1376 Cognitive neuroscience and neuropsychology

Shared neural correlates for language and tool use
in Broca’s area
Satomi Higuchia, Thierry Chaminadeb, Hiroshi Imamizua,c and Mitsuo Kawatoa
Functional MRI was used to test predictions from a theoryof the origin of human language. The gradual theory
suggests that human language and tool-use skills havea similar hierarchical structure, and proposes that toolmanipulation skills are related to the origin and evolution ofhuman language. Our results show an overlap of brain
activity for perceiving language and using tools in Broca’sarea. The location of this overlap suggests that language
and tool use share computational principles for processing
complex hierarchical structures common to these twoabilities. The involvement of monkeys’ homologous region
during tool use suggests that neural processes forcomputation of complex hierarchical structures exist in
primates without language, and could have been exapted
to support human grammatical ability. NeuroReport

Introduction
The evolutionary origin of language remains a controversial issue. Did it emerge suddenly in humans orarise slowly through the adaptation of existing primate
ability(ies), such as manual skills? One prominent gradual
theory supposes that tool-use and tool-making skills
are related to language evolution, as both abilities have
similar hierarchical organization [1]. Language has ahierarchical structure, that is, grammar, a set of rules for
combining words in a meaningful order. Tool use hasa similar hierarchical structure, in which simple hand
movements are combined in a certain order to achieve
appropriate object manipulation. These combination
rules exist for different tools and have been called ‘action
grammar’ by Greenfield [1]. For example, when cutting
paper with scissors, one hand holds the piece of paper,and the other hand opens and closes the scissors
repeatedly, during which time a process of adaptation
occurs regarding the relative positions of the piece of
paper and scissors.
Behavioural experiments showed that non-human primates can acquire simple grammar skills, but are unable
to master the ‘phrase structure grammar level’, which ischaracteristic of human languages [2]. Human functional
neuroimaging showed a dissociation between the involvement of different parts of the inferior frontal gyrus(Broca’s area) in language: a part posterior to the pars
opercularis for simple grammar, and an anterior part in
Brodmann area 44 (BA44) for complex grammar processing [3]. Considering the central role of Broca’s area
in language, one can hypothesize that the anterior part0959-4965 c 2009 Wolters Kluwer Health | Lippincott Williams & Wilkins

20:1376–1381 c 2009 Wolters Kluwer Health | Lippincott
Williams & Wilkins.
NeuroReport 2009, 20:1376–1381
Keywords: Broca’s area, language, syntax, tool usea
ATR Computational Neuroscience Laboratories, Kyoto, Japan, bInstitut de
Neurosciences Cognitives de la Méditerranée, CNRS-Université de laMéditerranée, Marseille, France and cNational Institute of Information andCommunications Technology (NICT), Japan

Correspondence to Thierry Chaminade, Institut de Neurosciences Cognitives
de la Méditerranée, INCM UMR 6193 CNRS-Université de la Méditerranée,
31 Chemin Joseph Aiguier, 13402 Marseille Cedex 20, France
Tel: + 33 4 91 16 45 38; fax: + 33 4 91 16 44 98; e-mail: tchamina@gmail.com
Satomi Higuchi and Thierry Chaminade contributed equally to this study
Received 11 June 2009 accepted 28 July 2009of BA44 specifically evolved for grammatical aspectsof human language.
This issue has recently been revived by the discoveryof mirror neurons [4]. Mirror neurons in area F5 of themonkey ventral premotor cortex discharge both when themonkey performs a particular action and when it observes
another individual doing a similar action [5]. Functional
MRI (fMRI) and positron emission tomography experiments in these monkeys show that both action observation [6] and tool use [7] activate the arcuate sulcus in theinferior frontal cortex of these animals, a region thought
to be the homologue of Broca’s area in humans [8]. In
humans, neuroimaging studies established that a mirror
system exists in Broca’s area [5] and homology of monkey
F5 and human BA44 had been suggested from several
imaging studies [9]. It has been argued that mirror
systems provide a bridge between action and communication and could have formed the substrate of language
evolution [4].
F5 mirror neurons have been found to respond to the useof a tool by macaque monkeys after training [10], thenit follows that if human language is functionally basedon the primates’ neural substrate for tool-use [1], thesame neural computations within Broca’s area, the humanhomologue of F5, could be involved in both language andtool use. In contrast, if human language processing,particularly the processing of complex syntactic structures for sentence comprehension, is a unique humanspecialization without any counterparts in other animals[11], there should be no activity related to the use of
DOI: 10.1097/WNR.0b013e3283315570

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Language and tool use in Broca’s area Higuchi et al. 1377

tools in the pars opercularis region, BA44, involved incomplex grammar processing. To distinguish between
these two hypotheses, brain correlates of language andof tool-use tasks were measured in the same participants using fMRI, and the analysis focused on the overlap
between the two tasks in Broca’s area.

