual feedback for
manual manipulative actions, and later became effective in recognizing actions of others. Chapter VII
presents a simplified model of grasping (planar arm/hand) with increasing degrees of complexity in its
control. First, a biologically realistic stochastic gradient following visual feedback circuit that canperform precision grips is developed. Then a memory based neural feed-forward circuit is introduced
to augment the visual feedback servo circuit. After assessing the behavioral properties of the integrated
visual servo circuit, the chapter analyzes the activities of individual memory units in the feed-forward
circuit. The activities are converted into spike patterns using Poisson model of neural firing for a directcomparison with mirror neuron data. The results indicate that some of the feed-forward units’ firing
patterns are very similar to mirror neurons’, in spite the fact that the feed-forward activity is
characterized by a grasp error map. This supports the hypothesis that mirror neuron system initiallyevolved to serve as a visual servo circuit for manual manipulation.
Chapter VIII summarizes the key results and presents the predictions with high impact potential.
Chapter IX concludes the thesis by pointing out some open questions and recommending future
research directions.

42

CHAPTER II: BIOLOGICAL BACKGROUND

In this chapter, we review the literature on the brain areas involved in the mirror neuron system
functioning and the grasp related visuomotor transformation. We present major findings fromneurophysiological and neuroanatomical (connectivity) literature to form a background for modeling
chapters. The main regions of interest are intraparietal sulcus and premotor areas. A supplementary
review of the superior temporal sulcus and other parietal areas is included. The posterior parietal cortex
is involved in sensory-motor transformations, combining various sensory inputs and computing
representations that are used by the motor system to generate movements. In turn, premotor cortex is
involved in generating motor plans based on parietal representations of object affordances. The superior
temporal sulcus performs visual analysis of motion and form including biological motion providing
visual input to the parietal areas.

2.1

Abbreviations

7a, parietal area 7a; area PG
7b, parietal area 7b; area PF
7ab, PFG, parietal area 7ab, area PFG
7ip,parietal area 7ip
7m, mesial part of area 7; area PGm
F1, primary motor cortex; M1
F2, caudal part of dorsal premotor area; PMdc
F3, supplementary motor area; SMA
F4, caudal part of ventral premotor area; PMvc
F5, rostral part of ventral premotor area; PMvr
F6, pre-supplementary motor area; pre-SMA
F7, rostral part of dorsal premotor area; PMdr
SPL, superior parietal lobule
IPL, inferior parietal lobule
STS, superior temporal sulcus
IPS, intraparietal sulcus

2.2

IT, inferotemporal cortex
AIP, anterior intraparietal area; part of area 7
cIPS, caudal intraparietal sulcus; part of area 7
LIP, lateral intraparietal area, part of area 7
MIP, medial intraparietal area; part of area 5/7
VIP, ventral intraparietal area, part of area5/7
MST, medial superior temporal area; part of STS
MT, middle temporal area; part of STS
PE, parietal area PE; part of area 5
PEa, parietal area PEa; part of area 5
PEc, parietal area PEc; part of area 5
PO, parieto-occipital cortex
V6A, visual area 6A, area 19
S1, first somatosensory cortex, SI
S2, second somatosensory cortex, SII

Premotor areas

The macaque inferior premotor cortex is located ventral from the spur of the arcuate sulcus (seeFigure 2.1) and considered to be involved in reaching and grasping movements (Rizzolatti et al. 1988).
This region has been further partitioned into two sub-regions: F5, the rostral region, located along thearcuate and F4, the caudal part (see Figure 2.1).

5

Figure 2.1 Lateral view of macaque brain showing the areas of agranular frontal cortex and posterior parietal
cortex (adapted from Geyer et al. 2000). The naming conventions: frontal regions, Matelli et al.(1991); parietal
regions, Pandya and Seltzer (1982)

The neurons in F4 appear to be primarily involved in the control of proximal movements(Gentilucci et al. 1988), whereas the neurons of F5 are involved in distal control (Rizzolatti et al. 1988).

2.2.1

Area F5

Area F5 is one of the various agranular frontal areas of particular interest due to its complex
function (Matelli 1986). In the monkey, this area lies immediately caudal to the inferior arm of thearcuate sulcus. Stimulation and recording experiments showed that F5 is concerned with both hand andmouth movements. Hand movements are represented mostly in its dorsal part while mouth movements
tend to be ventrally (Rizzolatti et al. 1988). Little is known about the functional properties of mouth
neurons, however hand neurons were extensively studied.

2.2.1.1

Motor properties

Hand neurons discharge during specific goal-related movements such as grasping, tearing,manipulating and holding (Rizzolatti et al. 1988). Many of them are specific for a particular type of hand
movement (Rizzolatti et al. 1988). In addition, some F5 neurons become active at the presentation of
three-dimensional objects, in the absence of any overt movement, similar to AIP neurons that become
active when the monkey fixates on a presented object. In many cases these visually triggered discharge
requires a congruence of the presented object to the grip coded by the neuron (Murata et al. 1997a).
Rizzolatti et al. (1988) found that most F5 neuron firings correlated with specific goal related distal
motor acts rather than with single movements made by the animal 1 . Using the motor acts as theclassification criterion, they subdivided the neurons into different classes such as grasping-with-the-handand-the-mouth, grasping-with-the-hand and holding neurons. The discharge of many F5 neurons depended
on the way in which the hand was shaped during the motor act. For example the three main type ofneurons found by Rizzolatti et al. (1988) were precision grip, finger prehension and whole hand prehension
neurons. Furthermore, almost all of the neurons would discharge when the action was performed with
1 Some proximal type neurons have been identified as well.

6either hand. In addition, Rizzolatti et al. (1988) reported that 20% of the recorded neurons had visual
response properties and they required motivationally meaningful visual stimuli to be triggered.
Furthermore, they observed that, in the case of distal neurons, there was a relationship between the typeof prehension coded by the cells and the size of the stimulus (presented object) effective in triggering
the neurons. However, note that the purely motor related neurons constitute the majority of F5 neurons(Gallese 2002).

2.2.1.2

Visual properties: canonical neurons

Murata et al. (1997a) studied the properties of object related activity of F5 neurons. The result of
their study indicates that some F5 neurons encode object shapes in motor terms. That is, every time an
object is presented, its visual features are automatically translated into an internal motor representation.
The translation takes place whether a motor response is required or not. Therefore, these neurons are
not intention related.

Figure 2.2 A canonical neuron response during grasping of various objects in the dark (left to right and top tobottom: plate, ring, cube, cylinder, cone and sphere. The rasters and histograms are aligned with object
presentation. Small grey bars in each raster marks onset of key press, go signal, key release, onset of object
pulling, release signal, and object release, respectively. The peaks in ring and sphere object cases correspond to
the grasping of the object by the monkey (adapted from Murata et al. 1997a)

The similarity of the AIP and F5 visual neuron responses suggests that they may be part of avisuomotor transformation circuit. This view is supported by the reciprocal connections between F5 and
AIP (Sakata et al. 1997a). Figure 2.2 shows a canonical neuron’s response during motor execution. To
test whether the motor related activity was due to the vision of the object, the trial was performed in thedark. The neuron was primarily responsive for ring grasping and a lesser extend the sphere grasping.

7

The same neuron’s response in the object fixation, without any subsequent grasp requirement, isshown in Figure 2.3. It is important to note that the motor preference of the neuron is reflected in thevisual fixation condition as well.

Figure 2.3 The motor responses of the same neuron shown in Figure 2.2. The motor preference of the neuron is
also carried over to the visual preference (compare the ring and sphere histograms of both figures) (adaptedfrom Murata et al. 1997a)

2.2.1.3

Visual properties: mirror neurons

Recording studies of the rostral part of inferior area 6 (area F5) region showed that some of thevisual neurons were responsive to action observation (Gallese et al. 1996; Rizzolatti et al. 1996a;
Dipellegrino et al. 1992). The cells with action observation property have been located on the convexityof the bank of arcuate sulcus.. Like other F5 neurons, mirror neurons were active when the monkey
performs a particular class of actions. However, in addition the mirror neurons became active when themonkey observes the experimenter or another monkey performing an action (Gallese et al. 1996;
Rizzolatti et al. 1996a; Dipellegrino et al. 1992). In most of the mirror neurons, there was a clear relation
between the coded observed and executed action. The actions studied so far include grasping,manipulating and placing. The congruence between the observed and executed action varied. For someof the mirror neurons, the congruence was quite loose; for others, the general action (e.g. grasping) andthe way the action was executed (e.g. power grasp) had to match in order to activate to neuron (Gallese
et al. 1996; Rizzolatti et al. 1996a). An important observation was that mirror neurons required aninteraction between the experimenter and the object; the sight of the experimenter or the object alone
was not enough to trigger mirror activity. (Gallese et al. 1996; Rizzolatti et al. 1996a) All the neurons
were studied by examining their discharge while the experimenter performed a series of motor actionsin front of the monkey. These actions were related to food grasping and manipulation and other objects
grasping and manipulation. In order to verify whether the recorded neuron coded specifically handobject interactions a series of actions such as mimicking grasping without any object, prehension actions
with tools, mimicking grasp with spatially separated object were performed. All experimenter’s actions
were repeated on different positions (e.g. left,-right, far-close). Of the 532 recorded neurons, 92 of themshowed mirror property (i.e. they discharged both when the monkey made active movements andwhen it observed specific meaningful actions performed by the experimenter) (Gallese et al. 1996).
The two important aspects of the mirror neurons are (1) they are robust, they don’t habituate and(2) the distance of the experimenter to the monkey does not affect the response intensity of the cell.

8

Most of the neurons are active during observation of a single action: for example in the study ofGallese et al. (1996). 51/92 of the cells preferred only single action; 38/92 of the cells preferred two or
three actions; 3/92 of the cells were active for both hand or mouth grasps. The motor properties of theseneurons were indistinguishable from those of other F5 neurons. They had preference for certain actions:60/92 cells responded when the animal performed only a grasping action. 9/92 cells fired when the
animal grasped with his mouth. 11/92 of cells fired for both hand and mouth grasps (Gallese et al. 1996).
The remaining 14 neurons had the distribution: tearing (2), bringing to the mouth (2), manipulating (8).
The light and dark conditions were employed for 14 cells to test whether the motor property was a
result of self-hand vision. All the tested neurons confirmed that, the discharge was not due to self-vision(Gallese et al. 1996).

Figure 2.4 Activity of a cell during action observation (left) and action execution (right). There is no activity inpresentation of the object during both initial presentation and bringing the tray towards the monkey. The
vertical line over the histogram indicates the hand-object contact onset. (from Gallese et al., 1996).

Figure 2.4 shows the dual response property of mirror neurons. The recorded neuron in the figure
was silent during the presentation of the object, but started firing when the experimenter picked up theobject. The neuron, interestingly, did not fire during the time the tray was moved towards the monkey
and finally it started firing again when the monkey picked up the object. Note that during the period
when the tray was moved towards to monkey it could predict that he would grasp the object (Gallese etal. 1996)
Figure 2.5 shows the specificity of a grasp related mirror neuron where the experimenter
performed (A) a precision grip, (B) a whole hand prehension, and (C) mimicked a precision grip. The
notable property of this neuron is that miming the action was not effective in activating the neuron.

9

Figure 2.5 Visual response of a mirror neuron. A. Precision grasp B. power grasp C. mimicking of precision
grasp. The vertical lines over the histograms indicate the hand-object contact onset. (adapted from Gallese et al.,
1996)

In most mirror neurons, there is a relationship between the visual action they respond and the
motor action they code. The mirror neurons studied by Gallese et al. (1996) were divided into three,according to their visuomotor congruence: strictly congruent, broadly congruent and non-congruent. A
neuron was labeled as strictly congruent when the effective observed and executed actions match bothin terms of general action type (e.g. grasp) and in terms of how the action was executed (e.g. powergrasp). Figure 2.6 shows a strictly congruent neuron.

Figure 2.6 Example of a strictly congruent manipulating mirror neuron: A) The experimenter retrieved the foodfrom a well in a tray. B) Same action, but performed by the monkey. C) The monkey grasped a small piece offood using a precision grip. The vertical lines over the histograms indicate the hand-object contact onset(adapted from Gallese et al., 1996).

The number of strictly congruent neurons found was 29/92. The number of broadly congruent
neurons was 56/92 (Gallese et al. 1996). In the case of broadly congruent neurons, there was a link
between the executed action and the observed preferred action. These neurons were further subclassified according to their motor strictness: If a broadly congruent neuron fired only for one motor act(e.g. grasp) with only a single hand configuration (e.g. precision) then it would be of the first type. On
the other hand, if the neuron fired for one motor act but the way the action was performed did notaffect the firing then it would be of the second type. The third and last type of broadly congruent
neurons appear to be activated by the goal of the observed action (Gallese et al. 1996). Finally, theneurons with no apparent congruence were labeled as non-congruent (7/92). Figure 2.7 shows theclassification of F5 neurons including the mirror neuron types discussed.

10

F5 neurons

Mirror Neurons
Strictly congruent

Canonical Neurons

Non-congruent

Motor Neurons

Selective

Selective

Nonselective

Nonselective

Broadly congruent
Motor coding strict
Single motor coding; action may
be performed in multiple ways
Motor coding is hand grasping.
Visual coding however relates to
the goal of the action

Figure 2.7 The classification of area F5 neurons derived from published literature (Dipellegrino et al. 1992;
Gallese 2002; Gallese et al. 1996; Murata et al. 1997a; Murata et al. 1997b; Rizzolatti et al. 1996a; Rizzolatti andGallese 2001). All F5 neurons fire in response to some motor action. In addition, canonical neurons fire for object
presentation while the mirror neurons fire for action observation. The majority of hand related F5 neurons are
purely motor (Gallese 2002)(labelled as Motor Neurons in the figure)

Fogassi et al. (1998) found that area F5 was not the only area that had mirror neurons. The rostralpart of the inferior parietal lobule of the macaque monkey (area 7b or PF) also has neurons with similar
mirror properties. Although some neurons with strict congruence of the executed and observed action
have been found, the majority of the neurons studied had limited congruence (similarity) or nocongruence at all (Fogassi et al. 1998). 8/43 PF mirror neurons were strictly congruent; 9/43 had low
level of congruence (a similarity); and the majority (26/43) were non-congruent (Fogassi et al. 1998). The
main cortical input to area F5 comes from the inferior parietal lobe, and in particular areas AIP and PF(Matelli 1986). The similar properties of F5 canonical neurons with AIP neurons, and F5 mirror neurons
with PF neurons, suggests that these three areas work together for visuomotor transformation andaction recognition.

2.2.2

Area F4

Area F4 (see Figure 2.1) is connected with area F3 and to a lesser extent, to area F6 (Geyer et al.
2000). Area F4 projects to primary motor cortex (F1). The main parietal input to area F4 comes from VIP(Geyer et al. 2000). In area F4 the space is coded in body-parts-centred coordinate frame (e.g. centred on
the hand) (Fogassi et al. 1996). When the body-part-moves the coordinate system follows, but when thegaze moves the coordinate frame stays anchored on the body-part (Fogassi et al. 1996). Many of F4
neurons fire during reaching movements of the proximal arm but not the movements of the distal arm.
The neurons usually have somatosensory receptive fields that match the movement direction of thelimb (Gentilucci et al. 1988). It is suggested that VIP-F4 circuit transforms object locations into motor

11plans to reach towards them as area F4 sends descending projections to the brain stem and spinal
cord (Rizzolatti et al. 1998).

2.2.3

Areas F2 and F7 (dorsolateral prefrontal cortex)

Area F2 (see Figure 2.1) neurons can be grouped into three different classes: (1) signal related
neurons, (2) set-related neurons, and (3) movement-related neurons. (see Geyer et al. 2000 for a review).
Signal related neurons are activated right after visual instruction stimuli and have phasic response. Setrelated neurons show sustained activity after the instruction stimulus during the delay period.
Movement related neurons start firing after the trigger signal. Area F2 receives somatosensory input
from areas PEip and PEc, and visual input from areas MIP and V6A. Rizzolatti et al. (1998) suggested
that F2 can use the MIP and V6A inputs in controlling arm position during the transport of the hand to
spatial targets.

Figure 2.8 The macaque parieto-frontal projections from mesial parietal cortex, medial bank of the intraparietal
sulcus and the surface of the superior parietal lobule (adapted from Rizzolatti et al. 1998). Note that theBrodmann’s area 7m corresponds to Pandya and Seltzer's (1982) area PGm

Area F7 receives inputs from area 7m (Ferraina et al. 1997a; Ferraina et al. 1997b) (seeFigure 2.8). The neurons in area F7 fire in response to arm movements (Caminiti et al. 1991;
Crammond and Kalaska 1996) or visual stimuli (Shen and Alexander 1997b). However, in contrast to
area F2, area F7 visual response does not depend on a pending movement (di Pellegrino and Wise
1991). It appears that the 7m-F7 circuit is important for conditional movement selection (Geyer et al.
2000). The other projection to area F7 is from LIP (Lewis and Van Essen 2000), where saccade related
target memory activity is represented. The neuronal activity in LIP area can be modulated by attention
and eye position (see Colby and Duhamel 1996 for a review of LIP neuron responses). Thus, LIP-F7
circuit may be important for complex saccade control (Geyer et al. 2000).

12

2.2.4

Area F1 (the primary motor cortex)

Area F1 (see Figure 2.1) is organized somatotopically, where the body parts that require finer
movements are represented over a larger cortical surface than the body parts that require less precision.
Each neuron may contribute to multiple spinal neuron pools. The motor parameters that are encoded by
F1 neurons are usually a combination of the following physical parameters: force, rate of change offorce, joint position or the velocity of the movement (Pandya and Seltzer 1982). However, it is possible
to get meaningful physical parameters using a population of F1 neurons. Georgopoulos et al.
(Georgopoulos et al. 1982) trained monkeys to perform radial outward reaches to a target light.
Recording over a population of primary cortex neurons they showed that each neuron fired maximallyfor a direction (preferred direction), and fired less and less as the direction deviated form the preferred
direction. Given a population, the weighted sum of the preferred direction vectors, the population
vector, predicted the monkeys reaching direction.
The subcortical input to F1 is relayed by thalamus (see Matelli et al. 1989 for the distinct nuclei
projecting to F1). The corticocortical inputs to hand area of F1 comes primarily from supplementary
motor area (SMA) and to a lesser extent from the lateral premotor cortex. The other inputs are from area
1, 2 and 5 (Ghosh et al. 1987). Approximately half of the coriticospinal projections are formed by area F1
neurons (Dum and Strick 1991).

2.2.5

Areas F3 (SMA proper), F6 (pre-SMA)

Area F3 is somatotopically organized where arm and leg representations run as two oblique
dorsorostral-to-ventrocaudal directions (see Figure 2.1). In addition, area F3 has an orofacial
representation, while area F6 has only an arm representation (Luppino et al. 1991).
Areas F3 and F6 have different patterns of thalamic input indicating that they are part of different
motor loops with different functions (Luppino et al. 1991). Cortical input to area F3 originate mainly
from areas F2, F4, F5, F6 and F7, and the primary and secondary somatosensory cortices and theposterior parietal areas PE and Peci, and the cingulate and the primary motor cortex. On the other hand,area F6 is mainly connected with areas F5 and F7, followed by the prefrontal and cingulate cortex, F2,
F3 and F4, and to lesser extend with the posterior areas PG, PFG and superior temporal sulcus (Geyer et
al. 2000).

2.3

The superior temporal sulcus

In the macaques’s brain, posterior parietal cortex and the cortex of caudal superior temporal sulcus(STS) have been subdivided into numerous areas mainly involved in spatial analysis of the visualenvironment and in the control of spatially oriented behaviour (Maioli et al. 1998). The cortex ofsuperior temporal sulcus (STS) contains neurons that are selective for biological motion observationsuch as limb movements and full body motion. Perrett et al. (1990b) reported STS neurons that were
responsive to goal directed hand motion (Perret et al. 1990b; Perret et al. 1990a). PET studies showedthat STS in human shows strong activation during biologically meaningful visual stimuli (Bonda et al.
1996) including goal-directed hand actions. In monkeys, some of the STS neurons that are triggered bybiologically meaningful stimuli have two notable properties. Firstly, these neurons show responses togoal directed hand motion in a translation/scale/rotation invariant way (Perret et al. 1990b; Perret et al.
1990a). Secondly, these neurons do not require a pictorially realistic stimulus; they respond to point
light stimuli (Perret et al. 1990b; Perret et al. 1990a) where the stimulus is just the movement of a small
number of points. Bonda et al. (1996) also used this kind of stimulus − 3 lights for the arm and 2 for eachfinger − when they scanned the subjects during action observation.

13

2.4

Parietal Areas

Based on cytoarchitectonic and connectional criteria the inferior parietal lobule (Brodmann’s area7) includes areas 7a, 7b and 7ip (Cavada and Goldman-Rakic 1989). Area 7 reaches its highest
development in primates (Cavada and Goldman-Rakic 1989). Damage to this area can cause
impairments in spatial perception, neglect of sensory stimuli contralateral to the damage side, defects invisually guided reaching and occulomotor control (Ratcliff 1991; Stein 1991). Cavada & Goldman-Rakic(1989) divides area 7 in sub-areas of 7m, 7a, 7b, and 7ip. Area 7m is located on the medial surface of thehemisphere. This corresponds to Pandya and Seltzer's (1982) area PGm. Areas 7a, 7b lie on theconvexity of the posterior parietal lobule (Cavada and Goldman-Rakic 1989). These regions correspondto Pandya and Seltzer's (1982) PG and PF respectively . Pandya and Seltzer's (1982) also distinguish thesubdivisions of PGop and PFop in the lateral opercular part of PG and PF and area Opt in caudal PG.
Area 7ip is situated in the posterior bank of intraparietal sulcus and referred as POa by Pandya and
Seltzer (1982). In addition, the posterior half of 7ip corresponds to functionally defined areas VIP(Maunsell & Van Essen, 1983) and LIP (Andersen et al., 1985). Figure 2.9 shows the intraparietal sulcus(opened) and neighbouring parietal regions using Pandya and Seltzer (1982) nomenclature.

2.4.1

The anterior intraparietal area (AIP)The anterior part of the lateral bank of the intraparietal sulcus (area AIP) (see Figure 2.9) is
involved in extracting visual properties of objects relevant for grasping (Sakata et al. 1997a; Sakata et al.
1998; Sakata et al. 1995; Murata et al. 1996).

Figure 2.9 The intraparietal sulcus opened to show the anatomical location of AIP in the macaque (adapted fromGeyer et al. 2000)

Neurons in area AIP are active either in relation to the grasping behavior alolne or in relation to thevision of objects (Sakata et al. 1998; Sakata et al. 1997b; Taira et al. 1990). Some of the latter type are
active exclusively for visual fixation. In one study, 21% of cells studied responded to simply fixating an
object (visual-related), others (37%) were active only when a movement is being made to manipulate theobject (motor-related) (Taira et al. 1990). However, many cells (37%) fell somewhere between these two
extremes (visual-dominant) (Taira et al. 1990). Figure 2.10 shows the response of a visual-dominantneuron during different experimental conditions.

14

Figure 2.10 An AIP visual-dominant neuron activity under three task conditions: Object manipulation in thelight, object manipulation in the dark and object fixation in the light. The neuron is active during fixation andholding phase when the action is performed in light condition. However, during grasping in dark the neuronshows no activity. The fixation of the object alone without grasping also produces a discharge (adapted from
Sakata et al. 1997a)

The neuron shown in Figure 2.10 is active during fixation and holding phase when the action is
performed in light condition. However, in grasping-in-dark condition the neuron shows no activity. The
fixation of the object alone without grasping also produces a discharge, however the activity is less than
the grasping-in-light condition.
.

Figure 2.11 Activity the same neuron in Figure 2.10 during fixation of different objects. The neuron show
selectivity for horizontal plate (adapted from Sakata et al. 1997a)

In addition, some of these neurons show object specificity (object-type visual-dominant neurons)
which responds to the sight of complex objects such as a knob-in-groove and a plate-in-groove (Sakata

15

et al. 1997a). Figure 2.11 shows response profile of the same neuron in Figure 2.10 for different objects
during fixation. The neuron has a strong preference for the plate shaped object.

Figure 2.12 An AIP visual-dominant neuron’s axis orientation tuning and object fixation response is shown. The
neuron fires maximally during the fixation of a vertical bar or a cylinder. The tuning is demonstrated in thelower half of the figure (adapted from Sakata et al. 1999)

Furthermore some object-type visual-dominant neurons, show tuning according to the orientationof the longitudinal axis or the surface orientation of flat objects (Sakata et al. 1999; Murata et al. 2000).
An example of an object-type visual-dominant neuron that showed tuning for the axis orientation
regardless of the shape is presented in Figure 2.12. Top row shows the strong response of the neuron toa vertical cylinder, a square column, and a vertical knob-in-groove in the fixation condition. The bottom
row of Figure 2.12 demonstrates the tuning of the neuron for different axis orientations.
The muscimol-induced lesions of area AIP lead to a significant deficit in monkey's ability to grasp
objects (Sakata et al. 1997a; Gallese et al. 1994). The grasping movements become clumsy anduncoordinated, and as a result, the monkey is unable to shape his hand and orient his wrist
appropriately for objects that are presented. However, the monkey can still execute the basic sequenceof the task employed (Sakata et al. 1997a; Gallese et al. 1994).

2.4.2

The caudal intraparietal sulcus (c-IPS)

The lateral bank of the intraparietal sulcus (c-IPS) is involved in three-dimensional analysis ofobjects (Sakata et al. 1997a; Sakata et al. 1999). Some of these binocular visual neurons are selective forthe orientation of the axis of the objects (AOS neurons) and some are selective for the surface orientationof the objects (SOS neurons) (Sakata et al. 1997a; Sakata et al. 1999). AOS neurons prefer long and thinobjects as visual stimuli and are tuned to the three-dimensional axis orientation of the objects in space.
Figure 2.13 shows the response of an AOS neuron when the object is viewed in binocular viewing

16

condition. Figure 2.14 shows the same neuron’s response when the visual information is limited to theleft or right eye indicating that binocular cues are important for driving the AOS neuron shown. SOS
neurons prefer broad and flat objects as visual stimuli (Sakata et al. 1999). Complementary to AOS
neurons; they are tuned to the surface orientation of objects in three-dimensional space (see Figure 2.15).

Figure 2.13 Response of an axis-orientation-selective (AOS) neuron in the caudal part of the lateral bank of theintraparietal sulcus (c-IPS) to a luminous bar tilted 45° forward (left) or 45 backward (right) in the sagittal plane.
The monkey views the bar with binocular vision. The line segment under the histograms mark the fixation startand the period of 1 second. (adapted from Sakata et al. 1999)

It is suggested that c-IPS is a higher center for stereopsis, which integrates various binoculardisparity signals received from the V3 complex and other prestriate areas to represent the neural codefor geometric features of objects (Sakata et al. 1997a; Sakata et al. 1997b).

Figure 2.14 The response of the same neuron in Figure 2.13, for monocular vision conditions for the left andright eyes. (adapted from Sakata et al. 1999)

Sakata et al. (1997a) suggested that c-IPS could send projections to AIP and thus, contribute to thevisual adjustment of the shape of the hand grip and/or hand orientation for manipulation and grasping.
Figure 2.15 shows a SOS neuron that is selective for a surface that is 135 degrees tilted around thesagittal axis

17

Figure 2.15 Orientation tuning of a surface-orientation selective (SOS) neuron. First row: Stimuli presented.
Middle row: responses of the cell with binocular view. Last row: responses of the cell with monocular view(adapted from Sakata et al. 1997a)

2.4.3

Areas VIP, MIP and LIP

The intraparietal regions VIP, MIP and LIP (see Figure 2.9) encode the space around the animal
with multiple reference frames for different movement purposes (Colby and Goldberg 1999). A crude
separation is that VIP is involved in ultra-near space (less than 5cm from the face) (Colby et al. 1993b),
MIP with stimuli within reaching distance (Colby and Duhamel 1991) and LIP with far visual stimuli(Colby and Goldberg 1999).
LIP coding has been implicated as attentional (Gottlieb et al. 1998), decision-related (Shadlen andNewsome 2001; Shadlen and Newsome 1996), visual target memory related (Gnadt and Andersen 1988)
and motor intention related (Snyder et al. 2000; Snyder et al. 1997). Colby and Goldberg (1999)
suggested a unifying functional role for LIP that it encodes the representation of salient spatial locations(with attentional tuning). They noted the distinctive property of neurons in LIP that their firing was nottied to any particular modality and the representation was limited to attended objects and theirlocations.
Neurons in LIP have retinotopic receptive fields, where they carry visual, memory, and saccaderelated signals that describe stimuli in terms of the distance and direction of the stimulus or saccade
location relative to the center of gaze (Colby and Goldberg 1999). VIP neurons represent visual locations
using a continuum of eye centred to a head centred spatial reference frames (Bremmer et al. 1999;
Duhamel et al. 1997). Eskandar and Assad (1999) found neurons with reaching-related activity encoding
stimulus features, such as location and direction of stimulus motion. In addition, MIP neurons
maintained the memory of a reach target during the delay period of a memory-guided reach task orwhen the target is obscured (Eskandar and Assad 1999; Snyder et al. 1997). When the hand direction
and the visual target direction were disassociated through a well designed set up2, it was found that
2 The monkeys were trained to use a joystick to guide a spot of light to a circular target. While the animal fixated,

two spots within two circular targets appeared, oriented along the preferred/null axis of the cell. The monkey used18

MIP neuron activity correlated more with the hand direction than the object location. The opposite
was true for LIP neurons (Eskandar and Assad 1999) .

2.4.4

Areas 7a and 7b (PG and PF)

The experimental findings indicate that area 7a, together with other inferior parietal lobule sectors,
is involved in spatial coding. Researchers suggested various types of spatial encoding for area 7a. Stein(1991) suggested that area 7a represented extra-personal space. Andersen et al. (1999) suggested thatarea 7a represents targets in a world-centered coordinate frame. It has been shown that area 7a neurons
are involved in the analysis of motion evoked during locomotion or by the manipulation of objects by
the hands (Siegel and Read 1997). The different interpretation of area 7a responses can be due to either
the non-homogenous functional distributions of neurons or due to the experimental setup differences(see the reviews: Andersen et al. 1997; Wise et al. 1997).
It has been found that reach-related activity in area 7a signaled specific phases of the motor
performance (MacKay 1992). Further, it has been suggested that it could be used by the frontal lobe tofacilitate upcoming elements of a motor sequence, including terminal corrections (MacKay 1992). Motter
et al. (1987) identified visually sensitive and insensitive neurons in area 7a (Motter and Mountcastle
1981; Motter et al. 1987). The Neurons insensitive to visual stimuli comprised the fixation, oculomotor,
and projection-manipulation classes, which were suggested to be involved in initiatives toward action(Motter and Mountcastle 1981). Most of the visually sensitive neurons were activated from large andbilateral response areas that excluded the foveal region. The visually sensitive neurons were responsive
to stimulus movement and direction over a wide range of velocities. The movement vectors pointed
either inward toward the center or outward toward the perimeter of the visual field. For bilaterally
activated neurons, the vectors pointed in opposite directions in the two half-fields (opponent vector
organization). Motter and Mountcastle (1981) suggested that the neurons could signal motion in theimmediate surround.
Constantinidis and Steinmetz (1996) showed that a population of neurons in area 7a was active
during the delay period of a spatial memory task that did not require a motor response directed toward
the stimulus. Thus, it is suggested that the activity could represent a short-term memory trace for the
spatial location of the stimuli (Constantinidis and Steinmetz 1996). In accordance with the spatial
memory hypotheses, Maunsell (1995) indicated that the object location coding in area 7a was capable ofrepresenting visual stimuli without ever falling into the corresponding receptive field.
Another functional aspect of area 7a, the attentional tuning was studied by Constantinidis andSteinmetz (2001). Their results indicate that area 7a neurons represent the location of the stimulus that
attracts the animal's attention and can provide the spatial information required for directing attention toa salient stimulus in a complex scene (Constantinidis and Steinmetz 2001).
According to our view the fundamental and unifying property of area 7a neurons, is that they canpotentially be used to monitor the relation of body parts with respect to objects once they are fixated. A
population of neurons that detect the motion of visual stimuli inwards to (or outwards from) the
fixation point can encode the kinematics aspects (e.g. proximity) of a movement to satisfy a goal such asreaching or grasping. There is evidence that when humans perform reaching movements, they fixate totarget objects or obstacles to plan reach actions (Johansson et al. 2001), which can be thought of
the joystick to move one of the spots toward the opposite target. On 'visible’ trials, the moving spot remained
visible throughout its trajectory, and the opposite spot disappeared at the start of movement. On 'occluded' trials,
both spots disappeared without moving as soon as the animal moved the joystick, and the spot being guided thenreappeared near the target, as if it had been moving smoothly behind an occluder.

19

registering the relevant locations in area 7a as a saliency map. This proposal is supported by the factthat the removal of areas 7a, 7ab and LIP caused marked inaccuracy in reaching in the light to visualtargets but had no effect on reaching in the dark (Rushworth et al. 1997). In contrast, the removal ofareas 5, 7b and MIP caused misreaching in the dark, but had little effect on reaching in the light.
Therefore, Rushworth et al. (1997) suggested that the two divisions of the parietal cortex organize limb
movements in distinct spatial coordinate systems: area 7a/7ab/LIP are essential for spatial coordinationof visual motor transformations whereas areas 5/7b/MIP is essential for the spatial coordination of arm
movements in relation to proprioceptive and efference copy information.
Other parietal areas that can be involved in hand-object relation signals are area 7m (Ferraina et al.
1997a; Ferraina et al. 1997b), and area V6a and area PEc (Caminiti et al. 1999; Battaglia-Mayer et al. 2000;
Ferraina et al. 2001; Marconi et al. 2001).
Conventionally, area 7b is considered to be a somatosensory area (Andersen et al. 1990). Robinson
and Burton (1980b) studied the somatic response properties of neurons from area SII and area 7b. Onehalf of the recorded 7b neurons responded only to somatic stimulation. Many neurons in the lateralparts of area 7b were vigorously activated by tactile stimulation. In spite the majority of somatic
responses, some visual responses from area 7b were noted. The visual responses of 7b neurons were notstudied in detail either because it was not the focus of interest (as in Robinson and Burton 1980a) or due
to the complex response properties. In fact, it is possible to find considerable unimodal visual 7b
neurons as well as the neurons that respond only to visual stimulation (Dong et al. 1994). The visual
responses of 7b neurons can be based on the signals carried by the small projections from the visual
cortical areas (Andersen et al. 1990).
Fogassi et al. (1998) studied some of area 7b neurons’ visual properties. They found that theactivity of some neurons were triggered by the observation of various hand actions performed by theexperimenter. The neurons had motor properties similar to mirror neurons of area F5 (see section
2.2.1.3). The congruence between the action performed by the monkey and the observed action wasusually low. The connection of area F5 with area 7b (Fogassi et al. 1998) indicates an intimate relation
between 7b and F5 mirror neurons. Currently there are no detailed data on 7b mirror activity. However,unpublished results (Fogassi 1999) indicate that in addition to those neurons that have similar
properties as F5 mirror neurons there exist mirror-like neurons that fire for simple arm/hand movement
observations (in contrast to complete action observations).

2.5

Connectivity and other brain regions

According to Cavada and Goldman-Rakic (1989) 7m, 7a, 7ip are extensively connected with anumber of visual areas located on the medial surface of the hemisphere and in the depths of parietooccipital and intraparietal sulci. Areas 7m, 7a, 7ip, and to a much lesser extend 7b, are reciprocallyconnected with the visual temporal cortex, principally with the cortex of the superior temporal sulcus(STS) (Cavada and Goldmanrakic 1989). Although the density of 7b connections with the visual motion
cortex of STS is largely surpassed by the extensive connections of 7b with somatosensory areas theinterconnections of 7b with the visual regions are established through anterior 7ip, and the transitional
cortex 7ab between 7a and 7b (Cavada and Goldmanrakic 1989).

20

Figure 2.16 The reconstructed connectivity of area 7a. The thickness of the arrows represent the strength of theconnection. (adapted from Bota 2001)

Findings from the same study also confirm that AIP is connected with area 7b. Area 7ip is uniqueamong posterior parietal areas in its direct and indirect connections with the IT cortex (Cavada andGoldmanrakic 1989) and may form one of the object information channel to area AIP (Sakata et al.
1997b).Figure 2.16 and Figure 2.17 shows the reconstructed connectivity of areas 7a and 7b; while Figure
2.18 shows the reconstructed connectivity of AIP (Bota 2001).

21

Figure 2.17 The reconstructed connectivity of area 7b. The thickness of the arrows represent the strength of theconnection. (adapted from Bota 2001)

Andersen et al. (1990) suggests two types of processing for area 7a, each one following a different
path. First path originates from visual area V4, which is believed to have an important role in patternand color processing, and reaching to area 7a. Second path is the motion processing input originatingfrom the middle temporal area (MT) and relayed via medial superior temporal area (MST) or LIP(Andersen et al. 1990). MT lies on the posterior bank of the superior temporal sulcus, while MST lies on
the anterior bank of the same sulcus (Kandel et al. 2000; Maioli et al. 1998). MT projects to MST and toother areas in the parietal cortex concerned with visuospatial function. The preprocessed visual input
from V1 is further elaborated in MT, where the firing pattern of neurons reflect the speed and directionof motion of visual targets (Kandel et al. 2000). Barnes and Pandya (1992) report that area 7a (PG-Opt) isreciprocally connected to STS and suggest that the visuospatial analysis that is associated with posterior
intraparietal lobule could be amplified in the multimodal regions of STS. Therefore, the neurons ofmultimodal areas of the STS could be involved in analyzing the position of the body in relation to theenvironment (Barnes and Pandya 1992).

22

Figure 2.18 The reconstructed connectivity of area AIP. The thickness of the arrows represent the strength of theconnection. (adapted from Bota 2001)

AIP receives input from other areas of the posterior parietal cortex such as 7b (Neal et al. 1990). In
addition, this region has very significant recurrent cortico-cortical projections with area F5 of theinferior premotor cortex (Matelli et al. 1994; Sakata et al. 1997b). Figure 3.1 illustrates the visuomotor
stream for hand action as well other related structures. Also see Figure 2.18 for the reconstructedconnectivity diagram (Bota 2001) for AIP.
The anterior cingulate cortex is somatotopically organized and has direct connections with the
motor and premotor cortices, suggesting that among 7 areas 7b has preferential access to motor centers(Cavada and Goldmanrakic 1989). Area 7b is distinguished from other areas with its prominentconnections with somatosensory related areas including S1, S2, the vestibular cortex, area 5 and the
granular insular cortex. The only subdivision of area 7 that is connected to primary sensory cortex (S1)
is area 7b (Cavada and Goldman-Rakic 1989). The heaviest connection of area 7b is with S2 it is likelythat all body representation in S2 is connected to 7b (Cavada and Goldman-Rakic 1989). The connection
to granular insular cortex is wide spread which contains high proportion of somatic-sensitive neurons.
The connections of area 5 with 7b are topographic: the region of area 5 buried in the anterior bank of
IPS, which is involved in forelimb mechanisms, is the source of strongest projection from area 5 to area
7b (Cavada and Goldman-Rakic 1989).
We conclude our discussion of anatomical connections by summarazing the connectivity offunctionally defined intraparietal regions. Area 7a receives input from LIP (Andersen et al. 1990; Lewis
and Van Essen 2000), MIP (Boussaoud et al. 1990; Lewis and Van Essen 2000; Bota 2001) and VIP23(reviewed in Maunsell 1995; Lewis and Van Essen 2000). Interested readers can find more details
about these connections at the NeuroHomology Database Website3 (Bota 2001 and citations therein). The
premotor projections of these intraparietal areas include the regions F2 and F4 (Luppino et al. 1999) as
reviewed by Geyer et al.(2000).

2.6

Mirror neurons in humans

There is an unsettled debate about mirror neurons’ function. It is suggested that mirror neurons
may form the basis of understanding (Fadiga et al. 2000; Umilta et al. 2001), and imitation (Arbib 2001;
Rizzolatti and Arbib 1999) and even language in human (Rizzolatti and Arbib 1998). Thus, research formirror neuron existence in human became necessary to support the idea that mirror neuron
involvement in. cognitive tasks.
Grafton et al. (1996) using positron emission tomography (PET), scanned subjects under three
conditions, one of them being the control condition (object viewing). The other two were observing
grasping actions of common objects and imagining themselves doing the same grasp actions. Grafton etal. (1996) used only precision grasps. The imagined-minus-control and observation-minus-control
results were compared. The activation pattern was different. In their analysis, they categorized theactivations into lateral activations and medial/dorsal activations. The lateral activation is relevant forour discussion4. In the observation condition, the activity locations were left rostral superior temporalsulcus (STS), left inferior frontal cortex (area 45), and the left rostral inferior parietal cortex (area 40). In
addition, there was some activation found in the rostral part of the left intraparietal sulcus. However,
the imagined grasping activated the left inferior frontal (Broca’s area or area 44) and middle frontal
cortex, left caudal inferior parietal cortex (area 40) 5 . Based on these findings, Grafton et al. (1996)
suggested that the areas active during grasping observation might form a circuit for recognition ofhand-object interactions, whereas the areas active during imagined grasping might be a humanhomologue of the action observation and execution matching system found in monkeys (mirror
neurons). Their conclusion was that humans, as in monkeys, had a similar cortical circuit that wasinvolved in representing observed grasping. Unfortunately, Grafton et al. (1996) did not include theself-execution condition in the experimental setup. Therefore, it cannot be concluded that the areas
activated in this study have the dual property of the mirror neurons (the activation during self-action
and observation of the same action performed by the demonstrator). In addition, note the discrepancy
that the human homologue of the monkey F5, namely Broca’s area (Rizzolatti and Arbib 1998), was not
activated during grasp observation but only during imagined grasping.
In another study Grafton et al. (1997) used positron emission tomography (PET) imaging to test
whether the observation of tools activates premotor areas without any overt motor demand6. Toolobservation strongly activated the left dorsal premotor cortex. Silent tool-use naming activated Broca's
area, the left dorsal premotor cortex (more than the observation case), the left supplementary motor
area and the left ventral premotor cortex. These data indicate that, in human, F5 canonical type ofneurons may exist in the left ventral premotor cortex, which can be triggered by object observation.

