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 language in shadow


E' mai capitato che qualcuno, ben lontano dal senso figurato della frase, abbia concretamente chiesto la vostra testa? Capita talvolta, ed a me ed ai miei allievi e capitato di ricevere simile cortese invito dai ricercatori dell'Università di Ferrara. Certo, per la scienza questo ed altro, ma in fondo la nostra collaborazione richiesta riguardava  alcuni libri ideati dal sottoscritto e realizzati con la collaborazione della classe. Una sola piccola aggiunta:  la motilità delle nostre mani e le nostre cervici   da sottoporre ad analisi delle strumentazioni. Di che si trattava? Di alcuni dei nostri libri relativi all'"arte nera", detta anche umbromania o più volgarmente:"ombre cinesi". Agli scienziati interessava capire i meccanismi segreti del cervello umano quando quest'ultimo si opparoccia alla creazioni di immagimni attraverso la simbologia delle mani. Il resto, per chi è pratico della lingua inglese è tutto, a seguire, riportato da una importante rivista scientifica internazionale...










language in shadow

Luciano Fadiga

University of Ferrara, Ferrara, Italy and Italian Institute of Technology, Genova, Italy

Laila Craighero, Maddalena Fabbri Destro, and Livio Finos



University of Ferrara, Ferrara, Italy

Nathalie Cotillon-Williams and Andrew T. Smith

Royal Holloway, University of London, London, UK

Umberto Castiello

Royal Holloway, University of London, London, UK and University of Padova, Padova, Italy

The recent finding that Broca’s area, the motor center for speech, is activated during action observation

lends support to the idea that human language may have evolved from neural substrates already involved

in gesture recognition. Although fascinating, this hypothesis can be questioned because while observing

actions of others we may evoke some internal, verbal description of the observed scene. Here we present

fMRI evidence that the involvement of Broca’s area during action observation is genuine. Observation of

meaningful hand shadows resembling moving animals induces a bilateral activation of frontal language

areas. This activation survives the subtraction of activation by semantically equivalent stimuli, as well as

by meaningless hand movements. Our results demonstrate that Broca’s area plays a role in interpreting

actions of others. It might act as a motor-assembly system, which links and interprets motor sequences for

both speech and hand gestures.



Several theories have been proposed to explain

the origins of human language. They can be

grouped into two main categories. According to

‘‘classical’’ theories, language is a peculiarly human

ability based on a neural substrate newly

developed for the purpose (Chomsky, 1966;

Pinker, 1994). Theories of the second ‘‘evolutionary’’

category consider human language as

the evolutionary refinement of an implicit communication

system, already present in lower

primates, based on a set of hand/mouth goaldirected

action representations (Armstrong,

Stokoe, & Wilcox, 1995; Corballis, 2002; Rizzolatti

& Arbib, 1998). The classical view is supported

by the existence in humans of a cortical

network of areas that become active during

verbal communication. This network includes

the temporalparietal junction (Wernicke’s

area), commonly thought to be involved in

sensory processing of speech, and the inferior

frontal gyrus (Broca’s area) classically considered

to be the speech motor center.

Correspondence should be addressed to: Luciano Fadiga, Department of Biomedical Sciences and Advanced Therapies, Section

of Human Physiology, University of Ferrara, via Fossato di Mortara 17/19, I-44100 Ferrara, Italy. E-mail:

This work was supported by EC grants ROBOT-CUB, NEUROBOTICS and CONTACT to LF and LC by European Science

Foundation (OMLL Eurocores) and by Italian Ministry of Education grants to LF, and by a Research Strategy Fund to UC.

We thank Attilio Mina for helpful bibliographic suggestions on animal hand shadows, Carlo Truzzi for creating the hand shadows

stimuli, and Rosario Canto for technical support.