Methods
Participants

Sixteen healthy (seven females and nine males, age
range 18–35 years), right-handed [12], volunteers participated in this study, which was approved by the ethics
committees of the Advanced Telecommunications Research Institute. They gave their written informed
consent to the experimental procedure and signed aparticipation agreement. All participants were native
Japanese speakers.
Design and experimental conditions

The fMRI experiment consisted of five conditions(EXECUTION, IMAGERY, HOLD, STORY and REVERSE). Participants practiced the experimental tasks
outside the MRI scanner before actual scanning. As
participants were highly familiar with tools used in theexperiment, they all reported being able to performthe tool-use EXECUTION and tool-use IMAGERY
without difficulty. The tasks used to investigate language(STORY and REVERSE) did not entail any difficulties
requiring training.
Participants in the scanner were instructed about thecondition in the coming trial by sound stimuli consistingof beeps varying in number and pitch. Conditions
were repeated three times within each session andeach condition lasted for 40 s except HOLD, which was
repeated six times and lasted for 20 s. The order ofthe conditions was randomized within each repetition(except HOLD, a control condition that occurred in
the second and fifth positions in each session for theparticipants to rest after every two conditions except
the first in the session. See lower panel of Fig. 1).
Tool-use EXECUTION condition (see Fig. 1, upper
panel): the participants were asked to manipulate
appropriately one of three common tools (pencil, scissors
and chopsticks) with their right hand while their arm
rested on an arm rest to prevent head movement.
Participants were able to see their hands, position of apiece of paper or beads and the tools through two mirrors
without image reversal. In the pencil task, participants
were given a piece of paper that had lines printed with a
2 cm gap between each line and asked to draw a spiralcontinuously between two adjacent lines with a pencil. In
the scissors task, participants were given a piece of paperthat had lines printed with a 6 mm gap between eachline and were asked to cut along one line at a time withthe scissors. In the chopsticks task, participants were
given several 5-mm sized round shaped beads suspended
on a thread and instructed to pick up one of the beads
and move it to the other side with chopsticks. These
three tools were chosen as examples of sequential
behaviour. In the case of the scissor task, the actionof opening and closing the hand to cut is defined as asingle stroke, repeating such stroke equates to asequence. As only one tool was used per session,
participants underwent three sessions, with the tool
order randomized across participants.
Tool-use IMAGERY condition: participants were asked
to imagine that they were manipulating the tools as
they did in the EXECUTION condition while they held
the appropriate tool and looked at its target (e.g. paper).
This condition was used to isolate cognitive aspects oftool use, such as planning (present in IMAGERY andEXECUTION) from purely motor aspects that should
not be active in IMAGERY.
Tool-use HOLD condition: the participants were asked
to hold the tool and look at the target object without
imagining using the tool.
STORY condition: participants listened to a famous
Japanese fairy-tale and to explanations of the story
narrated by a professional Japanese storyteller. All
participants knew the story and each STORY trial
consisted of a different part of the story or explanations.
REVERSE condition: participants listened to the same
story played backwards. This condition, that has the same
amplitude spectrum of the waveform than the narration,
but no meaning, was used as a control condition for
STORY.
Data acquisition

A 1.5 T MRI scanner (Shimadzu-Marconi Magnex
ECLIPSE 1.5 T, Shimadzu Corp., Kyoto, Japan) locatedat the Advanced Telecommunications Research Institute
Brain Imaging Center was used to obtain blood-oxygen
level-dependent contrast functional images. Images
weighted with their apparent transverse relaxation time(T2*) were obtained with an echo-planar imaging (EPI)
sequence (repetition time = 5 s, echo time = 50 ms, flip
angle = 901). A total of 369 image volumes (64  64  64
voxels at 3-mm isotropic resolutions that gave a total
field-of-view 192  192 mm2) were acquired over 30 min.
In a separate session, high-resolution whole-brain images
were acquired from each participant to improve thelocalization of activation foci using a T1-weighted threedimensional radio frequency spoiled Fourier-acquired
steady-state technique (RF spoiled FAST) covering thewhole brain.