3 http://brancusi.usc.edu/scripts/webmerger.exe?/database/homologies-main.html
4 The rostral part of the left supplementary motor area (SMA-proper), and the right dorsal premotor cortex werealso activated in grasp observation
5 The left rostral SMA-proper and left dorsal premotor cortex were also activated in imagined grasping
6 Silent naming of the presented tools was also studied

24

Iacoboni et al (1999) used functional magnetic resonance imaging (fMRI) to study the brain
regions involved in imitation. Their paradigm had three observation conditions and three observationexecution conditions. In the observation-execution conditions, imitative and non-imitative behavior of
simple finger movements was compared. In the imitative condition, participants had to execute theobserved finger movement. In the two non-imitative conditions, participants had to execute the same
movement in response to spatial or symbolic cues The imitation task, when contrasted to non-imitative
tasks, activated three areas: the left frontal operculum (Broca’s area or area 44), the right anteriorparietal region, and the right parietal operculum. The Broca’s area and right anterior parietal region was
also active during observation conditions. Iacoboni et al (1999) argued that Broca's area was activated
due the action-observation as Broca’s area is the human homologue of monkey area F5 (Rizzolatti and
Arbib 1998).
However, the data is not conclusive since, the Broca’s area was active for all observation cases, notonly the action observation. Krams et al (1998) in a similar study found that the Broca’s region was more
active during action preparation compared to action preparation-and-execution conditions. In bothconditions the visual stimuli presented was the same and consisted of a hand drawing with a mark on afinger indicating the action to be prepared for. Krams et al. (1998) argued that Broca’s are was involvedin action suppression (see Krams et al. 1998 for a detailed discussion). However, in both studies, theactions were intransitive; they did involve an object to be manipulated. In contrast, the majority of
mirror neurons require an object and the action together; the miming of the action is not effective(Gallese et al. 1996).
In one study the motor cortex was stimulated using transcranial magnetic stimulation techniquewhile the subjects (1) observed an experimenter grasping 3D-objects, (2) looked at the same 3D-objects,(3) observed an experimenter tracing geometrical figures in the air with his arm and (4) detected thedimming of a light (Fadiga et al. 1995). During the conditions of (1)-(4) the motor evoked potentials
were recorded from the hand muscles. Fadiga et al. (1995) found that motor evoked potentials increased
when the subjects observed movements. The motor evoked potential patterns reflected the pattern ofmuscle activity recorded when the subjects executed the observed actions. Therefore Fadiga et al. (1995)
concluded that in humans there is an action observation and execution matching system, which issimilar to monkey action recognition system (mirror neurons). This study showed that the effect ofexecuting and observing the same action performed by others is similar. However, the localization ofaction observation and execution matching system was not possible with motor evoked potential
recordings.
Hari et al. (1998) using a different technique (magnetoencephalogram) showed that the observationof object manipulation activated the primary motor cortex. Hari et al. (1998) recorded neuromagnetic
oscillatory activity of the human precentral cortex while subjects were (1) idle, (2) manipulating a small
object, and (3) observing another individual performing the same task. The left and right median nerves
were stimulated alternately (inter stimulus interval, 1.5s) at intensities exceeding motor threshold, andthe poststimulus rebound of the rolandic 15-to 25-Hz activity was quantified (Hari et al. 1998). The
rebound was diminished during action observation as it did in action execution case (the observation
suppression magnitude was 31-46% of the suppression during object manipulation). Hari et al. (1998)
concluded that the human primary motor cortex was activated during observation as well as executionof the motor tasks since the 15-to 25-Hz activity mainly originates from the precentral motor cortex.
Nishitani and Hari (2000) showed that the inferior frontal area was active during both execution
and observation of hand actions which confirmed the existence of a mirror system in human. In contrast
to several PET studies (e.g. Grafton et al. 1996; Decety et al. 1997; Rizzolatti et al. 1996b), Broca’s area

25

was active during action observation while area 45 was not active. Therefore, the study of Nishitaniand Hari (2000) not only shows that the human brain is endowed with a mirror neuron system but also
supports the hypothesis that Broca’s area is the locus of action observation and execution matchingsystem, which is consistent with the homology between Broca’s area and area F5 (Rizzolatti and Arbib
1998).
Buccino et al. (2001) used fMRI to localize action recognition circuitry in humans for actions
performed with different effectors. The subjects were presented with transitive and intransitive actions
performed with mouth, hand and foot. Observation of both object- and non-object-related actions
determined a somatotopically organized activation of premotor cortex. In addition, Buccino et al. (2001)
found that during the observation of object-related actions, an activation -also somatotopically organizedwas present in the posterior parietal lobe (Buccino et al. 2001). Buccino et al. (2001) argued that when
individuals observe object-related actions, an internal replica of the motor act and the result of an
object-related analysis are automatically generated in the ventral premotor cortex and the parietal lobe
respectively. This result suggests that the observation and execution matching system is not constrained
to hand actions but could be a general strategy used in the primate brain for interacting with theenvironment.

2.7

Summary

The posterior parietal cortex is involved in sensory-motor transformations, combining various
sensory inputs and computing representations that are used by the motor system to generate
movements. In particular AIP extract object features relevant for grasping. Other parietal areas such as
VIP, MIP and LIP are involved in spatial aspects of object representations. These areas project to motor
and premotor cortices enabling specific movement planning. Area F5 is involved in grasp planning
while F4 is involved in reaching movement planning. The visual areas in the superior temporal sulcus
perform visual analysis of form and motion including biological stimuli and provide parietal networks
with motion related and, for some sectors, highly processed visual input. Chapter 3 will factor theconnectivity specified in this chapter when developing Mirror Neuron System (MNS) model. The
neurophysiology of area F5 will guide the modelling presented in this thesis throughout. We will
implicate AIP and c-IPS as coding the object affordances serving as inputs to MNS and Learning toGrasp Models (LGM) of Chapters 5 and 6. We implicate target location schema to be represented inareas MIP/VIP/LIP, without specifying the neural region level assignment. Area 7a will combine thehand and object related visual inputs into an internal representation on which area 7b and F5 can beadapted to form mirror neurons.

26

3

CHAPTER III: MIRROR NEURON SYSTEM MODEL

Mirror neurons within a monkey's premotor area F5 fire not only when the monkey performs acertain class of actions but also when the monkey observes another monkey (or the experimenter)
perform a similar action. It has thus been argued that these neurons are crucial for understanding ofactions by others. This chapter offers the ‘hand-state’ hypothesis as a new explanation of the evolutionof this capability: the basic functionality of the F5 mirror system is to elaborate the appropriate feedback– what we call the hand state – for opposition-space based control of manual grasping of an object. Given
this functionality, the social role of the F5 mirror system in understanding the actions of others may beseen as an exaptation gained by generalizing from self-hand to other's-hand. In other words, mirror
neurons first evolved to augment the ‘canonical’ F5 neurons by providing visual feedback on ‘handstate’, relating the shape of the hand to the shape of the object.
First, we introduce the MNS (Mirror Neuron System) model of F5 and related brain regions interms of basic schemas. Then we aggregate them into three ‘grand schemas’ − Visual Analysis of Hand
State, Reach and Grasp, and the Core Mirror Circuit − for each of which we present a usefulimplementation. The MNS model shows how the mirror system can learn to recognize actions already inthe repertoire of the F5 canonical neurons. The chapter, in particular, shows how the connectivity
pattern of mirror neuron circuitry can be established through training, and that the resultant network
can exhibit a range of novel, physiologically interesting, behaviors during the process of action
recognition.

3.1

The mirror neuron system for grasping and FARS model

The macaque inferior premotor cortex has been identified as being involved in reaching andgrasping movements (Rizzolatti et al. 1988). This region has been further partitioned into two subregions: F5, the rostral region, located along the arcuate and F4, the caudal part (see Figure 3.1). The
neurons in F4 appear to be primarily involved in the control of proximal movements (Gentilucci et al.
1988), whereas the neurons of F5 are involved in distal control (Rizzolatti et al. 1988). Rizzolatti et al.
(1996a; Gallese et al. 1996). discovered a subset of F5 hand cells, which they called mirror neurons(Gallese et al. 1996; Rizzolatti et al. 1996a). Like other F5 neurons, mirror neurons are active when themonkey performs a particular class of actions, such as grasping, manipulating and placing. However, in
addition, the mirror neurons become active when the monkey observes the experimenter or anothermonkey performing an action. The term F5 canonical neurons is used to distinguish the F5 hand cells
which do not posses the mirror property but are instead responsive to visual input concerning a suitably
graspable object. The canonical neurons are indistinguishable from the mirror neurons with respect totheir firing during self-action. However they are different in their visual properties – they respond to
object presentation not action observation per se (Murata et al. 1997a).

27

Figure 3.1 Lateral view of the monkey cerebral cortex (IPS, STS and lunate sulcus opened). The visuomotor
stream for hand action is indicated by arrows (adapted from Sakata et al., 1997)

Most mirror neurons exhibit a clear relation between the observed and executed actions for which
they are active. The congruence between the observed and executed action varies. For some of themirror neurons, the congruence is quite loose; for others, not only must the general action (e.g.,
grasping) match but also the way the action is executed (e.g., power grasp) must match as well. To be
triggered, the mirror neurons require an interaction between the hand motion and the object. The visionof the hand motion or the object alone does not trigger mirror activity (Gallese et al. 1996).
It has thus been argued that the importance of mirror neurons is that they provide a neuralrepresentation that is common to execution and observation of grasping actions and thus that theseneurons are crucial to the social interactions of monkeys, providing the basis for understanding of actions
by others through their linkage of action and perception (Rizzolatti and Fadiga 1998). Below, we offer
the Hand-State Hypothesis, suggesting that this important role is an exaptation of a more primitive role,
namely that of providing feedback for visually-guided grasping movements. By exaptation we mean the
exploitation of an adaptation of a system to serve a different purpose (in this case for social
understanding) than it initially developed for (in this case, visual control of grasping). We will thendevelop the MNS (Mirror Neuron System) model and show that the system can exploit its ability torelate self-hand movements to objects to recognize the manual actions being performed by others, thus
yielding the mirror property. We also conduct a number of simulation experiments with the model andshow that these yield novel predictions, suggesting new neurophysiological experiments to further
probe the monkey mirror system. However, before introducing the Hand-State Hypothesis and the
MNS model, we first outline the FARS model of the circuitry that includes the F5 canonical neurons andprovides the conceptual basis for the MNS model.
Studies of the anterior intraparietal sulcus (AIP; Figure 3.1) revealed cells that were activated by
the sight of objects for manipulation . In addition, this region has very significant recurrent corticocortical projections with area F5 (Matelli 1984; Sakata et al. 1997a). In their computational model for28

primate control of grasping (the FARS – Fagg-Arbib-Rizzolatti-Sakata – model), Fagg and Arbib(1998) analyzed these findings of Sakata and Rizzolatti to show how F5 and AIP may act as part of avisuo-motor transformation circuit, which carries the brain from sight of an object to the execution of aparticular grasp. In FARS model, the findings of Sakata (on AIP) and Rizzolatti (on F5) were interpreted
as showing that AIP represents the grasps afforded by the object while F5 selects and drives theexecution of the grasp (Fagg and Arbib 1998). The term affordance (adapted from Gibson 1966) refers toparameters for motor interaction that are signaled by sensory cues without invocation of high-levelobject recognition processes. The model also suggests how F5 may use task information and otherconstraints encoded in prefrontal cortex (PFC) to resolve the action opportunities provided by multiple
affordances. Here we emphasize the essential components of the model (Figure 3.2) that will ground theversion of the MNS model presented below. We focus on the linkage between viewing an affordance ofan object and the generation of a single grasp.

AIP
AIP
DorsalStream:dorsal/ventral
streams
AffordancesWays to grab
this “thing”
Task Constraints(F6)
Working Memory
Working Memory (46)(46)
Instruction
Stimuli
Instruction
Stimuli (F2)
(F2)
Task Constraints (F6)PFC

VentralStream:Recognition

F5“It’s a mug”

IT

Figure 3.2 AIP extracts the affordances and F5 selects the appropriate grasp from the AIP ‘menu’. Various biases
are sent to F5 by Prefrontal Cortex (PFC) which relies on the recognition of the object by Inferotemporal Cortex(IT). The dorsal stream through AIP to F5 is replicated in the MNS model(1) The dorsal visual stream (parietal cortex) extracts parametric information about the object being
attended. It does not "know" what the object is; it can only see the object as a set of possible affordances.
The ventral stream (from primary visual cortex to inferotemporal cortex, IT), by contrast, recognize
what the object is and passes this information to prefrontal cortex (PFC) which can then, on the basis of
the current goals of the organism and the recognition of the nature of the object, bias F5 to choose theaffordance appropriate to the task at hand.
(2) AIP is hypothesized as playing a dual role in the seeing/reaching/grasping process, not only
computing affordances exhibited by the object but also, as one of these affordances is selected andexecution of the grasp begins, serving as an active memory of the one selected affordance and updating
this memory to correspond to the grasp that is actually executed.
(3) F5 is hypothesized as first being responsible for integrating task constraints with the set ofgrasps that are afforded by the attended object in order to select a single grasp. After selection of asingle grasp, F5 unfolds this represented grasp in time to govern the role of primary motor cortex (F1)in its execution.

29(4) In addition, the FARS model represents the way in which F5 may accept signals from areas F6(pre-SMA), 46 (dorsolateral prefrontal cortex), and F2 (dorsal premotor cortex) to respond to task
constraints, working memory, and instruction stimuli, respectively, and how these in turn may be
influenced by object recognition processes in IT (see Fagg and Arbib 1988 for more details), but these
aspects of the FARS model are included in MNS model.

3.2

The hand-state hypothesis

The key notion of the MNS model is that the brain augments the mechanisms modeled by the
FARS model, for recognizing the grasping-affordances of an object (AIP) and transforming these into a
program of action, by mechanisms which can recognize an action in terms of the hand state whichmakes explicit the relation between the unfolding trajectory of a hand and the affordances of an object.
Our radical departure from all prior studies of the mirror system is to hypothesize that this systemevolved in the first place to provide feedback for visually-directed grasping, with the social role of themirror system being an exaptation as the hand state mechanisms become applied to the hands of others
as well as to the hand of the animal itself.

3.2.1

Virtual fingers

As background for the Hand-State Hypothesis, we first present a conceptual analysis of grasping.
Iberall and Arbib (1990) introduced the theory of virtual fingers and opposition space. The term virtual
finger is used to describe the physical entity (one or more fingers, the palm of the hand, etc.) that is used
in applying force and thus includes specification of the region to be brought in contact with the object(what we might call the ‘virtual fingertip’). Figure 3.3 shows three types of opposition: those for the
precision grip, power grasp, and side opposition. Each of the grasp types is defined by specifying two
virtual fingers, VF1 and VF2, and the regions on VF1 and VF2 which are to be brought into contact withthe object to grasp it. Note that the "virtual fingertip" for VF1 in palm opposition is the surface of thepalm, while that for VF2 in side opposition is the side of the index finger.

Figure 3.3 Each of the 3 grasp types here is defined by specifying two "virtual fingers", VF1 and VF2, which aregroups of fingers or a part of the hand such as the palm which are brought to bear on either side of an object tograsp it. The specification of the virtual fingers includes specification of the region on each virtual finger to bebrought in contact with the object. A successful grasp involves the alignment of two "opposition axes": theopposition axis in the hand joining the virtual finger regions to be opposed to each other, and the opposition axis in
the object joining the regions where the virtual fingers contact the object. (Iberall and Arbib 1990)

The grasp defines two ‘opposition axes’: the opposition axis in the hand joining the virtual finger
regions to be opposed to each other, and the opposition axis in the object joining the regions where thevirtual fingers contact the object. Visual perception provides affordances (different ways to grasp theobject); once an affordance is selected, an appropriate opposition axis in the object can be determined.

30

The task of motor control is to preshape the hand to form an opposition axis appropriate to the chosenaffordance, and to so move the arm as to transport the hand to bring the hand and object axes intoalignment. During the last stage of transport, the virtual fingers move down the opposition axis (the‘enclose’ phase) to grasp the object just as the hand reaches the appropriate position.

3.2.2

The hand-state hypothesis

We assert as a general principle of motor control that if a motor plant is used for a task, then afeedback system will evolve to better control its performance in the face of perturbations. We thus ask,
as a sequel to the work of Iberall and Arbib (1990), what information would be needed by a feedback
controller to control grasping in the manner described in the previous section. Modeling of thisfeedback control is presented in Chapter 7, using a simplified hand/arm. In this chapter, our aim is toshow how the availability of such feedback signals in the primate cortex for self-action for manual
grasping can provide the action recognition capabilities which characterize the mirror system.
Specifically, we offer the following hypothesis.
The hand-state hypothesis: The basic functionality of the F5 mirror system is to elaborate theappropriate feedback – what we call the hand state – for opposition-space based control of manual
grasping of an object. Given this functionality, the social role of the F5 mirror system in understanding
the actions of others may be seen as an exaptation gained by generalizing from self-hand to other'shand.
The key to the MNS model, then, is the notion of hand state as encompassing data required todetermine whether the motion and preshape of a moving hand may be extrapolated to culminate in a
grasp appropriate to one of the affordances of the observed object. Basically a mirror neuron must fire if
the preshaping of the hand conforms to the grasp type with which the neuron is associated; and theextrapolation of hand state yields a time at which the hand is grasping the object along an axis for whichthat affordance is appropriate.
Our current representation of hand state defines a 7-dimensional trajectoryF(t) = (d(t), v(t), a(t), o1(t), o2(t), o3(t), o4(t))
with the following components (see Figure 3.4):
Three components are hand configuration parameters:a(t): Index finger-tip and thumb-tip apertureo3(t), o4(t): The two angles defining how close the thumb is to the hand as measured relative to theside of the hand and to the inner surface of the palm
The remaining four parameters relate the hand to the object. o1 and o2 components represent theorientation of different components of the hand relative to the opposition axis for the chosen affordancein the object whereas d and v represents the kinematics properties of the hand with reference to thetarget location.
o1(t): The cosine of the angle between the object axis and the (index finger tip – thumb tip) vectoro2(t): The cosine of the angle between the object axis and the (index finger knuckle – thumb tip) vectord(t): distance to target at time tv(t): tangential velocity of the wrist

31
Object opposition axis

Aperture (a(t))

Thumb angle 1(o3(t))

Grasp Axis

Distance (d(t))

Velocity (v(t))
Thumb angle 2(o4(t))

Axis disparity 2 (arccos(o2(t)))

Hand opposition axis
(thumb, index knuckle)
Hand opposition axis
(thumb, index fingertip)
Axis disparity 1 (arccos(o1(t)))

Figure 3.4 The components of hand state F(t) = (d(t), v(t), a(t), o1(t), o2(t), o3(t), o4(t)). Note that some of thecomponents are purely hand configuration parameters (namely v,o3,o4,a) whereas others are parameters
relating hand to the object

In considering the last four variables, note that only one or two of them will be relevant ingenerating a specific type of grasp, but they all must be available to monitor a wide range of possible
grasps. We have chosen a set of variables of clear utility in monitoring the successful progress ofgrasping an object, but do not claim that these and only these variables are represented in the brain.
Indeed, the brain's actual representation will be a distributed neural code, which we predict willcorrelate with such variables, but will not be decomposable into a coordinate-by-coordinate encoding.
However, we believe that the explicit definition of hand state offered here will provide a firm
foundation for the design of new experiments in kinesiology and neurophysiology.
The crucial point is that the availability of the hand state to provide feedback for visually-directed
grasping makes action recognition possible. Notice that we have carefully defined the hand state interms of relationships between hand and object (though the form of the definition must be subject tofuture research). This has the benefit that it will work just as well for measuring how the monkey’s own
hand is moving to grasp an object as for observing how well another monkey’s hand is moving to grasp
the object. This, we claim, is what allows self-observation by the monkey to train a system that can beused for observing the actions of others and recognizing just what those actions are.

3.3

The MNS (mirror neuron system) model

We now present a high level view of the MNS (Mirror Neuron System) model in terms of the set ofinteracting schemas (functional units: Arbib 1981; Arbib et al. 1998) shown in Figure 3.5, which define the32

MNS (Mirror Neuron System) model of F5 and related brain regions. The connectivity shown in
Figure 3.5 is constrained by the existing neurophysiology and neuroanatomy of the monkey brain(reviewed in Chapter 2). We have already introduced areas AIP and area F5, dividing the F5 grasprelated neurons into (i) F5 mirror neurons which are, when fully developed, active during certain selfmovements of grasping by the monkey and during the observation of a similar grasp executed byothers, and (ii) F5 canonical neurons, namely those active during self-movement and object vision but not
for recognition of the action of others. Other brain regions also play an important role in mirror neuron
system functioning in the macaque’s brain for which the readers are referred to Chapter 2.

Visual Cortex

Object features
cI PS

Objectaffordance
extraction

7b Object affordance-hand state
association

AI P

H and
shape
recognition
H andmotiondetection
STS

Integrate
temporalassociation

A ction
M irrorFeedback recognition
H and-Object
spatial relation
analysis
7aF5canonical
M otorprogram(Grasp)(M irrorN eurons)

M otorprogram(Reach)F5mirrorF4

M otorexecution
M1

ObjectlocationM I P/LI P/V I P

Figure 3.5 The MNS (Mirror Neuron System) model. (i) Top diagonal: a portion of the FARS model. Object
features are processed by cIPS and AIP to extract grasp affordances, these are sent on to the canonical neuronsof F5 that choose a particular grasp. (ii) Bottom right. Recognizing the location of the object provides parameters
to the motor programming area F4 which computes the reach. The information about the reach and the grasp istaken by the motor cortex M1 to control the hand and the arm. (iii) New elements of the MNS model: Bottom
left are two schemas, one to recognize the shape of the hand, and the other to recognize how that hand ismoving. (iv) Just to the right of these is the schema for hand-object spatial relation analysis. It takes information
about object features, the motion of the hand and the location of the object to infer the relation between handand object. (v) The center two regions marked by the gray rectangle form the core mirror circuit. This complex
associates the visually derived input (hand state) with the motor program input from region F5canonicalneurons during the learning process for the mirror neurons. The grand schemas introduced in section 3.2 areillustrated as the following. The “Core Mirror Circuit” schema is marked by the center grey box; The “Visual
Analysis of Hand State” schema is outlined by solid lines just below it, and the “Reach and Grasp” schema isoutlined by dashed lines. (Solid arrows: established connections; dashed arrows: postulated connections)

The subsystem of the MNS model responsible for the visuo-motor transformation of objects into
affordances and grasp configurations, linking AIP and F5 canonical neurons, corresponds to a key
subsystem of the FARS model reviewed above. Our task is to complement the visual pathway via AIP
by pathways directed toward F5 mirror neurons which allow the monkey to observe arm-handtrajectories and match them to the affordances and location of a potential target object. We will then33

show how the mirror system may learn to recognize actions already in the repertoire of the F5canonical neurons. In short, we will provide a mechanism whereby the actions of others are‘recognized’ based on the circuitry involved in performing such actions. The Methods section provides
the details of the implemented schemas and the Results section confronts the overall model with virtual
experiments and produces testable predictions.

3.3.1

Overall function

In general, the visual input to the monkey represents a complex scene. However, we here sidestep
much of this complexity (including attentional mechanisms) by assuming that the brain extracts twosalient sub-scenes, a stationary object and in some cases a (possibly) moving hand. The overall system
operates in two modes:(i) Prehension: In this mode, the view of the stationary object is analyzed to extract affordances;then under prefrontal influence F5 may choose one of these to act upon, commanding the motor
apparatus to perform the appropriate reach and grasp based on parameters supplied by the parietal
cortex. The FARS model captures the linkage of F5 and AIP with PFC, prefrontal cortex (Figure 3.2). In
the MNS model, we incorporate the F5 and AIP components from FARS (top diagonal of schemas in
Figure 3.5), but omit IT and PFC from the present analysis.
(ii) Action recognition: In this mode, the view of the stationary object is again analyzed to extractaffordances, but now the initial trajectory and preshape of an observed moving hand must be
extrapolated to determine whether the current motion of the hand can be expected to culminate in a
grasp of the object appropriate to one of its affordances.
We do not prespecify all the details of the MNS schemas. Instead, we offer a learning model which,given a grasp that is already in the motor repertoire of the F5 canonical neurons, can yield a set of F5
mirror neurons trained to be active during such grasps as a result of self-observation of the monkey's own
hand grasping the target object. (How such grasps may be acquired in the first place is a topic of current
research.) Consistent with the hand-state hypothesis, the result will be a system whose mirror neurons
can respond to similar actions observed being performed by others. The current implementation of the MNSmodel exploits learning in artificial neural nets.
The heart of the learning model is provided by the Object affordance-hand state association schema
and the Action recognition (mirror neurons) schema. These form the core mirror (learning) circuit, marked
by the gray slanted rectangle in Figure 3.5, which mediates the development of mirror neurons via
learning. The simulation results of this article will focus on this part of the model. Section 3.4.3.1
presents in detail the neural network structure of the core circuit. As we note further in the Discussionsection, this leaves open many problems for further research, including the development of a basic
action repertoire by F5 canonical neurons through trial-and-error in infancy and the expansion andrefinement of this repertoire throughout life.

3.3.2

Schemas explained

As shown in the caption of Figure 3.5, we encapsulate the schemas shown there into the three‘grand schemas’ of Figure 3.6(a). These guide our implementation of MNS. Our earlier review of theneuroscience literature in Chapter 2 justifies our initial hypotheses, made explicit in Figure 3.5, as towhere these finer-grain schemas are realized in the monkey brain. However, after we explain thesefiner-grain schemas, we will then turn to our present simulation of the three grand schemas which isbased on overall functionality. Nonetheless, the neural structure of Core Mirror Circuit yields
interesting predictions for further neurophysiological experimentation.

34

3.3.2.1

Grand schema 1: reach and grasp

Visual Input

Object features schema: The output of this schema provides a coarse coding of geometricalfeatures of the observed object. It thus provides suitable input to AIP and other regions/schemas.
Object affordance extraction schema: This schema transforms its input, the coarse coding ofgeometrical features of the observed object provided by the Object features schema, into a coarse coding
for each affordance of the observed object.
Motor program (grasp) schema: We identify this schema with the canonical F5 neurons, as in the
FARS model. Input is provided by AIP's coarse coding of affordances for the observed object. We
assume that the output of the schema encodes a generic motor program for the AIP-coded affordances.
This output serves as the learning signal to the Action-recognition (Mirror neurons) schema and drives
the hand control functions of the Motor execution schema.

Reach and Grasp Schema
Object Affordance

Visual Analysis
of Hand State

Grasp CommandCore
MirrorCircuitHand State

Action Code(a)
Object Affordance

Hand State

Grasp CommandCore Mirror Circuit

Action Code(b)
Figure 3.6 (a) For purposes of simulation, we aggregate the schemas of the MNS (Mirror Neuron System) modelof Figure 3.5 into three "grand schemas" for Visual Analysis of Hand State, Reach and Grasp, Core Mirror
Circuit. (b) For detailed analysis of the Core Mirror Circuit, we dispense with simulation of the other two grandschemas and use other computational means to provide the three key inputs to this grand schema

Object location schema: The output of this schema provides, in some body-centered coordinate
frame, the location of the center of the opposition axis for the chosen affordance of the observed object.
Motor program (reach) schema: The input is the position coded by the Object location schema,
while the output is the motor command required to transport the arm to bring the hand to the indicatedlocation. This drives the arm control functions of the Motor execution schema.
The motor execution schema determines the course of movements via activity in primary motor
cortex M1 and "lower" regions.
We next review the schemas which (in addition to the previously presented Object features andObject affordance extraction schemas) implement the visual system of the model:

3.3.2.2

Grand Schema 2: Visual Analysis of Hand State

The hand shape recognition schema takes as input a view of a hand, and its output is a
specification of the hand shape, which thus forms some of the components of the hand state. In the35current implementation these are a(t), o3(t) and o4(t). Note also that we implicitly assume that theschema includes a validity check to verify that the scene does contain a hand.
The hand motion detection schema takes as input a sequence of views of a hand and returns as
output the wrist velocity, supplying the v(t) component of the hand state.
The hand-object spatial relation analysis schema receives object-related signals from the Object
features schema, as well as input from the Object Location, Hand shape recognition and Hand motion
detection schemas. Its output is a set of vectors relating the current hand preshape to a selectedaffordance of the object. The schema computes such parameters as the distance of the object to the hand,
and the disparity between the opposition axes of the object and the hand. Thus the hand statecomponents o1(t), o2(t), and d(t) are supplied by this schema. The Hand-Object spatial relation analysis
schema is needed because, for almost all mirror neurons in the monkey, a hand mimicking a matchinggrasp would fail to elicit the mirror neuron's activity unless the hand's trajectory were taking it toward
an object with a grasp that matches one of the affordances of the object. The output of this visual
analysis is relayed to the Object affordance-hand state association schema which drives the F5 mirror
neurons whose output is a signal expressing confidence that the observed trajectory will extrapolate tomatch the observed target object using the grasp encoded by that mirror neuron.

3.3.2.3

Grand Schema 3: Core Mirror Circuit

The action recognition schema – which is meant to correspond to the mirror neurons of area F5 –receives two inputs in our model. One is the motor program selected by the Motor program schema; theother comes from the Object affordance-hand state association schema. This schema works in two modes:
learning and recognition. When a self-executed grasp is taking place the schema is in learning modeand the association between the observed hand-state (Object affordance-hand state association schema) andthe motor program (Motor program schema) is learned. While in recognition mode, the motor program
input is not active and the schema acts as a recognition circuit. If satisfactory learning (in terms ofgeneralization and the range of actions learned) has taken place via self-observation then the schema
will respond correctly while observing other’s grasp actions.
The object affordance-hand state association schema combines all the hand related information as
well as the object information available. Thus the inputs to the schema are from Hand shape recognition(components a(t), o3(t), o4(t)), Hand motion detection (component v(t)), Hand-Object spatial relation analysis(o1(t), o2(t), d(t)) and from Object affordance extraction schemas. As will be explained below, the schema
needs a learning signal (mirror feedback). This signal is relayed by the Action recognition schema and, isbasically, a copy of the motor program passed to the Action recognition schema itself. The output of thisschema is a distributed representation of the object and hand state match (in our implementation the
representation is not pre-specified but shaped by the learning process). The idea is to match the object
and the hand state as the action progresses during a specific observed reach and grasp. In the current
implementation, time is unfolded into a spatial representation of ‘the trajectory until now’ at the inputof the Object affordance-hand state association schema, and the Action recognition schema decodes the
distributed representation to form the mirror response (again, the decoding is not pre-specified but isthe result of the back-propagation learning). In any case, the schema has two operating modes. First is
the learning mode where the schema tries to adjust its efferent and afferent weights to ensure the rightactivity in the Action recognition schema. The second mode is the forward mode where it maps the handstate and the object affordance into a distributed representation to be used by the Action recognition
schema.

36

The key question for this chapter’s modeling will be to account for how learning mechanisms
may shape the connections to mirror neuron in such a way that an action in the motor program
repertoire of the F5 canonical neurons may become recognized by the mirror neurons when performedby others. In Chapter 5 and Chapter 6 we will present models that can learn a repertoire of grasping
actions.
To conclude this section, we note that our modeling is subject to two quite different tests: (i) its
overall efficacy in explaining behavior and its development, which can be tested at the level of theschemas (functional units) presented in this article; and (ii) its further efficacy in explaining andpredicting neurophysiological data. As we shall see below, certain neurophysiological predictions are
possible given the current work, even though the present implementation relies on relatively abstract
artificial neural networks.

3.4

Schema implementation

Having indicated the functionality and possible neural basis for each of the schemas that will makeup each grand schema, we now turn to the implementation of these three grand schemas. We
implement the three grand schemas so that each functions correctly in terms of its input-output
relations, and so that the Core Mirror Circuit contains model neurons whose behavior can be tested
against neurophysiological data and yield predictions for novel neurophysiological experiments. The
Core Mirror Circuit is thus the heart of MNS model that enables us to produce testable predictions(Figure 3.6b), but in order to study it, there must be an appropriate context, necessitating theconstruction of the kinematically realistic Reach and Grasp Simulator and the Visual Analyzer for Hand
State. The latter will first be implemented as an analyzer of views of human hands, and then will haveits output replaced by simulated hand state trajectories to reduce computational expense in our detailed
analysis of the Core Mirror.

3.4.1

Grand schema 1: reach and grasp

We first discuss the Reach and Grasp Simulator that corresponds to the whole reach and grasp
command system shown at the right of the MNS diagram (Figure 3.5). The simulator lets us move fromthe representation of the shape and position of a (virtual) 3D object and the initial position of the(virtual) arm and hand to a trajectory that successfully results in simulated grasping of the object. In
other words the simulator plans a grasp and reach trajectory and executes it in a simulated 3D world(see Chapters 5 and 6 for neural realization of this schema). Trajectory planning (for example Kawato
and Gomi 1992; Kawato et al. 1987; Jordan and Rumelhart 1992; Karniel and Inbar 1997; Breteler et al.
2001) and control of prehension(Hoff and Arbib 1993; see Wolpert and Ghahramani 2000 for a review),
and their adaptation, have been widely studied. However, our simulator is not adaptive − its sole
purpose is to create kinematically realistic actions. A similar reach and grasp system was proposed(Rosenbaum et al. 2001; Rosenbaum et al. 1999) where a movement is planned based on the constraint
hierarchy, relying on obstacle avoidance and candidate posture evaluation processes (Meulenbroek et
al. 2001). However, the arm and hand model was much simpler than ours as the arm was modeled as a
2D kinematics chain. Our Reach/Grasp Simulator is a non-neural extension of FARS model functionality
to include the reach component. It controls a virtual 19 degrees DOF arm/hand (3 at the shoulder, 1 forelbow flexion/extension, 3 for wrist rotation, 2 for each finger joints with additional 2 DOFs for thumb
one to allow the thumb to move sideways, and the other for the last joint in the thumb) and provides
routines to perform realistic grasps. This kinematics realism is based on the literature of primate reachand grasp experiments (Jeannerod et al. 1995; for human see Hoff and Arbib 1993 and citations therein;
for monkey see Roy et al. 2000). During a typical reach to grasp movement, the hand will follow a ‘bell-

37

shaped’ velocity profile (a single peaked velocity curve). The kinematics of the aperture between
fingers used for grasping also exhibits typical characteristics. The aperture will first reach a maximum
value that is larger than the aperture required for grasping the object and then as the hand approaches
to the target the hand encloses to match the actual required aperture for the object. It is also important
to note that in grasping tasks the temporal pattern of reaching and grasping is similar in monkey andhuman (Roy et al. 2000). Of course, there are inter-subject and inter-trial variability in both velocity andaperture profiles (Marteniuk and MacKenzie 1990). Therefore in our simulator we captured thequalitative aspects of the typical reach and grasp actions, namely that the velocity profiles have single
peaks and that the hand aperture has a maximum value which is larger than the object size (see Figure
3.7, curves a(t) and v(t) for sample aperture and velocity profiles generated by our simulator) . A grasp
is planned by first setting the operational space constraints (e.g., points of contact of fingers on theobject) and then finding the arm-hand configuration to fulfill the constraints. The latter is the inverse
kinematics problem. The simulator solves the inverse kinematics problem by simulated gradientdescent with noise added to the gradient (see Appendix 11.1.2 for a grasp planning example). Once thehand-arm configuration is determined for a grasp action, then the trajectory is generated by warpingtime using a cubic spline. The parameters of the spline are fixed and determined empirically to satisfy
aperture and velocity profile requirements. Within the simulator, it is possible to adjust the target
identity, position and size manually using a GUI or automatically by the simulator as, for example, intraining set generation.
Hand state values(normalized to 0.0 – 1.0 range)
d(t)

o3(t)
o4(t)
a(t)
o2(t)
v(t)
o1(t)
0.0

Normalized time

1.0

Figure 3.7 (Left) The final state of arm and hand achieved by the reach/grasp simulator in executing a powergrasp on the object shown. (Right) The hand state trajectory read off from the simulated arm and hand during
the movement whose end-state is shown at left. The hand state components are: d(t), distance to target at time t;v(t), tangential velocity of the wrist; a(t), Index and thumb finger tip aperture; o1(t), cosine of the angle between
the object axis and the (index finger tip – thumb tip) vector; o2(t), cosine of the angle between the object axis andthe (index finger knuckle – thumb tip) vector; o3(t), The angle between the thumb and the palm plane; o4(t), Theangle between the thumb and the index finger

Figure 3.7 (left) shows the end state of a power grasp, while Figure 3.7 (Right) shows the timeseries for the hand state associated with this simulated power grasp trajectory. For example, the curvelabeled d(t) show the distance from the hand to the object decreasing until the grasp is completed; while38

the curve labeled a(t) show how the aperture of the hand first increases to yield a safety margin larger
than the size of the object and then decreases until the hand contacts the object.

Figure 3.8 Grasps generated by the simulator. (a) A precision grasp. (b) A power grasp. (c) A side grasp

Figure 3.8(a) shows the virtual hand/arm holding a small cube in a precision grip in which the index
finger (or a larger "virtual finger") opposes the thumb. The power grasp (Figure 3.8(b)) is usuallyapplied to big objects and characterized by the hand’s covering the object, with the fingers as one virtual
finger opposing the palm as the other. In a side grasp (Figure 3.8(c)), the thumb opposes the side ofanother finger. To clarify the type of heuristics we use to generate the grasp, Appendix 11.1.2 outlines
the grasp planning and execution for a precision pinch.

3.4.2

Grand schema 2: visual analysis of hand state

Visual Analysis of Hand State Schema is a non-neurophysiological implementation of a visual
analysis system to validate the extraction of hand parameters from a view of a hand, by recovering theconfiguration of a model of the hand being seen. The hand model is a three dimensional 14 degrees of
freedom (DOF) kinematic model, with a 3-DOF joint for the wrist, two 1-DOF joints(metacarpophalangeal and distalinterphalangeal) for each of the four fingers, and finally a 1-DOF joint
for the metacarpophalangeal joint, and a 2-DOF joint for the carpometacarpal joint of the thumb. Notethe distinction between ‘hand configuration’ which gives the joint angles of the hand considered in39isolation, and the ‘hand state’ which comprises 7 parameters relevant to assessing the motion andpreshaping of the hand relative to an object. Thus, the hand configuration provides some, but not all, ofthe data needed to compute the hand state.
To lighten the load of building a visual system to recognize hand features, we marked the wrist
and the articulation points of the hand with colors. We then used this color-coding to help recognize
key portions of the hand and used this result to initiate a process of model matching. Thus, the first stepof the vision problem was color segmentation, after which the three dimensional hand shape wasrecovered.

3.4.2.1

Color segmentation and feature extraction

One needs color segmentation to locate the colored regions on the image. Gray level segmentation
techniques cannot be used in a straightforward way because of the vectorial nature of color images(Lambert and Carron 1999). Split-and-Merge is a well-known image segmentation technique in image
processing (Sonka et al. 1993), recursively splitting the image into smaller pieces until somehomogeneity criterion is satisfied as a basis for reaggregation into regions. In our case, the criterion ishaving similar color throughout a region. However, RGB (Red-Green-Blue) space is not well suited forthis purpose. HSV (Hue-Saturation-Value) space is better suited since hue in segmentation processes
usually corresponds to human perception and ignores shading effects (Russ 1998 Chapters 1 and 6).
However, the segmentation system we implemented with HSV space, although better than the RGB
version, was not satisfactory for our purposes. Therefore, we designed a system that can learn the bestcolor space.
Figure 3.9(a) shows the training phase of the color expert system, which is a (one hidden-layer) feedforward network with sigmoidal activation function. The learning algorithm is back-propagation with
momentum and adaptive learning rate. The given image is put through a smoothing filter to reducenoise in the image before training. Then the network is given around 100 training samples each ofwhich is a vector of ((R, G, B), perceived color code) values. The output color code is a vector consisting of
all zeros except for one component corresponding to the perceived color of the patch. The training builds
an internal non-linear color space from which it can unambiguously tell the perceived color. This
training is done only at the beginning of a session to learn the colors used on the particular hand. Thenthe network is fixed as the hand is viewed in a variety of poses.