# 2006 Psychology Press, an imprint of the Taylor & Francis Group, an informa business


SOCIAL NEUROSCIENCE, 2006, 1 (2), 7789 DOI:10.1080/17470910600976430

However, the existence of areas exclusively

devoted to language has increasingly been challenged

by experimental evidence showing that

Broca’s area and its homologue in the right

hemisphere also become active during the observation

of hand/mouth actions performed by

other individuals (Aziz-Zadeh, Koski, Zaidel,

Mazziotta, & Iacoboni, 2006; Decety et al., 1997;

Decety & Chaminade, 2003; Grafton, Arbib,

Fadiga, & Rizzolatti, 1996; Gre`zes, Costes, &

Decety, 1998; Gre`zes, Armony, Rowe, & Passingham,

2003; Iacoboni, Woods, Brass, Bekkering,

Mazziotta, & Rizzolatti, 1999; Rizzolatti et al.,

1996). This finding seems to favor the evolutionary

hypothesis, supporting the idea that the

linguistic processing that characterizes Broca’s

area may be closely related to gesture processing.

Moreover, comparative cytoarchitectonic studies

have shown a similarity between human Broca’s

area and monkey area F5 (Matelli, Luppino, &

Rizzolatti, 1985; Petrides, 2006; Petrides & Pandya,

1997; von Bonin & Bailey, 1947), a premotor

cortical region that contains neurons discharging

both when the monkey acts on objects and

when it sees similar actions being made by

other individuals (Di Pellegrino, Fadiga, Fogassi,

Gallese, & Rizzolatti, 1992; Gallese, Fadiga,

Fogassi, & Rizzolatti, 1996; Rizzolatti, Fadiga,

Gallese, & Fogassi, 1996). These neurons, called

‘‘mirror neurons,’’ may allow the understanding

of actions made by others and might provide a

neural substrate for an implicit communication

system in animals. It has been proposed that this

primitive ‘‘gestural’’ communication may be at

the root of the evolution of human language

(Rizzolatti & Arbib, 1998). Although fascinating,

this theoretical framework can be challenged by

invoking an alternative interpretation, more conservative

and fitting with classical theories of the

origin of language. According to this view, humans

are automatically compelled to covertly

verbalize what they observe. The involvement of

Broca’s area during action observation may

therefore reflect inner, sub-vocal speech generation

(Gre`zes & Decety, 2001). Clearly, an

experiment determining which of these two

interpretations is correct, could provide a fundamental

insight into the origins of language.

We investigated here the possibility that Broca’s

area and its homologue in the right hemisphere

become specifically active during the

observation of a particular category of hand

gestures: hand shadows representing animals

opening their mouths. These stimuli have been

selected for two main reasons. First, by using

these stimuli it was possible to design an fMRI

experiment in which any activation due to covert

verbalization could be removed by subtraction:

the activation evoked while observing videos

representing stimuli belonging to the same semantic

set (i.e., real animals opening their

mouths), and expected to elicit similar covert

verbalization, could be subtracted from activity

elicited by hand shadows of animals opening their

mouths. Residual activation in Broca’s area after

this critical subtraction would demonstrate the

involvement of ‘‘speech-related’’ frontal areas in

processing meaningful hand gestures. Second,

hand shadows only implicitly ‘‘contain’’ the

hand creating them. Thus they are interesting

stimuli that might be used to answer the question

of how detailed a hand gesture must be in order

to activate the mirror-neuron system. The results

we present here support the idea that Broca’s

area is specifically involved during meaningful

action observation and that this activation is

independent of any internal verbal description

of the seen scene. Moreover, they demonstrate

that the mirror-neuron system becomes active

even if the pictorial details of the moving hand

are not explicitly visible. In the case of our

stimuli, the brain ‘‘sees’’ the performing hand

also behind the appearance.



Participants were 10 healthy volunteers (6 females

and 4 males; age range 1932, mean 23).