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1378 NeuroReport 2009, Vol 20 No 15

Fig. 1

Pencil task

Scissor task
6 mm
( )
2 cm

Touch both sides of the lines

Cut each line with three strokes

Chopstick task

5 mmMove one bead at a time. Move until
all beads are moved to the left,then move all beads to the right

Example of the blocked design
EXECUTION
40 s

HOLD
20 s

STORY
40 s

IMAGERY
40 s

HOLD
20 s

REVERSED
× 3 times
40 s

EXECUTION, STORY, IMAGERY and REVERSED were in random order
Top panel: task instructions in the EXECUTION condition (scissor, pencil and chopstick). Bottom panel: organization of scanning sessions.

Data processing and statistics

Statistical Parametric Mapping (SPM) 2 software [13] wasused for image processing and statistical analysis. The
first three volumes of each session were discarded to allow
for T1 equilibration, whereas the remaining 120 image
volumes were unwrapped [14] and realigned to the first
volume; these realigned volumes were used to create amean image. Estimated head movements did not exceed
the acquired voxel size. T2 and T1 structural images
were aligned to the mean EPI image and then spatiallynormalized to the Montreal Neurological Institute (MNI;
Montreal, Canada) reference brain. The normalized
images of 2  2  2 mm3 were spatially smoothed for thegroup analysis using the full-width-half-maximum 6 mm
Gaussian kernel. Though the exact location of Broca’s areacannot be resolved, it is generally agreed that it includes
the dysgranular region of BA44 and granular BA45. To
focus on activity in Broca’s area, EPI images were thus
restricted to all voxels included in a cytoarchitectonicallydefined probabilistic map of BA44 and BA45 in the left
hemisphere [15]. We did not apply smoothing to these
EPI images in order to identify task-related activity
voxelwise for individual participant analysis.
Parameter estimates for the EXECUTION, IMAGERY,
HOLD, STORY and REVERSE trials were determined by
fixed-effect analysis for each participant using a box–carfunction convolved with a hemodynamic response function and high-pass filtering (cut-off frequency 400 ms).
Significance was assessed using voxel-wise t-statistics
assembled into statistical parametric maps.

Results
Three contrasts of interest were computed [EX:EXECUTION–HOLD, IM: IMAGERY–HOLD and LG(for language): STORY—REVERSE]. The resulting contrast images for each participant were used to compute a
random-effect analysis of variance (Table 1 and Fig. 2) to
identify voxels that were activated during language perception (LG), tool use (conjunction between EX and IM)
and both language perception and tool use (conjunction
between EX, IM and LG). The experimental conditions
and contrasts were chosen to control for somatic andauditory sensory feedback. Conjunctions were computed
as the minimum statistical value of the contrast images[16], that is, all individual contrasts used for calculating
the conjunction are significant at the threshold used. As
this implementation of conjunction is conservative andprovided our strong hypotheses on the involvement ofregions within the left inferior frontal gyrus in the tasks
used, all contrasts were thresholded at a P value of lessthan 0.001 uncorrected. In addition, most of the activatedclusters survive false discovery rate corrections for multiple
comparisons at a P value of less than 0.05 (Fig. 2).

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Language and tool use in Broca’s area Higuchi et al. 1379

Table 1Results of the random-effect analysis
ClusterPeakaCytoarchitectonic composition

No. of voxels
Language
521

Coordinates (MNI)

No. of assigned
voxelsAssigned area

x

y

z

Z-value

Cytoarchitectonic probabilities

255
165

BA45
BA44

– 52

24

18

4.53

BA45 (80%), BA44 (20%)

4

BA45

– 40

14

28

3.33

BA 44 (50%)
BA44 (40%), BA3a (10%),BA4p (10%)

9Tool use
32

29

BA44

– 50

2

20

3.43

2

1

BA44

– 58

10

4

3.13

BA44 (40%), BA45 (10%)