40
(a)

Preprocessing

One hidden layer
feed-forward
neural network

Network Weights(Color Expert)

Neural Network Training

Hand image for training(b)Color segmentation
System augmented
with the trainedneural network

Features

Hand Image input for
actual segmentation
Color segmentation using the Color Expert

Figure 3.9 (a) Training the color expert, based on colored images of a hand whose joints are covered with
distinctively colored patches. The trained network will be used in the subsequent phase for segmenting image.
(b) A hand image (not from the training sample) is fed to the augmented segmentation program. The color
decision during segmentation is done by consulting to the Color Expert. Note that a smoothing step (not shown)is performed before segmentation

Figure 3.9(b) illustrates the actual segmentation process using the ‘color expert’ to find each regionof a single (perceived) color (see Appendix 11.1.1 for details). The output of the algorithm is thenconverted into a feature vector with a corresponding confidence vector giving a confidence level foreach component in the feature vector. Each finger is marked with two patches of the same color.
Sometimes it may not be possible to determine which patch corresponds to the fingertip and which to
the knuckle. In those cases, the confidence value is set to 0.5. If a color is not found (e.g., the patch may
be obscured), a zero value is given for the confidence. If a unique color is found without any ambiguity
then the confidence value is set to 1. The segmented centers of regions (color markers) are taken as theapproximate articulation point positions. To convert the absolute color centers into a feature vector we
simply subtract the wrist position from all the centers found and put the resulting relative (x,y)
coordinate into the feature vector (but the wrist is excluded from the feature vector as the positions are
specified with respect to the wrist position).

3.4.2.2

3D hand model matching

Our model matching algorithm uses the feature vector generated by the segmentation system toattain a hand configuration and pose that would result in a feature vector as close as possible to the
input feature vector (Figure 3.10). The scheme we use is a simplified version of Lowe’s (1991); see
Holden (1997) for a review of other hand recognition studies.

41

Feature Vector

Result of feature extraction

Initial Configurationof Hand Model

Final Configurationof Hand Model

Figure 3.10 Illustration of the model matching system. Left: markers located by feature extraction schema.
Middle and Right: initial and final stages of model matching. After matching is performed a number ofparameters for the Hand configuration are extracted from the matched 3D model

The matching algorithm is based on minimization of the distance between the input feature andmodel feature vector, where the distance is a function of the two vectors and the confidence vector
generated by segmentation system. Distance minimization is realized by hill climbing in feature space.
The method can handle occlusions by starting with ‘don't cares’ for any joints whose markers cannot beclearly distinguished in the current view of the hand
The distance between two feature vectors F and G is computed as follows:D( F , G ) = ( Fi − Gi ) 2 Ci f Cig
where subscripting denotes components and Cf, Cg denotes the confidence vectors associated withF and G. Given this result of the visual processing – our hand shape recognition schema – we can clearlyread off the following components of the hand state, F(t):a(t): aperture of the virtual fingers involved in graspingo3(t), o4(t): the two angles defining how close the thumb is to the hand as measured relative to theside of the hand and to the inner surface of the palm (see Figure 3.4). The remaining components caneasily be computed once the object affordance and location is known. The computation of thecomponents:
d(t): distance to target at time t, andv(t): tangential velocity of the wristo1(t): Angle between the object axis and the (index finger tip – thumb tip) vectoro2(t): Angle between the object axis and the (index finger knuckle – thumb tip) vector
constitute the tasks of the hand-object spatial relation analysis schema and the hand motion detection
schema. These require visual inspection of the relation between hand and target, and visual detection ofwrist motion, respectively. Section 3.5.3 presents justifies the visual analysis of hand state schema byshowing MNS performance when the hand state was extracted by the described visual recognition
system based on a real video sequence. However, when we turn to modeling the Core Mirror Circuit in
the next section, we will not use this implementation of visual analysis of hand state but instead, tosimplify computation, we will use synthetic output generated by the reach/grasp simulator to emulate
the values that could be extracted with this visual system. Specifically, we use the hand/grasp simulator

42

to produce both (i) the visual appearance of such a movement for our inspection (Figure 3.7, left), and(ii) the hand state trajectory associated with the movement (Figure 3.7, right). Especially, for training weneed to generate and process too many grasp actions, which makes it impractical to use the visual
processing system without special hardware as the computational time requirement is too high.
Nevertheless, we need to show the similarity of the data from the visual system and the simulator: We
have already shown that the grasp simulator generates aperture and velocity profiles that are similar to
those in real grasps. Of course, there is still the question of how well the our visual system can extract
these features and more importantly how similar are the other components of the hand state that we did
not specifically craft to match the real data. Positive evidence will be presented in Section 3.5.3.

3.4.3

Grand Schema 3: core mirror circuit

As diagrammed in Figure 3.6(b), our detailed analysis of the core mirror circuit does not require
simulation of the visual analysis of hand state and of reach and grasp so long as we ensure that it
receives the appropriate inputs. Thus, we supply the object affordance and grasp command directly tothe network at each trial. (Actually, we conduct experiments to compare performance with and without
an explicit input which codes object affordance.) For the hand state input, rather than providing visual
input to the visual analysis of hand state schema and have it compute the hand state input to the coremirror circuit, we use our reach and grasp simulator to simulate the performance of the observed primate– and from this simulation we extract (as in Figure 3.7) both a graphical display of the arm and hand
movement that would be seen by the observing monkey, as well as the hand state trajectory that would
be generated in its brain. We thus use the time-varying hand state trajectory generated in this way toprovide the input to the model of the core mirror circuit of the observing monkey without having tosimultaneously model its visual analysis of hand State. Thus, we have implemented the core mirror
circuit in terms of neural networks using as input the synthetic data on hand state that we gather fromour reach and grasp simulator (however see Section 3.5.3 for a simulation with real data extracted byour visual system). Figure 3.13 shows an example of the recognition process together with the type of
information supplied by the simulator.

3.4.3.1

Neural network details

In our implementation, we used a feed-forward neural network with one hidden layer. In contrast
to the previous sections, we can here identify the parts of the neural network as Figure 3.5 schemas in a
one-to-one fashion. The hidden layer of the model neural network corresponds to the object affordancehand state association schema, while the output layer of the network corresponds to the action recognition
schema (i.e., we identify the output neurons with the F5 mirror neurons). In the following formulation
MR (mirror response) represents the output of the action recognition schema, MP (motor program)denotes the target of the network (copy of the output of motor program (grasp) schema). X denotes the
input vector applied to the network, which is the transformed Hand State (and the object affordance).
The transformation applied is described in the next subsection. The learning algorithm used is backpropagation (Rumelhart et al. 1986) with momentum term. The formulation is adapted from (Hertz etal. 1991).

43

Activity propagation (forward pass)MRi = g  ∑ Wij g  ∑ w jk X k  
 k

 j
Learning weights from input to hidden layer

Wij = Wij + η (t )δWij + µWijold , where






 j

 k



δWij = g ′ ∑Wij g  ∑ w jk X k  (MPi − MRi )Wold = W
Learning weights from hidden to output layer

w jk = w jk + η (t )δw jk + µwold
jk , where




 k



δw jk = g ′ ∑ w jk X k  X kwold
jk = w jk
The squashing function g we used was g ( x ) = 1 /(1 + e−x) . η and µ are the learning rate and themomentum coefficient respectively. In our simulations, we adapted η during training such that if theoutput error was consistently decreasing then we increased η . Otherwise, we decreased η . We kept µ

as a constant set to 0.9. W is the 3x(6+1) matrix of real numbers representing the hidden-to–output
weights. w is the 6x(210+1) (6x(220+1) in the explicit affordance coding case) matrix of real numbers
representing the input to hidden weights, and X is the 210+1 (220+1 in explicit affordance coding case)component input vector representing the hand state (trajectory) information. (The extra +1 comes fromthe fact that the formulation we used hides the bias term required for computing the output of a unit in
the incoming signals as a fixed input clamped to 1)

3.4.3.2

Temporal to spatial transformation

The input to the network was formed in a way to allow encoding of temporal information without
the use of a dynamic neural network, and solved the scaling problem. The input at any time represented
the entire input from the start of the action until the present time t. To form the input vector, each of theseven components of the hand state trajectory to time t is fitted by a cubic spline (see Kincaid andCheney 1991 for a formulation), and the splines are then sampled at 30 uniformly spaced intervals. The
hand state input is then a vector with 210 components: 30 samples from the time-scaled spline fitted tothe 7 components of the hand-state time series. Note then that no matter what fraction t is of the total
time T of the entire trajectory, the input to the network at time t comprises 30 samples of the hand-state
uniformly distributed over the interval [0, t]. Thus the sampling is less densely distributed across the
trajectory-to-date as t increases from 0 to T.
An alternative approach would be to use an SRN (simple recurrent neural network) stylearchitecture to recognize hand state trajectories. However, this raises an extra quantization orsegmentation step to convert the continuous hand state trajectories to discrete states. With ourapproach, we avoid this extra step because the quantization is implicitly handled by the learning
process.

44

Normalized aperture

1.0

Action seen so far

0.0

0.0

0.66
Normalized time

1.0

Figure 3.11 The scaling of an incomplete input to form the full spatial representation of the hand state As an
example, only one component of the hand state, the aperture is shown. When the 66 percent of the action iscompleted, the pre-processing we apply effectively causes the network to receive the stretched hand state (thedotted curve) as input as a re-representation of the hand state information accessible to that time (represented
by the solid curve; the dashed curve shows the remaining, unobserved part of the hand state)

Figure 3.11 demonstrates the preprocessing we use to transform time varying hand statecomponents into spatial code. In the figure, only a single component (the aperture) is shown as an
example. The curve drawn by the solid line indicates the available information when the 66% of thegrasp action is completed. In reality a digital computer (and thus the simulator) runs in discrete time
steps, so we construct the continuous curve by fitting a cubic spline to the collected samples for thevalue represented (aperture value in this case). Then we resample 30 points from the (solid) curve toform a vector of size 30. In effect, this presents the network with the stretched spline shown by thedotted curve. This method has the desirable property of avoiding the time scaling problem to establish
the equivalence of actions that last longer than shorter ones, as it is the case for a grasp for an object far
from to the hand compared to a grasp to a closer object. By comparing the dotted curve (what the
network sees at t = 0.66) with the ‘solid + dashed’ curve (the overall trajectory of the aperture) we cansee how much the network’s input is distorted. As the action gets closer to its end the discrepancy
between the curves tends to zero. Thus, our preprocessing gives rise to an approximation to the final
representation when a certain portion or more of the input is seen. Figure 3.12 samples the temporal
evolution of the spatial input the network receives.

Normalized aperture

Normalized aperture

Normalized aperture

66% completed

Normalized time

Normalized time

80% completed

50% completed

Normalized time

Normalized time

90% completed

100% completed
Normalized aperture

Normalized aperture

40% completed

Normalized aperture

45

Normalized time

Normalized time

Figure 3.12 The solid curve shows the effective input that the network receives as the action progresses. At eachsimulation cycle the scaled curves are sampled (30 samples each) to form the spatial input for the network.
Towards the end of the action the networks input gets closer to the final hand state

3.4.3.3

Neural network training

The training set was constructed by making the simulator perform various grasps in the followingway.
(1) The objects used were a cube of changing size (a generic size cube scaled by a random scale
factor between 0.5 and 1.5), a disk (approximated as a thin prism), a ball (approximated as adodecahedron) again scaled randomly by a number between 0.75 and 1.5. In this particular trial, we did
not change the disk size. In the training set formation, a certain object always received a certain grasp(unlike the testing case).
(2) The target locations were chosen form the surface patches of a sphere centered on the shoulder
joint. The patch is defined by bounding meridian (longitude) and parallel (latitude) lines. The extent of
the meridian and parallel lines was from -45° to 45°. The step chosen was 15°. Thus the simulator made
7x7 = 49 grasps per object. The unsuccessful grasp attempts were discarded from the training set. For
each successful grasp, two negative examples were added to the training set in the following way. The
inputs (group of 30) for each parameter are randomly shuffled. In this way, the network was forced tolearn the order of activity within a group rather than learning the averages of the inputs (note that the
shuffling does not change mean and variance). The second negative pattern was used to stress that the
distance to target was important. The target location was perturbed and the grasp was repeated (to theoriginal target position).
Finally, our last modification in the backpropagation training algorithm was to introduce a random
input pattern (totally random; no shuffling) on the fly during training and ask the network to produce
zero output for those patterns. This way we not only biased the network to be as silent as possible
during ambiguous input presentation but also gave the network a higher chance to reach global
minima.
It should be emphasized that the network was trained using the complete trajectory of the handstate (analogous to adjusting synapses after the self-grasp is completed). During testing, in contrast, theprefixes of a trajectory were used (analogous to predictive response of mirror neurons while observing a

46

grasp action). The network thus yielded a time-course of activation for the mirror neurons. As weshall see in the Results section, initial prefixes yields little or no mirror neuron activity, and ambiguous
prefixes may yields transient activity of the ‘wrong’ mirror neurons.
We thus need to make two points to highlight the contribution of this study:(1) It is, of course, trivial to train a network to pair complete trajectories with the final grasp type.
What is interesting here is that we can train the system on the basis of final grasp but then observe thewhole time course of mirror neuron activity, yielding predictions for neurophysiological experiments
by highlighting the importance of the timing of mirror neuron activity.
(2) It is commonly understood that the training method used here, namely back-propagation, is notintended to be a model of the cellular learning mechanisms employed in cerebral cortex. This might be amatter of concern were we intending to model the time course of learning, or analyze the effect ofspecific patterns of neural activity or neuromodulation on the learning process. However, our aim hereis quite different: we want to show that the connectivity of mirror neuron circuitry can be establishedthrough training, and that the resultant network can exhibit a range of novel, physiologicallyinteresting, behaviors during the process of action recognition. Thus, the actual choice of training
procedure is purely a matter of computational convenience, and the fact that the method chosen is nonphysiological does not weaken the importance of our predictions concerning the timing of mirror
neuron activity.

3.5

Simulation results

In this study, we experimented with two types of network. The first has only the hand state as the
network input. We call this version the non-explicit affordance coding network since the hand state willoften imply the object affordance in our simple grasp world. The second network we experimented with– the explicit affordance coding network − has affordance coding as one set of its inputs. The number ofhidden layer units in each case was chosen as 6 and there were 3 output units, each one corresponding
to a recognized grasp

3.5.1

Non-explicit affordance coding experiments

We first present results with the MNS model implemented without an explicit object affordance
input to the core mirror circuit. We then study the effects of supplying an explicit object affordance
input.

3.5.1.1

Grasp resolution

In Figure 3.13, we let the (trained) model observe a grasp action. Figure 3.13(a) demonstrates theexecuted grasp by giving the views from three different angles to show the reader the 3D trajectory
traversed. Figure 3.13(b) shows the extracted hand state (left) and the response of the (trained) coremirror network (right). In this example, the network was able to infer the correct grasp without any
ambiguity as a single curve corresponding to the observed grasp reaches a peak and the other twounits’ output are close to zero during the whole action. The horizontal axis for both figures is such thatthe onset of the action and the completion of the grasp are scaled to 0 and 1 respectively. The verticalaxis in the hand state plot represents a normalized (min=0, max=1) value for the components of thehand state whereas the output plot represents the average firing rate of the neurons (no firing = 0,
maximum firing = 1). The plotting scheme that is used in Figure 3.13 will be used in later simulation
results as well.

47

(a)

(b)

d(t)

1.0

Firing rate

Hand statevaluesnormalized
to 0.0 – 1.0
range
o3(t)
o4(t)
a(t)
v(t)
o1(t)
o2(t)
0.0

0.0
Normalized time

1.0

0.0

Normalized time

1.0

Figure 3.13 (a) A single grasp trajectory viewed from three different angles to clearly show its 3D pattern. The
wrist trajectory during the grasp is marked by square traces, with the distance between any two consecutive
trace marks traveled in equal time intervals. (b) Left: The input to the network. Each component of the handstate is labelled. (b) Right: How the network classifies the action as a power grasp: squares: power grasp output;
triangles: precision grasp; circles: side grasp output. Note that the response for precision and side grasp isalmost zero

It is often impossible (even for humans) to classify a grasp at a very early phase of the action. For
example, the initial phases of a power grasp and precision grasp can be very similar. Figure
3.14demonstrates this situation where the model changes its decision during the action and finallyreaches the correct result towards the end of the action. To create this result we used the "outer limit" ofthe precision grasp by having the model perform a precision grasp for a wide object (using the wide
opposition axis). Moreover, the network had not been trained using this object for precision grasp. In
Figure 3.14(b), the curves for power and precision grips cross towards the end of the action, whichshows the change of decision of the network.

48

(a)

(b)

1.0

Firing rate

Precision
grasp

Power
grasp

0.0
0.0

Normalized time

1.0

Figure 3.14 Power and precision grasp resolution. The conventions used are as in the previous figure. (a) The
curves for power and precision cross towards the end of the action showing the change of decision of the
network. (b) The left shows the initial configuration and the right shows the final configuration of the hand

3.5.1.2

Spatial perturbation

We next analyze how the model performs if the observed grasp action does not meet the object.
Since we constructed the training set to stress the importance of distance from hand to object, we
expected that network response would decrease with increased perturbation of target location.

Firing rate

1.0

0.0
0.0

Normalized time

1.0

Firing rate

1.0

0.0
0.0

Normalized time

1.0

Figure 3.15: (Top) Strong precision grip mirror response for a reaching movement with a precisionpinch. (Bottom) Spatial location perturbation experiment. The mirror response is greatly reduced when
the grasp is not directed at a target object. (Only the precision grasp related activity is plotted. The othertwo outputs are negligible.)
Figure 3.15 shows an example of such a case. However, the network's performance was nothomogeneous over the workspace: for some parts of the space the network would yield a strong mirror

49

response even with comparatively large perturbation. This could be due to the small size of the
training set. However, interestingly, the network’s response had some specificity in terms of thedirection of the perturbation. If the object’s perturbation direction were similar to the direction of handmotion then the network would be more likely to disregard the perturbation (since the trajectory prefix
would then approximate a prefix of a valid trajectory) and signal a good grasp. Note that the network
reduces its output rate as the perturbation increases, however the decrease is not linear and after acritical point it sharply drops to zero. The critical perturbation level also depends on the position in
space.

3.5.1.3

Altered kinematics

Normally, the simulator produces bell-shaped velocity profiles along the trajectory of the wrist. In
our next experiment, we tested action recognition by the network for an aberrant trajectory generated
with constant arm joint velocities.

1.0

Firing rate

Firing rate

1.0

0.0
0.0

0.0
Normalized time

1.0

0.0

Normalized time

1.0

Figure 3.16 Altered kinematics experiment. Left: The simulator executes the grasp with bell-shaped velocity
profile. Right: The simulator executes the same grasp with constant velocity. Top row shows the graphicalrepresentation of the grasps and the bottom row shows the corresponding output of the network. (Only theprecision grasp related activity is plotted. The other two outputs are negligible.)

The change in the kinematics does not change the path generated by the wrist. However, thetrajectory (i.e., time course along the path) is changed and the network is capable of detecting thischange (Figure 3.16). The notable point is that the network acquired this property without our explicit
intervention (i.e. the training set did not include any negative samples for altered velocity profiles). Thisis because the input to the network at any time comprises 30 evenly spaced samples of the trajectory up
to that time. Thus, changes in velocity can change the pattern of change exhibited across those 30
samples. The extent of this property is again dependent on spatial location.

50

It must be stressed that all the virtual experiments presented in this section used a single trained
network. No new training samples were added to the training set for any virtual experiment.

3.5.1.4

Grasp and object axes mismatch

The last virtual experiment we present with non-explicit affordance coding explores the model’s
behavior when the object opposition axis does not match the hand opposition axis. This example
emphasizes that the response of the network is affected by the opposition axis of the object being
grasped. Figure 3.17 shows the axis orientation change for the object and the effect of this perturbationon the output of the network. The arm simulator first performed a precision grasp to a thin cylinder.
The mirror neuron model’s response to this action observation is shown in Figure 3.17, leftmost panel.
As can be seen from the plot, the network confidently activated the mirror neuron coding precision
grip. The middle panel shows the output of the network when the object is changed to a flat plate but
the kinematics of the hand is kept the same. The response of the network declined to almost zero in thiscase. This is an extreme example – the objects in Figure 3.17 (rightmost panel) have opposition axes 90°
apart, enabling the network to detect the mismatch between the hand (action) and the object. With lesschange in the new axis the network would give a higher response and, if the opposition axis of theobjects were coincident, the network would respond to both actions (with different levels of confidence
depending on other parameters).

Firing rate

1.0

Firing rate

1.0

0.0
0.0

0.0
Normalized time

1.0

0.0

Normalized time
1.0

Figure 3.17 Grasp and object axes mismatch experiment. Rightmost: the change of the object from cylinder to aplate (an object axis change of 90 degrees). Leftmost: the output of the network before the change (the network
turns on the precision grip mirror neuron). Middle: the output of the network after the object change. (Only theprecision grasp related activity is plotted. The other two outputs are negligible.)

3.5.2

Explicit affordance coding experiments

Now we switch our attention to the explicit affordance coding network. Here we want to see theeffect of object affordance on the model’s behavior. The new model is similar to that given before exceptthat it not only has inputs encoding the current prefix of the hand state trajectory (which includes handobject relations), but also has a constant input encoding the relevant affordance of the object undercurrent scrutiny. Thus, both the training of the network, and the performance of the trained network
will exhibit effects of this additional, affordance, input.
Due to the simple nature of the objects studied here, the affordance coding used in the present
study only encodes the object size. In general, one object will have multiple affordances. The ambiguity
then would be solved using extra cues such as the contextual state of the network. We chose a coarse
coding of object size with 10 units. Each unit has a preferred value; the firing of a unit is determined by
the difference of the preferred value and the value being encoded. The difference is passed through a
non-linear decay function by which the input is limited to the 0 to 1 range (the larger the difference, the51smaller the firing rate). Thus, the explicit affordance coding network has 220 inputs (210 hand state
inputs, plus 10 units coarse coding the size). The number of hidden layer units was again chosen as 6
and there were again 3 output units, each one corresponding to a recognized grasp.
We have seen that the MNS model without explicit affordance input displayed a biasing effect ofobject size in the Grasp Resolution subsection of Section 5.1; the network was biased toward power grasp
while observing a wide precision pinch grasp (the network initially responded with a power grasp
activity even though the action was a precision grasp). The model with full affordance replicates thegrasp resolution behavior seen in Figure 3.12. However, we can now go further and ask how the
temporal behavior of the model with explicit affordance coding reflects the fact that object information
is available throughout the action. Intuitively, one would expect that the object affordance would speed
up the grasp resolution process (which is actually the case, as will be shown in Figure 3.19).
In the following two subsections we look at the effect of affordance information in two cases: (i)where we study the response to precision pinch trajectories appropriate to a range of object sizes; and(ii) where on each trial we use the same time-varying hand state trajectory but modify the object
affordance part of the input. In each case, we are studying the response of a network that has beenpreviously trained on a set of normal hand-state trajectories coupled with the corresponding object
affordance (size) encoding.

3.5.2.1

Temporal effects of explicit affordance coding

To observe the temporal effects of having explicit coding of affordances to the model, we choose a
range of object sizes, and then for each size drive the (previously trained) network with both affordance(object size) information and the hand-state trajectory appropriate for a precision pinch grasp
appropriate to that size of object. For each case we looked at the model’s response. Figure 3.18 shows
the resultant level of mirror responses for 4 cases (tiny, small, medium, big objects). The filled circles
indicate the precision activity while the empty squares indicate the power grasp related activity. Whenthe object to be grasped is small, the model turns on the precision mirror response more quickly andwith no ambiguity (Figure 3.18, top two panels). The vertical bar drawn at time 0.6 shows the temporal
effect of object size (affordance). The curves representing the precision grasps are shifted towards theend (time = 1), as the object size gets bigger. Our interpretation is that the model gained the property ofpredicting that a small object is more likely to be grasped with a precision pinch rather than a power
pinch. Thus the larger the object, the more of the trajectory had to be seen before a confident estimation
could be made that it was indeed leading to a precision pinch. In addition, as we indicated earlier, theexplicit affordance coding network displays the grasp resolution behavior during the observation of a
precision grip being applied to large objects (Figure 3.18, bottom two panels: the graph labeled big
object grasp and to a lesser degree, the graph labeled medium object grasp).

52

Tiny object

Small object

Medium object

Big object

Figure 3.18 The plots show the level of mirror responses of the explicit affordance coding object for an observed
precision pinch for four cases (tiny, small, medium, big objects). The filled circles indicate the precision activity
while the empty squares indicate the power grasp related activity

We also compared the general response time of the non-explicit affordance coding implementation
with the explicit coding implementation. The network with affordance input is faster to respond thanthe previous one.

Firing rate

1.0

0.0

0.0

Normalized time

1.0

Figure 3.19 The solid curve: the precision grasp output, for the non-explicit affordance case, directed to a tiny
object. The dashed curve: the precision grasp output of the model to the explicit affordance case, for the same
objectMoreover, it appears that − when affordance and grasp type are well correlated − having access tothe object affordance from the beginning of the action not only lets the system make better predictions
but also smoothes out the neuron responses. Figure 3.19 summarizes this: it shows the precision

53

response of both the explicit and non-explicit affordance case for a tiny object (dashed and solid
curves respectively).
Tiny object

Small object

Medium object

Big object

Bigger object

Biggest object

Figure 3.20: Empty squares indicate the precision grasp related cell activity, while the filled squares represent
the power grasp related cell activity. The grasps show the effect of changing the object affordance, while
keeping a constant hand state trajectory. In each case, the hand-state trajectory provided to the network is
appropriate to the medium-sized object, but the affordance input to the network encodes the size shown. In thecase of the biggest object affordance, the effect is enough to overwhelm the hand state’s precision bias.

3.5.2.2

Teasing apart the hand state and object affordance components

We now look at the case where the hand state trajectory is incompatible with the affordance of theobserved object. In Figure 3.20, the plot labeled medium object shows the system output for a precision
grasp directed to a medium-sized object whose affordance is supplied to the network. We thenrepeatedly input the hand state trajectory generated for this particular action but in each trial use an
object affordance discordant with the observed trajectory affordance (i.e., using a reduced or increased
size of the object). The plots in Figure 3.20 show the change of the output of the model due to thechange in the affordance. The results shown in these plots tell us two things. First, the recognition
process becomes fuzzier as the object gets bigger because the larger object sizes biases the network
towards the power grasp. In the extreme case the object affordance can even overwhelm the hand stateand switch the network decision to power grasp (Figure 3.20, graph labeled biggest object). Moreover, forlarge objects, the large discrepancy between the observed hand state trajectory and the size of theobjects results in the network converging on a confident assessment for neither grasp.
Secondly, the resolution point (the crossing-point of the precision and power curves) shows aninteresting temporal behavior. It may be intuitive to think that as the object gets smaller the network’s
precision decision gets quicker and quicker (similar to what we have seen in the previous section).
However, although this is the case when the object is changing size from big to small, it is not the casewhen the object size is getting medium to tiny (i.e., the crossing time has a local minimum between thetwo extreme object sizes, as opposed to being at the tiny object extreme). Our interpretation is that the
network learned an implicit parameter related to the absolute value of the difference of the handaperture and the object size such that the maximum firing is achieved when the difference is smallest,that is when the hand trajectory matches best with the object. This will explain why the network has
quickest resolution for a size between the biggest and the smallest sizes.

54
1.00

Time of crossing

0.95

0.90
0.85

0.80

0.75
0.70
0

50

100

150

200

250

300

Object size

Figure 3.21 The graph is drawn to show the decision switch time versus object size. The minimum is not at theboundary, that is, the network will detect a precision pinch quickest with a medium object size. Note that thegraph does not include a point for "Biggest object" since there is no resolution point in this case (see the final
panel of Figure 3.19)

Figure 3.21 shows the time of resolution versus object size in graphical form. We emphasize thatthe model easily executes the grasp recognition task when hand-state trajectory matches object
affordance. We do not include all the results of these control trials, as they are similar to the cases
mentioned in the previous section.

3.5.3

Justifying the visual analysis of hand state schema

Before closing the results of this chapter, we would like to present a simulation run using a realvideo input to justify our claim that hand state can be extracted from real video and used to drive thecore mirror circuit.

Figure 3.22 The precision grasp action used to test our visual system is depicted by superimposed frames (notall the frames are shown)

55
Frame 4

Frame 8

Frame 12

Frame 16

Frame 20

Frame 24

Frame 28

Frame 33

Figure 3.23 The video sequence used to test the visual system is shown together with the 3D hand matching
result (over each frame). Again not all the frames are shown

The object affordances are supplied manually as we did not address object recognition in ourvisual system. However, the rest of the hand state is extracted by the hand recognition system as
described in Section 3.4.3. Figure 3.22 depicts the precision grasp action used as input video for thesimulation.The result of the 3D hand matching is illustrated in Figure 3.23. The color extraction is
performed as described in the Visual Analysis of Hand State section but not shown in the figure. It
would be very rewarding to perform all our MNS simulations using this system. However, the qualityof the video equipment available and the computational power requirements did not allow us to collectmany grasp examples to train the core mirror circuit. Nevertheless, we did test the hand state extracted
by our visual system from this real video sequence on the MNS model that has already been trainedwith the synthetic grasp examples.

56

Firing rate

1.0

0.5

0.0
0.0

Normalized time

0.8

1.0

Figure 3.24 The plot shows the output of the MNS model when driven by the visual recognition system whileobserving the action depicted in Figure 3.22. It must be emphasized that the training was performed using thesynthetic data from the grasp simulator while testing is performed using the hand state extracted by the visualsystem only. Dashed line: Side grasp related activity; Solid line: Precision grasp related activity. Power grasp
activity is not visible as it coincides with the time axis

Figure 3.24 shows the recognition result when the actual visual recognition system provided thehand state based on the real video sequence shown in Figure 3.23. Although the output of the network
did not reach a high level of confidence for any grasp type, we can clearly see that the network favoredthe precision grasp over the side and power grasps. It is also interesting to note a similar competition(this time between side and precision grasp outputs) took place as we saw (Figure 3.14) when the grasp
action was ambiguous.

3.6

Discussion and predictions

3.6.1

The hand state hypothesis

Because the mirror neurons within monkey premotor area F5 fire not only when the monkey
performs a certain class of actions but also when the monkey observes similar actions, it has beenargued that these neurons are crucial for understanding of actions by others. Indeed, we agree with theimportance of this role and indeed have built upon it elsewhere, as we now briefly discuss. Rizzolatti etal. (1996b) used a PET study to show that both grasping observation and object prehension yield highly
significant activation in the rostral part of Broca's area (a significant part of the human language system)
as compared to the control condition of object observation. Moreover, Massimo Matelli (in Rizzolattiand Arbib 1998) demonstrated a homology between monkey area F5 and area 45 in the human brain(Broca's area comprises areas 44 and 45). Such observations led Rizzolatti and Arbib (1998) building on
Rizzolatti et al. (1996a) to formulate:
The Mirror System Hypothesis: Human Broca’s area contains a mirror system for grasping which
is homologous to the F5 mirror system of monkey, and this provides the evolutionary basis forlanguage parity - i.e., for an utterance to mean roughly the same for both speaker and hearer. This adds
a neural “missing link” to the tradition that roots speech in a prior system for communication based on
manual gesture.
Arbib (2001) then refines this hypothesis by showing how evolution might have bridged from anancestral mirror system to a ‘language ready’ brain via increasingly sophisticated mechanisms forimitation of manual gestures as the basis for similar skills in vocalization and the emergence of

57

protospeech. In some sense, then, the present paper can be seen as extending these evolutionary
concerns back in time. Our central aim was to give a computational account of the monkey mirror
system by asking (i) What data must the rest of the brain supply to the mirror system? and (ii) How
could the mirror system learn the right associations between classification of its own movements andthe movement of others? In seeking to ground the answer to (i) in earlier work on the control of hand
movements (Iberall and Arbib 1990) we were led to extend our evolutionary understanding of themirror system by offering:
The hand state hypothesis: The basic functionality of the F5 mirror system is to elaborate theappropriate feedback – what we call the hand state – for opposition-space based control of manual
grasping of an object. Given this functionality, the social role of the F5 mirror system in understanding
the actions of others may be seen as an exaptation gained by generalizing from self-hand to other'shand.
The hand state hypothesis provides a new explanation of the evolution of the ‘social capability’ ofmirror neurons, hypothesizing that these neurons first evolved to augment the ‘canonical’ and ‘pure
motor’ F5 neurons by providing visual feedback on ‘hand state’, relating the shape of the hand to theshape of the object.

3.6.2

Neurophysiological predictions

We introduced the MNS (Mirror Neuron System) model of F5 and related brain regions as anextension of the FARS model of circuitry for visually-guided grasping of objects that links parietal area
AIP with F5 canonical neurons. The MNS model diagrammed in Figure 3.5 includes hypotheses as tohow different brain regions may contribute to the functioning of the mirror system. Chapter 6
undertakes the neural implementation of Grasp Learning (area F4, F2 and F5). This chapter focused on
the Core Mirror Circuit by aggregating the other functionality into three ‘grand schemas’ − visual
analysis of hand state, reach and grasp. Thus we only claim that core mirror circuit is relevant forneurophysiological predictions. We developed the visual analysis of hand state schema to the point ofdemonstrating algorithms powerful enough to take actual video input of a hand (though we simplified
the problem by using colored patches) and produce hand state information. The reach and grasp
schema then represented all the functionality for taking the location and affordance of an object anddetermining the motion of a hand and arm to grasp it (however see Chapter 6 for a detailed neural
implementation of this circuit grounded in neurophysiology and infant behavior). As the main aim of
this chapter was to analyse the core mirror circuit we showed that if we used the reach and grasp
schema to generate an observed arm-hand trajectory (i.e., to represent the reach and grasp generator of
the monkey or human being observed), then that simulation could directly supply the corresponding
hand-state trajectory, and we thus use these data so that we can analyze the core mirror circuit schema(Figure 3.6(b)) in isolation from the visual analysis of hand state. However note that we have also
justified the visual analysis of hand state schema by showing in a simulation that the core mirror circuit
can be driven with the proposed vision system without any synthetic data from the reach and grasp
schema.
Moreover, the hand state input (regardless of being synthetic or real) was presented to the network
in a way to avoid the use of a dynamic neural network. To form the input vector, each of the sevencomponents of the hand state trajectory, up to the present time t, is fitted by a cubic spline. Then thisspline is sampled at 30 uniformly spaced intervals; i.e., no matter what fraction t is of the total time T of
the entire trajectory, the input to the network at time t comprises 30 samples of the hand-state uniformly
distributed over the interval [0, t]. The network is trained using the full trajectory of the hand state in a
specific grasp; the training set pairs each such hand state history as input with the final grasp type as58

output. On the contrary, when testing the model with various grasp observations, the input to the
network was the hand state trajectory that was available up to that instant. This exactly parallels theway the biological system (the monkey) receives visual (object and hand) information: When themonkey performs a grasp, the learning can take place after the observation of the complete (self)
generated visual stimuli. On the other hand, in the observation case the monkey mirror system predicts
the grasp action based on the partial visual stimuli (i.e. before the grasp is completed). The network
thus yields a time-course of activation for the mirror neurons, yielding predictions forneurophysiological experiments by highlighting the importance of the timing of mirror neuron activity.
We saw that initial prefixes will yield little or no mirror neuron activity, and ambiguous prefixes may
yield transient activity of the ‘wrong’ mirror neurons.
Since our aim was to show that the connectivity of mirror neuron circuitry can be establishedthrough training, and that the resultant network can exhibit a range of novel, physiologicallyinteresting, behaviors during the process of action recognition, the actual choice of training procedure ispurely a matter of computational convenience, and the fact that the method chosen, namely backpropagation, is non-physiological does not weaken the importance of our predictions concerning thetiming of mirror neuron activity.
With this we turn to neurophysiological predictions made in our treatment of the Core Mirror
Circuit, namely the ‘grounding assumptions’ concerning the nature of the input patterns received by
the circuit and the actual predictions on the timing of mirror neuron activity yielded by our simulations.
Grounding assumptions: The key to the MNS model is the notion of hand state as encompassing
data required to determine whether the motion and preshape of a moving hand may be extrapolated toculminate in a grasp appropriate to one of the affordances of the observed object. Basically a mirror
neuron must fire if the preshaping of the hand conforms to the grasp type with which the neuron isassociated; and the extrapolation of hand state yields a time at which the hand is grasping the object
along an axis for which that affordance is appropriate. What we emphasize here is not the specificdecomposition of the hand state F(t) into the seven specific components (d(t), v(t), a(t), o1(t), o2(t), o3(t),o4(t)) used in our simulation, but rather that the input neural activity will be a distributed neural code
which carries information about the movement of the hand toward the object, the separation of thevirtual fingertips and the orientation of different components of the hand relative to the opposition axis
in the object. The further claim is that this code will work just as well for measuring how well anothermonkey’s hand is moving to grasp an object as for observing how the monkey’s own hand is moving tograsp the object, allowing self-observation by the monkey to train a system that can be used forobserving the actions of others and recognizing just what those actions are.
We provided experiments to compare the performance of the Core Mirror Circuit with andwithout the availability of explicit affordance information (in this case the size of the object) tostrengthen our claim that it is indeed adaptive for the system to have this additional input available, as
shown in Figure 3.6(b). Note that the "grasp command" input shown in the figure serves here as a
training input, and will, of course, plays no role in the recognition of actions performed by others.
Also we have given a justification of the visual analysis of hand state schema by showing in asimulation that the core mirror circuit can be driven with the visual system we implemented without
requiring the Reach and Grasp simulator provide syntetic data.
Novel Predictions: Experimental work to date tends to emphasize the actions to be correlated withthe activity of each individual mirror neuron, while paying little attention to the temporal dynamics ofmirror neuron response. By contrast, our simulations make explicit predictions on how a given (hand59state trajectory, affordance) pair will drive the time course of mirror neuron activity – with non-trivial
response possibly involving activity of other mirror neurons in addition to those associated with theactual grasp being observed. For example, a grasp with an ambiguous prefix may drive the mirror
neurons in such a way that the system will, in certain circumstances, at first give weight to the wrong
classification, with only the late stages of the trajectory sufficing for the incorrect mirror neuron to bevanquished.
To obtain this prediction we created a scene where the observed action consisted of grasping awide object with precision pinch (thumb and index finger opposing each other). Usually this grasp isapplied to small objects (imagine grasping a pen along its long axis versus grasping it along its thincenter axis). The mirror response we got from our core mirror circuit was interesting. First, the system
recognized (while the action was taking place) the action as power grasp (which is characterized byenclosing the hand over large objects; e.g. grasping an apple) but as the action progressed the model
unit representing precision pinch started to get active and the power grasp activity started to decline.
Eventually the core mirror circuit settled on the precision pinch. This particular prediction is testable
and indeed suggests a whole class of experiments. The monkey has to be presented with unusual or
ambiguous grasp actions that require a ‘grasp resolution’. For example, the experimenter can grasp a
section of banana using precision pinch from its long axis. Then we would expect to see activity frompower grasp related mirror cells followed by a decrease of that activity accompanied by increasing
activity from precision pinch related mirror cells.
The other simulations we made leads to different testable predictions such as the mirror response
in case of a spatial perturbation (showing the monkey a fake grasp where the hand does not really meetthe object) and altered kinematics (perform the grasp with different kinematics than usual). The former
is in particular a justification of the model, since in the mirror neuron literature it has been reported thatthe spatial contact of the hand and the object is usually required for the mirror response (Gallese et al.
1996). On the other hand, the altered kinematics result predicts that an alteration of the kinematics willcause a decrease in the mirror response. We have also noted how a discrepancy between hand state
trajectory and object affordance may block or delay the system from classifying the observed
movement.
In summary, we have conducted a range of simulation experiments – on grasp resolution, spatial
perturbation, altered kinematics, temporal effects of explicit affordance coding, and analysis ofcompatibility of the hand state to object affordance – which demonstrate that the present model is not
only of value in providing an implemented high-level view of the logic of the mirror system, but also
serves to provide interesting predictions ripe for neurophysiological testing, as well as suggesting newquestions to ask when designing experiments on the mirror system.

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4

CHAPTER IV: MULTILAYER SUPERVISED HEBBIANLEARNING AND PROBABILITY CODING

This chapter introduces a learning and data generation model that can be employed in multilayered circuits. The architecture that we develop in this chapter will be used in the Grasp Learning
Models of Chapters 5 and 6. The adaptation of the network weights is performed in a hebbian fashion
based on a reinforcement signal. In the general reinforcement learning framework the learning problem
is formulated as an agent acting in an environment that returns rewards based on the actions of theagent and state of the environment (Sutton and Barto 1998). By acting, the agent can (and usually does)change the state of the environment. The goal of the agent is to maximize its total reward in the longrun, possibly in infinite future (Sutton and Barto 1998). Unlike other optimization based learning
methods, reinforcement learning can be implemented by biological circuits. The supervised Hebbianlearning that we introduce in this chapter is a special case of the general reinforcement learning. We will
use the terms supervised Hebbian and reinforcement learning interchangeably.

4.1

Neural coding

Although there is no agreement on the exact coding neurons employ in the brain we in general
adopt a population coding approach where information is represented in the activities of a group of
neurons. What we mean by the activity of a neuron is the average firing rate. We do not reject otherpossibilities such as interval coding where the timing of the spikes carry information but we adopt
average firing rate. There is large amount of experimental data showing that a populating coding
scheme is employed in the brain (e.g. see Georgopoulos 1986). The term preferred-stimulus is used toindicate the stimulus that causes a neuron to fire maximally. It is observed that neurons would fire forthe stimuli which are not the best, with a decreasing rate as the stimuli diverges from the preferred one.
In most cases, the population code is thought to be encoding a single variable (like the orientation of anedge)(Zemel et al. 1998). However, the population can be involved in encoding more than the value of avariable such as the variance and uncertainty of the variable (Zemel et al. 1998). Indeed there are cases
where the probability distributions of the variables are more adequate than the single values as wheninsufficient information exists to differentiate between two values of the variable (stimuli), or when
multiple values underlie the input (former case, place cells in the hippocampus (O'Keefe andDostrovsky 1971); the latter case directional motion detecting cells in MT (Newsome et al. 1989)).
We adapt the probabilistic interpretation of the population coding (Anderson 1994; Zemel et al.
1998) to represent multiple values or options given the input stimuli. For example, given a sphere shaped
object, what is the most natural representation of a parameter that specifies the direction (e.g. top,
down, right, etc.) from which the animal should grasp the object? The most general answer to thisquestion is to have a representation to encode the parameter with its probability distribution. Indeed, in
this example, the sphere can be grasped in very many ways. We view each layer in a network as
representing the possible choices for the next layer. When the animal needs to act based on the61processed input then it samples over the output to generate the movement7 possibly by a winner-takeall mechanism.
The ‘usual’ way of using a neural network to perform density estimation is much like a function
approximation, where the network is asked to give a single output (the value of the probability density
function) given an input (see Bishop 1995). In the architecture we proposed, a neural structure is used tocompute a normalized histogram in terms of population activity. Besides biological relevance, byrepresenting the distribution as a population code, we gain the power to use the network’s output as
inputs to other networks or layers without an extra decoding step.

