Figure 1 diagrams the most common types of responses seen in the nucleus
rotundus. In each diagram, the length of the vector indicates response mag-
nitude and the direction of the vector indicates the direction of movement of
the target on the tangent screen, 0° being vertical and 90° being anterior.
Figure 1A shows the variations in response seen as a target is moved in
various directions. Clearly, the maximum response is seen at 135°, The
circled I at 315° indicates that movement in this direction caused an inhi-
bition of spontaneous activity of the neurone. Thus, a "315° min/max" axis
is defined. This pattern was elicited by a 2° diameter, 3-mm-thick, black
cardboard target. Such targets were commonly the most "efficient" visual
stimuli in that they usually elicited the largest amplitude and most para-
metrically selective responses seen in any given rotundal unit. Thus,

Figure 1B shows the respanse elicited in the same cell by a projected white
spot of light, also of 2° diameter. Clearly, the response to the moving
light spot is not so directionally selective as the dark-target response.
Figure 1C shows amplitudes of the responses of the same neurone to horizontal
movements of targets of the indicated sizes. This unit is nonselective for
size; that is, the response intensity is independent of target size. The
response pattern of Figure 1D shows a "size selective" unit, so called
because the response intensity is clearly a function of target size.

The smallest targets used subtended 4 min of arc. About 10 percent of
the units tested responded weakly or moderately, to this stimulus; this
response suggests an ultimate angular threshold for this system of less than
2 min of arc. The two most common rotundal response patterns were the combi-
nations of the configurations in Figures 1A and 1D (directionally selective
for small dark targets) and those in Figures 1B and 1C (nonselective for
anything but movement).

About 40 percent of the directionally sensitive cells also show a dead
zone in their response pattern; that is, a unit will respond to an appro-
priate stimulus only if the stimulus moved in a straight line through a
distance of more than 2-10° of arc. This is not a latency phenomenon,
because the size of the dead zone is not a function of stimulus velocity, and
the stimulus may be moved within the dead zone in any manner and for any
length of time without affecting the firing of the unit. The diameter of the
dead zone was, as indicated, always in the range of 2-10° and, for any given
unit, of constant size. Surprisingly, dead zones were seen in units selec-
tive for large targets as well as in those selective for small stimuli.

The neurones selected for examination in these studies showed little
adaptation to repeated presentation of a stimulus. However, about 10 percent
of all rotundal units encountered do show some kind of adaptation phenomena.
About a third of these are directionally selective cells requiring priming;
that is, after a rest period of more than 5 min, during which there was no
movement in the visual field, the initial 1-3 s of stimulation evokes only
generalized, nonselective response patterns. The selective response patterns
develop rapidly after this initial lethargy and remain stable and consistent

3



10.

il.

12.

13.

REFERENCES

Benowitz, L. I., and H. J. Karten: Organization of the Tectofugal
Visual Pathway in the Pigeon. J. COMP. NEUROL. 167:503-520, 1976.

Bishop, P. 0.: Central Nervous System; Afferent Mechanisms and
Perception. ANN. REV. PHYSIOL. 29:427-484, 1967.

Bisti, S., R. Clement, L. Maffei, and L. Mecacci: Spatial Frequency
and Orientation Tuning Curves of Visual Neurones in the Cat: Effects
of Mean Luminance. EXP. BRAIN RES. 27:335-345, 1977.

Cotter, J. R.: Visual and Nonvisual Units Recorded from the Optic
Tectum of Gallus Domesticus. BRAIN BEHAV. EVOL. 13:1-21, 1976.

Dow, B. M.: Central Mechanisms of Vision: Parallel Processing.
FED. PROC. 35(1):54-59, 1976.

Giorgetti de Britto, L. R., M. Brunelli, W. Francesconi, and F. Magni:
Visual Response Pattern of Thalamic Neurones in the Pigeon. BRAIN RES.
97:337-343, 1975.

Hughes, C. P., and A. L. Pearlman: Single Unit Receptive Fields and
the Cellular Layers of the Pigeon Optic Tectum. BRAIN RES. 80:365-377,
1974,

Jassik-Gerschenfeld, Dora, and J. Guichard: Visual Receptive Fields of
Single Cells in the Pigeon's Optic Tectum. BRAIN RES. 40:303-317, 1972.