1Language and tool use
44

1

BA44

– 50

6

34

3.09

BA44 (40%) BA6 (10%) BA3b (10%)

28
2

BA44
BA6

– 50

8

36

4.69

BA44 (30%), BA6 (10%)

BA, Brodmann area; Language, LG; Tool use, conjunction between EX and IM; Language and tool use: conjunction between LG, IM and EX (P < 0.001 uncorrected).
Number of voxels assigned to cytoarchitectonic area in the maximum probability maps [17]. Note that the summation is not equal to the cluster size because the maps do
not cover the entire cortical surfaces.

aSignificantly activated clusters were located using theprobabilistic map of BAs [15] implemented in the SPM
Anatomy toolbox [17]. Those probabilities were shownin Table 1. The group analysis identified significantly
activated clusters for the contrast LG in Broca’s area,
both BA44 and BA45. The voxels of the larger cluster
were assigned to BA44 and BA45. The probability of theassignment to BAs at the peak coordinates of LG cluster
was 80% for BA45 and 20% for BA44. The conjunction
analysis between EX and IM yielded significantly activatedclusters related to tool use in Broca’s area. The voxels of
the most largely activated cluster was assigned to BA44,
with no voxel assigned to BA45. The probability of theassignment to BA at the peak coordinates of this cluster
was 40% for BA44, while assignment to BA3p and BA4p
was as low as 10%. The conjunction between LG, EX andIM showed an overlap of activity in the dorsal part of BA44.
Voxels in this cluster were assigned to BA44 (28 of 44,
64%) and BA6 (two of 44, 5%). The peak of this cluster
was assigned probabilistically to BA44 (30%) and, with lessprobability, to BA6 (10%). Altogether, cytoarchitectonic
probabilities corroborate the localization of this cluster toBA44 of Broca’s area.
The image at the centre of Fig. 2a shows group mean
activity rendered on the mean of individual participants’normalized T1-structural images. Bar graphs of Fig. 2a
indicate percent signal changes from control conditions(IM, EX and LG) at the peaks of the three activatedclusters illustrated at the centre and detailed in Table 1.
The signal changes were averaged across sessions andthen participants. As shown in the upper bar graph of
Fig. 2a, the peak of the middle cluster (x = – 50, y = 8
and z = 36) is significantly activated in the threecontrasts. The peak in the posterior cluster (x = – 52,
y = 2, z = 20; right graph) is significantly activated in
the two contrasts related to tool use (IM and EX).

In contrast, at the peak of the anterior cluster (x = – 52,
y = 24, z = 18; left graph), a significant increase in activity
was only found for the contrast LG. Figure 2b shows
results of a typical participant, indicating that the activity
pattern is similar to the above group analysis. Out of the
16 participants in the study, eight showed significantly
activated voxels for the conjunction of language and tooluse (IM, EX and LG) in the posterior part of BA44 at a
P value of less than 0.001 uncorrected, and 15 at P valueof less than 0.01 uncorrected.

Discussion
A cluster responding to verb generation and a task usuallyassociated with the mirror system, action observation, waspreviously reported in Broca’s area [18]. The tasks inthe present experiment are complementary, perception of
language and execution of action, in order to fully assess
the activity of this area during the execution and theperception in the two fields of research. The overlap ofactivity between tasks related to language and tool use in
the dorsal part of BA44 found in the group analysis (seeFig. 2a) and also present in 15 of the 16 participants (seeresults from a typical participant in Fig. 2b) suggests thatsimilar neural computations are used for both language
perception and skills related to tool use.
Broca’s area has an important role in unifying semantics,
syntax and phonetic processes, and is important for bothlanguage production (verb generation) and comprehension (listening to a story) [19]. Both language production
and comprehension rely on the sequential applicationof syntactic rules used to combine a finite number ofsymbols to form and understand meaningful sentences[20]. It was reported that the posterior part of Broca’sarea, comprising the dorsal part of BA44, is involved inthese syntactic aspects of language [11]. Thus, finding

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1380 NeuroReport 2009, Vol 20 No 15

Fig. 2(a)[− 50,8,36]
∗∗

0.5

∗∗

0.4
0.3

∗∗

0.2
0.1
0
IM
[− 52,24,18]