4.2

Operation of the proposed network

In the abstract setting, we posit an agent that takes actions and the environment (can include theagent itself) returns rewards or binary signals indicating whether the action was ‘good’ or ‘bad’. Some
information of the environment may be available to the agent as input. We denote the output of theagent with y(t), the input as x(t) and the reward returned by r(t). We are interested in constructing a
network that can be implemented using neural units to achieve: (1) estimation of the probability
distribution of the reward given an input, and (2) generating outputs that return rewards
approximating the probability distribution of the reward.
We will use X(t) to denote the input instead of the x(t) to emphasize that in general the input canbe the output of a different layer.
A layer is composed stochastic units (Hertz et al. 1991). The layer generates an output based on theprobability distribution represented by Y(t), the firing potentials of the stochastic units (described
below). We introduce layers Xe, Ye as memory traces (a rudimentary form of the 'eligibility traces' of
Sutton and Barto 1998) for keeping the memory of activities of layers X and Y, respectively (we will use‘memory trace’ and ‘eligibility’ terms interchangeably in this chapter). The connectivity between layers
X and Y is established through the weight matrix W. The network operates as the following:
1. Input X (t ) is presented

X e (t ) = X (t )3. Ynet (t ) = g (W (t ) X (t ))2.

0, z < 0
 z, z ≥ 0

where g ( z ) = 
4.

Y (t )Y (t ) = N net∑ Ynetk (t )
k =1

5.

For k=1,..,N Y fire (t ) = H (ϕ ) with probability Yk(t), where ϕ non-negative small (<<1) uniformknoise term and H is the step function
6.

 FTA(Y fire ), with Pr(1 − α )where FTA stands for First-Fire Take All process
k* = 
 unif ([1, N ]), with Pr(α )7 Here we don’t exclude the fact that different biasing mechanisms may reshape the final output

62

7.

y (t ) = ∑ P k e−δ ( k , k * )2σ 2, where Pk is the preferred action associated with unit k and σ2 is thekvariance determining the size of the weighted sum range−δ ( k , k * )
2σ e2

8.

Y (t ) = e

9.

Wij (t ) = Wij (t − 1) + ηr (t − 1) X ei (t − 1)Ye j (t − 1) , where η is the learning rate parameterke, for k=1,..,N

The steps 1-2, is standard: the input is propagated via a weight matrix to form the net input. Step 3
applies a threshold operation to eliminate negative net inputs. Step 4 converts the net input into firing
potentials by normalization. The function of steps 5 and 6 is not as apparent. Each stochastic unit fires
with probability that is equal to its firing potential (computed in Step 4). However, the spike generation
timing is variable due to uniform noise (Step 5). Step 6 has two modes of operation. With probability α,a random unit is selected from Y as a winner (k*), and with probability 1-α, a FirstFire-Take-All8 process
is applied on the stochastic units to find real winner (k*).
Let us consider the case where no exploratory moves are performed (α=0), then what is the
distribution of k*? The Steps 5 and 6 generate winner k*s such that E (Y fire | k = k ) = Y (k ) holds for allk*

k9. In essence we implement an approximate universal data generation (see Leydold and Hormann 2000
for a review) method that is open to neural implementation. Step 7 implements a local population
vector computation around the winning unit. The distance metric δ defines how similar the neurons’
preferred values are. This metric imposes a topological relation between the units through the learning
rule. Step 8 creates eligibility traces to register the activated regions for the next cycles weight update.
Step 9 updates the weights in a supervised Hebbian learning fashion (or reinforcement learning update
as in Willams’ (1992) REINFORCE). The weight update rule creates a normalized histogram of the
reward yielding input patterns: Claim: Given input Xm , one of the S distinct input vectors, at time stepp, Y(k) approximates the probability distribution of the reward. Proof: We are given the distinct input
patterns as (X1, X2, .., Xs). We prove the claim with the following assumptions:
1. Memory trace of Y is concentrated on a single point (let Z(t)=Ye(t) for notional convenience).
2. The rewards returned by the environment are non-negative
3. Number of the training inputs is far larger than the number of distinct input patterns (p>>S)
4. α=1Given a randomly initialized network, When we apply the inputs X0, X1, X2 …, Xp-1 according to thelayer update equations (1-9) above we get: (the subscripts denote the time step while the superscripts
denote the pattern number.)

8 FTA is proposed for spiking neurons analogously to winner take all. Given a set of neurons, and a time interval

FTA will return the one which fires first in the given interval. FTA can be implemented using lateral inhibition in
biological networks
9 Given large number of action generations (p) and large number of output units (S), the expected value of thenumber of firings of unit k is p*Y(k). At each cycle, the selection of the winner is uniformly distributed (Step 5) overthe population of units that are firing. By the law of large numbers the expected number of units that fire can beapproximated with Gaussian distribution with some mean (µ) and variance (σ2). Thus the expected number of aunit will fire and become winner can be approximated as p*Y(k)/µ. Thus the normalized histogram of the winners(k*) over a large data generation will approximate Y.

63

Ynet (1) = g (W0 X 1 )Ynet (2) = g ((W0 + ηr1 Z 1 X 1T ) X 2 )Ynet (3) = g ((W0 + ηr1 Z 1 X 1 + ηr2 Z 2 X T2 ) X 3 )T

LYnet ( p ) = g ((W0 + ηr1 Z 1 X 1T + ηr2 Z 2 X T2 + K + ηrp −1 Z p −1 X Tp −1 ) X p )Noting that the argument of g is nonnegative and the initial weights’ (W0) contribution can bemade arbitrarily small we can write:

Ynet ( p ) = W0 X p + ηr1Z1 X 1T X p + ηr2 Z 2 X 2T X p + K + ηrp−1Z p−1 X Tp−1 X p
If the input patterns that generate the rewards are approximately mutually orthogonal then we canwrite:

Ynet ( p ) ≈ η X ps

2

∑

Z∈V

r s Z s where s is from 1,..,S (s indexes the distinct input patterns)

Here, V is the set of Z’s that appear with Xs in the expression for Ynet(p). Therefore Ynet(p) is thetotal reward for each Z in V. If the reward returns are binary, then Ynet(p) becomes (unnormalized)
histogram of the occurrence of rewards. Thus, step 4 generates the normalized histogram.
In simulations, we observed that mild violation of the assumptions used in the proof does deformthe final representation in Y. However, the value of α requires some comment. This parameter controls
how much the layer is exploring as opposed to exploiting the current probability distribution. The
learning rate, η, should be reduced as the layer starts exploiting more. When η and α are chosen
constant non-zero values, in the limit, the layer degenerates into a winner-take-all circuit. To see thisobserve that in the expression of Ynet(p) each presentation of input is accompanied by a Z value which is
the indicator of the unit (and its neighborhood) that determined the action.

Ynet ( p ) = W0 X p + ηr1Z1 X 1T X p + ηr2 Z 2 X 2T X p + K + ηrp−1Z p−1 X Tp−1 X p
When α=0, Z does not depend on the current state of the layer. If α>0 then the action generation
will pick actions from a neighborhood of the actions that returned reward (with probability α). That is
the terms of Ynet(p) will be biased. Thus, the histogram computed by the layer will be sharper. In
practice, having small α (α<0.2), reflects the reward distribution in the layer and provides enoughexploitation that the learning is faster than trial and error (i.e. α=0 case). The Hebbian update we use in
Step 9 although, biologically realistic, does not limit the weight growth. In practice, either a weightnormalization or use of an adaptive learning rate that tends to zero is required if the weights need to bebounded.
The analysis when the rewards can be negative is similar. A non-zero Ynet(P) can be split into
negative and positive reward terms and written in this form:

Ynet ( p ) ≈ η X ps

2

(∑

Z∈V +

)

r s Z s − ∑Z∈V − r s Z s where V+ is the set of Z’s that appear with Xk forwhich rk>0 and V- is the set of Z’s that appear with Xk for which rk<=0. This simply tells us that given an
input Xs at time step p, the firing potential is represented as the difference of two distributions: thepositive reward distribution and the negative reward distribution. An intuitive example would be thesituation where an action of the agent returns +1 or –1 with equal probability (regardless of state of theenvironment). Then the learning will generate a Ynet distribution where the action is represented as
returning 0 reward.

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4.3

Testing the proposed architecture

We present two example problems to demonstrate that the architecture we proposed can learn togenerate actions that capture the distribution of the reward. In both cases, we take an environment withknown reward distribution and we let the agent interact with the environment with the learning rules
specified in the previous sections. After the training, we check whether, by interacting with theenvironment, the network was able to discover the underlying distribution.
In the next chapter we will use this architecture for multivariate action domains, so we chose a
two-dimensional action space to make sure that the architecture is adequate for the grasp learning tasksof the next chapters.

4.3.1

Deterministic environment

The test problem is defined as the following. The agent acts by generating a vector (x, y) where
each component is from the interval [ –1, 1]. Then the environment returns a deterministic reward of +1
if (x*x+y*y) <0.25 and –1 otherwise (Figure 4.1). We used 400 (20x20 grid) neurons to represent theoutput in the layer. The topology of the layer is reflected through the specification of the distancemetric, δ. We defined the distance metric as the usual Euclidean metric over the 2D action space.

Figure 4.1 The elevated circular region corresponds to the area defined by the equation (x*x+y*y) <0.25. The
environment returns +1 as the reward if the action falls into the circular region, otherwise –1 is returned.

In the learning simulations, the agent generated the actions from its action probability distribution(Y) with 0.5 probability and performed exploratory trials with 0.5 probability10 (i.e. α=0.5). Figure 4.2
shows the evolution of the network outputs (Y) subject to the learning rules specified in the previous
sections. The firing potential (Y) is shown as a grid to allow comparison with the environment
distribution.

10 Depending on the task, as the learning progresses α can be adjusted

65

Figure 4.2 The adaptation of the firing potential of the stochastic units are shown as a series of evolving 3D
maps. (left to right and top to bottom)

Figure 4.2 only confirms that the firing potentials of the output units capture the reward
distribution. We have to test our assertion that the generation of actions by using Steps 5 and 6 of theprevious section approximates the distribution of the environment. Figure 4.3, shows that the actions
generated with the dynamics we proposed in the previous section leads to a histogram thatapproximates the environment’s reward distribution (compare to Figure 4.1).

66

Figure 4.3 The normalized histogram of the actions generated over 60000 samples11. Note that the actions
generated captured the environment’s reward distribution (see Figure 4.1).

4.3.2

Stochastic environment

The environment we defined above was simple: it was deterministic and the set of actions thatwould yield reward was convex. Now we confront the architecture we proposed with a more realistic
case, where the reward distribution is multimodal and the rewards are returned stochastically. Given an
action (x, y) the environment returns a reward of +1 with the probability:p ( x, y ) =

1
2 2πσ

2

∫e

( x −0.5 ) 2 + ( y −0.5 ) 2
2σ2( x + 0.5 ) 2 + ( y + 0.5 ) 2

+e

2σ 2

,

( x , y )∈R

where σ2 = 0.1 and R is the rectangular grid of size 0.05x0.05 where (x,y) falls in.
The distribution is the summation of two Gaussian centered on (0.5, 0.5) and (-0.5,-0.5), hence
double peaked. (Figure 4.4)

Figure 4.4 The stochastic environment’s double peaked reward distribution (see text for the explanation)

11 We arbitrarily generated 60000 actions. The larger the number of samples the better the approximation ofunderlying distribution.

67

Figure 4.5 Some snapshots showing the phases of learning of the layer in the stochastic environment where thereward distribution has two peaks (see Figure 4.4).

The evolution of the layer’s firing potential presented in Figure 4.4 shows differential phases thanthe unimodal deterministic environment. First, the peaks are sorted out as isolated sharp peaks withdifferent heights. Then the potentials settle on equal height peaks capturing the input distribution(Figure 4.4).
Similar to what we did in the deterministic environment case, we generated actions using thetrained layer to test whether the distribution of the generated action matches the input reward
distribution. Figure 4.6 shows the normalized histogram of the actions generated. The main structure of
the environment was captured (compare to Figure 4.4).

68

Figure 4.6. The normalized histogram of 6000012 data points (actions) generated by the trained layer in thestochastic environment depicted in Figure 4.4.

4.3.3

Combining multiple layers

The main aim of introducing the proposed architecture is to combine them for more complex
computations. In a hypothetical problem, layers A and B independently compute some parameters. A
third layer, layer C uses the output of layer A and B to generate the final output of the combined
network. The output of C depends on both A and B. Therefore C has to discovered the action
distribution give the inputs from A and C. The combining layer performs this via a synaptic
multiplication (we drop the time dependency and use matrix notation for clarity). The subscript e isused to denote the eligibility traces as before. The synaptic input channels of C and the corresponding
weights are denoted with CsynA, CsynB; and WsynA, WsynB
Compute the net synaptic inputs:
synA
Cnet
= g (W synA AeT )
synB
Cnet
= g (W synB BeT )0, z < 0
 z, z ≥ 0

where g ( z ) = Compute the normalized synaptic inputs:

C synAC synA = N net∑ CnetsynA,kk =1

C synBC synB = N net∑ CnetsynB,k
k =1

Combine the normalized synaptic inputs13:

12 We arbitrarily generated 60000 actions. The larger the number of samples the better the approximation of theunderlying distribution.
13 The * operator performs component-wise multiplication.

69
synA

synB

C *C
C= N
∑ CksynA * CksynB
k =1

The action generation from layer C, is the same is in the single layer case (Steps 5-8). The synaptic
weight update is based on the eligibility of layers. The parameter λ denotes the learning rate for thesynaptic connections.
synA
synA
Wnew
= Wnew+ λrCe AeT
synB
synB
Wnew
= Wnew+ λrCe BeT,sChapters 5 and 6 will present the learning to grasp models. The architecture described here will be
used as the mechanism of learning and grasp plan generation. We avoid non-biological computationsin the architecture presented here so that we can make realistic prediction with models that use thisarchitecture (Chapter 6). The weight adaptation that is offered in this chapter is based on reinforcement
signal and thus biologically plausible. The parameters are represented as local population vectors andhence are open to neurophysiological predictions.
The layer structure we proposed, in essence, computes a histogram of the input patterns that yieldrewards. The action that brings reward causes a weight strengthening between the eligibility trace of
the unit coding the input stimuli and the eligibility trace of the neuron coding the action. The output
trace left is broader than the input (Step 8). This way the weight strengthening not only increases the
chance of the neuron that coded the rewarding output to become active next time but also it increases
the chance of neighboring output units becoming active as well.

4.4

Summary

We introduced a neural network architecture composed of stochastic units with the following
working principle. Each stochastic unit receives a net input that is the value after the input vector ispassed through a linear transformation (weight multiplication) followed by a threshold operation. Thenthe units belonging to the same layer are normalized so that their activity sums up to 1. The normalized
value of each unit is called the units firing potential. Then each unit fires stochastically according to its
firing potential. However, the firing timing is variable and the unit which fires first (in a given a cycle
period) suppress its peers (becomes the winner). The value output from the layer is computed as a local
population vector summation. The memory traces of which unit fired is kept for the next cycle when the
reward signal would be available for updating the weights. If the output generated returned positive
reward then the connections that contributed to the firing are enhanced; if the output was a negative
reinforcement then the weight that contributed to the output generation are reduced.
This simple reinforcement learning based layer is able to represent the probability distribution of
reward conditioned on the input. A very intuitive way to look at the network is to notice that each unit
is like a counter, counting how many times it is involved in positive-reward situations. The negative
weights, the threshold operation and variable reward (i.e. non binary) makes the mathematical analysis
nontrivial. Nevertheless, we presented some proofs with certain assumptions and showed thearchitecture works as we described.
The network is based on biologically realistic computations. Reinforcement learning, population
coding, lateral inhibition/shunting (for FTA) and stochastic spike generation (based on the firing
potential) are biologically feasible computations. This will enable us to use the architecture in Grasp
Learning Model (LGM) of Chapter 6.

70

In next chapters we will combine layers, each of which is a network of the type we presented
here to develop more complex networks. In Chapter 5 we use the multilayer network for infant grasp
learning (ILGM). Chapter 6 instantiates the Chapter 5’s multilayer grasp learning model as a network ofbrain regions with respect to monkey neurophysiology and neuroanatomy, which enables us to performneural level analyzes yielding to neurophysiological predictions.

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5

CHAPTER V: INFANT GRASP LEARNING

This chapter presents a computational model of infant grasp learning constrained by infant motor
development studies. Key elements of the infancy period, namely elemental motor schemas, theexplorative nature of infant motor interaction and inherent motor variability are captured in the model
to produce testable predictions and explain how an existing behavior (reaching) yields a more complex
behavior (grasping) through exploratory learning.

5.1

Motivation

Many research fields focus on discovering the principles of limb movement control. Neuralnetwork researchers address problems of internal representation, learning and execution; Roboticists
solve the problems of kinematics and dynamics (Arbib and Hoff 1994) and Computational
neuroscientists try to understand principles how the biological systems manage motor control. From acomputational point of view, once the fingers to use and/or the wrist position, and the targets of thefingers on the object, are specified kinematics of grasping can be formulated using inverse kinematics
methods (Sciavicco and Siciliano 2000). Inverse kinematics methods are based on reducing various
kinematics error functions (readers are referred to Arbib and Hoff (1994) for a review of models of reachto grasp).
Although it has been suggested that human grasping involves separate control of digits so as tobring the fingers to their targets as in inverse kinematics methods (Smeets and Brenner 2001; Smeets
and Brenner 1999), the general view is that hand transport and finger movements are controlled
separately (see Jeannerod et al. 1998). We used the former approach when we studied the Mirror
Neuron System Model (MNS) for generating grasp actions to provide visual input stimuli for the MNSmodel (Chapter 3). However, we will take a very different approach for infant grasp learning.
From the viewpoint of an infant, what does ‘error’ mean? How is the finger-to-target assignment
made? These are the questions that motivate our modeling study of infant grasp learning. This Chapter
is built on the notion that infants initially neither have a concept of minimizing ‘error’ nor know how tomatch their hands to objects for grasping; however, they do sense the effects of their motor acts whichenables them to adjust their behaviors.

5.2

Infant reach and grasp

A child learns its own possibilities of action in the environment (affordances) through exploratory
behavior (Jeannerod et al. 1998). By 2-3 months, infants start exploring their bodies as they move in theenvironment, they babble and touch their own body. They are actively involved in investigating theintermodal redundancies, temporal and spatial relations of their self-perception (Smeets and Brenner2001). As new skills are acquired, new action domains are opened for the infant. Infants progress from acrude ability of reaching at birth to finer reaching and further grasping ability around four months ofage. Infants learn to overcome problems associated with reaching and grasping by interactive searching(Berthier et al. 1996; von Hofsten 1993). The precision grasp appears around 12-18 months of age(Berthier et al. 1999).

72

To grasp successfully infants have to learn how to control their arms and, further, to match theabilities of their limbs with affordances presented by the environment (Bernstein 1967; Gibson 1969;
Gibson 1988; Thelen 2000). Our study focuses on the latter problem; that is discovering how to generate
grasps that match the affordances presented by the objects in the environment. Rochat and Morgan(1995) have shown that infants are aware of visual, proprioceptive and haptic consequences of theirlimb movements.
The onset of reaching and grasping marks a significant achievement in infants’ functional
interactions with their surroundings. The advent of voluntary grasping of objects is preceded by several
weeks in which the infant engages in arm movements and fisted swipes in the presence of visible
objects (von Hofsten 1984). The term visually guided reaching generally refers to the infants having
available continuous vision of the hand and target, whereas visually elicited reaching refers to the visionof the target, followed by a ballistic hand movement. Clifton et al. (1993) questioned the hypothesis thatthe earliest accurate reaching behavior is visually guided and appears around 3-5 months (Clifton et al.
1993). They tested seven infants repeatedly between 6 and 25 weeks of age using glowing objects in thelight condition and sounding objects for the dark condition. Infants first contacted the object in bothdark and light conditions at almost the same ages (mean ages: 12.3 weeks for light, 11.9 weeks for dark
condition). Infants first grasped the object in light condition at 16.0 weeks and in the dark at 14.7 weeks.
Even though this was not a statistically significant difference, there is other evidence that the self-visionof the hand may retard successful grasp in infants younger than 5 months of age. This could be due tothe attentional load that is brought by the existence of two objects in the visual field (Streri 1993). Clifton
et al. (1993) argued that since infants could not see their hand or arm in the dark, their early success incontacting the glowing and sounding objects indicated that proprioceptive cues, not sight of the limb,
guided their early reaching. This shows that early reaching (and grasping –evidenced in the followingtext) is performed using an open-loop strategy, because it appears that, the initial localization (glow or
the sound of the object) was enough to perform successful movement planning. Reaching in the lightdeveloped in parallel with reaching in the dark, suggesting that visual guidance of the hand is notnecessary to achieve object contact. It is also noteworthy that infants showed great individual
differences. Onset for touch varied between 7 and 16 weeks, while onset for grasp varied between 11
and 19 weeks. The greatest discrepancy (light versus dark conditions) in onset of reach and grasp was 4
weeks. There were three infants out of seven with this discrepancy. Interestingly for all the three infants
the behavior occurred earlier in the dark.
An infant, once contacted an object, will occasionally try to grasp it (Clifton et al. 1993). The
enclosure reflex disappears around six moths of age and it takes four more weeks of infancy to stabilize
the grasp (Clifton et al. 1993). It is suggested that the fractionated control of finger movements is notpossible since this task requires the cortico-motoneuronal system, which has not fully developed at thisage. (Lantz et al. 1996). Before nine months of age, the infant grasp lacks the anticipation of theorientation and size of the object (Rosenbaum 1991). Infants adjust their grasps after touching theobjects. In contrast, adults adjust their distance between the thumb and the other fingers according to
the size of the object during the hand transport. This holds even though infants younger than ninemonths old are physically able to vary their grip size, for they can spread their fingers farther apart once
they have felt a large object (von Hofsten and Ronnqvist 1988). It appears that in early infancy thefractionated control of fingers is mainly driven by somatosensory feedback.
Butterworth et al. (1997) studied the development of prehension in infants by video recording thegrasping behavior of babies from 6 to 20 months of age using objects of different shapes and different
sizes. The infants were divided into four groups according to their age. The objects used were wooden

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cubes and spheres with sizes of 0.5cm, 1cm, 2cm and 3cm. Butterworth et al. (1997) classified the grips
used in the grasps according to two broad categories of power and precision grips. The power grip had
subdivisions of ulnar grasp, hand grasp, palm grasp and radial palm grasp while the precision grip had
subdivisions of scissor grasp, inferior forefinger grasp, inferior pincer grasp and pincer grasp (Figure5.1). The main result of this study was that both power and precision grips were observed in infants
older than 6 months of age and there is a developmental trend such that in the early second year theoccurrence of power grips decreased while the occurrence of precision grips increased, and eventuallybecame the dominant mode of prehension. Furthermore, the size rather than shape (cube vs. sphere)
determined the grasp type (Butterworth et al. 1997). The younger infants did not employ a consistentpattern of grasping for small objects whereas the older infants developed preferential grasp patterns forcertain sizes (0.5 cm, pincer grasp; 2 cm, forefinger grasp) (Butterworth et al. 1997).

Power Grips

Precision Grips

Ulnar grasp

Hand grasp

Scissor grasp

Palm grasp

Radial Palm grasp

Inferior pincer grasp

Inferior forefinger grasp

Pincer grasp

Figure 5.1 Infant grip configurations can be divided in two categories: power and precision grips. Infants tend toswitch from power grips to precision grips as they grow (adapted from Butterworth et al. 1997)

Lockman et al. (1984) investigated the development of infants’ prehensile adjustments regarding
the orientation of objects. They compared the performance of groups of 5 and 9 months old infants (8infants in each group). The infants were presented wit a dowel with two orientations, vertical andhorizontal. In the trials, if the infant did not initiate a grasp when the dowel is revealed, theexperimenter attracted the attention of the infant to encourage him/her to grasp the dowel. If the infant
did not grasp but touched the dowel, the trial was terminated and excluded from the analysis. The handorientations were analyzed by recording the orientations at four points in time: 1) at the beginning (withthe first forward movement of the hand); 2) When the hand passed the midpoint between the first point
and the object position; 3) at the time of first contact of the hand with the dowel; 4) and at the end whereat least one digit closed around the dowel. The principal finding was that 9 months old infants oriented
their hands appropriately earlier during the reach to grasp than did 5 months old infants. Furthermore,
the two age groups differed at the last two stages of the grasp (touch and enclosure) whereas the earlier
parts of their reaches were similar.

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In another related study, 102 infants between 4-8 months old were grouped according to theirage and was studied their grasping behavior as a function of object shape and size using seven
combinations of objects (Newell et al. 1989). The main finding of this study is that the youngest age
group (4 months) required the addition of the haptic system for successful grasp whereas the oldest age
group (8 months) mainly relied on information from the visual system to differentiate grip
configuration according to the object properties. They found that there was a remarkable similarity
between the grasp configurations achieved, irrespective of whether they are visually planned or
haptically adjusted.
Butterworth et al. (1997) show that the young infants display a wide variety of grip types that wereconventionally not attributed to 6-8 months old infants (Halverson 1931),which is in agreement with
our simulations. Lockman et al. (1984) used a single object with different orientations in such a way thatthe infant’s inability to plan according to the target can be detected. An inappropriate handconfiguration would cause a big discrepancy between the hand orientation and the object orientation.
Finally, Newell et al. (1989) inform us that the older infants’ visually programmed and younger
infants’ haptically adjusted grasp configurations are very similar. This strongly suggests that the earlier
haptic grasping phase serves as the training stimuli for visual grasp planning circuit in infant brain. We
use the reviewed studies to constrain and design the Learning to Grasp Model, and evaluate its
relevance to infant learning through explicit comparisons.

5.3

Neural maturation versus interactive learning

The corticospinal tract is one of the main neural substrate for independent finger control (Triggs etal. 1998): Firstly, corticospinal projections terminating in the ventral horn innervating hand muscles
predict independent finger use for small objects (Bortoff and Strick 1993). Secondly, lesioning thecorticospinal tract prevents the development of the independent finger movement in infant animals(Lawrence and Hopkins 1976), and impairs independent finger movements. Human patients recoveringfrom corticospinal lesions initially tend to perform synergistic movement of all the fingers as in a power
grip (Denny-Brown 1950; Lassek 1954).
Given these data, it is tempting to theorize that infants’ late grasping development is due to neuralmaturation. This view is embraced by maturational-based theories (Bradley 2000). However correlation
studies are not conclusive for it is not known whether other variables account for the observed behavior(Bradley 2000). In contrast, learning-based theories consider the environment and infants’ interaction
with it as the main factor in shaping infant behavior (Bradley 2000) . The model, we propose interacts
with its environment (plans and executes grasp actions) and observes the consequences of its actions(grasp feedback) and modify its internal parameters (corresponding to neural connections) such thatcertain patterns (grasp plans) are selected and refined amongst many other possibilities. Thus, in thissense, our model conforms the learning-based views of motor development.
Infants lack the ability to fully utilize their vision for grasping during the period of early grasping(Newell et al. 1989; Rosenbaum 1991). Nevertheless, infants, as reviewed in the previous section, cangrasp objects and even adjusts their grasp actions according to object’s visual properties. Thus, we
propose that infant grasp learning is mediated by neural circuits specialized for grasp planning, which
can function with limited visual analysis of the object, probably position and rough size. The macaquemonkey was shown to have a specialized circuit for grasping in which parietal areas extract object
affordances (information relevant for grasping) (Taira et al. 1990) and relay those to premotor cortex.
Then the premotor cortex with various contextual and intention related bias signals performs grasp

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selection/execution task (see Fagg and Arbib 1998 for a modeling study). It is very likely that a similar
circuit exists in human (Jeannerod et al. 1995) which is adapted in infancy to provide skillful grasping in
adulthood.
We present Infant Learning to Grasp Model (ILGM) in two stages. The first stage is the period
when infants are unable to incorporate object affordance into grasp plans while the second phase iswhen infants start incorporating object information into grasps. Although we favored learning-based
theories of motor development, ILGM is compatible with both maturational- and learning-based motor
development schools since in either case, with different reasons though, the affordance information
cannot be used by the grasp learning circuit in early infancy but it becomes available as development
progresses.
In the rest of the chapter, we analyze ILGM via simulation experiments, and present behavioral
responses and make comparisons where experimental data is available. When no data is available, we
produce useful predictions that can be experimentally tested.

5.4

Infant Learning to Grasp Model (ILGM)

With the term learning to grasp we mean to learn how to make motor plans in response to sensory
stimuli such that the open loop execution of a plan leads to a successful grasp. There is strong behavioral
evidence that early grasping is based on open-loop control and does not use visual feedback (Clifton etal. 1993; Clifton et al. 1994; von Hofsten and Ronnqvist 1988; Streri 1993). Chapter 7, studies the visualfeedback control of grasping in a simplified setting
We first describe a generic schema level architecture of Learning to Grasp Model. Later sections
use the general architecture introduced here to conduct simulation experiments. We propose threecomputational layers relevant for grasping: Hand Position, Virtual Finger, Wrist Rotation layers. In
general, the input to our network is the affordance of the target, which can vary from a single quantity
indicating the existence of a graspable object to the full description of the object in terms of its
affordances (e.g. size, orientation, etc.). In later sections when running simulations, we engage layers
according to experimental requirements. For example to simulate early infant grasp learning, we
effectively disable Affordance layer and analyze learning with tactile feedback. The affordances are
represented using population-coding scheme and encoded algorithmically (i.e. no visual processing for
object recognition and feature extraction is done). We use Affordance layer or Input terms
interchangeably to conform the context. The layers we introduced here encode motor parameters that
constitute a minimal set for specifying grasp actions and based on behavioral studies and monkey
neurophysiology. We make use of monkey studies by postulating that monkey and human motor
development follows similar patterns In fact the kinematics of reach to grasp movements of themacaque monkey and human is very similar (Roy et al. 2000) and homologous brain structures are
involved in motor tasks (Jeannerod et al. 1995) .
Adult grasping studies suggests that reach and grasp components of a grasping action is
independently programmed (Jeannerod and Decety 1990). This implies that the position of the fingers(hand configuration) on the object determined first, and then based on the hand configuration wristorientations and arm configuration are determined. However in the infant, reaching component
dominates: infants first learn how to reach and then learn to adjust their hands to match according totheir ballistic reach (Clifton et al. 1993; Clifton et al. 1994; von Hofsten and Ronnqvist 1988; Streri 1993).
Therefore, we suggest that a grasp planning inversion takes place after infants become skillful. The
inversion is required because intended manipulations after a grasping action determines how humans
grasp the objects. If one were planning to grab a tennis ball with the aim of throwing it far, probably a

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power grasp would be preferred. On the other hand, if he/she were going to pass it to a person next tohim, a (tripod) precision grasp would be more appropriate.

5.4.1

Layers of infant learning to grasp model

In accordance to infant development, we propose that infants explore the space around the objects(and occasionally touch them) they interact. Thus, infants’ early reaches can be considered object
centered. Early reaching is variable (see Bradley 2000 for a review); the variability must be reduced forsuccessful grasping. We posit the Hand Position layer as specifying the approach direction; that is theobject centered (allocentric) position of the hand from where it will approach the target.
Given an approach direction, the orientation of the wrist has to be determined. For example, whenapproaching a sphere from the bottom side, a large wrist supination is required while approachingfrom the front a wrist flexion would be required. We posit the Wrist Rotation layer to learn the possible
wrist orientations given the allocentric hand position information relayed from Hand Position Layer.
Wrist Rotation layer also receives projections from the Affordance layer, because in general, different
objects afford different set of approach-direction and wrist-rotation pairs.
The Virtual Fingers layer indicates which finger synergies will be activated given an input. This
layer’s functionality is fully utilized in adult grasping. When infants start learning to grasp, they firstengage all of their fingers in a synergistic way. When infants start to control their digits independently
to match object shape, this layer can be engaged in learning the possible virtual finger activations. In thesimulations that will be presented in this chapter, the Virtual Fingers Layer is always used to specify asynergistic control of the fingers but is included in the ILGM description for completeness. As will beshown, this does not refrain us from reproducing infant behavior and generating testable predictions.

Virtual Finger
Layer
ObjectAffordance(Size, Axis,
Position)

Wrist Rotations
Layer

Motor Cortex

SpinalCord

Parietal Cortex
Hand Position
Layer

Premotor Cortex

Somatosensory
cortexReinforcement Signal

Grasp
Evaluation

Figure 5.2 The structure of the Infant Learning to Grasp Model. The individual layers are trained based on
somatosensory feedback

The layers we proposed are in one-to-one correspondence with Iberall and Arbib’s (1990) schemas
for grasping. The schemas of Preshape, Approach Vector and Orient correspond to the ILGM layers ofVirtual Fingers, Hand Position and Wrist Rotation (Iberall and Arbib 1990).
The layer architecture we introduced in Chapter 3 is instantiated (as a population of neurons) forthe parameters, allocentric hand position, virtual fingers and wrist rotations that determine a grasp
plan. The key features of the architecture introduced in Chapter 4 are that it is capable of representing
multiple choices of actions and it is open to biasing. The model, after learning, will retain a menu of

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grasp actions that can be retrieved based on the affordance. The menu then can be biased to satisfy
task constraints. Figure 2.1 shows schematically the structure of the ILGM. The task division of brain
regions for implementing the schemas left to the next chapter, in which we probe the possible brain
localization of grasp learning based on the monkey neurophysiology. For now, we only give an overall
view of grasping circuit. Parietal areas extract object affordances and relay them to the premotor cortex,
which is the center implicated in grasp programming. In turn, premotor cortex makes a grasp plan andinstructs the spinal cord and motor cortex for execution. The result of the plan is integrated in the firstsomatosensory cortex (SI). Output of somatosensory cortex mediates the adaptation of the grasping
circuit.

5.4.2

Functional description of ILGM layers

Hand Position layer determines where the hand will be with respect to the object during grasping.
Intuitively, this represents the side from which the hand will grasp the object. The frame of reference forthis parameter is allocentric. The coordinate system we choose for this parameter is spherical (see Figure5.3). Our preliminary simulation showed that this choice is advantageous over a rectangular coordinate
system because the spherical representation was less sensitive to errors in radius component while therectangular coordinate system had the same sensitivity for all the components. The encoding used is as
described in Chapter 4: the neural layer represents a probability distribution and the values are read of
by local population vector computation. Given an object, the layer represents the feasible positions forthe hand. Any item from this position ‘menu’ can be selected by external circuits. However, we simulate
the grasping circuit autonomously, by processing the input and generating a grasp program according
to the probability distributions represented in ILGM layers (but see Fagg and Arbib 1998 for prefrontal
biases for grasp selection ).

Figure 5.3 Hand Position layer specifies the approach direction of the hand towards the object. The
representation is allocentric (centred on the object). Geometrically the space around the object can be uniquely
specified with the vector (azimuth, elevation, radius). The Hand Position layer generates the vector by a local
population vector computation. The locus of the local neighbourhood is determined by the probability
distribution represented in the firing potential of Hand Position layer neurons (see Chapter 4, for details)

Virtual Fingers layer specifies the fingers that will be activated, and with what strength. We use
three virtual fingers: thumb, index finger, and the remaining three fingers acting together. The

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processing is parallel to the Hand Position Layer’s flow. However, this does not mean that this layer
has the right to decide the virtual fingers on its own: the virtual fingers that cannot yield grasping are
negatively reinforced and hence do not appear in the learned ILGM.
Wrist Rotation layer funnels all the information about the object (affordance) and the Hand
Position and Virtual Finger layers’ output. Thus, the output of this layer represents the possible wristorientations given the (1) object related input, (2) output of Hand Position layer (3) output of Virtual
Fingers layer in terms of a conditional probability distribution. The parameters generated in this layer
determine the movements of wrist extension-flexion (tilt), wrist supination-pronation (bank) and ulnar
and radial deviation (heading).

5.5

Joy of grasping

Infants are almost preoccupied with manual manipulation. Infants would play with their own
hands; manipulate objects given to their hands, and play with rattles before they can reach to grasp forthem as young as 2 months of age (Bayley 1936). Infants, once contacted the object, occasionally would
try to grasp it (Clifton et al. 1993). We suggest that the tactile stimuli induced neural signals motivate
infants to engage in grasping and holding. However, we do not model the mechanisms of ‘joy ofgrasping’ induced by tactile sensation but instead use a physical substitute to emulate the feedback that
infant would receive when grasping an object
Through ‘joy of grasping’ infants explore and learn actions that lead to grasp-like experiences.
What we call ‘joy of grasping’ can be considered as Sporns and Edelman’s (1993) adaptive value of anaction. Sporns and Edelman’s (1993) postulate three concurrent steps for sensorimotor learning: (1) The
spontaneous movement generation (2) development of the ability to sense the effects of movements,
eventually allowing neural selection to be guided by adaptive value (3) actual selection of movements
based on the adaptive value. Furthermore, it is argued that selection in the nervous system is mediatedmainly via synaptic change (Sporns and Edelman 1993; Sporns et al. 2000) supporting our model’s
relevance to infant learning.
The model we develop in the chapter will show how sensory feedback shapes infant reaches into
grasp actions via explorative learning and produce testable predictions (see Sporns and Edelman 1993
for a simple reach learning architecture based on similar principles).

5.5.1

Mechanical grasp stability

A successful grasp requires that the object stays stable in the hand (must not drop or move)(MacKenzie and Iberall 1994), which is physically defined as the following (Fearing 1986)(1) The net force (Fnet) acting on the object must be zero
M

Fnet = ∑ N i ( Fi • N i ) where Fi denotes the force applied by the fingers at contact i and Ni
1denotes the normal of the surface that is involved in the contact. M denotes number of contact points of
the hand on the object.
(2) The net torque (Tnet) acting on the object must be zeroM

Tnet = ∑ ( Pi − Pc ) × N i ( Fi • N i ) where Pi is the contact position and Pc is the center of the mass of1

the object.
(3) For any force acting on the object, the angle between the directions of the force with the surface
normal must be less than a certain angle φ. This angle is defined through the finger and contact surface
dependent coefficient µ with the relation:

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φ = tan µ−1

The constant µ satisfies the property that if Fn and Ft are the normal and tangential components ofan applied force then there will be no slip ifµFn > Ft
(4) The magnitude of the grasping force should be adaptable to prevent any displacement due toan external force.
Net
TorqueNet
Force

Center of mass

Index finger
Thumb

Figure 5.4:The grasp stability we used in the simulations is illustrated for a hypothetical precision pinch grip
(note that this is a simplified, the actual hand used in the simulations has five fingers)

5.5.2

Implementing the grasp stability

The parameters generated by Virtual Fingers layer determine how much each virtual finger isactivated. By converting these values to forces exerted on the object during contact, ILGM, in theory,can discover the force values that will stabilize the object. However, in our preliminary simulation
studies, we have seen that learning to grasp required excessive grasp trials to discover the force
balance14. As mentioned before we do not intend to model the details of the tactile feedback system ouraim is to compute a value that captures the joy (behavioral reward) of the infant during grasping or aneural signal (neural level reward) that indicates a stable grasp. Therefore, we concentrated on thequestion of whether, given an object, the simulated hand’s contact configuration could afford a stablegrasp. We formulated the problem as a constrained minimization problem with the cost function E.
M
F • NiE ( Fi ) = α Fnet + (1 − α ) Tnet + β ∑ cos −1 ( i)Fi N ii =1

Fi > f min , ∀i = 1..M
The values α and β determine relative contributions of the individual costs terms to the total costfunction, E. The first two terms capture the grasp stability conditions (1) and (2); the last term captures
14 In fact, human hand is endowed with compensatory spinal feedback loops to stabilize grasping in addition to thefeed-forward mechanisms to specify finger forces (see Rothwell 1994; Johansson and Westling 1987a,1987b).

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the grasp stability condition (3) 15 . The value fmin is an arbitrary positive constant to avoid thedegenerate solution (Fi=0).