Jassik-Gerschenfeld, Dora, Francoise Minois, and Francoise Conde-
Courtine: Receptive Field Properties of Directionally Selective Units
in the Pigeon's Optic Tectum. BRAIN RES. 24:407-421, 1970.

Karten, H. J., and W. Hodos: A Stereotactic Atlas of the Brain of the
Pigeon (Columba livia). (Johns Hopkins University Press, Baltimore,
1967.)

Karten, H. J., and W. Hodos: Telencephalic Projections of the Nucleus
Rotundus in the Pigeon (Columba livia). J. COMP. NEUROL. 140:35-52,
1970.

Kimberly, R. P., A. L. Holden, and P. Bamborough: Response
Characteristics of Pigeon Forebrain Cells to Visual Stimulation.
VISION RES. 11:475-478, 1971.

Lettvin, J. Y., H. R. Maturana, W. S. McCulloch, and W. H. Pitts:
What the Frog’s Eye Tells the Frog's Brain. PROC. I.R.E. 47:1940-1951,
1959.

10


response patterns are also seen. One type, the "left turn" neurone, responds
only if something the size and shape of a human stands more than 1 m from the
bird and pivots or turns sharply to the left (five units) or right (two
units). These and other equally whimsical cells occur chiefly in the most
lateral and anterior part of the rotundus. Furthermore, some of our very
first unit studies suggested that excitability as well as size and direc-
tional preferences could be affected by substantial changes in ambient
illumination (3) or by electrical stimulation in brain stem areas tradition-
ally associated with the "reticular activating system" concept (unpublished
observations). Because, say, directional selectivity can also be affected
by such things as dark vs. light stimuli (Figure 1), it is apparent that the
response characteristics of rotundal neurones depend, to an uncomfortable
extent, on the minutiae of the experimental arrangements.

B. Regional Distribution of Responses

Perhaps the simplest categorization of rotundal cells is: directionally
selective vs. not selective. In Figure 3 we have plotted, for each cell in
each of 10 tracks, whether it was directionally selective. A 10-track subset
of the total was used to keep Figure 3 fairly simple. The two different
classes of directionally sensitive cells were plotted because they differ
pharmacologically, but they should be considered as one group here.

DIRECTIONAL RESPONSES OF ROTUNDAL
WIDE-FIELD NEURONES

~~
%
«pet py

Re OTN
eT Nn
eee ee py
x xe peeD
«os xe poppe,
ns ae

pre

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eet
a

ee
\ proxsd ‘ee py

ong’ 78
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\
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% NO DIRECTIONAL PREFERENCES
@, DIRECTION OF MIN/MAX AXIS =~ v4
Se, ASYMMETRIC RESPONSES ~~
een 2
eo
_-—

Figure 3. Visual response patterns seen in 10 selected electrode tracks are
plotted against a diagram of a sagittal section through the center of the
nucleus rotundus. The neurones were classified according to their responses
to different directions of stimulus movement as described in Figures 1 and 2.
There is a clear tendency for units without directional selectivity or
preferences to cluster in the posterior third of rotundus.

5



throughout the remainder of the examination. The other units show complex
patterns of adaptation, usually a function of the stimulus parameters, that
have not been examined in detail (17) but are generally similar to those
described for tectal units by Woods and Frost (20).

Although rotundal responses have been categorized to some extent in the
preceding paragraphs, these categories are neither complete nor mutually
exclusive. Indeed, it seems as if every possible combination of size,
directional, and brightness response preference has been seen. Figure 2
shows some of the various response patterns that can be seen during one
electrode penetration. Figure 2A shows a cluster of three units that have
the "common" pattern. Figure 2B is similar but the min/max axis is rotated
45°; there is no inhibitory response to movement and there are equal
responses to small dark and small light targets.

Kn
E. DARK, SMALL,
ASYMMETRIC ~ —

a D. LARGE

Figure 2. An illustration of typical response patterns seen in the course
of single electrode penetration. The first three units in sequence responded
only to small dark targets with some directional sensitivity (A). The next
unit (B) was similar but with different directional preferences, and it
responded to either dark or light spots. Neurone (C) responded only to a
dark bar (8° x 1°) moved downwards. Cell (D) responded only to a very large
dark target, greater than 30°, moving downwards. Unit (E) is similar,
again, to (A) and (B).