0.5
0.4

EX

LG

0.5

0.3

0.4

0.2

0.3

0.1

0.2

0

0.1

− 0.1

0

− 0.2

− 0.1
IM

EX

[− 52,2,20]
∗∗

0.6

∗∗

∗

IM

LG

EX

LG

X = − 50
(b)

2.0
1.8
1.6
1.4
1.2
1.0
0.8
0.6
0.4
0.2
0

∗∗

∗∗

[− 50,24,18]∗∗[− 60,10,18]
IM

2.5[− 54,12,34]

EX

LG

∗∗

3.0
∗∗

2.5

2.0

2.0
1.5

∗∗

1.5
1.0

2.0

0.5

0.5

0

0
IM

EX

LG

IM

EX

LG

X = –53
Activity in Broca’s area related to tool use and language. (a) Results of a random-effect analysis superimposed on sagittal sections of the average ofour participants’ normalized T1 images (cyan: LG; red: conjunction EX and IM; yellow: conjunction of LG, EX and IM.) Histograms show average
percent signal change from control condition (IM, EX, LG) averaged across sessions and then participants ( ± standard error). *Significant at
P < 0.001 uncorrected; **P < 0.05 FDR corrected. (b) Activity from a typical participant superimposed on sagittal sections of the normalized
individual T1 image. Histograms show the mean percent signal change averaged across the three sessions (color codes in figure and histogramsand error bars follow Fig. 2a).

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Language and tool use in Broca’s area Higuchi et al. 1381

activity in the dorsal part of BA44 for the contrast used
to show language-related activities (LG) suggests thatin the present experiment, this dorsal part of BA44 is
involved in these syntactic aspects of language perception. The tool-use tasks used in our study included thesequential application of learned rules, that is, ‘action
grammar’, for the appropriate control of tool–target
interactions (see Methods). It is known that observationof sequenced biological actions activates Broca’s area[21]. In agreement with our hypothesis, the execution or
imagination of sequential actions in the tool-use tasks
used here (IM and EX) also activates Broca’s area.
The cluster activated by both tool use and language (IM,EX and LG) is located in the dorsal part of BA44. Thispart of Broca’s area was recently proposed to be devoted
to grammatical aspects of language [11] and specificallyto complex hierarchical sequential processing (e.g.
understanding of embedded sentence), but not for
simpler forms of grammar processing devoid of hierarchical structure [3]. As application of sequentially organizedrules is a common feature between the tasks used in thisexperiment, comprehension of complex sentences andcorrect sequential use of common tools, the overlap ofbrain activity supports our hypothesis that the same neuralprocesses are used to process these complex hierarchicalstructures despite the difference between their cognitive
fields, language and motor control, respectively. Furthermore, these data, together with earlier findings of common
activity for execution and perception of language andaction [18], suggest that this region is part of a mirror
system devoted to the processing of complex hierarchicalstructures. The homologue region in the right hemisphereis more activated for the execution of a complex form oftool making, that possess a hierarchical structure, thanfor a simpler form of tool-making devoid of such a structure, and this hierarchical involvement was interpreted inrelation to the evolution of language [22]. In addition, theuse of a common system for execution and perception ofboth language and action may maximize the computational
power of limited neural resources.

records activate the same left inferior frontal cortex
region [23]. Thus, our finding of an overlap of activity inBA44 supports the gradual view that the neural correlatesof sequentially organized behaviour, exemplified by tooluse, were already present in a rudimentary form in ourlast common ancestors with primates, and were later
exapted to support language in humans [1].

Acknowledgement
This study was supported, in part, by the National
Institute of Information and Communications Technology (NICT-KARC).

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There are similarities between language and tool use interms of their underlying computational principles, inparticular, their hierarchical structure. The overlap ofbrain activity reported in the present experiment ina region devoted to processing of complex grammar
suggests that the same neural processes underlie thesesimilar computational principles between language andtool use. This system could be uniquely human [20] andcould have been first devoted to language before being
gradually expanded and adapted for tool use. Yet, inmonkeys, neural correlates of tool use include the depthof the arcuate sulcus [7], the putative homologue ofhuman BA44 [8]. In addition, modern humans performing
the oldest form of tool making found in archaeological

17

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19
20
21

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