5.6

Learning approach direction with palm orienting behavior

To test the hypothesis that goal directed reaching could be the basis of infants’ early grasp learning
we mimicked the infants’ elemental hand behaviors: we implemented palm orienting behavior andenclosure reflex in the 3D hand/arm which we developed for Reach and Grasp schema of Chapter 3.
During the neonatal period when an infant reaches towards an object, his/her hand is usually open(von Hofsten 1982). Although this behavior disappears before the second month of age; it resumes
around the third month of postnatal age (see Bradley 2000). It has been suggested that enclosure reflex
constitutes the first stage of grasping (Twitchell 1970; see Streri 1993 for a review). In our model wewanted to test whether reflex based grasps can be factored into grasp plans so that instead of arandomly directed reach (before learning stage), the infant can use the reinforced directions that yieldappropriate contact with the object so that enclosure of the hand yields a stable grasp.
The simulation is set up as the following. The model generates a grasp plan. In this restricted case,the grasp is determined by the (allocentric) hand position parameter which is a triplet describing a pointwith respect to the target. The value is read off from the population activity of the neurons in the Hand
Position layer (see Chapter 4 for details of layer operations). Initially, the value is random since weinitialize the weights to small random values. The Hand Position layer captures the infant’s variable
reaches towards the visual targets. The task of learning is then to narrow down the variability to
account for only appropriate approach directions (for a given object at a certain location).
After a grasp plan (approach direction) is generated, the hand starts executing the reach action
specified by the Hand Position parameter. During the reach, the wrist is rotated so that the palm normal
always points to the target object. From literature, we know that infants (except a one month period)
open their hand while they are reaching for objects (von Hofsten 1982) and orient their palms towards
the them (see Streri 1993 pages 46-47).
As the model generates grasp plans and executes them, it receives rewards from those plans thatyield grasp or close-to-grasp actions. In the implementation, the model receives negative reward forplans not yielding stable grasps. However, when the grasp error, E is small (e.g. the grasp is close tostable) the model receives a positive reward that is proportional to e-E. Thus, an almost-grasp programis encouraged which enables the model to have a higher chance of producing similar plans. This makes
our approach goal directed and different from pure trial and error learning.

5.6.1

Simulation results

Figure 5.5, right panel, illustrates a discovered grasp (i.e. approach direction) by the model. The
model, by interacting with the object, learned that it is possible to grasp the object from the bottom side.
The grasp plan our model generates is defined by a triplet (α,β,r) (α stands for azimuth; β for elevation
and r for radius) as shown in Figure 5.3. If we sum over the radius we can represent the grasp plan as apair and plot it as shown in Figure 5.5, left panel. We can think of this plot as the normalized histogramof (α,β) pairs generated by the model over many trials. The plot tells us that the model prefers grasp
directions from α > 00 (below the object) and β <900 (right and/or front of the object). The position of theobject allowed the arm to grasp the object from bottom and front/right. For example, a trial with anapproach to the object from the top does not yield a stable grasp (the length of the arm limits the

81position of the hand. Those positions that could not be reached do not yield a stable grasp when thehand contacts the object).
p(β,α )
α

3600

α

-900

β

900

α

00

Figure 5.5 The trained model’s Hand Position layer is shown as a 3D plot. One dimension is summed to reducethe 4D map to a 3D map. Intuitively the map says: ‘when the object is above the shoulder and in front grasp itfrom the bottom’

We also tested the model when the object is located at a different place in the workspace.
p(β,α )

3600
-900

β

α
900

00

Figure 5.6: The output of the trained model’s target position layer is shown as a 3D plot. One dimension issummed to reduce the 4D map to a 3D map. The object is on the left side of the (right handed) arm. Intuitively,
the map says ‘when the object is on the left side grasp it from the right side of the object’

This time the object is placed rather low in the workspace on the left side of the (right-handed) arm.
Here we observe that the model discovered that a grasp directed to the right hand side of the object islikely to result in a stable grasp. Figure 5.6 shows the results of this simulation. Figure 5.7 shows the
distribution of the Hand Position layer during training. Initially the probability distribution of approachdirections was set randomly. The distribution gets a regular pattern via learning and the reward
yielding regions gain higher levels of activity.

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β

β

β

α

β

α

α

β

β

α

α

β

α

β

α

α

Figure 5.7 The learning evolution of the distribution of the Hand Position layer is shown as a 3D plot. Note thatthe 1000 neurons shown represent the probability distribution of approach directions. Initially, the layer is nottrained and responds in a random fashion to the given input. As the learning progresses, the neurons gain
specificity for this object location.

5.6.2

Conclusions and predictions

The simulation results showed that goal directed reaching with palm orienting behavior is enoughfor generating power grasps. The model predicts that infants will narrow their reach variability whenpresented with objects that they can interact with. Furthermore, the variability reduction will be more
pronounced for the space where they could grasp objects.

5.7

Is infant palm orienting learned or innate? Learning the wrist orientation

In this section, we deprive the simulator from auto palm-orienting behavior to test whether the
infant palm-orienting behavior can be mediated via learning, rather than being innate. Although there
are accounts that infants usually orient their hands during reaching so to increase the likeliness of acontact between palm and the object (von Hofsten 1982), to our knowledge, there is no account ofinnateness of this behavior. The period we are modeling corresponds to early grasping in development
when the object affordance is not available to the grasping circuit, either because of maturational
shortcomings or because the complexity of learning holds back the motor development (in accordance
to maturational- and learning-based theories of motor development, respectively).
In terms of learning task, ILGM has to discover the distribution of wrist movements (supinationpronation, extension-flexion, ulnar/radial deviation) for multiple approach directions. Presented withthe object, Hand Position layer produces the distribution of possible approach directions. The selection
is relayed to Wrist Rotation layer. Then, Wrist Rotation layer computes the distribution of feasible wrist

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orientations conditioned on the generated hand position. Virtual Finger layer generates synergistic
parameters effectively learning a single parameter to dictate the enclosure speed of the hand as a whole.

5.7.1

Simulation results

The model learned to generate parameters to perform power and precision grasps, and many
variations of the two. The most abundant grip generated was the power grip and its variations.
Precision type grasps were less frequently generated.
In earlier studies, it was thought that infants were unable to demonstrate precision grips during
grasping (Halverson 1931). The newer studies showed that, when infants are tested in properconditions, perform precision grips occasionally (Butterworth et al. 1997; Newell et al. 1989). ILGM
simulation results are in accordance with this finding. The fact that power grasp is inherently easier
manifests itself in both infants and ILGM simulations: As long as the object is brought in contact withthe palm, an enclosure (as in palmar reflex) is likely to produce power grasp. Figure 5.8, shows thegrasping of a cube with a power grasp plan generated by learned ILGM.

Figure 5.8 ILGM planned and performed a power grasp after learning. Note the supination (and to a lesser
extent extension) of the wrist required to grasp the object from the bottom side

The learned precision grasp varieties were mainly involved the engagement of fingers other thanthumb and index finger. Figure 5.9 shows two examples for this. Usually the object is secured between
three or four fingers, thumb opposing the center of remaining fingers. This emergent grasping behavior
is in accordance with the theory of virtual fingers and opposition spaces (Iberall and Arbib 1990) andhuman tripod grasping (Baud-Bovy and Soechting 2001).

Figure 5.9 Two learned precision grips (left: three fingered; right four fingered) are shown. Note that the wrist
configuration for each case. ILGM learned to combine the wrist location with the correct wrist rotations tosecure the object

Figure 5.10 show examples of two finger precision grasps which were less frequently generated
than the three or four fingered precision grasps. These results show that even without object affordance,
precision type grips can emerge from a circuit adapted using supervised Hebbian learning, which canbe employed by infants.

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Figure 5.10 ILGM was able to generate two fingered precision grips. However these were less than the three orfour finger grips

5.7.2

Conclusions and predictions

The result shows that even without object affordance, performing reaches directed towards theobject from various allocentric positions and associating the grasp-yielding wrist orientations withallocentric positions, and a variety of grips, including the precision grip, can be learned predicting theresults of the study of Butterworth et al. (1997). Thus, infant can learn to select the ‘right’ grasp from thegrasp ‘menu’ based on internal motives or environmental constraints. There are two observations thathave to be made: Firstly, the secondary learning mentioned here is easier to master. Infants only have toassociate the object properties (and the context) to the correct configuration that they have alreadyachieved. Secondly, no extrinsic to intrinsic transformation is required because a posture that yields a
successful grasp has already been discovered. In computational terms, supervised learning can takeplace.

5.8

Task constraints shape infant grasping

The normative developmental phases of infant prehension starts with palmar reflex, followed bypower grips; and finally, ends with dexterous finger-thumb opposition precision grips (Halverson 1931;
see Newell et al. 1989 for a review). However, this early view has been challenged by advanced
recording techniques and careful experimental conditions (Newell et al. 1989; Butterworth et al. 1997). If
a variable (e.g. infant grip configuration) is dynamically context specific, the experimental approach
may be too artificial to reveal its effect on motor control (Bradley 2000). For example, the posturalrequirements could have been a factor in masking infant grasp abilities in the earlier infant motor
development studies (Newell et al. 1989; Bradley 2002). Task constraints may be viewed as including
the goal of the task or the rules that constrain the response dynamics (Newell 1986). Some examples oftask constraints are the object properties such as size and shape (Newell et al. 1989). To verify the
hypothesis that infant grasping is shaped by task constraints we designed a simulation experiment witha physical constraint as the following.
In the earlier simulations of ILGM we presented the object without constrains, hanging in space,thus the model could grasp the object from all anatomically possible directions. However, this is not
usually the case for the infant. For example, infants often interact with objects that lay on flat surfaces
such as the floor or table. A small object on a horizontal table is grasped best by opposing index finger
and thumb with an approach from top.

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Figure 5.11 The cube on the table simulation set up. ILGM interacts with the object with the physical constraintthat it has to avoid collision with the table

We simulated the situation by presenting ILGM with a small cube placed on a horizontal plane(Figure 5.11). The plane constituted a physical obstacle for many grasp attempts. Thus, when thesimulated hand/arm collided with the table, a negative reward was returned to ILGM. We let ILGM
interact with the cube on the table and analyzed the acquired grasping behavior.

5.8.1

Simulation results

ILGM with the cube on the table task condition was unable to acquire power grasps (whole handprehension). The grasp attempts of the model that would result in a whole hand prehension resulted innegative rewards as the fingers always collided with the table surface. Thus, the grasp plan parameters
yielding power grasps were not represented in the grasp repertoire after learning.
The approach directions for avoiding the collision were learned perfectly. LGM always attempted
to grasp the cube from top. Figure 5.12 shows typical precision grips executed by ILGM after learning.
The grasp ‘menu’ acquired was composed of grasps with wrist positions above the object. The contact
points on the cube showed variability (see Figure 5.12).

Figure 5.12 ILGM learned a ‘menu’ of precision grips with the common property that the wrist was placed well
above the object. The orientation of the hand and the contact points on the object showed some variability. Two
example precision grips are shown in the figure

Many of the precision grips that were learned involved supportive fingers other than the thumb and theindex finger. However, two finger precision grips were also acquired (see Figure 5.13).

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Figure 5.13. ILGM acquired thumb opposing index finger precision grips

Most of the precision grips learned correspond to inferior forefinger grasp (Figure 5.12) andinferior pincer grasp (Figure 5.13) , according to classification of Butterworth et al. (1997) (see Figure5.1). One of the interesting observations is that ILGM assimilated the object affordances into the grasp‘menu’ it learned. By comparing Figure 5.12 and Figure 5.13, we see that the opposition axes used forgrasping were 90 degrees apart. In both grasps of Figure 5.12, the thumb was placed on the left surfaceof the cube whereas in Figure 5.13, it was placed on the surface that is parallel and closer to thepresumed infant.

5.8.2

Conclusions and predictions

Clearly, it is not possible to grasp a small object with the whole-hand grip without further
manipulating (e.g. dropping or raking) the object or without deforming the hand to a pincher grasp(readers are encouraged to grasp a pellet from a table without using precision grip). Infants, during
early grasping phase (4-6 months of age), certainly contact the surface before they can grasp the objects
as they use tactile senses for grasping (Newell et al. 1989). However, we predict that infants’ ability to
grasp small objects from a hard, flat surface using whole-hand precision would be a rare, if not
impossible, occasion. On the other hand it has been shown that infants are able to use various precision
grips (Newell et al. 1989; Butterworth et al. 1997; Corbetta et al. 2000) which is in full accordance with
our findings. It appears that older infants are more interested in small objects compared to younger
infants. ILGM explains why, as infants grow older, prefer to approach objects from top (Fagard 2000)
with the answer that from-top approach is the most natural way to grasp small objects in a constrained
condition like the one we presented (i.e. small object on the hard flat surface).
The simulation results of cube on the table task (combined with earlier simulation results) havenontrivial consequences. To be precise, ILGM simulation results:• Predict that infant even without object affordance input, that is during the age of earlygrasping, can perform precision grasp• Show that task constrains shape motor development and support the view that development ofprecision grips is mediated by task constraints.
• Show that object affordances could be represented in infants’ grasp repertoire in spite the factthat they are unable to access/extract object affordance information. This result is very
important because it is a proof that tactile learning can train/modulate the visuomotor learning
in infancy. A corollary prediction is that infants learn to extract affordance of the objects they
can grasp.
• Predict (in relation to the preceding item) that object (visual) affordances would be heavily
represented in the motor and sensory areas of human cerebral cortex for objects that wemanipulate often. For example, presented with a drill, carpenter’s neural circuits would extract
more elaborate affordances than a fisherman’s would.

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5.9

Affordance input matters

Until now, we simulated infant grasp learning assuming that vision of the object is not used toadjust grasp plans according to object features. Therefore, we can associate the earlier ILGM infancy
period of two months to six months of age. In this section, we introduce affordance input to ILGM andassociate the model with infancy period of nine months and after.
This section is reserved for simulating the study of Lockman et al. (1984) and compare ILGM
results with their infant data. Lockman et al. (1984) used infants of 5 and 9 months of age and compared
their performance in orientating their hands to a dowel presented in horizontal and vertical position(see 5.2 section for more details). To replicate their experimental condition, we let the affordance of theobject (orientation) to be relayed to ILGM preferentially for 5 and 9 months of age. We presented acylinder to ILGM analogous to a dowel. With the (realistic –see section 5.2) assumption that information
about the axis orientation (i.e. affordance of the object) is not available to the grasp planning circuit
during early infancy (5 months of age) and that it becomes available later in development (9 months ofage), we effectively disabled the orientation encoding16 when simulating the younger infants’ grasp
learning whereas when simulating older infants’ learning we enabled the orientation coding in the
Affordance layer. We refer to the former case as the poor-vision and the latter as the full-vision condition.
We predicted that the infants without affordance input would not be able to factor the object
orientation into their motor plans. To make the experiment a little bit more interesting, we also included
a third, diagonal orientation condition in addition to the existing horizontal and vertical orientation
conditions.
Lockman et al. (1984) used orientation difference between the hand and the dowel as a measure of
how much infants adapted their hand orientations to the target. The experimenters scored thedifference between the hand orientation of infants and the dowel. Lockman et al. (1984) used 0 for fullmatch and 4 for maximal mismatch (i.e. the difference between the orientations of the hand and the
dowel was closer to 90 than 67.5 degrees). Each of the sixteen infants performed eight grasps totaling
128 grasps. The grasp definition used by Lockman et al. (1984) however, was relaxed: a finger wrapping
the dowel would be counted as a grasp. In our simulation, when ILGM was learning we used our grasp
stability measure; when data collecting for the analysis, to be compatible with Lockman et al. (1984), we
included cases where the grasp stability was not achieved.

Figure 5.14 The three cylinder orientations and grasp attempts by the poor vision condition.

Figure 5.14, centre grasp does not satisfy our grasp stability criterion but conforms to the definitionof Lockman et al. (1984).The right two grasps do not satisfy the grasp stability criterion

16 by clamping it to a random value

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5.9.1

Simulation results

Figure 5.14 shows the orientations and the cylinder we used in the simulation. The grasp actions
shown were performed by ILGM in the poor-vision condition. With our grasp stability measure, we
observed that in 10 trials the horizontal cylinder could be grasped six times, The vertical cylinder could
be grasped four times and the diagonal cylinder could not be grasped at all. Using the convention of
Lockman et al. (1984), we saw that the horizontal cylinder could be grasped eight times, the verticalcylinder five times and the diagonal cylinder seven times. The numbers indicate that withoutaffordance input (orientation) the grasp learning was not satisfactory.

5.9.2

Comparison of ILGM with Lockman et al. (1984)

We first compare the averaged data from Lockman et al. (1984) and data from our simulator overmultiple runs (128). We compare the performance of the infants and the simulator for the verticaloriented 17 cylinder (see Figure 5.15, right panel). Figure 5.15, left panel shows average orientation
match score versus reach progression for infants and for the simulation. The diamonds over dashed line
indicates the 5 months old infants’ performance. The 9 months old infants adjusted their hands better
than the younger ones as indicated with diamonds over solid line.
2.5

2.0

1.0

0.0
start

midlinetouch

Figure 5.15 The orientation match of the hand and the cylinder is illustrated. Dashed line with diamonds: 5months old infants; Solid line with diamonds: 9 months old infants; Dashed line with circles: ILGM with noaffordance; Solid line with circles: ILGM with affordance (infant data from Lockman et al. (1984)). Right panel
illustrates the object orientation used for the simulation and for the infants in this comparison

The simulated ILGM data is shown with the same line style, but data points are marked withcircles. Although the absolute scores differ between simulation and infant case, the performance
improved in the full-vision case similar to the performance improvement for 9 months old infants.
Moreover, the performance increment of ILGM and Lockman et al.’s (1984) infants were comparable.

5.9.3

ILGM kinematics analysis (five months of age)

Now we try to infer what the model learned. When we analyzed individual errors made by thesimulator, we observed six typical error curves (Figure 5.16). We grouped the error curves into rows todifferentiate the mode of operation learned. The columns, from left to right, correspond to horizontal
cylinder, diagonal cylinder and vertical cylinder. Note that top-left graph is flat and shows almost zeroerror whereas the other two graphs in the same row show flat curves with higher error.

17 We excluded the horizontal case, because for the horizontal cylinder ILGM learned an underarm grasp that is notobserved in infants. The issue will be discussed later in the text.

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Figure 5.16 The hand orientation and cylinder orientation difference curves for individual trials. The columns
from left to right correspond to horizontal, diagonal and vertical orientations. The upper row flat class of error
curves, lower row non-flat class for error curves (see text for explanation)

Lockman et al. (1984) found that infants start their reaches with horizontal orientation so that theirinitial errors for the horizontal dowel are low. Based on this finding the initial configuration of the hand
was set to a horizontal posture in our simulations. In accordance with Lockman et al. (1984)
observations, ILGM made more corrections for the vertical cylinder case (bottom-right panel in Figure5.16) and less for the horizontal case. From this we can infer that in the upper row trials of Figure 5.16,
ILGM model used a grasp plan appropriate for horizontal orientation. As can be seen from the bottomright panel, the model can occasionally perform a vertical cylinder adaptation too (remember that thearchitecture of ILGM allows representation of multiple grasp plans). However, the model cannot
differentiate the two grasping strategies. Thus, the model learns a strategy to increase its chance tomake successful grasps. Since the initial hand posture is close to horizontal, it is intuitive that thedominant mode of grasp planning becomes the one best suited for horizontal cylinder, as it requires lesscorrection (Lockman et al. 1984). The model replicates this observation as the horizontal cylinder could
be grasped most frequently.

5.9.4

ILGM kinematics analysis (nine months of age)

ILGM in the full-vision condition learns to perform grasps similar to 9 months of age infants. We
present the plots of difference of hand orientation and cylinder orientations in Figure 5.17

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Figure 5.17 The hand orientation and cylinder orientation difference curves while ILGM was executing fourtypes of grasp in the full-vision condition. Left two figures are two typical error curves for the horizontal
cylinder. Note that the two horizontal case error patterns reflect the two possible grasps: from the bottom andfrom the top. The third and fourth are typical error curves for the diagonal and vertical cylinders respectively

The left two panels show the difference in orientations for the horizontal cylinder case. The flat
curve corresponds to the easy grasp that could be observed in poor-vision condition also. The other highcurvature one corresponds to a bottom grasp of the cylinder as shown in the left panel of Figure 5.18. To
our knowledge, there is not report of bottom whole hand grasping during infancy. (Lockman et al.
(1984) also did not observe this kind of grasp). This may be due to the general experimental set up; orthe inability of infants to work against gravity. In our simulation, we did not address the dynamics ofthe arm. Therefore, both grasp actions are equal in their reward value. One could incorporate a penalty
term for energy use in the ILGM reward computation (which evaluates how well the a grasp action hasbeen). This would tilt the balance of grasp choice towards the easy grasp. It would be interesting to findout the developmental course of this particular grasp and the underlying reasons why it does notappear early in development. One explanation could be that gravity helps infants to contact with theobject earlier as infants engages in arm movements and fisted swipes in the presence of visible objects(von Hofsten 1984). Thus, the infant has more experience approaching objects from the top and front.
When approaching from the bottom the gravity works against the infant since the infant has tocounteract gravity to grasp the object. One notable property of this bottom grasp is that it did notappear when we simulated ILGM for replicating 5 months of age infant behaviour; because ILGM had
to find a strategy that will work for three orientations and hence had no exploration potential to
discover alternative grasps. Fagard (2000) found that hand orientation at object contact changed withage. Horizontal orientation (the easy grasp) decreased and vertical ones increased from 5 months old
infants to 12 months old infants18.

18 Orthogonal to this finding, the precise grasping from above became more predominant in infants older than 9months of age.

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Figure 5.18 The grasps performed after ILGM learned the association between the wrist rotations and the object
affordance (orientation)

5.10 Summary and conclusion
This chapter presented the Infant Learning to Grasp Model (ILGM) and presented simulations
yielding nontrivial predictions. We first showed that even having a very limited set of behaviors andvisual input, explorative learning could yield grasping behavior and reduce the variability of grasping
actions. Then we studied the palm orienting behavior and test whether it could be acquired throughinteractive learning. The results of this study showed that object affordance was not a prerequisite forlearning the set of correct wrist orientations. ILGM learned a ‘grasp menu’ including precision grips,
which could be retrieved based on the approach direction.
In our simulations, the side grasp was not discovered. Although infants do not exhibit side grasps(opposition of thumb to side of index finger), we would like to point out the possible reason. The neuralarchitecture we introduced in Chapter 4 is capable of learning any reward yielding grasp plan.
However, the physics modeling of the arm and the objects is not realistic. We did not model contact
forces. Therefore, thumb opposing the side of the finger cannot be counteracted by the side of the finger.
Except for the palm, the forces can only be exerted in the directions determined by joint angles of eachfinger.
It should be emphasized that, the point of our modeling was not to give a realistic rigid dynamics
model of the arm/hand but rather propose a grasping architecture that can learn to program grasps aslong as a correct reward signal is given by the environment. The learning we demonstrated, and thevariety of grasps we could generate met our aim.
During development, infants have to deal with constraints and find ways to act within thelimitations of the environment and the context. We investigated the possibility that task constraints may
play a role in shaping infant’s grasping behavior. We simulated a situation where a small cube wasplaced on a table. The model was asked to interact with this simple environment. The grasping
configurations learned by the model reflected the task constraints. The model could not acquire any
whole hand prehension grasps but acquired grasps that reach the cube from the top avoiding a collision
with the table.
Finally we analyzed what affordance may add to ILGM by simulating the experimental set up of
Lockman et al. (1984). With this simulation we showed not only the improvement in grasp execution(measured as the orientation match between infant’s hand and the target dowel) but also the similarityof the improvement pattern was comparable to Lockman et al.’s (1984) results, which indicates that
ILGM captured the behaviour of 5 and 9 months age infants via differential affordance access.
Combining the summarized simulations we explicitly state that ILGM:• Predicts that infants, even without object affordance input (i.e. during the age of earlygrasping), can perform precision grasp

92•

Shows that task constrains shape motor development and supports the view thatdevelopment of precision grip is mediated by task constraints.
• Shows that object affordances could be represented in infants’ grasp repertoire in spite thefact that infants’ are unable to access/extract object affordance information.
• Predict that the distribution of object (visual) affordance in motor and sensory areas inhuman cerebral cortex would reflect the frequency of their manipulation.
The last two results are very important because it shows that tactile learning can train andmodulate the visuomotor learning during infancy. By projecting this statement back to infants, wepredict that infants learn to extract visual affordances of the objects they interact with.

5.11 Discussion
The simulations with ILGM explored both the early grasping period when infants are unable tofactor object affordance into grasp plans and the period when they start using visual input for grasp
planning. We captured the infancy period by limiting the visual input available to the model.
From a maturational-based theory point of view, ILGM should correlate more with aphylogenetically older grasping circuit with limited access to visual areas. One candidate for such a
circuit is the primary motor cortex that receives object location information from the superior colliculus.
As the cortical control becomes dominant while the infant is growing, motor cortex leaves the graspplanning task to higher cortical areas, probably to premotor cortex, in adulthood.
From viewpoint of learning-based theory motor development, infant and adult grasping circuits
are identical but infants have to sort out the flux of information they receive and organize them into
useable schemas by interactive learning. In contrast to maturational-based theories, learning-based
theories suggest that development of motor abilities is the consequence of learning by trial and error tocontrol motor schemas that are genetically determined in their rudimentary forms (Bradley 2000). Thus,
grasp planning and execution mechanism can manifest itself only after the infant has interacted enoughwith the environment. This is the period required for infant to master his/her sensorimotor skills, whichstarts from birth and continues until the first year of life. The movements of newborns are usuallytreated as unintentional, purposeless or reflexive muscle activities (van der Meer et al. 1995), probably
with a bias from maturational-based theories. However, there exists strong evidence that infants engage
in learning and exploring actively as early as 10 days of age. van der Meer et al. (1995) recorded
spontaneous arm-waving movements of newborns while they were allowed to see only the arm they
were facing, only the opposite arm on a video monitor, or neither arm. The newborns’ hands were
pushed downward in the direction of the toes. When the newborns could see their arms, either directlyor via the video screen, they opposed the forces and moved normally, effectively preferring to havefeedback on their movements. The findings indicate that newborns control their arm movements aslong as they can receive visual feedback even when they have to oppose external forces. This shows thatbabies at a very early age start exploring and collecting data indicating that their visuomotor learning
hardware is functioning soon after birth.

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6

CHAPTER VI: NEUROPHYSIOLOGICAL VIEW OF LEARNING
TO GRASPIn Chapter 5, we presented the schema level model of grasp learning (ILGM) without spelling out
the brain regions that contribute to learning. In this chapter, we constrain ILGM withneurophysiological and neuroanatomical data to pin down the brain regions involved in grasp learning.
Our analysis leads to two alternative hypothesis of primate grasp circuit. We present evidence for bothhypothesis and analyze the one that is best explained by experimental data through simulation. In
particular, we propose the Affordance-based Grasp Learning model (LGM) which meets theneurophysiological and neuroanatomical constraints and functional requirements derived from ILGM.
Thus, ILGM is functionally equivalent to LGM. We will refer the reader to Chapter 5, when the material
to be presented is already introduced there unless it is necessary to have an overlap to keep the Chapter
self-contained.
Our analysis of grasp learning in terms of neurophysiology complements the Mirror Neuron
System model we presented in Chapter 3. The simulation results enable us to explain the mechanism ofgrasp learning in terms of brain circuits and show how adaptation shapes the visuomotortransformation that enables primates to select and execute suitable grasps based on the object
affordances leading to units with properties similar to F5 canonical neurons. Through simulation
experiments, we make explicit predictions, which can be tested experimentally and used for refining
and validating (or invalidating) the model we propose.

6.1

Grasp learning circuit and mirror neurons are complementary networks

One of the basic assumptions of the Mirror Neuron System (MNS) model (Chapter 3) was that selfobservation of grasping was the training stimuli adapting parietal and premotor circuits of MNS model
for action recognition. Using schema methodology (Arbib et al. 1998), the grasp learning and execution
were encapsulated under the Reach and Grasp Schema, which included a set of algorithmic routines
implementing reach and grasp execution based on techniques from robotics. Learning to Grasp Model(LGM) of this chapter serves also, as the biologically realistic schema, substituting the engineered Reach
and Grasp Schema of MNS. Figure 6.1 highlights the relevant regions for grasp learning using theschema level view of MNS that we have presented in Chapter 3.

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Object recognition
IT

Object features

Visual Cortex

c-IPS

Hand shaperecognition& HandmotiondetectionSTS

Objectaffordance
extraction

Area F5AIP
F5non-mirror
Motor Program(Grasp)Object affordance hand state
association
7b

Hand-Object
spatial relation
analysis
7aActionRecognition(MirrorNeurons)

Motor
execution
F1

F5mirror
F4

Motor Program(Reach)Objectlocation
MIP/LIP/VIP

Figure 6.1: The overall MNS model. The grey background rectangle shows the focus of this chapter. In addition
to the areas shown, area F2 will be posited as being involved in grasp planning.

6.2

Introduction to primate grasping

Many possible grasps can be applied to objects and they require many control parameters to be
adjusted based on the object and hand properties. Iberall and Arbib (1990) introduced the theory ofvirtual fingers and opposition space for reducing the complexity of the grasping task. The term virtual
finger is used to describe the physical entity (one or more fingers, the palm of the hand, etc.) that is used
in applying force and thus includes specification of the region to be brought in contact with the object(‘virtual fingertip’). Figure 6.1 shows three types of opposition: those for the precision grasp, powergrasp, and side grasp. Each of the grasp types is defined by specifying two virtual fingers, VF1 and VF2,
and the regions on VF1 and VF2 which are to be brought into contact with the object to grasp it. Notethat the "virtual fingertip" for VF1 in palm opposition is the surface of the palm, while that for VF2 inside opposition is the side of the index finger. The grasp defines two "opposition axes": the opposition
axis in the hand joining the virtual finger regions to be opposed to each other, and the opposition axis in
the object joining the regions where the virtual fingers contact the object. Visual perception provides
affordances (different ways to grasp the object); once an affordance is selected, an appropriate opposition
axis in the object can be determined. The task of motor control is to preshape the hand to form an
opposition axis appropriate to the chosen affordance, and to so move the arm as to transport the handto bring the hand and object axes into alignment.

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Figure 6.2 Left: precision grasp (pad opposition); Middle: Power grasp (palm opposition); Right: Side grasp(side opposition). Each of the 3 grasp types here is defined by specifying two ‘virtual fingers’, VF1 and VF2,
which are groups of fingers or a part of the hand such as the palm which are brought to bear on either side of an
object to grasp it. The specification of the virtual fingers includes specification of the region on each virtual
finger to be brought in contact with the object. A successful grasp involves the alignment of two "opposition
axes": the opposition axis in the hand joining the virtual finger regions to be opposed to each other, and the
opposition axis in the object joining the regions where the virtual fingers contact the object (adapted from Iberall
and Arbib 1990)

From a robotics viewpoint, we can model the grasping process by extending the techniques
available for trajectory planning by formulating the grasp planning as an inverse kinematics problem.
Indeed, we used this approach when we studied the Mirror Neuron System Model to generate grasp
actions for providing visual input stimuli for the MNS model (Chapter 3). However, in this chapter, wetake a learning approach and propose a model that learns to generate successful grasp plans via
exploration and selection. By doing so we aim at satisfying these goals:
1. Shed light on the possible organization of the primate premotor circuit involved in grasp
planning by offering biologically realistic learning rules and structures.
2. Complement our earlier work on the Mirror Neuron System, by substituting theengineered grasp-planning module of Chapter 3 with biologically realistic and selforganized grasp-planning circuit
3. Form a solid basis for hypotheses about Mirror Neuron System development andvisuomotor learning in parietal and premotor circuits, which can be experimentally tested
and further investigated with modeling studies following the structure we propose.

6.3

Neural correlates of infant reach and grasp

The corticospinal tract is one of the main neural substrate for independent finger control (Triggs etal. 1998). Firstly, corticospinal projections terminating in the ventral horn innervating hand muscles
predict independent finger use for small objects (Bortoff and Strick 1993). Secondly, lesioning thecorticospinal tract prevents the development of the independent finger movement in infant animals(Lawrence and Hopkins 1976), and impairs independent finger movements. Human patients recoveringfrom corticospinal lesions initially tend to perform synergistic movement of all the fingers as in a power
grip (Denny-Brown 1950; Lassek 1954). More evidence is presented by Olivier et al. (1997). Hinde andRowell (1964) observed that dexterous grooming was not observed in infant macaques until 6 months ofage. Lawrence and Hopkins (1976) reported that in rhesus monkey, the earliest signs of skillful handuse appear around 2-3 months and stabilizes as a mature pattern at 7-8 months. Galea and Darian-Smith(1995) reported that performance on a reach-and-grasp test (with infant macaques) reached adult levels

96around 6 months. More importantly, this correlated with the emergence of an adult-like distributionof cortical motor areas contributing to the corticospinal tract. Armand et al. (1997) showed that at birth
CM projections from primary motor cortex are very weak or not present. It is not very clear how muchinformation these weak projections may carry at an early age. However Flament et al. (1992) reported
that the earliest EMG responses to transmagnetic stimulation as in the adult could not be obtained
before 2-3 months of age.
The division of function between premotor and motor cortex projecting to corticospinal tract is notwell studied. The primary motor cortex has circuitry to facilitate grasping once a proper contact withthe object is established (Rothwell 1994). Certain primary motor cortex neurons that control the finger
muscles have cutaneous receptive fields on the skin that likely encounter obstacles and may be
stimulated when a movement is caused by the neurons’ activity (Rothwell 1994). Similarly, the joint
receptors, tendon organs and muscle spindles have afferent organization such that if the
microstimulation of a certain primary motor cortex patch produces a movement in one direction thenthe passive movement of the same joint in the opposite direction is likely to excite that area of the cortex(Rothwell 1994). This means that, at least for spindles, if a muscle is passively stretched, the afferents ofthe spindles will activate primary motor cortex neurons, which would in turn produce contraction of
the same muscle (Rothwell 1994). Thus, the intrinsic wiring of the primary motor cortex can enablegrasping and holding of the object once it is touched. Fogassi et al. (2001) showed with reversible
inactivation studies that the (precise) grasping behavior is compromised when a muscimol injection wasmade to a certain part of area F5. Area F5 is divided into two main sectors based on cytoarchitectonics(Rizzolatti et al. 1988): the F5 sector lying on the cortical convexity (F5 convexity) and the part buried in
the arcuate sulcus (F5 bank). Both sectors have neurons that respond to visual stimuli. The visualneurons of F5 bank respond to the presentation of three-dimensional objects, usually, in a congruent
way with their motor responses in terms of grip type and size (Rizzolatti et al. 1988; Murata et al.
1997b). The visual neurons in F5 convexity fire when the monkey observes an individual performing
certain actions involving object interaction (Gallese et al. 1996; Rizzolatti et al. 1996a). The former
neurons are named ‘canonical neurons’, whereas the latter ones are named ‘mirror neurons’. Although
the muscimol injection to the region of F5 mirror neurons did not impair grasping behavior (only aslowing down was observed), an injection made to F5 bank impaired (precise) grasping (Rizzolatti et al.
1996a). The hand was not adjusted according to the object size and shape. Nevertheless, the monkeys
could perform the grasp after they touched the object. Interestingly, the grasp for large objects appearedalmost unaffected (Murata et al. 1997b). In one of the monkeys tested, the use of the contralateral hand
was largely impaired with F5 bank injection. This monkey often refused to make reaching-to-grasp
movements toward small objects and, when it made them, grasping was clumsy and the hand shape
was inappropriate for the object size and shape. A large sphere and a large cylinder, however, were
grasped almost normally (Fogassi et al. 2001). The other monkey had similar deficits but to a lesser
extent. In both monkeys, the ipsilateral hand performance was also compromised (when the muscimol
injection was strong). It is important to note that, finger dexterity was not abolished when F5 bank wasinactivated because after contact with the object the grasps could be completed. This is very similar tothe description of grasp performance during early grasping phase of human infancy (von Hofsten andRonnqvist 1988). Fogassi et al. (2001) also injected muscimol in the hand region of motor cortex (F1). The
result was a strong impairment in the capacity of the grasping of the hand contralateral to the injection
site. Unlike F5 injection, the ipsilateral hand was not impaired (Fogassi et al. 2001). Both monkeys with
F1 injection, could reach the tray that holds the object, but with a stereotypical flat hand configuration
after which they retrieved (i.e. used their hands like a rake) rather than grasped the objects. The hand

97

section of area F1 receives rich projections from area F5 (Matelli 1986). We can argue that F5
modulates F1 hand related neurons so as to engage them in a precision grasp in the following way. We
know that neither area F1 nor area F5 alone is enough to perform a precision grip (Fogassi et al. 2001)
and area F5 neurons become preferentially active when the animal performs grasping actions withvarying degrees of grip specificity (Rizzolatti et al. 1988; Murata et al. 1997b; Rizzolatti et al. 2000). Thus,
we suggest that area F1 needs to be modulated by area F5 in order to carry on the dexterous grasp
actions. This proposal is also supported by human imaging studies. Ehrsson et al. (2000) showed, using
fMRI, that when the human subjects performed power grasp, the primary motor cortex of thecontralateral hemisphere showed increased activity whereas when the subjects performed precision
grasp both hemispheres were activated. Importantly, the dominant activity was observed in the(ipsilateral) ventral premotor cortex, which is the homologue of monkey F5 (Gallese et al. 1996;
Rizzolatti and Arbib 1998). Ehrsson et al. (2000) suggested that the control of fingertip actions with a
precision grasp is mediated with neural circuits that are different than the circuits involved in powergrasp, which are phylogenetically older. Further support for this proposal comes from the studies ofMuir and Lemon (1983). Some primary motor cortex cells that project to motoneurons that mobilize
hand muscles are active during precision grasp execution but not for a power grasp execution, albeit thesame muscles can be mobilized in both grasps. This indicates that there exists a skilled grasping circuit,which uses some part of primary cortex for its exclusive function. Then, how much visual information isavailable to phylogenetically older (primary motor cortex) grasping circuit and how well can it learn
sensory motor associations (as opposed to the fixed motor plans)? Shen and Alexander (1997a) showedthat the neurons in motor cortex participate in sensory and/or associative (context-dependent)
processing of spatial information relevant to visually guided reaching movements. They have foundmany neurons in motor cortex that showed behavior-correlated discharge that depended on thevisuospatial target of the monkey’s instructed reach, irrespective of the limb trajectory used (asexpected, there were also a substantial proportion of neurons with limb-dependent activity as well).
This means that the primary motor cortex neurons indeed can encode motor plans based on visual cuesthat are not tied to certain muscle groups.

6.4

Primate grasp development hypotheses

We now present two alternative hypotheses of primate grasp development that will guide us inlocating the specific brain areas involved in grasp learning in the following sections.

6.4.1

Hypothesis I: two coexistent grasping circuits

The first hypothesis is that the early power-like grasp is mainly controlled by area F1 and F4 (forthe reach component), and involvement of area F5 is not substantial. The review in the previous section
suggests the existence of a phylogenetically older lower level grasp circuit that does not requirepremotor regions and can work with limited visual analysis of the object, probably position and roughsize. The power grasp appears early in development but it takes longer to mature a precision type ofgrip (Lockman et al. 1984; Fagard 2000). In addition, infants lack the ability to fully utilize vision forgrasping before the precision grip becomes part of their grasp repertoire (Rosenbaum 1991). Ehrsson etal. (2000) suggested that the control of fingertip actions with a precision grasp is mediated with different
neural circuits than the phylogenetically older circuits for power grasp.
Hypothesis I explains the emergence of skillful finger use as the following. The visual control ofdexterous finger use (e.g. precision grip) is learned by area F5 by associating the performance of thelower level grasp circuit with the visual analysis of the object performed by parietal cortex (AIP). Area
F5 modulates grasp selection and the activity in the lower level grasp circuit. The modulation and98

selection are based on the high level goals of the individual (prefrontal influences based on context),
affordances extracted by parietal cortex, the lower level grasp plans and the actual grasping
performance (success or failure).

6.4.2

Hypothesis II: single grasping circuit
V6A

Object recognition
IT

Object features

Visual Cortex

c-IPS

Hand shaperecognition& HandmotiondetectionSTS

Objectaffordance
extraction

Motor Program(Grasp)F2

AIP
F5non-mirror
Motor Program(Grasp)Object affordance hand state
association
7b

Hand-Object
spatial relation
analysis
7aActionRecognition(MirrorNeurons)
F5mirror

Motor
execution
F1
Motor Program(Reach)F4

Objectlocation
MIP/LIP/VIP

Figure 6.3 The two possible organization of learning to grasp circuit are shown. According to Hypothesis I, two
grasping circuits exist; the phylogenetically older one located in area F1 (hatched background) and the newer
one in the premotor cortex (solid background). According to Hypothesis II, F1 is involved in only executing thepremotor cortex instructed movements. LGM is based on the latter hypothesis. The details of LGM are shown in
Figure 6.4. Note that we introduced area F2 for complementing the MNS structures. The visual input to area F2
originates from MIP (not shown) and V6a

The alternative hypothesis is that learning to grasp circuit is distributed over a large area in the
premotor cortex including area F5, with access to direct object affordance input from AIP; and area F1 is
responsible for the execution of the plan instructed by area F5 (see Figure 6.3). According to thishypothesis, the inability of infants to perform adult-like grasps can be explained by theunderdevelopment of AIP for affordance extraction and the inability of infants to control their limbs, orthe computational complexity of AIP-F5 learning. The former corresponds to the maturational-based
theory of motor development; while the latter corresponds to learning-based theories (see Chapter 5).
We will introduce Affordance-based Learning to Grasp Model (LGM) based on Hypothesis II,
which means that LGM will be the model of grasp related visuomotor circuit of monkey premotor
cortex. LGM, being a simulated neural realization of Hypothesis II, will yield testableneurophysiological predictions.