All had normal or corrected vision, no past

neurological or psychiatric history and no structural

brain abnormality. Informed consent was

obtained according to procedures approved by

the Royal Holloway Ethics Committee. Throughout

the experiment, subjects performed the same

task, which was to carefully observe the stimuli,

which were back projected onto a screen visible

through a mirror mounted on the MRI head coil

(visual angle, 158/208 approximately). Stimuli

were of six types: (1) movies of actual human

hands performing meaningless movements; (2)

movies of the shadows of human hands representing

animals opening their mouths; (3) movies of

real animals opening their mouths, plus, as controls,

three further movies representing a sequence

of still images taken from the previously

described three videos. Hand movements were

performed by a professional shadow artist. All


stimuli were enclosed in a rectangular frame

(Figure 1 and online supplementary materials),

in a 640/480 pixel array and were shown in grey

scale. Each movie lasted 15 seconds, and contained

a sequence of 7 different moving/static

stimuli (e.g., dog, cow, pig, bird, etc., all opening

their mouths). The experiment was conducted as a

series of scanning sessions, each lasting 4 minutes.

Each session contained eight blocks. In each

session two different movie types were presented

in an alternated order (see Figure 1, bottom).

Each subject completed six sessions. The order of

sessions was varied randomly across subjects. The

six sessions contrasted the following pairs of

movie types: (1) C1/moving animal hand shadows,


C2/static animal hand shadows; (2) C1/


moving real hands, C2/static real hands; (3)


C1/moving real animals, C2/static real animals;


(4) C1/moving animal hand shadows,


C2/moving real animals; (5) C1/moving animal


hand shadows, C2/moving real hands; (6)


C1/moving real hands, C2/moving real animals.

Whole-brain fMRI data were acquired on a

3T scanner (Siemens Trio) equipped with an RF

volume headcoil. Functional images were obtained

with a gradient echo-planar T2* sequence

using blood oxygenation level-dependent

(BOLD) contrast, each comprising a full-brain

volume of 48 contiguous axial slices (3 mm thickness,

3/3 mm in-plane voxel size). Volumes were

acquired continuously with a repetition time (TR)

of 3 seconds. A total of 80 scans were acquired for

each participant in a single session (4 minutes),

with the first 2 volumes subsequently discarded to

allow for T1 equilibration effects. Functional MRI

data were analyzed using statistical parametric

mapping software (SPM2, Wellcome Department

of Cognitive Neurology, London). Individual

scans were realigned, spatially normalized and

transformed into a standard stereotaxic space, and

spatially smoothed by a 6 mm FWHM Gaussian

kernel, using standard SPM methods. A high-pass

temporal filter (cut-off 120 seconds) was applied

to the time series. Considering the relatively low

number of participants, a high-threshold, corrected,

fixed effects analysis, was first performed

by each experimental condition. Pixels were

identified as significantly activated if pB/.001

(FDR corrected for multiple comparisons) and

the cluster size exceeded 20 voxels. The activated

voxels surviving this procedure were superimposed

on the standard SPM2 inflated brain

(Figure 1). Clusters of activation were anatomically

characterized according to their centers of

mass activity with the aid of Talairach co-ordinates

(Talairach & Tournoux, 1988), of the

Muenster T2T converter (http://neurologie.unimuenster.

de/T2T/t2tconv/conv3d.html) and by

taking into account the prominent sulcal landmarks.

Furthermore, as far as Broca’s region is

concerned, a hypothesis-driven analysis was performed

for sessions (3)(6). In this analysis, a

more restrictive statistical criterion was used

(group analysis on individual subjects analysis,

small volume correction approach, cluster size

/20 voxels). Only significant voxels (pB/.005)

within the most permissive border of cytoarchitectonically

defined probability maps (Amunts,

Schleicher, Burgel, Mohlberg, Uylings, & Zilles,

1999) were considered. This last analysis was

performed with the aid of the Anatomy SPM

toolbox (Eickhoff et al., 2005). Subjects’ lips were

video-monitored during the whole scanning procedure.

No speech-related muscle activity was

detectable during video presentation. The absence

of speech-related motor activity during

video presentation was assessed in a pilot experiment,

on a set of different subjects, looking at the

same videos presented in the scanner while

electromyography of tongue muscles was recorded

according to the technique used by Fadiga,

Craighero, Buccino, and Rizzolatti (2002).