Figure 2C shows a very sharply tuned response to an 8° x 1° dark bar.
Figure 2D is similar but the response is only to targets greater than 20°,
while Figure 2E is a common variant on the Figure 1A response. More complex

4


IV. Discussion.

As we have seen, the available data suggests that nucleus rotundus is
functionally differentiated. Neurones in posterior rotundus tend to respond
to any image movement on the retina, whereas anterior rotundal responses
tend to be selective for such abstract qualities of the moving stimulus as
size, direction, contrast, velocity, etc. Ventral rotundal responses are
similar to anterior response patterns, but these cells seem more concerned
about brightness than the others. These are broad, even crude, distinctions.
There is evidence that suggests far more precise and complex localizations.
In some penetrations a series of "315° min/max" units would be followed by
a series of units that are not directionally selective but, say, size
selective. Further, in some penetrations a systematic variation in size or
directional selectivity of the units was seen as the micropipette moved
ventrally. Lastly, Benowitz and Karten (1) reported an anatomical parcel-
lation that was rather more complex than the functional parcellations seen
here.

Now, the characteristic response properties of rotundal units seem to
be determined in tectum (4, 7, 8, 9, 14, 17) or in retina (14). This
determination, taken together with the functional localization discussed
above and the characteristic wide visual field of rotundal neurones (6, 17),
suggest that the responses of all tectal neurones having some unique set of
response properties are summed and sent to a specific and unique subarea of
rotundus. That is, localization in tectum is a function of the spatial
localization of the stimulus; in rotundus it is a function of the responses
to some set of abstractions about the stimulus.

A good deal of recent research in mammalian visual function has
suggested that form perception depends on a kind of parallel processing (5)
in which the identification of the stimulus depends on an integration of the
outputs of numbers of neurones or neuronal systems, each responding to a
different subset of abstract stimulus qualities (19). In rotundus, each
subset of neurones seems to respond preferentially in the presence of some
defined set of stimulus qualities; that is, the firing of any given group
of rotundal neurones signifies that a stimulus of defined properties exists
somewhere in the visual field. This information is relayed to ectostriatal
"core" (11), where the response patterns are very similar to those in
rotundus (12). Ectostriatal "core," in turn, projects to ectostriatal
"belt," as does the hyperstriatal visual area, the functional homolog, perhaps,
of striatal cortex (11). Thus, the major area of integration of information
from two major avian visual projection pathways may be the ectostriatal
"belt," which thus may also be a major center controlling form and motion
perception in the bird.



Technical Report Documentation Page

T. Report No. 2. Government Accession No. 3. Recipient's Catalog No.
FAA-AM-7 7-22
a. Title and Subiitle 3. Report Date

October 197

6. Performing Orgonization Code

FUNCTIONAL LOCALIZATION IN THE NUCLEUS ROTUNDUS

&. Performing Organization Report No.

7. Author's)

Alvin M. Revzin

9. Performing Organization Name and Address 10. Work Unit No. (TRAIS)
FAA Civil Aeromedical Institute

P.O. Box 25082 TI. Centrect or Grant No.

Oklahoma City, Oklahoma 73125

13. Type of Report and Period Covered

12, Sponsoring Agency Neme ond Address
Office of Aviation Medicine
Federal Aviation Administration

800 Independence Avenue, S.W. 14. Sponsoring Agency Code
Washington, D.C. 20591

15. Supplementary Notes

This research was conducted under Tasks AM-A-76-TOX-30 and AM-A-77-TOX-30,

16. Abstrect

Work in this laboratory has suggested that the effects of psychoactive drugs on
visual performance may best be understood, and/or predicted, by studying
differential effects of the drugs on functionally differentiated sets of neurones
in visual projection systems in the brain. This study demonstrates that the nucleus
rotundus, an avian posterior thalamic visual relay nucleus homologous to parts of
the mammalian lateralis posterior/pulvinar complex, is divided into at least three
functionally distinct neurone subsets. The "posterior" rotundal cells respond to
any moving retinal image. Ventral rotundal cells respond preferentially to
intensity modulation of moving or stationary stimuli. Anterior rotundal neurones
respond preferentially to such abstract properties of moving stimuli as size,
velocity, and direction of movement. All subnuclei may be further subdivided by
function. The findings reinforce current theories which suggest that pattern
vision results from cortical integration of the outputs of many classes of pattern
selective visual projection system neurones. Preliminary findings are also
presented suggesting that effects of psychoactive drugs, such as ethanol, can
indeed be predicted or understood by studies on differential effects on neurones in

this model system.