6.5

Affordance-based learning to grasp model (LGM)

With the term learning to grasp we mean to learn how to make motor plans in response to sensory
stimuli such that the open loop execution of a plan leads to a successful grasp. There is strong behavioral
evidence that early grasping is based on open-loop control and does not use visual feedback (Clifton etal. 1993; Clifton et al. 1994; von Hofsten and Ronnqvist 1988; Streri 1993). Further, adult practiced

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movements move from a visual feedback control strategy to an open loop control strategy evidenced
by postural invariance studies in grasping movements. Desmurget et al. (1998) studied a prehension
task requiring subjects to grasp a cylindrical object presented at different locations with changing
orientations. The effect of initial arm posture was investigated. The results showed that individual
subjects had stereotypical grasping patterns resulting in fixed postures of the arm, which variedsystematically as a function of initial posture and object location and orientation (Desmurget et al. 1998).
Furthermore Grea et al. (2000) showed that the final posture to be reached is planned in advance andused as a control variable by the central nervous system. This was true even when the object jumped toa new location during the transport phase of the reach. The new position of the object could determine
the final arm posture with the same precision as a stationary target (Grea et al. 2000).
However, we do not claim that visual feedback is not used for reaching and grasping. On thecontrary, we suggest that when the task demands cannot be satisfied with existing motor schemas, thevisual feedback control becomes necessary. In Chapter 7, though in a simplified setting, we study thevisual feedback control of grasping. Current chapter addresses the issue of acquiring a grasp repertoirethat can generate suitable grasping based on the object affordances.
The link between open-loop grasp execution and the visual feedback based grasp execution ofChapter 7 is established through AIP-F5 learning in LGM. As will be shown LGM learning yields units
that show object selective responses similar to F5 canonical neurons. The favored hypothesis of Chapter
7 is that F5 canonical neurons, based on the object properties, gate F5 visual servo circuits. Thus,
Chapter 7 without loss of generality, will concentrate on a visual servo circuit specialized for precisiongrip learning and execution, which is presumably selected by a population of F5 canonical neurons.

6.5.1

Localizing learning to grasp model in primate cortex

We propose three computational layers relevant for grasping: Hand Position, Virtual Finger, Wrist
Rotation layers, as we functionally justified in Chapter 5. The affordance of the target can vary from asingle variable indicating the existence of a graspable object to the full description of an object in termsof its affordances, and is encoded in the Affordance layer. The affordances are represented using the
population-coding scheme and encoded algorithmically (i.e. no visual processing for object recognition
and feature extraction is performed). We use Affordance layer or the input terms interchangeably toconform the context
The parameters (hand position, virtual fingers and wrist rotations) encoded in LGM layers areabundantly represented in the premotor and motor cortices. Thus, it is not always possible to constrain
the localization of the layers with a high level of confidence. Nevertheless, we can minimize the numberof alternatives based on relevant literature as follows.
The wrist rotation parameters are represented in the primary motor cortex (area F1) in terms of
direction (i.e. independent of the muscle groups activated) (Kakei et al. 1999). The ventral premotor
cortex (area F5) neurons are involved in extrinsic coding of hand direction (Kakei et al. 2001). Area F2
has control over wrist movements and is organized similarly to area F1 in terms of somatotopic
organization (Fogassi et al. 1999); thus Wrist Rotation layer can be associated with F2 as well as with F1.
Premotor cortex (area F4) can potentially encode hand location with respect to the object (Fogassi et al.
1992; Fogassi et al. 1996), as it is the target of ventral intraparietal area (VIP) (Geyer et al. 2000), which is
involved in egocentric target representation (Duhamel et al. 1997). The VIP-F4 circuit, therefore, canplay an important role in reach and grasp planning in monkeys (Rizzolatti et al. 1998). Thus, it is
tempting to associate the Hand Position layer with area F4 and/or area F5. Recalling the object selective
motor properties of F5 neurons (see Chapter 2), we can posit F5 in performing the task of Virtual Finger
layer by instructing which configuration to use for a given object. In addition, Cisek and Kalaska (2002)

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presented evidence that the primate premotor cortex can simultaneously represent discrete
directional signals related to multiple alternative reaching actions. In this study, a monkey was asked toreach for possible targets, which were cued by a nonspatial ‘go’ stimulus. During the first period, while
the monkey was waiting for the go signal, two directional signals coexisted in the activity of neurons in
dorsal premotor cortex encoding the reach directions toward the two potential targets (Cisek andKalaska 2002). When the ‘go’ signal was given, the activity encoding the non-cued direction
disappeared and the remaining signal predicted the monkey's reach choice (Cisek and Kalaska 2002). Ina similar study by Hoshi and Tanji (2000), an additional cue was introduced to instruct the monkey touse its left or right hand when pointing one of the two targets. The results indicated that alternative
motor plans were represented in the dorsal premotor cortex before the action is uniquely determined.
Note that one of the main motivations behind the neural architecture we developed in Chapter 4 was tobe able to encode multiple action plans.
In the light of the above review and in accordance with Hypothesis II, we propose that area F5works closely with areas F4 and F2 to create a feasible grasp plan based on the object affordances
relayed via AIP (see Figure 6.4). The grasp plan is then, relayed to the primary motor cortex (F1) and thespinal cord for execution. The tactile feedback of the grasp is assimilated in the first somatosensory
cortex (SI), which mediates learning in parietal and premotor connections.

Virtual Finger
Layer
ObjectAffordance(Size, Axis,
Position)

AIP/MIP/VIP

F5Wrist Rotations
Layer

Motor Cortex

Spinal
Cord

F1

F2/F5
Hand Position
Layer (F4)F4/F5
Reinforcement Signal

Grasp
Evaluation

SI
Figure 6.4 The Learning to Grasp Model. F5 is implicated in all grasp related parameters. Dashed connections
indicate the direct corticospinal projections of premotor areas. Area F5 works with area F2 and F4 to transform
visual affordances signalled by parietal areas into a grasp plan. The grasp plan is then, relayed to primary motor
cortex (F1) and spinal cord for execution. The tactile feedback of the action is integrated in the firstsomatosensory cortex (SI), which mediates the adaptation of the parietal-premotor and inter-premotor
connections

The involvement of area F5 in multiple grasp parameter coding finds support by the finding thatmost F5 neurons were selective for grasping movements, but there were also reach related as well as
wrist rotation selective neurons (Rizzolatti et al. 1988). The multiplicity of motor representations (Wu et
al. 2000; Rizzolatti et al. 1988; Gentilucci et al. 1988) makes it impossible to rule out other alternatives
such as the view that F5 being exclusively involved in mapping object affordances to finger
configurations. This, in fact, points out the importance of our modeling. With our model, we aim to101

motivate neurophysiologists to challenge the model predictions with experiments, which will help
uncover the detailed functional roles of the premotor areas in grasp related visuomotor transformations.

6.5.2

What does cerebral cortex know about a grasp?

When a human infant or a monkey touches, many receptors in the hand transmit many signals
related to the contact such as the skin indentation and slip (Rothwell 1994; Johansson and Westling1987b; Johansson and Westling 1987a; Salimi et al. 1999b). The literature on the mechanisms of
mechanoreceptors and the transmission of their signals to the cortical areas is vast. Our intention is not
to model these mechanisms, but rather convince the reader (and ourselves) that a reinforcing signal
indicating a successful grasping is available to the learning-to-grasp circuit located in the premotor
cortex. Thus, we present here a brief but relevant data from the literature on the role of thesomatosensory cortex in representing the sensations of the hand, including grasping. The interested
reader is referred to other literature (e.g. Akoev et al. 1988; Willis and Coggeshall 1991) for detailed
information on mechanoreceptors and their functional organization.
The primary somatosensory cortex (SI) has somatic representation of the fingers and showsdifferential activity during grasping phases (Gardner et al. 1999; Ro et al. 2000). In one study, anterior SI
was found to be dominated almost exclusively by neurons with cutaneous receptive fields (88%) andposterior SI neurons were found to receive tactile inputs (51%) and deep inputs from muscle and joints(41%) (Debowy et al. 2001). Furthermore, Debowy et al. (2001) showed that during prehension
somatosensory cortex units signaled the formation of hand and object as a functional unit in combination
with other hand actions. Debowy et al. (2001) classified SI neurons, among others, as approach, contact,
contact-grasp, grasp-lift, manipulation and grasp inhibited neurons. In terms of tuning, they have foundneurons with grasp tuning, approach tuning, hold tuning and contact tuning.
Martin et al. (2000) examined the effects of blocking neural activity in cat sensory motor cortex(muscimol infusion) during early postnatal development on prehension. Grasping occurred on only
14.8% of trials with the limb contralateral to the infusion. In addition, the grasping was replaced byraking without distal movements. This data suggests that the normal development of skilled motor
behavior requires activity in the sensory motor cortex during early postnatal life.
Salimi et al. (1999) examined the receptive field properties of somatosensory cortex neurons inmonkeys during a precision grip task. The majority of the receptive fields found was cutaneous andcovered less than one digit. Two types of neurons were described: dynamic and static. The dynamic
neurons, showed a brief increase in activity beginning near grip onset, which quickly reduced even thepressure to the receptive field continued (Salimi et al. 1999a). Some of the dynamic neurons responded
to both skin indentation and release (Salimi et al. 1999a). The static neurons had higher activity during
the stationary holding phase of the task (Salimi et al. 1999a).
Based on the brief review above, we postulate that grasp success is signaled as a population
activity in the somatosensory cortex (SI) 19. In order to simulate and test the proposed grasp-learning
hypothesis we need to emulate the grasp success signal to drive the learning in LGM. We base theemulation on the physical definition of grasp stability as we did in Chapter 5. Of course, we do notclaim that such computation is performed in the primate brain. We are using the tenets of schema
methodology (Arbib et al. 1998) to substitute a biological reinforcement or success schema (‘joy ofgrasping’ of Chapter 5) with the engineered version for the sake of analysis.
19 The form of the signal is not the main issue here, what we are after is a neural representation of holding (stablegrasping). As a first approximation, we posit somatosensory cortex for this role without assigning an emotional
meaning to the signal. Prefrontal cortex may be involved in such motivation-based signal.

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6.5.3

Simulation level description of LGM layers

We have already introduced LGM layers in Chapter 5 as schemas. Now, we summarize thefunctional description of these layers to prepare the reader for neural level analyses.
Hand Position layer determines where the hand will be with respect to the object during grasping.
Intuitively, this represents the side from which the hand will grasp the object. The frame of reference forthis parameter is allocentric. The coordinate system we choose for this parameter is spherical. The
encoding used is as described in Chapter 4. Thus the neural layer represents a probability distributionof hand position values and the specific output is generated by a local population vector computation.
Virtual Fingers layer specifies which fingers will be activated, and with what strength. We use
three virtual fingers: thumb, index finger, and the remaining three fingers acting together. The
processing is parallel to the Hand Position Layer’s flow. However, this does not mean that this layer has
the right to decide the virtual fingers on its own. The virtual fingers that cannot yield grasping are
negatively reinforced; and hence do not appear in learned LGM.
Wrist Rotation layer combines all the information about the object (affordance) and the Hand
Position and Virtual Finger layers’ output. Thus, the output of this layer represents the possible wristorientations given the (1) object related input (affordances), (2) output of Hand Position layer (3) output
of Virtual Fingers layer in terms of a conditional probability distribution. The parameters generated inthis layer determine the movements of wrist extension-flexion (tilt), wrist supination-pronation (bank);
and ulnar and radial deviation (heading).
A typical scenario for grasp execution would be as the following:• A small box is presented in the workspace of the arm to the left of midline of the body.
• Hand Position layer computes the distribution of feasible approach directions and aselection is made according to the distribution, for example as ‘from top’
• The Virtual Finger layer works similarly. Let us assume that a selection is made such thatindex and thumb fingers are activated such that their trajectories coincide (a precisionpinch).
• Then, the Wrist Rotation layer combines the Virtual Finger and Hand Position layers’
parameters with the Affordance layer to compute a probability distribution for theapplicable (e.g. to the precision pinch approaching to the object from top) wristorientations. The grasp plan is complete when the final selection is made from the Wrist
Rotation layer.

6.5.4

Why LGM is relevant: good model versus bad model

Microstimulation studies ensure that there are neurons in the primary motor cortex and premotor
cortex that control finger digits, wrist movements, and reaching. This chapter provides a learning
mechanism to adapt the connectivity of premotor regions so that they act cooperatively to yield feasible
grasp plans. One of the main motivations of using a minimal set of grasp parameters was to test
whether learning by interacting with the environment, can shape neurons to have properties that we
did not manually encode. The emergent neuron properties such as the object selectivity are very
important because they justify that the structure and the learning proposed are adequate to capture thelearning for the grasp related visuomotor transformation in the primate since we bootstrapped thegrasp learning from a minimal set of elemental/postnatal abilities and behaviors summarized as thefollowing.
1. Motor abilities: infants are able to move their wrist, and fingers
2. Visuomotor abilities: infants reach for visual targets
3. Behaviors: infants explore the space with their hands through variable movements

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4.

Reflexes: infants are born with reflex behaviors helping them to shape their(visuo)motor abilities (e.g. enclosure reflex)
This is why we did not assume, for example, a layer of grasping neurons specialized for different
hand apertures. If we did so, those neurons and the objects with compatible sizes would be triviallyassociated via trial and error learning, which would not add anything to our knowledge. However, with
our approach we show that starting from a basic set of abilities/behaviors in accordance to infantdevelopment, complex neural properties emerge which yield predictions that can be experimentallytested. If the model is validated by comparing experimental findings to predictions of the model, we cansuggest that primate brain follows a similar strategy to develop visuomotor abilities by interacting withthe environment. Thus, a validated model will (1) bring new insights to primate visuomotortransformation and (2) enable us to make sound predictions with new simulation experiments. As will
be presented in later sections, LGM leads to the emergence of neurons with nontrivial properties suchas object preference, similar to those of F5 canonical neurons in monkey premotor cortex.

6.6

Wrist orientation-learning revisited: neural level analysis

Chapter 5 showed that Infant Learning to Grasp Model (ILGM) was able to learn how to adjust
wrist orientation and approach-direction via explorative learning. The model learned to generateparameters to perform power and precision grasps, and many variations of the two. The most abundant
grip generated was the power grip and its variations. Precision type grasps were less frequently
generated. In terms of learning task, the ILGM had to discover the distribution of wrist movements(supination-pronation, extension-flexion, ulnar/radial deviation) for multiple approach directions.
Presented with an object, Hand Position layer produced the distribution of possible approachdirections. The selection was relayed to Wrist Rotation layer. Then, Wrist Rotation layer computed the
distribution of feasible wrist orientations conditioned on the generated hand position. Virtual Fingers
layer dictated the enclosure speed of the hand.
Noting that ILGM being functionally equivalent to LGM, analyzed the behavioral aspects of grasp
learning, we now present a neural level analysis of the wrist-orientation learning of Chapter 5.

6.6.1

Neural level analysis

In this section, we analyze the activities of LGM layers. We will use two graphical representations:
one for the probability distribution represented by LGM units and one for the memory (or eligibility)
traces. The former map represents how likely the units would fire given the input and the context while
the latter represents the ‘generated parameter’ at the particular instant. A neurophysiological analogy
for the probability distribution would be a multi-electrode recording experiment. The normalized firing
histogram of the neuron population over many trials (with fixed input and the same experimental
conditions) would be very much comparable to what we call the probability distribution. Thus theprobability distribution graphs represent (1) population level activity of the neurons in a layer and (2)individual neurons’ preferred stimulus. The eligibility trace maps show the activity of neurons that are
involved in parameter generation in a single trial. Figure 6.5 shows the activity of the Hand Position
and Wrist Rotation layers (left two panels) as well as the memory traces (center two panels) for thegrasp shown in the right panel. Note that the preferred values of Hand Position and Wrist Rotation
layers are three-dimensional parameters. To visualize them we average the activities over an axis. For
Hand Position we average over radius axis. For Wrist Rotation layer we average over the ulnar/radialdeviation axis. These two axes are chosen because they are found to be least influential in generating
successful grasps.

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Data generation
uth
im
Az

-L
ay
er
Co
m
pu
tat
io
n

Eleva
tion

uth
im
Az

Hand Position (generated)

In
ter

Hand Position Distribution

Eleva
tion

Data generation

Exten
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n-Fle
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tio
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-P
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ati
pin
Su

n

Wrist Rotation Distribution

Exten
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n-Fle
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Pr
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i
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n

Wrist Rotation (generated)

Figure 6.5 The top-left shows the Hand Position layer output summed over the radius (approach direction is
encoded in spherical coordinates) as a 3D plot. The top-centre panel shows the sample generated from theHand Position distribution. Bottom-left shows the Wrist Rotation layer output summed over the heading axis asa 3D plot. The bottom-centre panel shows the parameters picked from the Wrist Rotation layer distribution.
Note that Wrist Rotation layer distribution depends on (i.e. represents a conditional distribution) the sample
picked from the Hand Position layer. The rightmost panel shows the executed grasp

The allocentric position encoded by top-center map roughly corresponds to a location higher thanthe object, which is also at the behind and right side of the object. This location determines the approachdirection of the hand (hand reaches for the object from that location). Given this approach the possible
wrist rotations that yield stable grasps are computed by Wrist Rotation layer. The bottom-left panel
shows the firing potential of units in this layer. Having a population level activity, we can interpret thestrategy ILGM learned. The Wrist Rotation probability distribution roughly says, as long as the wrist is
flexed between 30 to 80 degrees (tilted downward) then the grasp will succeed with the hand approachdirection encoded in the memory trace. Of course, there is no way to tell in advance, which of the
combinations will yield a precision pinch. Our general notion is among the performed grasps, there will
be precision grips, which will be picked and tuned by the premotor cortex.

6.6.2

LGM represents a ‘menu’ of grasps in terms of neural activity

Now we look at another grasp plan made by the same LGM (no new training). As we mentioned
earlier Wrist Rotation layer learns feasible wrist rotations based on the eligibility trace of the Hand
Position layer. This time Hand Position layer generated a different approach (Figure 6.6, top-center
panel), which changed the landscape of the Wrist Rotation layer’s distribution (bottom-left graph). The
wrist rotation parameter generation is shown in the bottom-center panel and the resulting grasp isshown in the right panel.
One of the important observation is that LGM was able learn a ‘menu’ of grasps which is open tobiasing. The bottom-left panel of Figure 6.6 explicitly shows that two distinct sets of wrist rotations
could be generated given the approach direction encoded in the memory trace of the hand position
parameter (Figure 6.6, top-center graph).

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Elevat
ion

uth
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Az

Elevatio

Hand Position Distribution

Exten
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n-Fle
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at
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Su

tio
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-P
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n

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Hand Position (generated)nExtens
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n-Fle
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p
Su

tio
ina

o
Pr
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tio
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Wrist Rotation (generated)

Wrist Rotation Distribution

Figure 6.6 Using the same LGM used for Figure 6.5, another grasp plan is generated (left four panels). The
resulting grasp is shown on the right. By comparing the grasp plan shown on the left four panels with of Figure
6.5’s grasp plan we see how the selection of a different approach direction (see the centre-top panels of both
figures) changed the Wrist Orientation distribution

Now we demonstrate the two options from the ‘grasp menu’. Figure 6.7, shows clearly thevariability of the grasp that can be encoded in LGM. In the upper panels the Wrist Rotation layer
specified maximum wrist extension with pronation (top-center panel). The resulting grasp is shown on
the upper-right panel. In the second trial, the generated wrist rotation instructed maximum supinationand small extension. The resulting grasp was very different although the hand approached the object
from the same location (the Hand Position layer is not shown).

Exten
sio

n-Fle
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Pr
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a
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n
Exten
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Wrist Rotation Distribution

Extens
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Wrist Rotation Distribution

n-Fle
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Wrist Rotation (generated)

Extens
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Wrist Rotation (generated)

Figure 6.7:Two very different grasp generation from the same LGM. Upper panel: Grasping with maximum
wrist extension with some pronation. Lower panel: Grasping with maximum wrist supination and small wrist

106
extension. Note that the Wrist Layer probability map is the same since the approach direction was chosen thesame (the small dots in the right most panels).

6.6.3

Predictions and discussion

LGM simulation in particular predicts that the premotor cortex neurons that are involved in
encoding limb movement parameters (e.g. wrist rotations) must be modulated by other movement
parameters (e.g. the direction of approach).
By generalizing grasp actions to general movements, we predict that complex movements cannot
be determined by a single layer. For example, the neurons controlling digits and wrist rotations aresegregated in area F2 (Fogassi et al. 1999); area F4 controls proximal while area F5 distal movements(Rizzolatti et al. 1988; Gentilucci et al. 1988). Somatotopic organization of multiple motor areas is anevident strategy of the primate motor cortex (see reviews: Wu et al. 2000; Geyer et al. 2000). Thus, thegeneral prediction we make is that the activities in these segregated regions must be modulated by theirrelated peers (e.g. hand-arm). For an experimenter the neurons of this nature would appear to have‘gain fields’ or appear to be modulated by other behavioral contexts.
Let us take a hypothetical but common experimental set up (for example see Georgopoulos et al.
1982). The experimenter wants to find the neurons encoding wrist extension-flexion in monkey. The
monkey places its arm on a table and performs wrist extension and flexion movements. The
experimenter locates the motor region that (e.g. F2) correlates very well with the monkey’s movement.
Can he say that this region encodes wrist extension/flexion? With the insights gained from oursimulation studies, we answer ‘no’. The activity could be well depend on other motor parameters, suchas posture. Indeed, this kind of modulation has been shown to exist in the primary motor cortex (Sergio
and Kalaska 1997) with reaching movements using different arm postures. The finding has also been
extended to the dorsal premotor cortex confirming that similar modulation exists in higher motor areas(Scott et al. 1997).
In fact, Arbib and Hoff (1994) noted the important distinction between neural activity that controls
movement versus neural activity that correlates with movement. We propose that to discover motor
circuits in the cortex the correlation studies (correlating behavior to neural firing) is not enough.
Simultaneous recording from anatomically connected regions must be required to understand thecomputational elements underlying the modulation or gain field phenomenon

6.7

Object axis selectivity: neural level analysis

Lockman et al. (1984) used subjects of 5- and 9-months of age and compared their performance inorientating their hands to a dowel presented in horizontal and vertical position (see Figure 6.8). To
replicate their experimental condition, we let the affordance of the object (orientation) to be relayed to
Learning to Grasp Model in accordance with our Hypothesis II (see Figure 6.3). We presented a cylinder
to LGM analogous to a dowel. To implement the premises of our hypothesis that the information about
the axis orientation (i.e. affordance of the object) is not available to the grasp planning circuit during
early infancy (5 months of age) and that it becomes available later in development (9 months of age), we
effectively disabled the orientation encoding for the simulation of younger infants’ grasp learningwhereas to simulate older infants’ case we enabled the orientation coding in their affordance input (seeChapter 5). The former case was referred as the poor-vision and the latter as the full-vision condition.
With this simulations we had two goals: (1) to compare the simulation results with of Lockman etal.’s (1984) and (2) to analyze the internal representation of the learned model. Chapter 5 compared themodel results with experimental data fulfilling (1). Now we present the internal representation analysis

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of LGM for both affordance and no affordance case representing 9 months and 5 months of age
infants respectively.

Figure 6.8 The grasps performed after LGM learned the association of hand rotations with the object orientation
input (full vision condition). Note that the left panel shows a bottom side grasp. All of the shown grasp
configurations satisfied grasp stability criterion

6.7.1

Neural level analysis

By analyzing the kinematics error curves of the orienting behavior, we concluded that there were
two modes of grasp planning (Chapter 5); but how correct is this? We answer this question by
examining the population level representations emerged by LGM learning.

Figure 6.9 In the poor-vision case, the hand rotation neurons in LGM show the same response for horizontal(left panel), diagonal (centre panel) and vertical (right panel) object presentations because of the lack of axis
orientation input

We are interested in deciphering the grasp planning strategy learned by LGM in poor-visioncondition. Figure 6.9 shows the Hand Rotation neurons of LGM: (from left to right) for horizontal,
diagonal and vertical cylinder presentation. The Hand Rotation distribution is almost identical since theaxis orientation information is not accessible to LGM in the poor-vision case. The Hand Rotation Layer
distribution confirms our inference from the kinematics: there are two peaks of neuron activity, whichcorresponds to the vertical and horizontal orientations of the hand during grasping.
However, note that the two possibilities could not be specialized for the different orientations andhence represented in all three cases. The peak at (-π/2, 0) indicates a wrist rotation that makes the angle
between the backside of the hand and the arm 90 degrees (full wrist extension), which is required forgrasping a centered horizontal object from the front side. On the other hand, the other peak at (-π/2,π/2)
indicates an additional supination of the hand, which is required for grasping vertical cylinder from thefront side. These values corresponds to the grasp configurations we kinematically observed in Chapter
5.

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Figure 6.10 When LGM has access to axis orientation information the Hand Rotation neurons represent different
plans in response to horizontal (left panel), diagonal (centre panel) and vertical (right panel) object presentations

In the full-vision case, we supply the orientation of the cylinder as an input to the LGM. Figure 6.10
shows the Hand Rotation neuron’s distribution for different orientations, for a direct comparison withpoor-vision case Figure 6.9. Now the neurons show preferential activity for different cylinder orientations.
Also we can see that in the horizontal orientation case the LGM have two alternative plans as evidenced
by the two peaks at the edges of the Hand Rotation neuron distribution shown in Figure 6.10, left panel.
Note that these two alternatives correspond to grasping the horizontal cylinder from top and bottom(left panel, Figure 6.10).
Similar multiple plan representation is also observed in the diagonal case (Figure 6.10, center
panel). The vertical cylinder case has a single grasp plan representation (Figure 6.10, right panel). We
can relate the Hand Rotation neuron activities of poor-vision and full-vision cases. We can see that thepoor-vision distributions are superimpositions of the three maps shown in Figure 6.10 with varying
degrees of inhibition on areas where a common activity was not observed. For example there is activity
around (-π/2,-π/2) in all three neuron responses (Figure 6.10), and hence the peak appeared in the
responses shown in Figure 6.9. However, the peak of activity (-π/2, -π), which is shared by horizontal
and diagonal orientations is not pronounced in Figure 6.9, because these neurons are not active when
the object is vertically oriented (Figure 6.10, right panel)

6.7.2

Conclusions and neurophysiological predictions

Based on the wrist rotation and hand position maps formed via learning we can make predictions
concerning the neural response properties of the premotor cortex. Up to now, we have used the term
Affordance or Input to LGM without specifying from where this information can be relayed to premotor
regions. Now we relate the emergent properties of the simulated neurons to affordances relayed.
The anterior part of the lateral bank of the intraparietal sulcus (area AIP) is implicated in extracting
visual properties of objects relevant for grasping (Sakata et al. 1997a; Sakata et al. 1998; Sakata et al.
1995; Murata et al. 1996). There is strong anatomical reciprocal connection between area F5 and area AIP(Matelli 1994, Sakata, 1997). Furthermore some AIP visually activated neurons, show tuning according
to the orientation of the longitudinal axis or the plane (surface) of flat objects (Sakata et al. 1999).
Therefore, the axis information can be extracted by area AIP and channeled to area F5. The lateral bankof the intraparietal sulcus (c-IPS area) is involved in three-dimensional analysis of objects (Sakata et al.
1997a; Sakata et al. 1999). Some of these binocular visual neurons are selective for the orientation of theaxis of the objects (AOS neurons). The c-IPS neurons may be the basis of AIP neuron properties (Sakata
et al. 1997a; Sakata et al. 1999).
Analogous to the AIP-like object representation found in area F5 (Murata et al. 1997a), our model
predicts that a premotor area that is connected with AIP or area F5 must have visually triggered
neurons that are selective for object orientations. Furthermore, we suggest that the area must have control

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over wrist rotations. Area F5 and F2 of the dorsal premotor cortex, satisfies the conditions we havelisted. Fogassi et al. (1999) found that F2 neurons responded to visual stimuli and showed by
microstimulation that the wrist joints were controlled within area F2. To our knowledge there is no
study probing the object orientation selectivity of neurons in area F2 and F5. We suggest that the
canonical neurons may have tuning fields according to the object orientation similar to the object typeneurons with orientation tuning in area AIP (Sakata et al. 1999).
To summarize, we predict that a sub-population of F5 canonical neurons or F2 neurons that are
involved in wrist control must have selectivity or tuning according to objects’ grasp relevant properties.
More specifically, we claim that a closer examination of F5 canonical neurons and/or area F2 neurons
would reveal orientation selectivity either in isolation or as a tuning mechanism over object selectivity.

6.8

Object size selectivity

The goal of this simulation is to investigate the emergent neural properties when Learning toGrasp Model is presented with objects of different sizes. The object size is accessible to LGM via the
Affordance layer and algorithmically coded (no object recognition and feature extraction is performed).

6.8.1

Simulation results

We used cubes of different sizes as objects. After the model interacted with the object, we identified
the grasps learned. For large object case, the model often generated power grasps, and some variations.
For small objects model generated precision grasps. The number of different precision grasp types wasless compared to the number of different type of power grasping observed for big objects. In otherwords, LGM formed a large ‘menu’ of power grasps but gained a small ‘menu’ of precision grasps20.
After the behavioral observation, we analyzed the unit level activity of Hand Position layer. Wrist
Rotation layer’s output was modulated by Hand Position layer’s activity (see the analyses in section
6.6).

Figure 6.11 The small object presentation produced two peaks of activity in the Hand Position layer
corresponding to the probability distribution of approach directions. The right panel shows the executed grasp
when the data generation was localized in the area pointed by the leftmost arrow.

Figure 6.11 shows a learned precision pinch and the activity of Hand Position layer. The small
object activated two peaks as indicated by the arrows in the figure. If a neurophysiologist recorded theactivity of the units in Figure 6.11 (each point on the 3D mesh represents a neuron with its average
20 Grasps with different wrist orientations are counted as different.

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activity as the z-axis), he would notice over many trials that those units are the most active ones. To
claim the specificity he still would need to compare the very same neuron with different object sizes.
We do the same and show that the activity is object-size specific (compare with Figure 6.12 and Figure6.13).
Figure 6.12 shows a power-like (radial palm grasp see Figure 5.1) grasp with the corresponding
Hand Position layer activity. This time the hypothetical experimenter would notice the unit indicatedwith the arrow fired maximally for the presentation of this object. Note that the activity locus isdifferent from the small object presentation (see Figure 6.11).

Figure 6.12: A large cube was grasped by securing the object between the thumb and the other fingers (rightpanel). The Hand Position layer activity is shown on the left panel. The neuron with largest activity is marked
with an arrow

As the last simulation we present the unit level activity when the model presented with the largest
object. The Hand Position layer showed a clear peak (Figure 6.13). In order to emphasize that thesesimulated neurons do not show unspecific activity, but rather are selective for object sizes, we compare
the locus of the neurons that the arrows point to in each figure (Figure 6.13;Figure 6.12; and Figure 6.11)

Figure 6.13 The largest object presentation and grasping. The Hand Position reflects a single reach direction as
indicated with an arrow

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Figure 6.14 shows the three activities superimposed after the axis are aligned. The maximum
activity regions are also linked to the corresponding object presentation. Notice that the peak activity
loci are not the same indicating that the neurons gained selectivity to object size.

Figure 6.14:The Hand Position layer activity is superimposed to demonstrate that the maximum activity loci areseparated for each object indicating selectivity for object size.

6.8.2

Conclusions and neurophysiological predictions

Even though we did not engage Virtual Finger layer in its full capacity (it controlled the fingers
synergistically) the Hand Position layer activity of LGM showed object specificity. Therefore, wesuggest new experiments to test whether F5 canonical object specificity is due to some other motor
parameter encoding. Although microstimulation of F5 neurons produces complex movements they do
not produce a grasping behavior, so the activity during grasping do not necessarily specify complete
grasp plan but rather a subset of motor parameters required for grasping. This is analogous to the LGM
layers differential contribution to the grasp plan. Therefore, the challenge to the experimentalists is tofind out whether F5 canonical activity alone specifies a grasp plan or not. Our prediction is negative
because, for example, in LGM simulations, the wrist rotations generated did not affect the activity ofHand Position neurons (analogous to F5 canonical neurons’ object related activity) but the grasp plan
was only complete with the Wrist Rotation layer’s contribution. Thus, F5 canonical neurons can be just apart of the grasp planning circuit.
To decipher the functional structure of the premotor grasping circuit, this hypothesis must beeither ruled out or validated. If it turns out that F5 neurons are specifying only a subset of grasp
parameters, new experiments must be designed to uncover the neuron properties of the areas connectedarea F5. Since our model predicts that if some neurons specify a grasp plan partially (by being
responsible for one parameter of the plan), the learning must shape the connections between theconnected regions to enable the cooperative computation that can yield compatible grasp parameters.
This is a nontrivial observation. if a hypothetical experimenter, investigating the encoding of grasp
parameters, finds out that112

1. Area A is responsible for wrist orientation
2. Area B is responsible for controlling the reach direction
3. If the activities of A and B are true control variables of wrist rotation and reach direction
Then, we claim that
1. Regions A and B must be anatomically connected (the connection may be a multi staged
one, such as A connected to C, C connected to B)
2. The synaptic strength of the connections between A and B encode the grasp selection
strategy of the grasping circuit
3. If the parameters are, in the physical sense, coupled then the dependency of parametersmust be captured in the connection between A and B
The claim (3) is based on the observation that the only way to produce coherent grasp plans is tocapture the physical coupling inherent in the movement. For example given a sphere, there areinfinitely many approach directions, which can be used for grasping (assume A encodes approachdirection). Similarly, there are infinitely many wrist orientations (assume B encodes wrist orientation).
The crucial observation is that, not all pairs of approach direction and wrist orientation are compatible.
For grasping, given A, B has to be determined or given B, A has to be determined because theparameters are coupled. With this setting, we further claim that:(1) If it is found that the connection between A and B is unidirectional (say from A to B) then (fromthe view point of the experimenter) the activity of B neurons must be tuned by the population activity A(2) Recording simultaneously from A and B can reveal the organization of visuomotor grasping
circuit as the following. If activity of A predicts the activity of B, better than the other way round (i.e.
activity of B predicts the activity of A) the underlying principle is that area A selects some of the grasp
parameters and then B, based on the selection of A, generates the remaining grasp parameters
In terms specific predictions, LGM predicts that F5 canonical neurons, to specify a grasp plan, musthave ‘gain fields’ based on other brain areas (which, behaviourally would appear to be based on othermovement parameters). A good example for such systematic relation (unfortunately, to our knowledge
only behaviourally) is the effect of arm posture on reach-related activity of motor cortex neurons(Caminiti et al. 1990; Caminiti et al. 1991; Sergio and Kalaska 1997). In these studies, it has been foundthat the reach encoding neurons have gain fields based on arm posture or position of the arm in theworkspace. These findings, combined with multiple action representations in the motor areas (Cisek
and Kalaska 2002) strongly indicate that the underlying circuit for reach generation have similar
properties as LGM.
The structure (the dependence relations of layers) we offered in LGM may not be the only
possibility. To uniquely determine the structure, neurophysiological studies must go beyond correlation
studies. LGM postulates the dependency of wrist rotations on the virtual fingers and approachdirection. Therefore, according to LGM, virtual fingers and approach direction predicts the wristorientation. Then LGM predicts that the wrist orientation coding neurons will have ‘gain fields’ basedon the virtual fingers selected and the approach direction determined. Whether LGM structure is rightcan be tested by experiments similar to reach and posture coupling experiments (Caminiti et al. 1990;
Caminiti et al. 1991; Sergio and Kalaska 1997; Scott et al. 1997).
An alternative structure for LGM would be to posit that the wrist rotations with virtual fingers are
determined first then based on those the approach direction is determined. This can be a feasible
alternative because the wrist orientations are important in determining the manipulative freedom of thehand once the object is secured. For example when grasping the knob of a door with the intention of
opening, we intentionally choose a ‘hard’ wrist orientation to have a large manipulative freedom (i.e.

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turning the knob to open the door). However, if we assume that the intended future action plans arealso relayed to wrist rotation layer (together with affordance of the object), LGM structure can accountfor such anticipatory grasp planning as well.
LGM presents a rich set of hypotheses that can be verified or falsified with clean-cut experiments.
We now, suggest that simultaneous recording experiments for premotor regions of F2, F5 bank(canonical neurons), F4 and wrist rotation encoding neurons of motor cortex (F1) must be performed tounderstand the underlying principles of grasp related visuomotor computation. A feasible experimental
setup would pick two pairs from (F2, F4, F5, F1) at a time and record from the two sites while themonkey is performing grasp actions directed to objects located at different positions with changing
orientations. The simultaneous pair-wise recording of areas F2, F4, F5 and F1 would require 6 sessions(F2- F4, F2-F5, F2 F1, F4-F5, F4-F1, F5-F1). We claim that, with rigorous analyses of these recordings
with reference to hand kinematics and object affordances (i.e. the location and orientation of the object,
and the monkey’s wrist rotations and approach direction) the structure of the cooperative computation
underlying grasping can be revealed.

6.9

Generalization: learning to plan based on object location

Up to now, we presented simulations where the objects were located at a fixed position in thespace. In general, wrist rotations and approach directions depend on the position of the object as well as
intrinsic object properties. Here we concentrate on the object location, but the analysis is valid for object
properties (as long as they are represented as population coded activities and relayed to LGM) such as
the orientation of the object. In fact we had already used multiple orientation learning when simulating
Lockman et al.’s (1984) experiments (sections 5.9 and 6.7). However, there, we did not perform
extensive analysis to show the generalization of the learning to novel orientations.
A given wrist rotation and approach direction that yield a stable grasp, in general, does notnecessarily yield a stable grasp when the object is moved to an other position as approach direction andwrist orientation parameters are coupled for a successful grasp. For example, we don’t grasp objects
that are located on the left of midline as the same way as we do when they are on the right side. In
addition, reach component of different grasp actions yield different absolute wrist orientations because
the absolute wrist orientations depend on the configuration of the arm. Thus, the grasp plan has to take
into account the location of the object. In this section we presents results showing that LGM can learn togenerate stable grasp plans for different locations and generalize well for the locations that has not been
experienced before. The generalization property is important from a neural network perspective. A
generalizing network does not need to memorize all possible grasp plans for each location and hence
does not fail for novel situations.

6.9.1

Simulation results

We trained LGM model by randomly21 placing a sphere in the workspace and letting the modelinteract with the object. The egocentric location of object is encoded algorithmically in the Affordancelayer using population coding. Note that there is evidence that objects are encoded in egocentricreference frames in the parietal cortex (Siegel 1998; Colby and Goldberg 1999) which projects topremotor cortex (Geyer et al. 2000).
After 10000 grasp attempts, the model acquired the ability to make grasp plans for objects locatedin the workspace. Figure 6.15 illustrates the learning achieved as superimposed images of completed
grasps. Note that the object locations were not used while the model was learning to grasp. The lower
21 The positions were generated randomly on the surface of a invisible sphere centered on the shoulder

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three grasp actions are anatomically hard to achieve but they were included for demonstrating therange of actions that LGM learned to grasp at. As in earlier simulations, the illustration in Figure 6.15
only depicts a possible grasp for each location out of many alternatives. We reran the trained model on
exactly the same object locations as in Figure 6.15. A set of different grasping configurations is selected
to show that LGM could both generalize and represent multiple grasp plans for each target location (seeFigure 6.16).

Figure 6.15 The trained Learning to Grasp Model executed grasps to objects located at nine different locations in
the workspace. The grasp locations were not used in the training. All of the grasps shown were stable

Figure 6.16 The same model used in generating Figure 6.15 was used to generate a different set of grasps. Again
all the grasps were stable.

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6.9.2

Summary and Conclusion

The crucial feature of LGM we implemented is that it can produce a variety of grasp plans basedon input. Furthermore, the layer structure is well suited for further refining or biasing (e.g. contextual or
motivational biases). For example, one can use different biasing when grasping an apple for eating orfor placing it in a shopping basket. The reinforcement framework also gives the flexibility to include
soft constraints in grasp evaluation such that the grasps that are not favorable (due to discomfort, excessenergy consumption, etc.) are not represented or represented with low probability. Thus thereinforcement signal (‘joy of grasping’ of Chapter 5 and ‘neural grasp stability’ representation of thischapter) can incorporate the anatomical and environmental constraints which are important in shaping
grasp development (Newell et al. 1989) or the adaptive value of Sporns et al.(1998)
We summarize the computational ingredients of grasp learning we proposed with LGM by tracing
the neural level computations through an example.
We will use Figure 6.17 to illustrate how the same input condition can give rise to different grasp
plans. First, the object is presented (bottom center). The object location is encoded in an egocentricreference frame using population coding (we use a spherical coordinate system) (the center plot). The
object location is transformed into approach direction distribution (the top-center) by Hand Position
layer. After approach direction generation, the center stream branches into two. On the left, theapproach direction is generated as (approximately) from bottom, indicated by the top-left plot. On theright, the approach direction is even lower but it is from the backside of the object as can be read-off
from the top-right plot.
Generate approach direction

ComputeWrist
distribution

Generate approach direction

Computeoffsetdistribution

Generatewrist
rotation

Generatewrist
rotation

Executeplan

ComputeWrist
distribution

Encodeobjectlocation

Executeplan

Figure 6.17 The internal mechanisms of representing and generating multiple grasp plans are shown. Solidarrows (except object encoding) denote learned connections while empty arrows indicate data generation. The

116
flow of operation starts with the presentation of the object (the bottom centre) and follows the arrows. At the
top-centre, the data generation can yield multiple approach directions. The two possible approach directions areshown creating two streams (left column and right column), each of which yields different grasp execution(bottom pictures of left and right column).

Based on this two approach directions two different wrist rotation distributions are computed by
the Wrist Rotation layer as indicated by the downward solid arrows on each side. This is followed bywrist rotation generation, which results in different wrist joint rotations in the left and right streams as
indicated with the downward empty arrows. The grasp actions that are instructed by the left and rightgrasp plans would yield the completed grasps shown on the bottom-left and bottom-right columns
respectively.