During the fMRI scanning volunteers observed

videos representing: (1) the shadows of human

hands depicting animals opening and closing their

mouths; (2) human hands executing sequences of

meaningless finger movements; or (3) real animals

opening their mouths. Brain activations were

compared between pairs of conditions in a block

design. In addition (4, 5, 6), each condition was

contrasted with a ‘‘static’’ condition, in which the

same stimuli presented in the movie were shown

as static pictures (e.g., stills of animals presented

for the same time as the corresponding videos).

The comparison between the first three ‘‘moving’’

conditions with each corresponding ‘‘static’’ one,

controls for nonspecific activations and emphasizes

the action component of the gesture.

Figure 1 shows, superimposed, the results of the

moving vs. static contrasts for animal hand

shadows and real animals conditions (red and

green spots, respectively). In addition to largely

overlapping occipito-parietal activations, a specific

differential activation emerged in the anterior


Figure 1 (See opposite for caption)


part of the brain. Animal hand shadows strongly

activated left parietal cortex, pre- and postcentral

gyri (bilaterally), and, more interestingly

for the purpose of the present study, bilateral

inferior frontal gyrus (BA 44 and 45). Conversely,

the only frontal activation reaching significance in

the moving vs. static contrast for real animals was

located in bilateral BA 6, close to the premotor

activation shown in an fMRI experiment by

Buccino et al. (2004) when subjects observed

mouth actions performed by monkeys and dogs.

This location may therefore correspond to a

premotor region where a species-independent

mirror-neuron system for mouth actions is present

in humans. A discussion of non-frontal activations

is beyond the scope of the present paper, however

the above threshold activation foci are listed in

Table 1. The results shown in Figure 1 on one side

seem to rule out the possibility that the inferior

frontal activity induced by action viewing is due

to covert speech, on the other side indicate that

the shadows of animals opening their mouths,

although clearly depicting animals and not hands,

convey implicit information about the human

being moving her hand in creating them. Indeed,

they evoke an activation pattern superimposable

on that evoked by hand action observation

(Buccino et al., 2001; Grafton et al., 1996; Gre`zes

et al., 2003; see Figure 1 and Table 1). To interpret

this result, it may be important to stress the

peculiar nature of hand shadows: although they

are created by moving hands, the professionalism

of the artist creating them is such that the hand is

never obvious. Nevertheless, the mirror-neuron

system is activated. The possibility we favor is

that the brain ‘‘sees’’ the hand behind the

shadow. This possibility is supported by recent

data demonstrating that monkey mirror neurons

become active even if the final part of the

grasping movement is performed behind a screen

(Umilta` et al., 2001). Consequently, the human

mirror system (or at least part of it) seems to act

more as an active interpreter than as a passive


The bilateral activation of inferior frontal

gyrus shown in Figure 1 during observation of

animal hand shadows cannot yet be attributed to

covert verbalization. This is because it survives

the subtraction of still images representing the

same stimuli presented in the moving condition,

which might also evoke internal naming. It could

be argued, however, that videos of moving

animals and animal shadows are dynamic and

richer in details than their static controls, and

might more powerfully evoke a semantic representation

of the observed scene, but this cannot

be stated with confidence. We therefore made a

direct comparison between moving animal hand

shadows and moving real animals. We narrowed

the region of interest from the whole brain (as in

Figure 1) to bilateral BA 44, the main target of

our study. This hypothesis-driven analysis was

performed by looking at voxels within the most

permissive borders of the probabilistic map of this

area provided by Amunts et al. (1999) by taking

as significance threshold the p value of .005

(random effect analysis). The results of this

comparison are shown in Figure 2B. As already

suggested by Figure 1 and Table 1, right and

(more interestingly) left frontal clusters survived

this subtraction. The first one was located in right

BA 44 (X/58, Y/12, Z/24), an area known to

be involved during observation of biological

action, either meaningful or meaningless (Gre`zes

et al., 1998; Iacoboni et al., 1999). The second one

is symmetrically positioned on the left side (X/


/50, Y/4, Z/22). Finally, two additional

clusters were present in Broca’s region. One was

more posterior, in that part of the inferior frontal

gyrus classically considered as speech related

(X//58, Y/12, Z/14; pars opercularis) and

one more anterior, within area 45 according to

the Talairach and Tournoux atlas (1988), (X/


/45, Y/32, Z/14; pars triangularis). This

finding agrees with our hypothesis and demonstrates

that the activation of Broca’s area during

action understanding is independent of internal

verbalization: if an individual is compelled to

verbalize internally when a hand-shadow representing

an animal is presented, the same individual

should also verbalize during the observation

of real animals.

