Titolo
La ricerca & la scienza
In collaborazione con Uniferrara
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.
INTRODUCTION
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: fdl@unife.it
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
www.psypress.com/socialneuroscience 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.
METHODS
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
78 FADIGA ET AL.
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).
RESULTS
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
LANGUAGE AREAS ACTIVATED BY HAND SHADOWS 79
Figure 1 (See opposite for caption)
80 FADIGA ET AL.
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
perceiver.
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).
LANGUAGE AREAS ACTIVATED BY HAND SHADOWS 81
TABLE 1
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
MNI TAL
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
Cuneus
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
Insula
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
Cerebellum
R 10 /80 /44 8 /80 /42 6.53
L /8 /78 /44 /8 /77 /33 5.61
Amygdala
R 22 /2 /22 22 /3 /18 3.85
L /18 /2 /22 /18 /3 /18 4.15
82 FADIGA ET AL.
TABLE 1 (Continued )
MNI TAL
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
Cuneus
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
Cerebellum
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
Insula
R 52 /22 18 51 /20 18 6.05
LANGUAGE AREAS ACTIVATED BY HAND SHADOWS 83
TABLE 1 (Continued )
MNI TAL
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
Precuneus
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
Cerebellum
R 46 /58 /32 46 /58 /24 3.55
L /48 /58 /32 /48 /58 /24 3.78
84 FADIGA ET AL.
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.
DISCUSSION
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 )
MNI TAL
x y z x y z T-value
Amygdala
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.
LANGUAGE AREAS ACTIVATED BY HAND SHADOWS 85
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)
86 FADIGA ET AL.
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.
LANGUAGE AREAS ACTIVATED BY HAND SHADOWS 87
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
REFERENCES
Amunts, K., Schleicher, A., Burgel, U., Mohlberg, H.,
Uylings, H. B., & Zilles, K. (1999). Broca’s region
revisited: Cytoarchitecture and intersubject variability.
Journal of Comparative Neurology, 412, 319
341.
Armstrong, A. C., Stokoe, W. C., & Wilcox, S. E.
(1995). Gesture and the nature of language. Cambridge,
UK: Cambridge University Press.
Aziz-Zadeh, L., Koski, L., Zaidel, E., Mazziotta, J., &
Iacoboni, M. (2006). Lateralization of the human
mirror neuron system. Journal of Neuroscience,
26(11), 29642970.
Bookheimer, S. (2002). Functional MRI of language:
New approaches to understanding the cortical
organization of semantic processing. Annual Review
of Neuroscience, 25, 151188.
Buccino, G., Binkofski, F., Fink, G. R., Fadiga, L.,
Fogassi, L., Gallese, V., et al. (2001). Action
observation activates premotor and parietal areas
in a somatotopic manner: An fMRI study. European
Journal of Neuroscience, 13, 400404.
Buccino, G., Lui, F., Canessa, N., Patteri, I., Lagravinese,
G., Benuzzi, F., et al. (2004). Neural circuits
involved in the recognition of actions performed by
nonconspecifics: An fMRI study. Journal of Cognitive
Neuroscience, 16, 114126.
Cantalupo, C., & Hopkins, W. D. (2001). Asymmetric
Broca’s area in great apes. Nature, 414(6863), 505.
Chomsky, N. (1966). Cartesian linguistics. New York:
Harper & Row.
Corballis, M. C. (2002). From hand to mouth. The
origins of language. Princeton, NJ: Princeton University
Press.
Decety, J., & Chaminade, T. (2003). Neural correlates
of feeling sympathy. Neuropsychologia, 41, 127138.
Decety, J., Gre`zes, J., Costes, N., Perani, D., Jeannerod,
M., Procyk, E., et al. (1997). Brain activity during
observation of actions: Influence of action content
and subject’s strategy. Brain, 120, 17631777.
Di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., &
Rizzolatti, G. (1992). Understanding motor events:
A neurophysiological study. Experimental Brain
Research, 91, 176180.
Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes,
C., Fink, G. R., Amunts, K., et al. (2005). A new
SPM toolbox for combining probabilistic cytoarchitectonic
maps and functional imaging data. Neuroimage,
25, 13251335.
Fadiga, L., Craighero, L., & Roy, A. C. (2006). Broca’s
area: A speech area? In Y. Grodzinsky & K. Amunts
(Eds.), Broca’s region. New York: Oxford University
Press.
Fadiga, L., Craighero, L., Buccino, G., & Rizzolatti, G.