17. Key Words Neurotoxicology, Visual 18. Distribution Stotement

System, Comparative Neurology, Document is available to the public

Comparative Neuropharmacology, Nucleus through the National Technical

Rotundus, Pigeon, Neuronal Functions, Information Service, Springfield,

Functional Differentiation Virginia 22161

T9. Security Classif. (of this report) 20, Security Classif. (of this page) Bi. No. of Pages | 22. Price
Unclassified Unclassified a1

Form DOT F 1700.7 (8-72) Reproduction of completed page authorized





14.

15.

16.

17.

18.

19.

20.

Pearlman, A. L., and C. P. Hughes: Functional Role of Efferents to the
Avian Retina: I. J. COMP. NEUROL. 166:111-122, 1976.

Revzin, A. M.: Flash Evoked Unit Response Patterns in the Diencephalon
of the Pigeon. FED. PROC. 25(1):395, 1966.

Revzin, A. M.: Unit Responses to Visual Stimuli in the Nucleus
Rotundus of the Pigeon. FED. PROC. 26:2238, 1967.

Revzin, A. M.: Some Characteristics of Wide-field Units in the Brain
of the Pigeon. BRAIN BEHAV. EVOL. 3:195-204, 1970.

Revzin, A. M., and H. J. Karten: Rostral Projections of the Optic
Tectum and the Nucleus Rotundus in the Pigeon. BRAIN RES. 3:264-276,
1967.

Sprague, J. M., J. Levy, A. De Berardino, and G. Berlucchi: Visual
Cortical Areas Mediating Form Discrimination in the Cat. J. COMP.
NEUROL. 172:441-488, 1977.

Woods, E. J., and B. J. Frost: Adaptation and Habituation

Characteristics of Tectal Neurons in the Pigeon. EXP. BRAIN RES. 27:
347-354, 1977.

11



Clearly, the cells showing no directional preferences tend to cluster in the
posterior third of the nucleus.

There is a good deal of overlap between categories, but the distribution
does suggest that the posterior third of rotundus differs from the remainder,
In six tracks in dorsal anterior rotundus the min/max axis of successive
directionally selective units rotated clockwise as the electrode was advanced
along the usual dorsoventral axis. This rotation of response axis, taken
together with the "left turn" cells, for example, suggests a high degree of
functional localization in rotundus, though the complexity of the responses,
the limited number of test patterns used, and the paucity of data on any
given neurone response pattern make verification impossible now.

Rotundal units also differ with respect to the size of their preferred
stimulus. So, in Figure 4, we have plotted size preferences seen in rotundal
units. We again used a 10-track subset of the total for simplicity but
sampled 10 tracks different from those used in Figure 3. Again, as in
Figure 3,the nonselective units, the ones fired by anything moving, tend to
be grouped in the posterior third of rotundus. There is a sampling error
here, though. Were all tracks plotted, the separation, though still clear,
would not be as sharp as it appears in this figure. In eight tracks
preferred stimulus size increased as the electrode advanced through the dorsal
half of anterior rotundus. This increase suggests, again, that there may be
a much higher degree of functional organization within rotundus than that
suggested in Figures 3 and 4, based, as they are, on quite simple
categorizations.

Although posterior rotundal responses have been described in terms of
single-unit responses, what occurs is, in fact, rather complex. Spontane-
ously active single units are fairly easy to isolate in this area, at least
in deeply anesthetized animals. In "posterior rotundus" the probability of
finding spontaneously active neurones increases with depth of anesthesia,
though the rate for any given unit does not increase with an increase in
anesthesia depth. The presence of a moving stimulus induces a characteristic
30-100 Hz rhythmic high frequency activity in the local EEG and algo causes
virtually every neurone in the area of the electrode to fire at rates of up
to 250/s. There is some tendency for the neurone firing to cluster on the
positive-going slope of the EEG waves. This evoked multiunit activity
usually makes ic difficult to discern whether the spontaneously active unit
shares its neighbor's excitement over the stimulus, though this is usually
the case. This pattern of activity is unique to posterior rotundus.