The finding that Broca’s area involvement

during observation of hand shadows is not

Figure 1 (opposite). Cortical activation pattern during observation of animal hand shadows and real animals. Significantly activated


voxels (pB/.001, fixed effects analysis) in the moving animal shadows and moving real animals conditions after subtraction of the

static controls. Activity related to animal shadows (red clusters) is superimposed on that from real animals (green clusters). Those

brain regions activated during both tasks are depicted in yellow. In the lowermost part of the figure the experimental time-course for

each contrast is shown (i.e., C1, moving; C2, static). Note the almost complete absence of frontal activation for real animals in

comparison to animal shadows, which bilaterally activate the inferior frontal gyrus (arrows).



Montreal Neurological Institute (MNI) and Talairach (TAL) co-ordinates and T-values of the foci activated during observation of

moving animal hand shadows, real hands, and real animals, after subtraction of static conditions


x y z x y z T-value

Animal hand shadows

Inferior frontal gyrus

BA 44

R 62 8 24 61 9 22 4.71

L /62 8 24 /61 9 22 4.58

BA 45

R 58 22 14 57 22 12 3.37

Precentral gyrus

BA 6

R 54 0 36 53 2 33 5.29

60 2 34 59 4 31 4.90

L /60 /2 36 /59 0 33 5.09


/60 0 18 /59 1 17 3.56


/60 /12 38 /59 /10 36 5.24

BA 4

R 54 /18 36 53 /16 34 7.97

Postcentral gyrus

BA 40

L /58 /22 16 /57 /21 16 5.92

BA 3

L /32 /38 52 /32 /34 50 6.53

BA 2

R 32 /40 66 32 /36 63 5.18

Superior parietal lobule

BA 7

R 26 /48 64 26 /44 61 6.24


BA 18

R 16 /100 6 16 /97 10 10.43


20 /96 8 20 /93 12 12.36


L /16 /104 2 /16 /101 7 5.09

Middle occipital gyrus

BA 18

R 42 /90 8 42 /87 12 7.78


L /28 /96 2 /28 /93 6 6.95

BA 19

L /40 /86 0 /40 /83 4 7.28


BA 13

R 54 /40 20 54 /38 20 6.35

Middle temporal gyrus

BA 37

R 54 /70 2 53 /68 5 10.95

Temporal fusiform gyrus

BA 37

R 42 /44 /16 42 /43 /11 7.52


L /44 /44 /16 /44 /43 /11 6.44


R 10 /80 /44 8 /80 /42 6.53


L /8 /78 /44 /8 /77 /33 5.61


R 22 /2 /22 22 /3 /18 3.85


L /18 /2 /22 /18 /3 /18 4.15


TABLE 1 (Continued )