(2002). Speech listening specifically modulates the
excitability of tongue muscles: A TMS study. European
Journal of Neuroscience, 15, 399402.
Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G.
(1996). Action recognition in the premotor cortex.
Brain, 119, 593609.
Grafton, S. T., Arbib, M. A., Fadiga, L., & Rizzolatti, G.
(1996). Localization of grasp representations in
humans by PET: 2. Observation compared with
imagination. Experimental Brain Research, 112,
103111.
Gre`zes, J., & Decety, J. (2001). Functional anatomy of
execution, mental simulation, observation, and verb
generation of actions: A meta-analysis. Human
Brain Mapping, 12, 119.
Gre`zes, J., Armony, J. L., Rowe, J., & Passingham, R. E.
(2003). Activations related to ‘‘mirror’’ and ‘‘canonical’’
neurones in the human brain: An fMRI study.
Neuroimage, 18, 928937.
Gre`zes, J., Costes, N., & Decety, J. (1998). Top-down
effect of strategy on the perception of human
biological motion: A PET investigation. Cognitive
Neuropsychology, 15, 553582.
Hopkins,W. D., & Leavens, D. A. (1998). Hand use and
gestural communication in chimpanzees (Pan troglodytes).
Journal of Comparative Psychology,
112(1), 9599.
Horwitz, B., Amunts, K., Bhattacharyya, R., Patkin, D.,
Jeffries, K., Zilles, K., et al. (2003). Activation of
Broca’s area during the production of spoken and
signed language: A combined cytoarchitectonic
mapping and PET analysis. Neuropsychologia, 41,
18681876.
Iacoboni, M., Woods, R. P., Brass, M., Bekkering, H.,
Mazziotta, J. C., & Rizzolatti, G. (1999). Cortical
mechanisms of human imitation. Science, 286, 2526
2528.
Luria, A. (1966). The higher cortical function in man.
New York: Basic Books.
Matelli, M., Luppino, G., & Rizzolatti, G. (1985).
Patterns of cytochrome oxidase activity in the
frontal agranular cortex of macaque monkey. Behavioral
Brain Research, 18, 125137.
Palmer, E. D., Rosen, H. J., Ojemann, J. G., Buckner,
R. L., Kelley, W. M., & Petersen, S. E. (2001). An
event-related fMRI study of overt and covert word
stem completion. Neuroimage, 14, 182193.
Petrides, M. (2006). Broca’s area in the human and
nonhuman primate brain. In Y. Grodzinsky & K.
Amunts (Eds.), Broca’s region. New York: Oxford
University Press.
Petrides, M., & Pandya, D. N. (1997). Comparative
architectonic analysis of the human and the macaque
frontal cortex. In F. Boller & J. Grafman (Eds.),
88 FADIGA ET AL.
Handbook of neuropsychology (Vol. IX, pp. 1758).
New York: Elsevier.
Pinker, S. (1994). The language instinct: How the mind
creates language. New York: William Morrow.
Rizzolatti, G., & Arbib, M. A. (1998). Language within
our grasp. Trends in Neuroscience, 21, 188194.
Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L.
(1996). Premotor cortex and the recognition of
motor actions. Cognitive Brain Research, 3, 131141.
Rizzolatti, G., Fadiga, L., Matelli, M., Bettinardi, V.,
Paulesu, E., Perani, D., et al. (1996). Localization of
grasp representations in human by PET: 1. Observation
versus execution. Experimental Brain Research,
111, 246252.
Schaffler, L., Luders, H. O., Dinner, D. S., Lesser, R. P.,
& Chelune, G. J. (1993). Comprehension deficits
elicited by electrical stimulation of Broca’s area.
Brain, 116, 695715.
Talairach, J., & Tournoux, P. (1988). Co-planar stereotactic
atlas of the human brain. New York: Georg
Thieme Verlag.
Umilta` , M. A., Kohler, E., Gallese, V., Fogassi, L.,
Fadiga, L., Keysers, C., et al. (2001). I know what
you are doing: A neurophysiological study. Neuron,
31, 155165.
Von Bonin, G., & Bailey, P. (1947). The neocortex of
Macaca mulatta. Urbana, IL: University of Illinois
Press.
Wilson, S. M., Saygin, A. P., Sereno, M. I., & Iacoboni,
M. (2004). Listening to speech activates motor areas
involved in speech production. Nature Neuroscience,
7(7), 701702.