There are also pharmacological differences between anterior and pos-
terior rotundal neurones. For example, ethanol inhibits anterior rotundal
spontaneous activities at very low doses, while posterior rotundal cells
show a complex, dose-dependent inhibitory-excitatory—inhibitory sequence of
changes (Revzin, in preparation). Nonvisual dorsal thalamic neurones are
usually inhibited by ethanol, but the threshold doses are three to five

6


III. Results.

A. Qualitative Description of Response Characteristics

Much of this material has previously been reported (15, 16, 17) and what
follows is, for the most part, a review and summary. About 80 percent of the
rotundal units had very large visual fields, ranging from 100° to 175° (15,
18). Most of the units with smaller fields were seen in the ventral quarter
of rotundus or as occasional units with large, long-duration spikes mixed
with other units in the posterior rotundus (see below).

/
/
{
\
\
7X a
X 7 ~. ~
O.TECT. Sy ~
o Ny / ( SY ~~.
s— \ N
270° g0°

180°
A. 315° MIN/MAX

I e—, Zz \°e—>
2, oo 26
ae weer iar amend
Bes LTT Beer

20° +s 20°8

40° o> 4o°°

C. DARK TARGET D. DARK TARGET

NONSELECTIVE SMALL

Figure 1. An illustration of some neurone response patterns found in the
nucleus rotundus. For each diagram the length of the arrow represents
response magnitude, the direction of the arrow indicates the direction of
stimulus movement. A circled I signifies an inhibition of spontaneous
activity. The uppermost neurone was interrogated with two stimuli, a small
dark cardboard target (A) and a projected spot of light of the same size (B).
In (A) a movement along the 315° axis produces an inhibition of ongoing
activity while the opposite movement, in the 135° direction, produces a
maximum response. This defines a "315° min/max" axis for this neurone. How-
ever, little directional sensitivity is apparent when this unit was tested
with a projected spot of light (B). This unit was also tested with dark
targets of various sizes (C). As shown, there is little variation in
response correlated with stimulus size. Responses to horizontal (90°) move-
ment are shown for simplicity though this class of cells simply does not
discriminate target size, whatever other selectivity characteristics the cell
may demonstrate. In (D) is shown response characteristics of a cell that
responds only to relatively small targets. Abbreviations: 0. Tect. = Optic
Tectum; Rt. = Nucleus Rotundus; Tr. 0. = Optic Tract; GLV = Lateral
Geniculate nucleus, pars ventralis.


FUNCTIONAL LOCALIZATION IN THE NUCLEUS ROTUNDUS

I. Introduction.

Recent work of Benowitz and Karten (1) has shown that the projections
from the optic tectum to the nucleus rotundus in the pigeon are spatially
organized with specific regions or layers of the optic tectum projecting to
specific, anatomically defined areas of rotundus. The present study, in
part a reexamination of previous data, was initiated to see whether regional
differences in rotundal functions could be correlated with the anatomical
areas defined by Benowitz and Karten (1).

II. Methods.

Extracellular unit recordings were taken from rotundal neurones in
urethane-anesthetized white Carneau pigeons. Projected spots of light or
black cardboard targets were moved against a light-gray tangent screen to
elicit visual responses in spontaneously active cells. The tangent screen
was mounted vertically, parallel to the parasagittal plane, at a distance
of 1.5 m from the pigeon's left eye. Absolute room illumination levels
varied but were usually in the low photopic range. Although more elaborate
data reduction techniques, such as poststimulus time histograms, were used,
most data were taken as subjective evaluations of the unit firing frequency
heard on the audio monitor (2, 13). A five-point intensity scale was used;
strong, moderate and weak excitation, no effect, and inhibition. Recording
techniques and equipment and electrode localization procedures were
conventional (10).

The sampling procedures were such that only spontaneously active
neurones were selected for detailed study, because the general procedure was
to advance the electrode until a spontaneously active unit was found and
then examine its characteristics. In 20 tracks we simply advanced the
electrodes in 50-ym increments and tested at each point to see if unit
activity was evokable. The data suggested that only one in three of the
visually driven neurones was spontaneously active. For the most part the
evoked responses of "active" and "quiet" neurones were similar, though it is
quite possible that "active" and "quiet" neurones represent functionally
distinct populations. More than 600 units or small clusters of units were
examined in 62 electrode penetrations. The tracks sampled activity in
rotundus throughout its rostrocaudal and dorsoventral extent. However, some
bias was present; the central, lateral, and dorsal areas of the nucleus were
sampled more extensively than medial and ventral zones.

For each isolated unit or cluster of units we determined field size,
directional responses for each of a wide range of target configurations,
responses to changes in ambient illumination, and responses to stationary
diffuse or discrete light flashes.