x y z x y z T-value

Real hands

Inferior frontal gyrus

BA 44

R 62 16 28 61 17 25 5.67

L /60 10 26 /60 12 23 3.64

Middle frontal gyrus

BA 6

R 34 /6 62 34 /3 57 5.30


L /24 /8 52 /24 /5 48 4.18

Superior frontal gyrus

BA 10

R 4 58 28 4 58 23 6.22

L /26 54 /2 /27 52 /4 4.14

Postcentral gyrus

BA 3

R 52 /20 40 51 /18 38 4.71

BA 7

R 28 /50 66 28 /46 63 12.50

BA 40

R 46 /32 54 46 /29 51 4.58


L /66 /22 14 /65 /21 14 3.37

Inferior parietal lobule

BA 40

R 62 /30 28 61 /28 27 4.02


32 /42 58 32 /38 55 8.23


L /50 /30 32 /50 /28 31 5.09


/34 /42 58 /34 /38 55 6.51

Superior parietal lobule

BA 7

L /32 /56 62 /33 /51 60 4.94


BA 18

L /20 /94 6 /20 /91 10 7.13

Middle occipital gyrus

BA 19

L /54 /76 2 /53 /74 6 7.42


/36 /62 14 /36 /59 16 7.60

Lingual gyrus

BA 17

R 10 /96 /8 10 /93 /2 5.74

Inferior occipital gyrus

BA 18

R 30 /94 /12 30 /92 /6 6.10


L /26 /96 /8 /26 /93 /2 6.69

Middle temporal gyrus

BA 37

R 52 /68 2 51 /66 5 7.78

Temporal fusiform gyrus

BA 37

R 46 /42 /18 46 /41 /13 5.45


L /46 /44 /16 /46 /43 /11 4.59


R 20 /82 /28 20 /81 /20 4.11


L /28 /56 /50 /28 /56 /39 5.10

Parahippocampal gyrus

BA 34

R 30 6 /18 30 5 /15 6.75


R 52 /22 18 51 /20 18 6.05


TABLE 1 (Continued )



x y z x y z T-value

Globus pallidus

R 16 2 2 16 2 2 4.10

L /16 0 /2 /16 0 /2 3.59


Real animals

Precentral gyrus

BA 4

L /62 /14 38 /61 /12 36 6.61

BA 6

R 36 /2 34 36 0 31 5.93


32 /12 52 32 /9 48 4.48


L /30 0 38 /30 2 35 10.43

Middle frontal gyrus

BA 47

L /46 48 /2 /46 46 /4 3.92

Superior frontal gyrus

BA 6

R 30 /8 72 30 /4 67 3.66

BA 8

R 20 30 56 20 32 50 6.13

Postcentral gyrus

BA 2

L /38 /40 70 /38 /36 66 4.56

BA 3

R 34 /36 54 34 /32 51 3.26


L /18 /44 76 /18 /39 72 3.35


BA 7

L /8 /54 46 /8 /50 45 6.08

Middle occipital gyrus

BA 18

R 20 /98 14 20 /94 18 11.75


L /20 /94 10 /20 /91 14 14.91

BA 19

R 38 /80 2 38 /77 6 7.21


L /40 /86 /2 /40 /83 2 9.88


/54 /76 2 /53 /74 6 8.43

Lingual gyrus

BA 18

R 14 /86 /14 14 /84 /8 5.40


L /6 /88 /10 /6 /86 /4 5.24

Limbic lobe-uncus

BA 28

L /28 8 /24 /28 7 /21 7.00

Superior temporal gyrus

BA 41

L /46 /40 12 /46 /38 13 3.77

Middle temporal gyrus

BA 21

L /54 /24 /8 /53 /24 /6 3.54

BA 37

R 52 /70 4 51 /68 7 8.03

Temporal fusiform gyrus

BA 37

R 44 /42 /20 44 /41 /15 6.50


L /46 /50 /20 /46 /49 /14 4.66


R 46 /58 /32 46 /58 /24 3.55


L /48 /58 /32 /48 /58 /24 3.78


explainable in terms of internal speech suggests

that, in agreement with other data in the literature,

this area may play a crucial role in action

understanding. However, it remains the fact that

Broca’s area is known as a speech area and its

involvement during overt and covert speech

production has clearly been demonstrated recently

(Palmer, Rosen, Ojemann, Buckner, Kelley,

& Petersen, 2001). The hypothesis we favor is

that this area participates in verbal communication

because it represents the product of the

evolutionary development of a precursor already

present in monkeys: the mirror neurons area F5,

that portion of the ventral premotor cortex where

hand/mouth actions are represented (see Petrides,

2006). Accordingly, in agreement with the characteristics

of area F5 neurons, Broca’s area should

respond much better to goal-directed action than

to simple, meaningless movements. To test this

possibility, we performed two further comparisons:

(1) The observation of human hands performing

meaningless finger movements versus the

observation of moving real animals opening their

mouths, to determine how much of the pars


opercularis activation was due to the observation

of meaningless hand movements; (2) The observation

of animal hand shadows versus the observation

of meaningless finger movements, to pit

the presence of hands against the presence of

meaning. The results are shown in Figure 2, C and

D, respectively. After comparison (1), although

the more dorsal, bilateral, BA 44 activation was

still present (Figure 2C, left: X//56, Y/10,


Z/26; right: X/58, Y/10, Z/24), no voxels


above significance were located in the pars


opercularis of Broca’s area. This demonstrates

that finger movements per se do not activate

specifically that part of Broca’s area. In contrast,

after comparison (2) a significant activation was

present in the left pars opercularis (Figure 2D;


X//58, Y/6, Z/4), demonstrating the involvement


of Broca’s area pars opercularis in processing

actions of others, particularly when

meaningful and thus, implicitly, communicative.


The finding that animal hand shadows but not

real animals or meaningless finger movements

activate that part of Broca’s region most intimately

involved in verbal communication support

a similarity between these stimuli and spoken

words. Animal hand shadows are formed by

meaningless finger movements combined to

evoke a meaning in the observer through the

shape appearing on a screen. Thus, when one

looks at them, the representation of an animal

opening its mouth is evoked. Words that form

sentences are formed by individually meaningless

movements (phonoarticulatory acts), which appropriately

combined and segmented convey

meanings and representations. Does this twofold

involvement of Broca’s area reflect a specific role

played by it in decoding actions and particularly

communicative ones? A positive answer to this

question arises, in our view, from the finding that

when observation of meaningless finger movements

is subtracted from observation of animal

hand-shadows, an activation of the left pars


opercularis persists.

The activation of Broca’s area during gestural

communication has already been shown in

deaf signers, both during production and perception.

This was interpreted as a vicariant involvement

of Broca’s area because of its verbal

specialization (Horwitz et al., 2003). In other

terms, according to this interpretation, Broca’s

area is activated because, by signing, deaf

people express linguistic concepts. In our study

TABLE 1 (Continued )



x y z x y z T-value


L /34 /6 /16 /34 /6 /13 3.70

Globus Pallidus

L /24 /10 /4 /24 /10 /3 4.93

Anterior Cingulate

BA 24

L /4 36 8 /4 35 6 4.70


Note: BA/Brodmann area; R/right hemisphere; L/left hemisphere; x, y, z/co-ordinates.


participants were presented with communicative

hand gestures but, in contrast to studies investigating

deaf people, the gestures were non-symbolic

even if able to address in an unambiguous

way a specific concept (e.g., a barking dog). Thus,

we show here, the involvement of Broca’s region

can not be explained in terms of linguistic

decoding of the gesture meaning. Conversely,

the results indicate that Broca’s region is involved

in the understanding of communicative gestures.

Figure 2 (See opposite for caption)


How can this ‘‘perceptual’’ function be reconciled

with the universally accepted motor role of

Broca’s area for speech? One possible interpretation

is that Broca’s area, due to its premotor

origin, is involved in the assembly of meaningless

sequence of action units (whether finger or

phonoarticulatory movements) into meaningful

representations. This elaboration process may

proceed in two directions. In production, Broca’s

area recruits movement units to generate words/

hand actions. In perception, Broca’s area, being

the human homologue of monkey area F5,

addresses the vocabulary of speech/hand actions,

which form the template for action recognition.

Our hypothesis is that, in origin, Broca’s area

precursor was involved in generating/extracting

action meanings by organizing/interpreting motor

sequences in terms of goal. Subsequently, this

ability might have been generalized during the

evolution that gave this area the capability to deal

with meanings (and rules), which share similar

hierarchical and sequential structures with the

motor system (Fadiga, Craighero, & Roy, 2006).