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7

CHAPTER VII: BIOLOGICALLY REALISTIC F5 VISUAL SERVOCIRCUITS FOR GRASPING AND EMERGENCE OF MIRRORNEURONS

It has been argued that mirror neurons forms the basis of understanding other’s actions (Gallese etal. 1996; Rizzolatti et al. 1996a; Rizzolatti et al. 2001a; Umilta et al. 2001). The goal of this chapter is tobring an alternative view that this cognitive function may be secondary to a role for the mirror neurons
in providing visual control signals for manipulation. Figure 7.1 shows the focus of this chapter. MNS
model is redrawn and the regions of interest are marked with the gray background rectangle. In
Chapter 3, we introduced the idea that the mirror neurons might be involved in visual feedback for
manipulation, but in implementation, we emphasized how the self-action observations yield mirror
neurons. In Chapter 6, we have studied how grasp alternatives can be formed and selected based on theobject affordance and showed the emergent object feature selective properties of the simulated
premotor neurons. In this chapter, for the sake of tractability, we use planar arm/hand model and focus
on precision grasps. However, it should be emphasized that the simplification we make does not reducethe value of the message we wish to communicate to experimentalists. The point of this chapter is not toshow the object selective properties of the F5 neurons, but to study the temporal aspects of grasping.
Specifically, we show that units that encode visually defined grasp errors can yield activities similar to
mirror neurons and suggest experiments to validate and challenge the visual feedback control
hypothesis of mirror neurons.

7.1

Motivation

First, we present a biologically realistic feedback circuit composed of leaky integrators that canvisually servo the hand to achieve grasping. Then we augment the circuit with a feed-forward controllerthat is composed of pattern matching neural units and present two alternative hypotheses that associate
the visual control signals with mirror neurons. We demonstrate that the visual feedback and feedforward grasping system can work with lower level motor control circuits by implementing a positionand velocity (PD) controller which receives its desired trajectory from the visual grasp control model.
Finally, we introduce a method to compare the controller unit activities with real mirror neuron
recording data and suggest explicit experiments to validate or invalidate our proposal that mirror
neurons are involved in visual control of grasping movements.

118
Object recognition
IT

Object features

Visual Cortex

c-IPS

Hand shaperecognition& Handmotiondetection
STS

Area F5

Objectaffordance
extraction
AIP

F5non-mirror
Motor Program(Grasp)Object affordance hand state
association
7b

Hand-Object
spatial relation
analysis
7aActionRecognition(MirrorNeurons)

Motor
execution
M1

F5mirror
F4

Motor Program(Reach)Objectlocation
MIP/LIP/VIP

Figure 7.1 The MNS model repartitioned to show the focus of this chapter. The grey background marks area ofinterest

7.2

The link between the mirror neuron system and grasp learning

To our knowledge, up to now, all research on the mirror system has focused on the operation of amirror system with the implicit assumption that it is developed for higher-level tasks (such as
understanding and imitation), without exploring the possible biological precursors. MNS (Chapter 3)
showed how observation of self-action may serve as the learning stimulus for shaping the mirror
neuron system but did not address the issue of why the brain might contain such learning hardware.
The standard answer is that it is there to help the animal recognize the actions of others by means ofsome similarity to its own actions. However, we wish to explore the hypothesis that the mirror system
can best be understood through exaptation of a system for visual feedback control for manual actions.
For a reaching task, the simplest visual feedback is some form of signal of the distance between
object and hand. This may suffice for grabbing bananas, but for peeling a banana, feedback on the shapeof the hand relative to the banana, as well as force feedback become crucial. The parameters that areneeded for such visual feedback have the ingredients of the hand state we used in MNS. We do notclaim that the hand state we defined exists in the brain but we do claim that such hand-object relations
must be represented in the primate brain. There are studies where neurons sensitive for observation ofhands approaching to the points of attention or fixation have been found (Siegel and Read 1997). Also
there are studies suggesting that the monkey parietal area have an allocentric representation of object
locations, which simply indicates that the distance between objects can be encoded in parietal cortex(Murata 2000).
With Learning to Grasp Model (LGM) (Chapter 5), we showed that it is possible to learn to generate
grasping movements based on available affordances. LGM is capable of generating precision grips, but
it does not have the machinery to visually servo the fingers to their targets on the object. In other words
LGM learns to generate grasp plans for open-loop control. We suggest that a visual feedback systemdevelops in area F5 augmenting the LGM grasp machinery. The fundamental idea is that LGM

119bootstraps F5 visual servo system by presenting examples of suitable grasps that trains the feedback
system. In this chapter, we present two possible organization of the manual visual servo circuit andperform simulations using one.
Here we do not use the control term strictly. It should be understood that the command sent fromarea F5 are higher level than the control command sent to actuators of a robot. In fact, in robotics the
proposed area F5 output would be considered as a trajectory plan for grasping which specifies the
kinematics aspects of the grasp but leaves the dynamics to the lower levels. In the next sections, weaddress the dynamics of the reach and grasp by giving a 2D model of grasping. It is known that F5
projects directly via the corticospinal tract to motoneurons that control finger muscles (Dum and Strick1991), these connections are not enough to perform a grasping action as the lesion of the primary motor
cortex (F1) completely disrupts the grasp execution (Fogassi et al. 2001). Therefore, our assumption thatthe premotor controller outputs are higher-level signals (in the sense that they require a subordinate
layer to interpret them) is in fact supported by neurophysiology.

7.2.1

Two Visual Control Hypotheses

Currently, there is no hand kinematics data synchronized with F5 firing. Therefore, it is notpossible to reliably assert the roles of different neurons in area F5. Nevertheless, we propose two likely
control structures for area F5. The first one (Figure 7.2) postulates that F5 canonical neurons mediate thecontroller development by priming or gating mechanism such that controllers are differentiallyassociated with different affordances relayed by AIP. F5 neurons that are recruited by F5 canonicalneurons form multiple feedback and feed-forward controller pairs (motor schemas or modules) andpartition the task space with inter-module competition and F5 canonical guidance.
Area F5
Object recognition
IT

Object features

Visual Cortex

cIPS

Hand shaperecognition& Handmotiondetection
STS

Gating/biasing

Objectaffordance
extraction
AIP

F5canonicalObject affordance hand state
association
7b

Feedback
commandF5motor-only+

Feed-forward
CommandHand-Object
spatial relation
analysis
7aF5mirror
F4

Motor
Program(Reach)Motor
execution
M1

Objectlocation
MIP/LIP/VIP

Figure 7.2 One alternative visual control structure for manipulation is shown within the MNS framework. The
mirror neurons generate feed-forward commands

The complexity of each module depends on the number of modules that share the task. If thesystem to be controlled is complex, it is beneficial to have modularity, as a better overall control

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performance can be achieved with controllers specialized for each separate task than with a single
super-complex controller for all the tasks. Wolpert and Kawato (1998; Haruno et al. 2001) proposed themultiple paired forward and inverse models for this kind of control scheme. Figure 7.2 expands the MNSmodel in accordance to this view. Note that the F5 neurons are now, split into three: canonical, mirror
and motor-only. The motor-only neurons send transient feedback commands to correct ongoinggrasping movements while the F5 mirror neurons provide the motor command to achieve the final
hand configuration or intermediate configurations as the subgoals of a grasping task. In the second
alternative control structure (Figure 7.3), feed-forward command is generated by canonical neurons,
and mirror neurons are implicated in feedback control of grasping.
Area F5
Object recognition
IT

Object features

Visual Cortex

cIPS

Hand shaperecognition& HandmotiondetectionSTS

Object affordance hand state
association
7b

Hand-Object
spatial relation
analysis
7aF5canonicalFeed-forward
command

Objectaffordance
extraction

F5motor-only
Feedback
commandAIP+
VisualManualControl Error
F5mirror

Motor
Program(Reach)Motor
execution
F1

F4
Objectlocation
MIP/LIP/VIP

Figure 7.3 Another alternative visual control structure for manipulation is shown within the MNS framework(compare with Figure 7.2). The mirror neurons generate feedback commands

In both alternatives, the visual control task is to
1. Compute a visually defined error based on the current state and the desired state
2. Generate a command to reduce the error
From a developmental point of view, the questions one might ask is what the error and the desired
state for the newborn are. Can we assume that from birth the circuits that compute visual error (e.g.
distance to target) exists in the primate brain? We argue that the answer is negative and postulate thatan LGM-like circuit trains the manual visual feedback control circuit. In intuitive terms, the animallearns how a successful grasp looks like by observing the performance of LGM-like circuit. Assuming
the animal learns to extract desired state in visual terms by observing LGM,22 we can study how neuralcircuits in area F5 may use this signal to function as a manual visual servo circuit. For example, for the
precision pinch schema, the desired state could be the contact of index and thumb fingers on the object
22 A desired state, given an object, could be simply a look up table of visual descriptions of a hand grasping theobject121

surface. The manually defined Hand State (Chapter 3) that monitors the relation of the hand to theobject could serve as the desired state. However, in the general setting, we assume that the desired stateis learnt from LGM based grasps.

7.2.2

Mirror neurons in feed-forward control (alternative I)

Figure 7.4, illustrates the basic manual visual feedback control circuit we propose for the structurethat posit mirror neurons as feed-forward command units. The canonical neurons act as gating units;
they select the appropriate feedback and feed-forward pairs based on the objects to be grasped. Basedon the F5 neurophysiology, we can suggest that there exists a single controller module (schema) for
different type of grasps (e.g. precision, power etc.).
Learning a visual servo based on LGM performance(closed loop grasping)

Hand andobjectLearning to Grasp Model (LGM)(open loop grasping)
SI (grasp feedback)

Affordance input
Feed-forward control

Hand configuration

Feed-forward
command [inverse
model]

Reinforcement
learning

LGM layers

hand

F5mirror
DesiredState

Visual Processing(STS/PPC)(supervised)learning the
successful grasps’
visualrepresentation

Current
State

Desired Stategeneration(lookup table or NN)

Feedback control

Feedback error learning

Stochastic Feedback
Controller

Change in handconfiguration
Changein handconfiguration

Lower Motor
Centers)

F5motor-only
Gating (responsibility
detection)

Hand

F5canonicalF5 F5/F4/F2

F1

Figure 7.4 The feedback and feed-forward control view of the F5 grasping circuit, alternative I: F5mirror
neurons learn to generate feed-forward command. The desired state is assumed to be available and is converted
to a correction motor command by F5motor-only units using stochastic gradient descent. F5canonical neurons
gate the feed-forward and feedback pairs.

The feedback controller receives the desired state and the current state. The aim of the servo circuit
is to generate signals (for simplicity we will assume the signals determine change in handconfiguration), such that the new state gets closer to the desired state. Note that we don’t define thestate. For MNS model, we defined a common state (hand state of Chapter 3) which could be used for all
the grasps that are accounted, which may not be a parsimonious choice for the brain. Here each module
may learn its own state. In intuitive terms, it means that each module, for its input can use the aspects of
the action they are in charge of controlling. The key point is that the state depends on the vision of thehand and the object. The simplest of such a state is the distance between the hand and the object, which isa good choice for a pointing task servo circuit, but a bad choice for a grasping servo circuit since it isclearly not enough to control a hand to perform a grasp action based on a single scalar parameter. Thereis psychophysical evidence that such visual servo systems do exist in man. Ghahramani et al. (1996) in a
psychophysical experiment, limited the visual feedback of finger position at one or two locations in theworkspace, where a discrepancy was introduced between the actual and visually perceived finger
position. The remapping induced changes in pointing task were largest near the locus of remapping and122decreased away from it. This pattern of pointing disturbance suggests that visual feedback is used by
the reach related visuomotor circuit of human during pointing.

7.2.3

Mirror Neurons in feedback control (alternative II)

Figure 7.5, illustrates the basic manual visual feedback control circuit we propose for the structurethat posits mirror neuron involvement in feedback control. The outputs of mirror neurons are converted
to motor commands by F5motor-only neurons. The feed-forward command is generated by canonicalneurons. Note that the output of mirror neurons cannot be interpreted as a feedback command in atrivial manner. Most mirror neurons increase activity during the approach phase where the grasp error isdecreasing. It can be argued that such neurons do not affect the overt movement because their targets inarea F1 are inhibited. Another explanation could be that the mirror neuron activity works via inhibition,
however this is unlikely because the microstimulation of F5 triggers movement. We propose that mirror
neurons, at any given instant, keep an error map based on their preferred action (e.g. precision grasp)
and visual stimuli.
Thus, the mirror neurons provide the feedback error (for their preferred actions), on which a
feedback command can be generated. It is up to some other neuron population (e.g. F5 motor-only
neurons) to produce a corrective command based on the population of mirror outputs relevant for theobject to be manipulated.
Learning a visual servo based on LGM performance(closed loop grasping)

Hand andobjectFeed-forward control
Feed-forward
command [inverse
model]

Learning to Grasp Model (LGM)(open loop grasping)
SI (grasp feedback)

Affordance input
Hand configuration

Reinforcement
learning

LGM layers

F5canonicalFeedback control
Visual Processing(STS/PPC)(supervised)learning the
successful grasps’
visualrepresentation

Feedback error learning
Current
error
Current
State

Convert visual error signal
to feedback command

Change in handconfiguration

Lower Motor
Centers)

F5motor-only

Error map generation

Hand

F5mirror
F5 F5/F4/F2

F1

Figure 7.5. The feedback and feed-forward control view of the F5 grasp circuit, alternative II: F5mirror neurons
learn to compute the error. The error is then converted to a correction motor command by F5motor-only units.
F5canonical generates the feed-forward command signal.

7.2.4

The target of implementation

We based our choice on the following observation. If F5 mirror neurons were lesioned in‘alternative I’ (the visual servo circuit that employs mirror neurons as feed-forward elements -Figure7.4), the model would fall back to feedback only mode and could perform the action but with the lack ofsynergy of having the target configuration (the feed-forward signal). Analogously, it has been shownthat inactivation of F5 mirror neurons in the monkey does not abolish the grasp but merely slows it. On
the other hand, when F5 canonical neurons are inactivated the grasps that require precision cannot be
executed. This agrees with ‘alternative I’ that F5 canonical neurons select the modules to be used in the123grasping tasks where precision is required (so that a feedback control is necessary). Therefore, we
favor F5 control structure that assigns the mirror neurons the role of feed-forward motor command
generation23(Figure 7.4).

7.2.5

The visual servo task

In the next section, we propose a biologically realistic visual feedback circuit that can work as anautonomously visual servo circuit for reaching and grasping. It must be noted that, the computational
background for this task is well established in robotics, although we do not use it here because of
biological implausibility. The required change in controller output (change in hand configuration) inorder to get closer to the desired state can be achieved using resolved motion rate control techniquesfrom robotics (Klein et al. 1995; Whitney 1969). The computation requires the determination of an input
dependent matrix to convert the (desired state-current state) vector direction to the correct gradient tobe followed by the control output. Once the module learns this relation, the hand configuration changes
for the precise positioning of fingers becomes possible. The visual servo circuit that will be presented
follows the gradient stochastically. However, stochastic or deterministic, the gradient following requires
constant monitoring of the hand and object to calculate the instant configuration changes.
It can be beneficial to determine the target configuration with one-shot computation (feed-forward
control). Adopting the ‘alternative I’ (discussed in section 7.2.4), we involve mirror neurons in
performing the feed-forward control function; that is given an object and hand in action the mirror
neurons report the hand configuration required to achieve a grasping configuration. Once the mirror
system has learned an action the animal can act faster, more accurate and in a more robust-toperturbation fashion using both feed-forward and feedback control outputs.

7.2.6

The feed-forward model learning

The feed-forward controllers are trained by observing the successful grasps performed by the
feedback controllers. The Reach and Grasp schema of Chapter 3 used inverse kinematics techniques for
implementing the feedback controller. There the desired states were defined differently for each grasp
type. The desired state information was defined algorithmically. With the LGM, we are one step ahead.
While LGM learns and performs exploratory grasp plans, the feedback controller(s) can learn thedesired states (successful grasp plans, even if rare) and the relation of input (visual) states to the output(motor) commands. Then, the learning in the feed-forward controllers can be accomplished in abiologically plausible way using feedback error learning (Gomi and Kawato 1993) since the error isreadily available as the output of the corresponding feedback controller. One alternative to feedback
learning is using ‘distal learning’ (Jordan and Rumelhart 1992) approach where first the forward modelis trained and then the inverse model is trained using the error that is propagated backward throughthe forward model. However, distal learning is less biological because of the error back propagation.
This relates our discussion to the multiple paired forward and inverse model architecture introduced by
Wolpert and Kawato (1998; Haruna et al. 2001).

7.3

Implementation: F5 manual visual control circuit for 2D arm

This section presents the visual control circuit implementation outlined in Figure 7.4. The next
section, focuses on the feedback controller module of Figure 7.4 and present a biologically plausiblemodel in the sense that it can be implemented by leaky integrator units. We sidestep the complexity of
23 However the activation of mirror neurons, as spelled in the next sections, is based on an explicit error map thatcoincides with the alternative structure’s (Figure 7.5), with the exception that the error metric is manually chosen,
not learned as it would be in the alternative structure.

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the 3D arm that we used in earlier chapters by switching to a 2D arm model, but we require thesystem to learn the reach component as well as the grasping component. In Chapter 6, we have seenthat learning the affordance-grasp associations produced selective populations for different grasps.
Here without loss of generality, we limit ourselves to precision pinch grasps and study the control
aspects based on kinematics properties of the reach and grasp movements.
Specifically we
1. Present a visual servo circuit using leaky integrators that can reach and grasp (section
7.3.1)
2. Propose a memory based feed-forward module and expand (1) into a feedback and feedforward control system (section 7.3.4)
3. Present simulation results demonstrating that (1) is effective
4. Present simulation results with a dynamics model of the arm showing that (1) and (2)improves controller performance
The results (3) and (4) are meant to convince the reader that the proposed visual controller basedon leaky integrators (feedback) and memory-based neural units (feed-forward) is adequate as a visual
servo circuit. The readers interested in the main results concerning the mapping between the mirror
neurons and the controller can skip to section 7.4 where we compare feed-forward units activity withreal mirror neuron recordings.

7.3.1

A leaky integrator model for F5 manual visual feedback circuit

For a feedback controller system, a desired behavior or an error signal showing the deviation fromthe desired behavior is required. For the grasping the desired behavior, is grasping the object. In thismodel, we assume that the visual error signal is available for defining the how close the hand is to its
final grasping configuration. A neural circuit can learn to generate the error signals based on theobserved successful grasp examples. However, we do not model the learning of error signal generationand concentrate on how the error signal can be used to perform feedback based grasps.
From a computational point of view, the visual error signal has to be converted into motor error todeterministically control the behavior of the system. In this model, we take a stochastic gradientapproach where the system determines its control output based on the commands it has sent in theprevious time steps. One of the goals of the model is to give a simple but autonomous neural circuit thatis open to neural implementation. Therefore, we avoid computations requiring programming constructs
such as if-then, but instead use differential equations to describe the system. Figure 7.6 shows theschema level view of the feedback controller. The visual processing encapsulates the process of
extracting a visual error based on the vision of the hand and the object. Lower Motor Centers
encapsulates the functionality involved in transforming the motor signal sent by the feedback controller
into neural signals sent to muscles. In later sections, we augment and detail the circuit to include thefeed-forward modulel.

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Visual Feedback
Controller(change in) handconfiguration

Lower Motor Centers

Extrinsic
error signal

hand

Visual Processing

objectFigure 7.6 The schema level view of the feedback controller. The visual processing encapsulates the process of
extracting an error based on the vision of the hand and the object. Lower Motor Centers encapsulates thefunctionality involved in transforming the motor signal into actual commands sent to muscles

The feedback controller sees outside world through its input (the extrinsic error signal) and affects
the environment through its output (the change in behavior) signal. For the task of grasping, we define
the output as the change of joint angles in the arm-hand.
The error signal is taken as the distance of the fingers used in grasping to the target location on theobject. In general, an object affords multiple grasps. However, the multiple affordances are not aconcern here since Chapter 5 showed how a menu of affordances can be formed and selected (see also
Fagg and Arbib 1998 for prefrontal influences on grasp selection) based on the object affordances. The
hand/arm model is a planar one and comprised of three links, a thumb with 1DOF an index finger with
2DOF. We only consider precision type grasp with varying aperture sizes24, which is defined by two
points on the object as targets for the fingertips (see Figure 7.8). The error signal25 is then, a fourdimensional (two planar coordinates) and the output is a five-dimensional (five joint angle changes)
vector. The computational elements we use are biologically realistic (e.g. integration, summation andshunting). We use leaky integrators as neural units. The representation we use is rate coding. The
output of a leaky integrator unit defines single parameter in contrast to the population coding we used
before. However, we can use single units without loss of generality because in theory we can expand aunit’s activity to a population activity and apply the single unit equations to a population with proper
weight coefficients. Figure 7.7 presents the detailed circuitry of the feedback controller module. The
figure represents the differential equations and the operations in a schematic form. The output of the
feedback controller is the change in joint angles (∆q), and the error signal that drives the circuit is thesum of the distances of the fingers to their targets (e(t)). The working principle is based on stochastic
gradient descent. The network tries a random move; if the move was efficient in reducing the error thenit is more likely to make a similar move. If it was a bad move, the movement is backed up. Although thestochastic gradient method is algorithmically very simple, it requires some care for implementing it as aset of differential equations. The merit in implementing an algorithm in terms of leaky integrators is toshow that the computation can be implemented in the brain. Once this is shown, the algorithm can be
encapsulated and used as a computational block (schema) in designing other brain circuits much like24 The simplifications we make in this chapter does not decrease the value of the message we would like tocommunicate to experimentalists. The point of this chapter is not to show the object selective properties of the F5neurons, but to study the temporal aspects of grasping.
25 The feedback circuit uses the Euclidean norm of the error signal while the vector form is used by the feed-

forward module

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the winner-take-all circuit (see Arbib 1989, chapter 4.4 for a leaky integrator implementation andmathematical analysis).

e(t)Extrinsic
error signal

+

∆e+

+

∫

-

∆e-

N

∫

Nfire

P

∫

Pfire
∆qr

randomperturbation

Absolute valueof the net input∆qp∫

Stochastic unit;
outputs 1 withprobability sgn(input),
0 otherwise

-∫

∆qn

+
+

Change in handconfiguration∆q+

Multiplicative gating
Corollary discharge

Figure 7.7 The leaky integrator implementation of the feedback circuit that solves the inverse kinematics
problem for precision grasping. See text for the explanation

The key stochastic elements of the circuit are the firing of the units P and N (random perturbation
can be considered as a background noise). The units P and N are leaky integrators where P follows thevalue of ∆e-(t), whereas N follows ∆e+(t). The variables ∆e-(t) and ∆e+(t) keep track of the change in error.
If the recent commands increased the error ∆e+(t) charges up, whereas if the recent commands
decreased the error ∆e-(t) charges up.

dP(t )= − P(t ) + ∆e − (t )dtdN (t )
τ= − N (t ) + ∆e + (t )dtτBoth parameters ∆e-(t) and ∆e+(t) are non-negative and have zero resting potential level. The change inerror is monitored with auxiliary parameter edelayed(t) which follows the error with a lag determined by
the time constant κ.

de(t ) delayed= −e(t ) delayed + e(t )dt11∆e + = e(t ) − e(t ) delayed + e(t ) − e(t ) delayed2211∆e − = − e(t ) + e(t ) delayed − e(t ) − e(t ) delayed
2
2

κ

(

)

(

)

At any instant, Pfire(t) and Nfire(t) are either 0 or 1 corresponding to the firing of the units P and N
respectively. The probability of each unit’s firing is determined as the following.

127

1
1 + e − βN ( t )1
Pr( Pfire (t ) = 1) =1 + e − βP ( t )Pr( N fire (t ) = 1) =β is the steepness parameter determining how quick the circuit is likely to respond to a change in error.
This parameter is not critical; however, we empirically found that setting it to a high value (~100) resultsin fast convergence. One noticeable fact is that, unlike many stochastic units (Hertz et al. 1991), theprobability is always greater than 0.5. The output of P and N units gate the three channels ∆qr, ∆qp, ∆qn
that sum up to give the net ∆q. These are defined as:∆q r (t ) = random − perturbation∆q p (t ) = Pfire (t )∆qold (t )∆q n (t ) = N fire (t )∆q old (t )The ∆qold keeps a history of the net output of the controller (∆q) with a time constant of ς.

ς∆q old (t )= − ∆q old (t ) + ∆q (t )dt

The net output is simply given by the summation of three sources. Note however that ∆qn is nonnegative and therefore its effect is reflected with a negation.

∆q(t ) = ∆q r (t ) + ∆q p (t ) − ∆q n (t )The net output intuitively interpreted as the following. If both P and N fired at the same time, claimingthat the error both increased and decreased, the net output is mainly determined randomly (by ∆qr). If
N fired but P did not fire, meaning that it is likely that the error was increasing due to recent
commands, then we try to undo the last commands (-∆qn). On the other hand, if the error was
decreasing (P fired but N did not fire) then we try to repeat what we did before. The final case is whenneither N nor P fires, which results in a random decision (∆qr).

7.3.2

Simulation: visual feedback control with leaky integrators

We implemented the proposed circuit using Matlab. For this section, the arm was implemented asa kinematics chain without dynamics. The reason was we wanted to avoid the coupling of the dynamics
of the arm with the feedback circuit’s internal dynamics. However, in later sections we introduce
dynamics as well. For solving the differential equations that define the circuit, we used Euler
integration with time step 0.01. The command is sent to (and in the kinematics case, applied
immediately to the arm’s configuration) at each 0.1 time units.

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Figure 7.8 Three grasping tasks executed by the feedback circuit proposed shown on the upper half of the
figure. The change of arm/hand configuration during the execution is illustrated by snapshots of the arm/hand.
Each hand figure is accompanied (lower half) by the error plot. The grasp execution is stopped (success) when
the sum of finger distances to their target was less than 2mms.

The Figure 7.8 show some example grasps performed together with the error plot. Each tick in thetime axis of the error corresponds to 0.1 time units. For example, the leftmost grasp required less than
100 commands while the rightmost harder grasp required more than 300 commands. The rightmost
grasp is harder because on the way to the target there are local minima to be overcome.

7.3.3

Simulation: feedback and lower motor centers

From a control theory point of view, it is important to ask the question how the lower motor centerswill work with the feedback circuit we proposed. To answer this question we first need to implement a
dynamics model of the arm and then design a motor controller, which tracks a given trajectory.
Simplest such a controller is a PD controller with suitable gains. Note that we implicitly assume that PD
controller is encapsulated in the lower level grasp schema that we have postulated to receive the outputof the visual servo output signals. Figure 7.9 shows the control system we implemented. For the arm,
we assumed that hand’s contribution is negligible and set the upper limb length as 0.25 meters andweight as 4kgs, and the distal limb length as 0.35 meters and weights as 3kgs. Assuming cylindricallinks and homogeneous mass with no gravity the 2D arm dynamics can be given by (Sciavicco andSiciliano 2000):τ 1 
 q&&1  q&1 τ  = M q&&  + F q& 
 2
 2
 2
Where M is the inertia matrix and F is the matrix of Coriolis and centrifugal forces. Note that we don’t
include a gravity term since we assumed no gravity.q1 and q2 are the joint angles of the shoulder and129

the elbow respectively. τ1 and τ2 denotes the corresponding torques. Single and double dot notationrefers to usual first and second time derivatives. The inertia matrix and the matrix of Coriolis andcentrifugal forces are given by: m1l12 + m2l22 m1l12 + m2 (4l12 + l22 + 4l1l2 cos(q2 ))
+

12
4
M =
2
2
m
l
m
l
l
l
q2 ))
(
+
2
cos(
2
2
2
2
1
2

+

12
4
m l l sin( q2 ) − q& 2 − (q&1 + q& 2 )F = 212
 q&

0
2
 1


m2l22 m2 (l22 + 2l1l2 cos(q2 )) 
+

12
4

2
2
m2l2 m2l2

+

12
4

The PD controller loop has to be faster than the visual feedback controller loop. Otherwise, the PD
controller will not be able to track the desired joint angles specified by the visual feedback controller. In
our simulations, we used 250 Hz. for the PD controller loop and 10 Hz for the visual feedback servo.
PD controller

τ

Limb

Intrinsic error
signalVisual feedback
Controller

q_desired+-q_actual

Extrinsic
error signal

Figure 7.9.The Visual feedback circuit generating desired trajectories for the ‘lower level motor centre’(implemented as a PD controller)

The cycle rate of the PD controller becomes more important when tracking high-speed trajectories.
The PD gains can be selected to reduce tracking error, but the cycle rate of the controller brings alimitation on that also. In this simulation, the position gain was chosen as 30 and the velocity gain waschosen as 10. In Figure 7.9, this speed effect can be observed. The bottom half of the Figure 7.10 shows
the tracking error and the followed path when the action took 2 seconds whereas the upper half shows
similar graphs when the action took 0.5 seconds. When the action was slow, the combination of visualfeedback circuit and the lower motor centers can work well (Figure 7.10, lower half). However, forhigher speeds the circuit is not very effective for precise guiding of the hand (Figure 7.10, upper half).

130

Figure 7.10 The slow (2 seconds) (lower half) and fast (0.5 seconds) (upper half) performance of the ‘visualfeedback servo’ + ‘PD controller’ system is shown. The right hand side graphs show the tracking error (of thewrist) versus time. In the slow case, the object can be grasped but in the fast case, it is missed

It is desirable to generate desired trajectories in ahead without requiring a correction afterwards. In
our simple visual feedback controller the system has to make a move; if it is not good it has to undo it
and perform another move and so on. The desired trajectory produced in this way is not very smooth
and would suffer from the feedback delays in a real robotics or biological system. The system we had
could work pretty well (Figure 7.10) because we assumed the feedback signal has no delays. Having
only the feedback signal as the corrective mechanism has severe consequence on the controller
performance when there is delay in feedback loop. To overcome this we can use a feed-forward
controller and issue the right command without requiring the feedback signal. The perturbations thatcannot be accounted for (external perturbations for example) have to be still taken care of by the
feedback controller. In the next section we augment the visual feedback servo circuit with a feedforward module addressing one of the important elements of the visual control of grasping circuit we
proposed (Figure 7.4) and show how the feed-forward units can behave as mirror neurons.

7.3.4

F5 Feed-forward visual control and mirror neurons

In this section, we augment the feedback controller of the previous section with a feed-forward
module. The feed-forward module is formed by neural units that are selective to visual grasping errors.
During any grasping action a number units activate based on their match on the object-hand relation.
The one that fires maximally specifies the current feed-forward command. We define the feed-forward
command in the visual control framework and introduce the mirror neurons as candidate for feedforward command formation.
We present our design of the circuit and present simulations performed using the planar arm/hand
we used in the previous section. Importantly we take a bold step and try to establish a link between F5
mirror neurons by comparing the activity of real F5 neurons with the simulated feed-forward units.

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7.3.4.1

Mirror neurons, inverting actions ?

The natural way to construct a feed-forward controller is to invert the controlled plant. If the plantis characterized by x=f(u), where x is the behavior of the system and u is the command used tomanipulate the plant, then if we can compute26 f-1(x) we will have a perfect feed-forward controller,
because the analytic relation u=f-1(x) unambiguously tells us what command u is required to achieve adesired behavior. Now let us motivate why F5 mirror neurons can be involved in such an inverse
computation. We know that F5 mirror neurons that are involved in encoding motor plans are activatedby the observation of similar actions (Gallese et al. 1996; Rizzolatti et al. 1996a). An inverse computation
in a visuomotor task is intuitively defined by: ‘given a visually defined desired behavior what is therequired motor representation?’ Thus, if the mirror neuron activity represents some part of a motor plan
then we can view them as elements of a feed-forward control system. Assuming a visual feedback
controller exist as we described in the previous section, then even without F5 mirror neurons we can
expect to have visual control of grasping with limited degradation (especially in slow movements thedelays in feedback becomes less severe). Indeed, in the study of (Fogassi et al. 2001) even though thegrasping movements were not abolished when F5 mirror neurons were inactivated, there was a slowing
in the grasping movements but the hand reaching and preshaping were intact. Although we argue infavor of F5 mirror region’s being an inverse model we need to emphasize that a single mirror neuron
itself cannot be an inverse model for a visual control task since the single neuron activity of a neuron ismuch too variable to encode a precise action. The activity of mirror neurons can be strictly selective forthe type of the grip used (e.g. precision or power grasp) or broad (Gallese et al. 1996; Rizzolatti et al.
1996a). If the mirror neurons encode motor plans, the plan must be represented in a distributed fashion.
Now we turn back to our visual controller and specify the possible input output parameters for the
feed-forward controller, which we advocated F5 mirror neurons for. In the simple grasping world we
defined, a feed-forward command would specify the (change of) arm configuration (the joint angles)
given the visual information about the object and the hand. The nature of the visual information
deserves some comment. The intrinsic grasp related object properties (affordance) are relayed to area F5
via AIP, which is reciprocally connected with F5 (Matelli 1986). The object location information can berelayed to area F5 via other parietal regions such as VIP (Duhamel et al. 1998; Colby et al. 1993a) or
premotor regions such as F4 (Fogassi et al. 1992; Fogassi et al. 1996). For grasping it is likely that area F4
and F5 work together with F4 being involved in the reach component and F5 in grasp component. Also
there is evidence that F2 may be involved in controlling wrist rotations (Raos et al. 1998). However, in
our simple grasp world we assume without loss of generality, that our inverse model specifies the fullarm configuration without explicitly making a task division over mentioned possible premotor regions.

7.3.4.2

Inverse kinematics and requirement for local representations

From a computational point of view the task of feed-forward command is simply stated as finding
the inverse mapping of f(u), which is the forward function describing how the plant behaves with given
command u. Our case f(.) function is referred as the forward kinematics mapping and f-1 is called theinverse kinematics mapping. Mathematically speaking f-1(.) may not exists because f(.) need not be oneto-one, that is f(u1)=f(u2) does not necessarily imply that u1=u2. In this case, the manipulator (e.g.
arm/hand) is called redundant. Even our simple arm/hand is redundant. To see this, simply note that thewrist can move without breaking the finger contacts on the object during a two-finger pinch. In theliterature there are many techniques to solve the inverse kinematics problem (Flash and Sejnowski 2001;

26 The inverse may not exist, which is one of the difficulties in learning a inverse model.

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Klein et al. 1995; Whitney 1969). In a redundant system, the inverse kinematics problem can besolved by introducing an extra optimization criterion such as minimum energy and shortest distance.
The commonly used resolved motion rate control (Whitney 1969) methods rely on the matrix called the[r]

Jacobian of the forward kinematics which is composed of the partial derivatives ∂f / ∂qi of theforward mapping function. The Jacobian transpose, pseudo-inverse of the Jacobian (with null space
optimisation), and the extended Jacobian (Klein et al. 1995) methods are widely used in robotics andcomputer graphics for mapping the extrinsic coordinates into joint angles (Sciavicco and Siciliano 2000).
However, we are interested in solving the task using neuron like units rather than pure engineering
techniques. There is also a plentiful of robotics neural network literature on learning inverse kinematics
functions (Tang and Wang 2001; Oyama et al. 2001a; D'Souza et al. 2001; Driscoll 2000). The key point insolving the inverse kinematics for a redundant manipulator is to employ a modular neural network(Oyama et al. 2001b) or to use locally specialized learning methods such as Locally Weighted
Regression (LWR) (Atkeson and Schaal 1995; Schaal et al. 2002). The reason is that usually the inverse
kinematics function is not convex, thus the average of two solution points may not be a valid solution
point. A homogeneous non-local neural network (e.g. a back-propagation feed-forward neural network)
averages over two solution points when queried with a non-trained point (unless a negative data pointin the region of query is manually added to the training set to disable the ‘wrong’ averaging). The
simplest locally weighted algorithm is the memory-based LWR (Atkeson 1992; Atkeson 1989; Atkeson
and Schaal 1995).

7.3.4.3

Memory based visual feed-forward control

The feed-forward module for the visual servo circuit uses the memory-based learning with nearest
neighbour (Atkeson and Schaal 1995). The reach model of Rosenbaum et al. (1995) showed thatsumming over postures is not a feasible strategy (Rosenbaum et al. 1999). Thus, when querying a point
we do not apply a weighted sum as in LWR but simply return the nearest match with a winner–take-all
circuit. This ensures that we never have a wrong answer to a query. In their planar kinematics grasp
simulator Rosenbaum et al. (1999) used the same approach with the additional explicit constraint
satisfaction criterion.
The learning takes place in this fashion: when the hand is performing a grasp action servo-ed by
the feedback controller new F5 feed-forward units are allocated when the hand configuration is notsimilar to any configuration encountered before. The instantiation of the configuration is based on joint
angles (and visual gating signals). As a new configuration is stored its corresponding visual
representation is stored along with it.

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Hand configuration (SI- SII)
Visual Processing(extrinsic error)

F5 memory based
feed-forward layer

Lower Level
Motor Control
Figure 7.11 The F5 mirror neurons viewed as the memory based feed-forward controller. The arrows below the
sheet of neurons indicate outputs while the arrows coming above the sheet indicate inputs

A F5 memory unit is activated to the extent that the hand configuration and the visual error fall into
its receptive field. The activity signals what change must be done given the extrinsic error and thecurrent hand configuration establishing an inverse kinematics circuit. In this model, the lower levelapplies a winner-take-all process on the activity of F5 feed-forward neurons. The result is then used formovement execution (Figure 7.11).
To our knowledge, there is no experimental data 27 as to how a grasp plan is represented in
premotor cortex. Therefore, we are not claiming that the brain uses exactly these mechanisms; butrather we are proposing a distributed feed-forward module that can supply a feed-forward signal
complementing the feedback signal. However, when we show later in this chapter that it is possible toobserve unit activities that are similar to mirror neuron activities, we suggest that the mirror neurons
may be involved in encoding visually defined grasp errors. It should be understood that our modelingin this chapter is not intended to be a proof that the premotor cortex works as we modeled, but rather
an important message to experimentalists that quantitative experiments are necessary to pin down themechanism of grasp planning and execution.
Now let us look into the details of our representation for F5 mirror neurons. There are two kinds of
inputs to F5 mirror units: (1) the somatosensory cortex input that signals the configuration of thehand/arm. We capture this input as a vector of joint angles of the arm/hand: s=[q1,q2,q3,q4,q5]T(shoulder angle, elbow angle, thumb angle, index finger angle, index finger second metacarpal angle),and (2) inputs from the visual centers described as the following. The visual input to feed-forward units
is a five dimensional vector x=[dx1,dy1,dx2,dy2,γA]. The first four components are the parameters are theerrors signaled by the feedback loop, namely the distances between fingertips and their contact targets
on the object. The last component represents the affordance of the object. In this model, we use only thesize of the object as the affordance. The parameter γ controls the relative importance of the error and theobject affordance input. Note that γA parameter plays the role of a soft gating network. As weadvertised earlier, F5 canonical neurons may implement an explicit gating network based on visualobject properties (Murata et al. 1997a) for biasing F5 mirror units. In that case, only the feedback error
signals would suffice, which is in full accordance with the learning structure we offered in Figure 7.4.
However, for the sake of implementation we embed the gating mechanism into the error signal. It must
27 Except that the qualitative description of selectivity of canonical and mirror neurons.

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be emphasized that x is purely defined within an extrinsic space. Thus, it can be applied to selfaction as well as the actions of others. However when learning (storing of hand configurations) the
recruitment of new units to store a configuration is based only on intrinsic parameters (s vector). The
circuit continually monitors the arm it controls (i.e. online learning); if the maximum activation basedon s input of the units is below a threshold a new unit is recruited. The hand configuration activity si ofunit i, is computed simply as the length of the vector between s and si (|s-si|) where s is the current
hand configuration and si is the stored configuration i. Figure 7.12 shows the acquired configurations
during the simulations of this chapter for six objects. In a general system for satisfactory performance
many more units are required (Rosenbaum et al. 1995; Rosenbaum et al. 1999; Rosenbaum et al. 2001).

Figure 7.12 The arm configurations that were acquired during 6 object grasping actions are shown. Each of thesuperimposed configurations is represented by a unit in the feed-forward layer

We mentioned (1) configuration dependent activation and (2) vision based activation. Now weneed to explain the mechanism of inverse mapping, that is, how the given visual information is mapped
to a motor plan. At any instant, during a grasp action, the vision based activity and the handconfiguration based activity lights up some candidate configurations. The task is to pick one of the units
as the best candidate and return its stored hand configuration as the next target (as the joint angles). In ageneral framework, a sophisticated way of combining activated units would be employed as in LWR
methods. We speculate that the brain circuits must have a reinforcement type of learning circuit to learn
to pick a chain of hand configurations that will satisfy extrinsic constraints (obstacle avoidance) andintrinsic constraints (such as minimum energy). However for simplicity we offer a heuristic for selecting
a configuration that will enable the system to generate reasonable trajectories so that we can test thesystem’s control performance and look at the properties of the units that are acquired. Our heuristic is
to pick the unit that maximizes the activity function: g i = e− (α ( dx1 ,dy1 ,dx2 ,dy2 ) +λ q − qi )where α and λ areconstants controlling the relative contributions of the intrinsic and extrinsic signals. Here there is a
subtle issue: the minimum of g may not be a right plan because the error vector [dx1,dy1,dx2,dy2] isrelative to the given object. To circumvent this problem there are two possible mechanisms that can beapplied: (1) having a gating mechanism which biases the correct subspace of the error space based on
the object affordance (this is the task we offered for F5 canonical neurons), (2) having a forward model ofthe arm/hand kinematics that predicts the error vector if the unit were selected and use this predicted
error [dx1,dy1,dx2,dy2]’ in the computation of g i = e−(α ( dx1 ,dy1 ,dx2 ,dy2 )′ +λ q − qi ). It is suggested that bothgating and forward model strategy is employed in the human brain from cerebellar motor prediction to135social prediction (Miall and Wolpert 1996; Wolpert et al. 1998; Wolpert et al. 2001). For our
simulations the winning unit is selected using the latter approach (we use a non-neural forward model).

7.3.5

Simulation: trajectory planning and controller performance

Although it is a standard result that use of feed-forward signals improves performance we need to
first show that the distributed feed-forward system we proposed does not degrade but improves theperformance as expected.

Figure 7.13 The trajectory generation with feedback and feed-forward control is illustrated for comparison with
Figure 7.8 (feedback-only system). In the lower panel the error graphs are plotted as error versus iteration. The
error is the sum of squared distances of the fingertips to their targets. The rightmost object was not grasped in
the training (a novel object/location). Thus the system could not make use of the feed-forward signal,
approximately after iteration 25 and switched to feedback only mode, resulting in slower positioning of thefingers on the target locations

For comparison purposes, we tested the speed of the desired trajectory generation. Figure 7.13
shows the three grasps that are performed using the feedback and a trained feed-forward controller.
The discrepancy of the errors at time=0 for Figure 7.13 and Figure 7.8 is due to the initial finger
configurations of the hand (but the arm started from exactly the same configuration). In fact, the initialerror for the middle grasp is larger in Figure 7.13.
The feed-forward control introduction to the system reduced the time required to output a desired
trajectory command by about four times. This means that when we actually connect the system to thelower level motor servo we can achieve 4 times frequency that of a feedback-only system could achieve.
This effectively gives a higher range of the PD gains for the lower level motor servo.
The system learned online while it was performing grasps using the feedback and feed-forward
model learned so far. The leftmost two grasp objects in Figure 7.13 were included in the training; thus,
the error curve goes down very fast since the feed-forward command can take care of most of the task
(as it acquired an inverse map during training). However, the rightmost object was presented the firsttime to the model. The feed-forward module could make use of the earlier experiences until step 25,
only partially between 25, and 40. After that point, the feedback servo worked alone. Thus, the136generation of the trajectory was slower. We did not use the lower level motor servo to be able to
make a fair comparison with Figure 7.7 of feedback-only system. Figure 7.14 shows the complete
systems’, i.e. the feed-forward, feedback and lower level feedback motor servo performance all working
together.

Figure 7.14 The feedback, feed-forward and lower level motor servo and the dynamic arm was simulated all
together. Upper half: The grasp lasted 0.5 seconds. Lower half: the grasp lasted 2 seconds. The fast movement
error reduced with a factor of 6 while the slow movement reduced with a factor of 10 in terms (compare with
Figure 7.10)

The plots in Figure 7.14 use the same scales as Figure 7.10, for direct comparison. A high degree of
improvement is observed as expected. The slower motion trajectory can be followed with 1/10 times
and the fast motion with 1/6 times the error made with only feedback controller. The reason for the poor
performance of the feedback only control case (Figure 7.10) is that the generated desired trajectories are
not very smooth, which causes the PD controller to overshoot and follow the trajectory harder. In
contrast when using the feed-forward controller, the generated trajectories are smooth. Note that both
PD controllers of the lower level motor servo used the same PD gains (30 for position and 10 for
derivative gain). The values were manually optimized for the feedback-only system and it was notpossible to increase the gains further to achieve better tracking. In Figure 7.14 even with the feedforward controller it looks like the system did not achieve a satisfactory grasp. However, note that we
required the simulator to complete the grasp in the allocated time; the system completes the grasp after
the allocated time with a negligible increase in the error (not shown).
We mentioned earlier that having memory-based feed-forward controller may allow explicit
planning using the controller representation. Here we demonstrate this fact by a simulation. An obstaclein the workspace for example, can be encoded as simple inhibition over the feed-forward units that

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encode hand configurations that would result in a collision with the obstacle. Figure 7.16 shows two
grasp examples in the top row where the effect of the obstacle is zero (the obstacle is drawn forreference). In the lower level the obstacle inhibits the cost function associated with the units that would
bring the hand in the obstacle. Considering the limited range of motions available to move the arm fromits initial position to the target, we can suggest that the representation we proposed allows generation of
non-trivial trajectories that can be automatically acquired (in contrast to set by heuristics) once thesystem is equipped with a learning mechanism that can do the planning (e.g. reinforcement learning).

Figure 7.15 The top row demonstrates two trajectory-planning examples for grasping without obstacle. The
bottom row demonstrates how new trajectories are formed by introduction of an obstacle as a local inhibition on
the feed-forward controller units

7.4

Feed-forward unit activity and mirror neurons

In this section, we focus on the unit level activities of the feed-forward controller and introduce amethod to compare the electrophysiological recordings from monkey mirror neurons with our feedforward units activities.
First we look at the population level activity of the feed-forward (F5 mirror neurons) that we
introduced in section 7.3.4.3 during various grasp actions. Figure 7.16 shows the unit activities of four
grasps as area level plots. Each plot consists of 157 neurons acquired during the learning phase (therows). The columns represent the time (note that in general the grasp actions take different time steps
for different grasps). The left edge of each graph is aligned with the start of the grasp actions. The rightedge is aligned with the completion of the grasps. We can see that different units are activated at
different times depending on the grasp action. It must be emphasized that this map is based on only
visual information and mainly dominated by the error patterns that occur during a grasp action. It is
likely to have similar errors during different grasps unless the map is modulated by object affordances.
We used the object size as a soft modulator by including it in the error computation. How much object

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related information is actually encoded in such a map in the primate is a topic of future research forexperimentalists. Our predictions and experiment suggestions for object specificity is presented in
Chapter 6. Our goal here is to show that a visual error-based activation of units can lead to similar firing
patterns of mirror neurons.
1.0

0.5

0.0

Figure 7.16 The feed-forward unit activations for four grasp observations shown as unit versus time. Each graphconsists of 157 neurons acquired during the learning phase (the rows). The columns represent the time

The activity of a feed-forward unit corresponds to average firing rate of a real neuron. We can map
the average firing rates during an action (observation activity only) to actual firings (neuron spikes)
using a Poisson distribution model of a neuron. The Poisson distribution is the extension of thebinomial distribution to the continuous case. Under the Poisson encoding model the probability of aneuron generating r spikes during (t, t+δr) for encoding a parameter x is given by (Snippe 1996; Sanger
1996; Zemel et al. 1998):

Pr(r | x) = e −< f ( x )>< f ( x) > rr!

where <> denotes the average firing rate and f() is the response function (or tuning function) of theneuron which actually determines the average firing rate activity one computes using a non-spiking
neural circuit model28. Zemel et al. (1998) suggest that a typical tuning function is proportional to a
Gaussian:f ( x) = βe−

( x − x pref ) 2
2σ 2

where xpref denotes the input that best activates the neuron; x is the current input to the neuron and β isa proportionality constant and σ2 is the variance determining the receptive field size. We used this formof activity function for F5 feed-forward controller units. We set β=1 and empirically determined a single
σ2 (0.1) value for all the neurons in our simulations.
The feed-forward units activation (the average firing rate) is determined by the activation function
we have defined in section 7.3.4.3. However, note that intrinsic contribution is set to zero during anaction observation (i.e. the activity is purely visual during observation). This can be accomplished in the
primate brain by shunting of intrinsic input when the animal is not engaged in any motor act. Notingthat in section 7.3.4.3 we defined x=[dx1,dy1,dx2,dy2,γA]T we can write the probability of a feed-forward
units firing based on the units preferred stimulus xpref and the current stimulus x as the following.

t +δt

28 δt is absorbed in the expectation operator <>. Formally < f (t ) >=∫ g (t )dt where g(t) is the instantaneoustfiring rate.

r r
r r
−( x − x pref )T ( x − x pref ) /( 2 σ 2 )rPr( firing | x ) = e − e
e

r r
r r
− ( x − x pref ) T ( x − x pref )

139

2σ 2

Now we can convert our average firing rates plotted in Figure 7.16 into spikes and make (qualitative)
comparisons with real mirror neuron data. The mirror neuron data available to us does not allow
comparisons based on kinematics of the observed actions. Therefore, instead we try to spot feedforward units that have firing profiles similar to those available to us.

Figure 7.17 A mirror neuron recorded during a grasp observation. On the left the raster plots; on the right thehistogram. The recording data shown spans 2 seconds. In addition, the hand start to move approximately attime = 1 second indicated by the vertical bar at the centre of the raster panel (Rizzolatti and Gallese 2001)

Figure 7.17 shows a real recording from Rizzolatti lab (Rizzolatti and Gallese 2001; Umilta et al.
2001), which is displayed using the tool we have developed (Oztop 2000). The recording shown spans
two seconds and the end of the rasters are aligned with the experimenter’s touch of the object. We did
not include the holding phase of the recordings for the comparison because different processes may be
involved in holding, which we did not model. Figure 7.18 (lower panel) shows one of the feed-forward
module unit’s activity that is produced using the Poisson model described above. The generated spikes
are shown as raster plots and histogram for a direct comparison. The raster plots corresponds to actual
trials in the real experimentation (10 trials), however in the simulation we collected the average firing
rate information via a single trial and run the Poisson spike generation multiple times (25 runs) The
histogram bin width is selected as 20ms for both experimental and the simulation case. The mirror
neuron in Figure 7.17 (same neuron is also shown in Figure 7.18, upper panel) shows an interesting
behavior: first, the activity of neuron rises but before contact with the object, around half way of thegrasp the activity reduces again. This type of behavior is not very well understood. If this mirror neuron
were involved in understanding the meaning of actions as suggested in the literature (Rizzolatti et al.
2001a; Rizzolatti et al. 2000; Umilta et al. 2001), then one is tempted to ask the question, why the firing is
inhibited prior to contact. To our knowledge, there is no satisfactory answer to the question and no
published explanation of such mirror activity. Here we demonstrate that such an activity can begenerated as a by-product of the visual servo circuit (the feed-forward module) that we implemented.

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Figure 7.18 Top row: Real mirror neuron recording during a precision grasp. Bottom row: One of the feedforward controller unit’s responses to vision of a grasping action. In the left panels, each raster row corresponds
to a trial (Poisson spike generation for the model). The right panels show the histograms. The rasters aligned
according to the contact of the hand with the object

We now switch our attention to a more common mirror neuron that increases its activity as theaction observed is progressing towards completion, which is in support for the mirror neuron
involvement in understanding the meanings of actions (Rizzolatti et al. 2001b). We can find many units
in the feed-forward module, which mimics the activity of this type of mirror neurons with different risetime profiles.

Figure 7.19. The similarity of a real neuron and model unit is demonstrated. Left two panels real mirror neuron
rasters and histogram. Right two panels are the model generated rasters and histogram. A slow increasing
activity is observed in both cases

In Figure 7.19, we picked one, which matches a real mirror firing profile (also shown in the same
figure). Note that no parameter fitting was done; the parameters of the model and the Poisson spike
generation process were the same as in the previous example.
Next, we present an interesting mirror neuron profile, which we could not replicate withoutchanging the receptive field size parameter (σ2). This neuron was silent as the background activity andstayed silent when the experimenter started the grasping action (Figure 7.20, left two panels). Before
contact, it started firing vigorously and stopped before holding phase. As the very first neuron we havepresented we suggest that this neuron must be involved in some processes other than understanding
because of the similar reasoning. When we tried to find this kind of activity in our feed-forward control
module at first we could not find such sharp profile units in any grasp action observation. However,when we reduced the receptive fields of the units we could get similar activity (Figure 7.20, right twopanels) although the timing of such activity could not be replicated (the length of the silent time after
the burst). However, this could be because we require the grasp to be completed for the simulator case.

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The real mirror activity shown is only until the contact of the hand to the object. Inspecting Figure
7.21 indeed reveals that the final portions of the grasping action do not change the population activity.
Nevertheless, it is certainly too daring to claim that the mirror neurons use the same error space weused for the simple grasp world we implemented. However, we would like to suggest that mirror
neurons can be involved some visual error computation for visual guidance of the hand during
grasping.

Figure 7.20 Left: a sharp mirror neuron activity, which could only be replicated with our simulator by reducing
the receptive field. Right: Similar response profile obtained from one of the feed-forward module units

When we look at the population activity of the feed-forward units with the smaller receptive field
we see that the main characteristics are preserved, but the tuning of the units become stricter (Figure7.21). In the general case, each unit may have their own receptive field sizes, which can adapt withexperience. The unit shown in Figure 7.20 is marked with an ellipse in Figure 7.21. The unit was
activated strongly for a short period of time and declined its activity rapidly. A group of other neurons
became active after the decline.

Figure 7.21 The population activity of feed-forward units with smaller receptive fields. The feed-forward unit
we used to match the real mirror firing profile in Figure 7.20 is marked with an ellipse

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8

CHAPTER VIII: CONCLUSIONSThe scope for the dissertation was set in Chapter 3 where (1) the visual feedback control of manual
manipulation hypothesis of F5 neurons and (2) the view that infant grasp learning precedes the mirror
neuron development were introduced, and (3) the assertion that self-grasp observation trains the mirror
neurons during infancy was made. Our study took a schema based approach to address (1), (2) and (3).
First (3) was modeled in Chapter 3, focusing on the Core Mirror Circuit. The context for the circuit
was provided by the functional schemas we implemented without intending to address neural
localization. This enabled us to concentrate on the Core Mirror Circuit thoroughly and make testablepredictions.
The view (2) motivated us in developing the Learning to Grasp Models. Chapter 5 developed abehavioral level model of infant grasp learning, while Chapter 6 localized the circuit in monkey brain.
Both chapters produced nontrivial predictions that can be experimentally tested.
Finally, Chapter 7 attempted to realize (1) through simplified but nevertheless adequate (according
to the F5 canonical priming hypothesis) simulation studies. It was shown that units encoding
kinematics based errors, could yield mirror neuron like responses. This is in full accordance with thesuggestion in Chapter 3 that, the degree of conformity of the hand movement and preshape to the object
affordance must be represented as a distributed neural code. This code in its simplest form is akinematics error function which we have elaborated in Chapter 7.
We concluded our modeling tour of action recognition and visuomotor transformation by handing
neurophysiologists an extensive set of testable predictions and hypotheses, and equipping the modelers
who are interested in understanding the cortical mechanism underlying the action recognition andvisuomotor learning, with an excellent starting guide.

8.1

Mirror neurons

Chapter 3 studied how self-executed grasp actions can adapt the parietal and premotor
connections to shape F5 neurons into mirror neurons. We used schema approach for the Visual Analysis
and Reach and Grasp components of the Mirror Neuron System (MNS). Therefore, theneurophysiological predictions pertaining to MNS model could be gathered only from the Core Mirror
Circuit, whose output corresponded to the mirror neurons (see Figure 3.5).
The key to the MNS model was the notion of hand state as encompassing data required todetermine whether the motion and preshape of a moving hand may be extrapolated to culminate in a
grasp appropriate to one of the affordances of the observed object. A mirror neuron had to fire if thepreshaping of the hand conformed to the grasp type with which the neuron was associated. Weemphasized that the specific decomposition of the hand state into the specific components that we had
used in our simulation was not the crucial issue. In fact, we suggested that a distributed neural codethat carries information about the movement of the hand toward the object, the separation of the virtual
fingertips and the orientation of different components of the hand relative to the opposition axis in theobject must be represented in monkey parietal or premotor cortices. The crucial property of the code we
predict is that it would work just as well for measuring how well another monkey’s hand is moving to143

grasp an object as for observing how the monkey’s own hand is moving to grasp the object. This
allows the self-observation of the monkey to train a system that can be used for observing the actions ofothers and recognizing just what those actions are.
Experimental work to date tends to emphasize the actions to be correlated with the activity of eachindividual mirror neuron, while paying little attention to the temporal dynamics of mirror neuron
response. Our simulations make explicit predictions on how a given (hand state trajectory, affordance)pair will drive the time course of mirror neuron activity. For example, we have shown that a grasp with
an ambiguous prefix (e.g. using precision grip for a large object) drives the mirror neurons in such a
way that the system at first gives weight to the wrong classification, with only the late stages of the
trajectory sufficing for the incorrect mirror neuron to be vanquished (grasp resolution).
The grasp resolution prediction is testable and indeed, suggests a whole class of experiments. The
monkey has to be presented with unusual or ambiguous grasp actions. For example, the experimentercan grasp a section of banana using precision pinch from its long axis. Then we would expect to see
activity from power grasp related mirror neurons followed by a decrease of that activity accompanied
by an increasing activity from precision pinch related mirror neurons. Our other simulations lead todifferent testable predictions such as the mirror response in case of a spatial perturbation (showing themonkey a fake grasp where the hand does not really meet the object) and altered kinematics (performthe grasp with different kinematics than usual). We have also noted how a discrepancy between handstate trajectory and object affordance may block or delay the system from classifying the observed
movement.
In summary, we have conducted a range of simulation experiments – on grasp resolution, spatial
perturbation, altered kinematics, temporal effects of explicit affordance coding, and analysis ofcompatibility of the hand state to object affordance – which demonstrate that MNS model is not only
valuable in providing an implemented high-level view of the logic of the mirror system, but also
provides interesting predictions that are ripe for neurophysiological testing, as well as suggesting newquestions when designing experiments on the mirror system.
Chapter 7 investigated the manual visual feedback hypothesis asserted in Chapter 3 through asimplified hand/arm system. We concentrated on a single grasp type. However, this does not weaken
the impact of the analyses we conducted since Chapter 6 demonstrated, through explicit simulations,that grasp learning gave raise to emergent neural properties comparable to F5 canonical neurons, which
are thought to be involved in gating mechanisms, selecting the feedback circuit best suited for the object
to be grasped. To be more specific, after LGM had mastered grasp learning, when we investigated theneural responses of LGM layers we found units that are selectively active for specific object sizes andorientations. Thus, we concluded that these were the canonical neurons of LGM. In parallel, Chapter 7
hypothesized that F5 canonical neurons implement a gating or priming mechanism based on the object
affordance. For example, given a small object the LGM canonical neuron with small object preference
would become active (as part of its grasp planning task, as shown in Chapter 6) priming the visualfeedback circuit (a subpopulation of F5 purely motor and mirror neurons) that is best suited for thecontrol for small object grasping (e.g. the visual servo circuit that is specialized for precision grip).
Although not modeled, a learning mechanism is proposed for the gating mechanism as well. The
canonical neurons not only prime the F5 visual feedback circuit for grasp execution but also they prime
the feedback circuits for learning ensuring that the neurons in a particular circuit will learn to control
specific grasps that are directed to objects for which the canonical neuron has selectivity.

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8.2

Grasp learning: infant development

ILGM simulations of Chapter 5 showed that even without object affordance, a variety of grips,
including the precision grip, can be learnt by actively interacting with the environment predicting theresults of the study of Butterworth et al. (1997).
We showed that task constraints are influential in shaping the grasp repertoire of infants via the
cube on the table task, which together with other simulation results enabled us to make useful predictions.
To be precise, Chapter 5
1. Predicted that infants in the period of early grasping, can perform precision grasps
2. Showed that task constraints shape motor development supporting the view thatdevelopment of precision grips is mediated by task constraints.
3. Showed that object affordances could be represented in infants’ grasp repertoire in spite thefact that the grasp planning circuit was unable to access/extract object affordance
information. This result is important because it implies that tactile learning can train thevisuomotor learning in infancy.
4. Predicted (as a corollary to 3) that object (visual) affordances would be heavily represented
in the motor and sensory areas of cerebral cortex for objects that are manipulated often.

8.3

Grasp learning: monkey neurophysiology

The simulation results of emergent object selectivity in LGM and the analysis of what it takes tocombine movement parameters into a coherent whole for a successful grasp enabled us to produce
nontrivial testable predictions.
Specifically, we predicted that area F2 must be having visually triggered neurons that are selective
for object orientations. Furthermore, we suggested that the area must have control over wrist rotations. We
further predicted that F5 canonical neurons would have tuning fields according to the object
orientation, similar to AIP visual dominant neurons (Sakata et al. 1999). Therefore, we asserted that acloser examination of area F2 and F5 canonical neurons would reveal orientation selectivity either inisolation or in the form of gain fields over existing object selectivity.
We generalized the above prediction and proposed a systematic way of interpreting neuralactivities to amend the shortcomings of analyses based on behaviour and neural firing correlation
paradigm.
If some population of neurons were to specify a grasp plan partially (by being responsible for one
parameter of the plan), a learning mechanism had to exist for shaping the connections between regionsthat specify the complementary grasp parameters. This implies that in order to specify a grasp plan F5
canonical neurons must have ‘gain fields’ based on other brain regions’ activity (the ‘gain fields’ would,
behaviorally appear to be based on movement parameters). Let us review the hypotheticalexperimenter we introduced in Chapter 6 to present our proposed systematic approach.
If the experimenter finds out that area A is responsible for some aspect (wrist orientation) of acomplex movement (reach-to-grasp) and that area B is responsible for controlling some other aspect(reach direction) of the movement and if the activities of A and B are true control variables determining
the movement then we claim that
(1) The region A and B must be anatomically connected (the connection may be a multi staged one,such as A connected to C, C connected to B)(2) The synaptic strength of the connection between A and B encodes the movement generation(grasping) strategy of the grasping circuit

145(3) If it is found that the connection between A and B is unidirectional (say from A to B) then(from the viewpoint of the experimenters) the activity of B neurons must be tuned by the population
activity A.
(4) The verification of (3) can be used to decipher the organization of visuomotor transformation
circuit by recording simultaneously from A and B. If activity of A predicts the activity of B better thanthe other way round (i.e. activity of B predicts the activity of A) then the underlying principle is thatarea A selects movement parameters, and B, based on the selection of A, generates other movement
parameter(s) completing (or further specifying) the movement plan.
We hereby explicitly suggest a methodology to uncover the roles of premotor areas in reach-tograsp movements. For a true understanding of premotor function, we strongly suggest that the
premotor regions of F2, F5 bank (canonical neurons), F4 and wrist rotation encoding neurons of motor
cortex (F1) must be investigated with simultaneous recording experiments. A feasible experimental design
would be to set up sessions for pair-wise recording of areas F2, F4, F5 and F1, in which the monkey
would be asked to reach and grasp for objects at various locations with changing orientations. We claimthat the rigorous analyses of neural firing, kinematics of the hand and the object condition will reveal
the mechanisms of grasp learning and planning by showing the structural and functional dependency
of premotor regions in specifying grasp parameters.

8.4

Grasp learning: neural architecture

The crucial feature of LGM inherited from the architecture we developed in Chapter 4 was that it
could represent and produce a variety of grasp plans conditioned on input, effectively learning arepertoire of grasp plans. The reinforcement framework we adapted in Chapter 4 gives LGM theflexibility to include soft constraints in grasp evaluation such that the grasps that are not favorable (dueto discomfort, excess energy consumption, etc.) are eliminated or represented with low probability.
Thus the reinforcement signal of Chapter 4, (joy of grasping of Chapter 5 and neural grasp stability ofChapter 6) can incorporate the anatomical and environmental constraints which are important in shaping
grasp development (Newell et al. 1989). The reinforcement signal can be viewed as the adaptive value ofaction that shapes the movement repertoire through selection (Sporns and Edelman 1993).
The simulation results of Chapter 5 and 6 showed that the architecture we introduced wasadequate for grasp learning by producing testable prediction for both infant development and formonkey neurophysiology. We showed the neural network competency of LGM by demonstrating its
generalization ability over novel input conditions while retaining the property of representing multiple
actions for a given input.

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9

CHAPTER IX: FUTURE WORK

9.1

Simultaneous learning in MNS model and LGM

While infants learn how to shape their reaching movements into grasping actions, they also
observe the visual stimuli they generate. The main hypothesis of the MNS model was that the visual
stimuli from the successful grasps were used to train the mirror neurons. To this date, there is no study
pinpointing any stage in development when the mirror neurons start to function fully. Our suggestionis that the MNS learning and grasp-learning overlap. The amount of the overlap may have importantconsequences on the organization of the two circuits. A very early learning in MNS may result in mirror
neurons that respond to premature grasping actions, as the training stimuli will be based on thepremature grasping attempts. A very late learning may result in delayed visuomotor development in
the infant. The effect of the overlap amount must be studied via simulation studies to produce
predictions to be tested by the experimenters. These studies will stimulate research on the developmentof mirror neurons, which is a lacking component of current mirror neuron research.

9.2

Going beyond grasping: learning the ‘hand state’

The MNS model was based on grasping movements and excluded some actions such as tearing
and twisting for which mirror activity has been observed. The MNS model must be extended with thehelp of new neurophysiological studies to account for other hand manipulation actions. In essence, thehand state we introduced must be extended to account for other actions. Although the first step would
be manually crafting the representation for the hand state to cover the excluded hand manipulation
actions, the major research direction would be to model the mechanisms of how the brain learns to
extract such a representation from the visual world. We have already outlined one alternative byclaiming that the hand state is used as the visual feedback for hand manipulation actions. Thus, acomputational model showing how a visual feedback mechanism may be bootstrapped by biologicallyrealistic neural circuits, would provide a general theory of mirror neuron development as well as
explaining the existence of mirror neuron system. Chapter 7 presented alternative feedback mechanisms
for grasping focusing on a single grasp type, namely the precision grasp. The models there viewed with
LGM (Chapters 5 and 6) should serve as a starting point for the interested researcher. As shown in
Chapters 5 and 6, the infant/model learns how to make open-loop reach and grasp movements via goal
directed trial and error learning. Then the circuits involved in visual feedback control are built based on
the observation of the self-executed ballistic grasps.

9.3

Tactile feedback for grasping

Infants’ early reaching and grasping movements are ballistic and usually require correction after
contact with the object. Infants use the tactile feedback to conform their hands to the shape of the object
reducing the number of trials they need to perform for adapting their ballistic reach and grasp planning.
Learning to Grasp Models that we have presented in Chapters 5 and 6 did not include the tactile
correction phase and required large number of grasping actions for learning. The modeling of tactile
feedback based grasping is not trivial and requires (1) a detailed physical modeling of the hand and the

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objects in terms of friction and contact forces and (2) a realistic model of mechanoreceptor signals at
the spinal and cortical levels. When combined with learning to grasp models of Chapters 5 and 6, thetactile feedback modeling research will provide a theory of how the tactile exploration can train avisuomotor mapping circuit, and generate predictions on the grasp development at the cortical andspinal level.

9.4

Learning to extract the right affordance

The neurophysiological findings assure that the visual affordances of objects are represented in themonkey brain. We extended the monkey studies to humans by assuming that object affordances wereavailable to the grasp programming centers and mirror neuron system without addressing the issue of
how and why the affordances were extracted from the vision of objects. The how part is one of the major
problems of computer vision, namely feature extraction and object recognition. The why part is thequestion of selecting the relevant features of an object for the motor task. The natural extension of thelearning studies presented in this thesis is to model learning of what feature is relevant given a set offeatures. The research on how to learn to associate relevant features of objects with the movement
parameters will present a more thorough view of the neural mechanisms of the visuomotortransformation that takes place for hand manipulation actions.

9.5

More realistic models of the limb and the brain regions

The arm/hand model we used was a kinematics chain, which was articulated by specifying theangles of each joint. A more realistic arm/hand would include muscles that are controlled with neuralsignals from the spinal cord and the cortex. Such an arm/hand system would allow research on theeffects of corticospinal pathway immaturity during infancy.
Using the schema methodology, we focused on various brain regions and implemented them withvarious levels of biological realism. A major contribution would be to replace the schemas that have noneural implementation with realistic neural circuits. For example, the visual analysis of the hand was
implemented using computer vision techniques with no neural implementation. In addition, theaffordances of the presented objects were encoded without actually performing feature extraction. Thus,
the two visual processes, the visual analysis of the hand and the object, stand as future researchchallenges.
While modeling the core mirror circuit of MNS model, we noted that the core mirror circuit could
be adapted using any supervised learning technique. The range of the neurophysiological predictions
would be greatly extended by implementing the supervised learning in terms of realistic neural circuits.
In particular, the temporal to spatial conversion required for the current implementation could be
avoided.
Depending on future experiments that address the timings of mirror neuron activities, a revision of
the MNS model might be required. The current modeling presented in this dissertation confronted
experimentalists with a range of nontrivial predictions that should stimulate experimenters in
conducting new experiments for testing the timing and population level activity of the neurons
involved in mirror neuron system and grasp planning, which in turn, must be factored into therevisions of the models presented in this dissertation.

9.6

Sensitivity analyses for the simulation parameters

In many of the presented simulation experiments, the parameter selection was based on empiricaltests. The dissertation studied a broad range of functionality with paying less attention to the effect of148parameter selection on learning. It was empirically observed that the parameters were not very
sensitive in the sense that the models would not collapse with small variations of the parameters.
However, the result of learning may show some differences according to the variations of theparameters. For example when studying the learning to grasp, we did not analyze the dependency of
the acquired ‘grasp menu’ properties to the simulation parameters. This study requires establishing amethod to quantify the properties of the ‘grasp menu’. Then using an extensive set of simulations, thedependency can be formulated. For example, one property of a ‘grasp menu’ can be chosen as the ratio
between the number of power grasps and the precision grasps acquired.

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11 APPENDIX

11.1 Mirror neuron system model (MNS)
The system was implemented using Java programming language on a Linux operating system. The
grasp simulator can be accessed using the URL http://www-clmc.usc.edu/erhan/models/MNS. The
simulation applet at this URL also includes a simplified version of the MNS model. The applet enables
the users to test the action recognition ability of the model.

11.1.1 Color segmentation
The segmentation system as a whole works as follows:
1. Start with N rectangles (called nodes), set thresholds for red, green and blue variances as
rV, gV, bV
2. For each node calculate the red, green, blue variance as rv, gv, bv
3. If any of the variance is higher than the threshold (rv>rV or gv>gV or bv>bV) then split thenode into four equal pieces and apply step 2 and step 3 recursively
4. Feed in the mean red, green and blue values in that region to the Color Expert to determine
the color of the node.
5. Make a list of nodes that are of the same color (add node to the list reserved for that color).
6. Repeat 2-5 until no split occurs.
7. Cluster (in terms of Euclidean distance on the image) the nodes and discard the outliers
from the list (use the center of the node as the position of the node). The discarding is
performed either when a region is very far from the current mean (weighted center) or it is
not "connected" to the current center position. The connectedness is defined as follows. The
regions A and B are connected if the points lying on the line segment joining the centers of
A and B are the same color as A and B. Once again, the Color Expert is used to determine
the percentage of the correct (colors of A and B) colors lying on the line segment. If thispercentage is over a certain threshold (e.g. 70%) then the regions A and B are taken as"connected". (This strategy would not work for a "sausage-shaped" region, but does workfor patches created by the coloring we used in the glove.)
8. For each pruned list (corresponding to a color) find the weighted (by the area of the node)mean of the clusters (in terms of image coordinate).
9. Return the cluster mean coordinates as the segmented regions center.
So we do not exactly perform the merge part of the split-merge algorithm. The return values fromthis procedure are the (x,y) coordinates of the center of color patches found. Another issue is how tochoose the thresholds. The variance values are not very critical. A too small value increases
computation time but does not affect the number of colors extracted correctly (though the returned
coordinates may be shifted slightly). To see why intuitively, one can notice that the center of a rectangle
and the centroid of the centers of the quarter rectangles (say after a split operation) would be the same.
This means that if a region is split unnecessarily (because the threshold variances were set to very small

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values) it is likely to be averaged out with our algorithm since it is likely that the four split rectangles
will have the same color and will be connected (with our definition of connectedness)

11.1.2

Reach and grasp schema precision grasp planning and execution••

Determine the opposition axis to grasp the object.
Compute the two (outer) points A and B at which the opposition axis intersects the object
surface. They serve as the contact points for the virtual fingers that will be involved in thegrasp.
• Assign the real fingers to virtual fingers. The particular heuristic we used in theexperiments was the following. If the object is on the right [left] with respect to the arm
then the thumb is assigned to the point A if A is on the left of [at a lower level than] B
otherwise the thumb is assigned to B. The index finger is assigned to the remaining point.
• Determine an approximate target position C, for the wrist. Mark the target for the wrist on
the line segment connecting the current position of the wrist and the target for the thumb afixed length (determined by the thumb length) away from the thumb target.
• Solve the inverse kinematics for only the wrist reach (ignore the hand).
• Solve the inverse kinematics for grasping. Using the sum of distance squares of the finger
tips to the target contact points do a random hill climbing search to minimize the error.
Note that the search starts with placing the wrist at point C. However, the wrist position is
not included in the error term.
• The search stops when the simulator finds a configuration with error close to zero (success)or after a fixed number of steps (failure to reach). In the success case the final configurationis returned as the solution for the inverse kinematics for the grasp. Otherwise failure-toreach is returned.
Execute the reach and grasp. At this point the simulator knows the desired target configuration interms of joint angles. So what remains to be done is to perform the grasp in a realistic way (in terms ofkinematics). The simplest way to perform the reach is to linearly change the joint angles from the initialconfiguration to the target configuration. But this does not produce a bell shaped velocity profile (norexactly a constant speed profile either because of the non-linearity in going from joint angles to end
effector position). The perfect way to plan an end-effector trajectory requires the computation of theJacobian. However we are not interested in perfect trajectories as long as the target is reached with abell-shaped velocity profile. To get the effect it is usually sufficient to modify the idea of linearlychanging the joint angles little bit. We simply modulate the change of time by replacing time with athird order polynomial that will match our constraints for time (starts at 0 climbs up to 1
monotonically). Note that we are still working in the joint space and our method may suffer from thenon-linearity in transforming the joint angles to end effector coordinates. However, our empiricalstudies showed that a satisfactory result, for our purposes, could be achieved in this way.

11.2 Learning to grasp models (ILGM and LGM)
The simulation environment is developed using Java programming language. The simulation
environment consists of a 3D kinematics arm model (see Chapter 3) and routines implementing theLGM circuit. Note that from an implementation point of view the learning to grasp circuits of Chapters
5 and 6 are essentially the same. In this section, we present a brief overview of the simulation
environment.
Thefurther
detailsareavailable
at
the
URL
http://wwwclmc.usc.edu/erhan/models/LGM.

166

The main behavior of the simulation system is determined by the resource file
‘KolParameters.res’. Many simulation parameters can be set within this file. However, some of theparameters are hard coded in the Java class files comprising the simulation system. The 3D positionsand vectors are defined using a spherical reference frame. The PAR, MER and RAD tags are used toindicate elevation, azimuth and radius components respectively.
Object position range parameters define the range of the object position in the workspace. In thefollowing segment of text, the first two correspond to the range of the elevation; the following twocorresponds to the range of azimuth and finally the last two corresponds to the range of radius.
minPAR
maxPAR
minMER
maxMER
minRAD
maxRAD

-45
45
-45
45
700
1300

Object location coding length parameters define how many units to allocate for representing eachposition component in the affordance layer. In the below setting, the object location will be represented
with 100 units.
obj_locPAR_code_len
obj_locMER_code_len
obj_locRAD_code_len

10
10
1

Object location coding variance defines the variance for population encoding of the object location.
obj_encode_var

1

Object axis orientation range parameters define the minimum and maximum allowed tilt of the object
around the z-axis (in the frontal plane). The number of units allocated for encoding the tilts (in threecoordinate axes) is hardwired in the file Motor.java
minTILT
maxTILT090

Base learning rate parameter is used as the common multiplier for all the learning rates in the grasp
learning circuit.
eta

0.5

LGM layer length parameters define the number of units to allocate for the layers generating the motor
parameters. BANK, PITCH and HEADING tags indicate the supination-pronation, wrist extensionflexion and radial/ulnar deviation movements respectively. (The Virtual Fingers layer in thesesimulations is not engaged fully as it is represented as a layer of ten units encoding the synergistic
enclosure speed of the hand.)
hand_rotBANK_code_len
9
hand_rotPITCH_code_len
9
hand_rotHEADING_code_len 1

The tags locMER, locPAR and locRAD indicate the approach direction vector components.
hand_locMER_code_len
hand_locPAR_code_len
hand_locRAD_code_len

7
7
1

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Learning session parameters define the behavior of the simulator during learning. For a learning
session, the simulator makes MAXBABBLE number of reach/grasp attempts. For each approachdirection, the simulator makes MAXROTATE grasping attempts. After MAXREACH reaches are done,
the next input condition is selected (e.g. the object is placed in a different position). After eachweightSave reach/grasp trials the learned connections are written to disk. Note that MAXBABBLE only
limits the maximum number of attempts the simulator will make. A particular simulation may be
stopped at any instant. The saved connection weights then can be used for testing the performance at alater time. Reach2Target parameter indicates which part of the hand should be used in reaching for theobject. The possible values are {INDEX, MIDDLE, THUMB} x {0,1,2} where 2 indicates the tip.
MAXREACH
MAXROTATEMAXBABBLE
weightSave
Reach2Target

5
7
10000
4500
INDEX1

Grasp stability parameters define the acceptable grasps in terms of physical stability. costThresholdspecifies the allowable inaccuracy in grasping. Ideally, the cost of grasping (a measure of the instability,
see Chapter 5.5) should be small indicating that the grasp is successful. Empirically, a value between 0.5
and 0.8 gives a good result for the implemented cost function. If the distance of the touched object to thepalm is less than palmThreshold and the movement of the object due to finger contact is towards thepalm then the palm is used as a virtual finger to counteract the force exerted by the fingers. The
negReinforcement parameter specifies the level of punishment returned when a grasp attempt fails.
Empirically values greater than –0.1 and less than 0 result in good learning. Generally, a large negative
reinforcement overwhelms the positively reinforced plans before they have chance to get represented in
the layers.
costThresholdpalmThreshold
negReinforcement

0.8
150
-0.05

Exploration and exploitation parameters specify how often to use the learned distribution to generate
grasp plans. A value of 1 means always use random parameter selection, while a value of 0 means
always generate parameters from the current distribution of the layer. The tag ‘rot’ indicates the Wrist
Rotation layer while ‘off’ indicates the Hand Position Layer.
rotRandomness
offRandomness

1
1# 1=full random 0=from the pdf# 1=full random 0=from the pdf

Now we present the simulation parameters used for learning to grasp experiments presented in
the thesis. The default values of the parameters given in the descriptions above will not be repeated.
Simulation parameters for sections 6.6.1 and 6.6.2, and Figure 5.8
hand_rotBANK_code_len
hand_rotPITCH_code_len
hand_rotHEADING_code_len
hand_locMER_code_len
hand_locPAR_code_len
hand_locRAD_code_len
MAXREACH
MAXROTATEMAXBABBLE

11
11
6
6
6
1
N/A
55
50000 (stopped at 16000)

168
weightSave
Reach2Target
costThresholdpalmThreshold
negReinforcement
rotRandomness
offRandomness

16000
MIDDLE0
0.75
125
-0.1
0.95
0.95

Simulation parameters for section 5.7 (except Figure 5.8)
hand_rotBANK_code_len
hand_rotPITCH_code_len
hand_rotHEADING_code_len
hand_locMER_code_len
hand_locPAR_code_len
hand_locRAD_code_len
MAXREACH
MAXROTATEMAXBABBLE
weightSave
Reach2Target
costThresholdpalmThreshold
negReinforcement
rotRandomness
offRandomness

11
11
6
6
6
1
N/A
55
50000 (stopped at 10000)
5000
INDEX0
0.75
125
-0.1
0.95
0.95

Simulation parameters for sections 5.9 and 6.7
hand_rotBANK_code_len
hand_rotPITCH_code_len
hand_rotHEADING_code_len
hand_locMER_code_len
hand_locPAR_code_len
hand_locRAD_code_len
MAXREACH
MAXROTATEMAXBABBLE
weightSave
Reach2Target
costThresholdpalmThreshold
negReinforcement
rotRandomness
offRandomness

12
7
1
1
1
1
1
25
200000 (stopped at 20000)
2500
MIDDLE0
0.85
150
-0.1
1
1

Simulation parameters for sections 5.8
hand_rotBANK_code_len
hand_rotPITCH_code_len
hand_rotHEADING_code_len
hand_locMER_code_len
hand_locPAR_code_len
hand_locRAD_code_len
MAXREACH
MAXROTATEMAXBABBLE
weightSave
Reach2Target
costThreshold

9
9
1
7
7
1
1
7
200000 (stopped at 45000)
4500
INDEX20.80

169palmThreshold
negReinforcement
rotRandomness
offRandomness

150
-0.05
1
1

Simulation parameters for section 6.9
maxRAD
hand_rotBANK_code_len
hand_rotPITCH_code_len
hand_rotHEADING_code_len
hand_locMER_code_len
hand_locPAR_code_len
hand_locRAD_code_len
MAXREACH
MAXROTATEMAXBABBLE
weightSave
Reach2Target
costThresholdpalmThreshold
negReinforcement
rotRandomness
offRandomness

1200
10
7
5
10
10
1
10
30
200000 (stopped at 50000)
10000
MIDDLE0
0.75
128
-0.1
1
1

Simulation parameters for section 6.8
hand_rotBANK_code_len
hand_rotPITCH_code_len
hand_rotHEADING_code_len
hand_locMER_code_len
hand_locPAR_code_len
hand_locRAD_code_len
MAXREACH
MAXROTATEMAXBABBLE
weightSave
Reach2Target
costThresholdpalmThreshold
negReinforcement
rotRandomness
offRandomness

9
9
1
7
7
1
10
10
200000 (stopped at 50000)
4500
INDEX1
0.8
150
-0.05
0.95
0.95