This proposal is in agreement with fMRI

investigations that indicate that Broca’s area is

not always activated during speech listening. In a

recent experiment Wilson, Saygin, Sereno, and

Iacoboni (2004) carried out an fMRI study in

which subjects (1) passively listened to monosyllables

and (2) produced the same speech

sounds. Results showed a substantial bilateral

overlap between regions activated during the

two conditions, mainly in the superior part of

ventral premotor cortex. Conversely, the activation

of Broca’s region was present only in some of

the studied subjects, in our view because the task

did not require any meaning extraction. This

interpretation is in line with brain imaging studies

indicating that, in speech comprehension, Broca’s

area is mainly activated during processing of

syntactic aspects (Bookheimer, 2002). Luria

(1966) had already noticed that Broca’s area

patients made comprehension errors in syntactically

complex sentences such as passive constructions.

Finally, data coming from cortical

stimulation of collaborating patients undergoing

neurosurgery, showed that the electrical stimulation

of the Broca’s area produced comprehension

deficits, particularly evident in the case of ‘‘complex

auditory verbal instructions and visual semantic

material’’ (Schaffler, Luders, Dinner,

Lesser, & Chelune, 1993). The data of the present

experiment, together with the series of evidence

presented above, are in agreement with those

theories on the origins of human language that

consider it as the evolutionary refinement of an

implicit communication system based on hand/

mouth goal-directed action representations

(Armstrong et al., 1995; Corballis, 2002; Rizzolatti

& Arbib, 1998). This possibility finds further

support from a recent experiment based on the

analysis of brain MRIs of three great ape species

(Pan troglodytes, Pan paniscus and Gorilla gorilla)

showing that the extension of BA 44 is larger

in the left hemisphere than in the right. While a

similar asymmetry in humans has been correlated

with language dominance (Cantalupo & Hopkins,

2001), this hypothesis does not fit in the case of

apes. It might be, however, indicative of an initial

specialization of BA 44 for communication. In

fact, in captive great apes manual gestures are

both referential and intentional, and are preferentially

produced by the right hand. Moreover,

this right-hand bias is consistently greater

when gesturing is accompanied by vocalization

(Hopkins & Leavens, 1998).

In conclusion, our results support a common

origin for human speech and gestural communication

in non-human primates. It has been

proposed that the development of human speech

is a consequence of the fact that the precursor of

Broca’s area was endowed, before the emergence

of speech, with a gestural recognition system

(Rizzolatti & Arbib, 1998). Here we have taken

a step forward, empirically showing for the

first time that human Broca’s area is not an

exclusive ‘‘speech’’ center but, most probably, a

motor assembly center in which communicative

Figure 2 (opposite). Results of the analysis focused on bilateral area 44. (A) Cytoarchitectonically defined probability map of the

location of left and right area 44, drawn on the Colin27T1 standard brain on the basis of Juelich-MNI database (Amunts et al., 1999).

The white cross superimposed on each brain indicates the origin of the co-ordinates system (x/y/z/0). The correspondence


between colors and percent probability is given by the upper color bar. (B), (C) and (D), significant voxels (pB/.005, random effects

analysis) falling inside area 44, as defined by the probability map shown in (A), in the three contrasts indicated in the Figure. Color

bar: T-values. Note the similar pattern of right hemisphere activation in (B) and (C), the similar location of the posterior-dorsal


activation of the left hemisphere in (B) and (C), and the two additional foci in the pars opercularis and pars triangularis of Broca’s


area in (B). Note, in (D), the survival of the activation in pars opercularis, after subtraction of real hands from animal hand shadows.

When the reverse contrasts were tested (real animals vs. either animal shadows or real hands), the results failed to show any

significant activation within area 44.


gestures, whether linguistic or otherwise, are

assembled and decoded (Fadiga et al., 2006). It

still remains unclear whether hand/speech motor

representations are mapped in this area according

to a somatotopic organization, or if Broca’s area

works in a supramodal way, by dealing with

effector-independent motor rules.

Manuscript received 31 May 2006

Manuscript accepted 1 August 2006

First published online 6 October 2006


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