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Journal of Physiology - Paris 99 (2006) 396–405
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The role of ventral premotor cortex in action execution
and action understanding
Ferdinand Binkofski
a
a,*
, Giovanni Buccino
b
Department of Neurology and Neuroimage Nord, University Hospital Schleswig-Holstein, Campus Luebeck, Ratzeburger Allee 160,
23538 Lübeck, Germany
b
Dipartimento di Neuroscienze, Sezione di Fisiologia, Universita’ di Parma, Italy
Abstract
The human ventral premotor cortex overlaps, at least in part, with Broca’s region in the dominant cerebral hemisphere, that is known
to mediate the production of language and contributes to language comprehension. This region is constituted of Brodmann’s areas 44
and 45 in the inferior frontal gyrus. We summarize the evidence that the motor related part of Broca’s region is localized in the opercular
portion of the inferior frontal cortex, mainly in area 44 of Brodmann. According to our own data, there seems to be a homology between
Brodmann area 44 in humans and the monkey area F5. The non-language related motor functions of Broca’s region comprise complex
hand movements, associative sensorimotor learning and sensorimotor integration. Brodmann’s area 44 is also a part of a specialized parieto-premotor network and interacts significantly with the neighbouring premotor areas. In the ventral premotor area F5 of monkeys, the
so called mirror neurons have been found which discharge both when the animal performs a goal-directed hand action and when it
observes another individual performing the same or a similar action. More recently, in the same area mirror neurons responding not
only to the observation of mouth actions, but also to sounds characteristic to actions have been found. In humans, through an fMRI
study, it has been shown that the observation of actions performed with the hand, the mouth and the foot leads to the activation of
different sectors of Broca’s area and premotor cortex, according to the effector involved in the observed action, following a somatotopic
pattern which resembles the classical motor cortex homunculus. On the other hand the evidence is growing that human ventral premotor
cortex, especially Brodmann’s area 44, is involved in polymodal action processing. These results strongly support the existence of an
execution–observation matching system (mirror neuron system). It has been proposed that this system is involved in polymodal action
recognition and might represent a precursor of language processing. Experimental evidence in favour of this hypothesis both in the
monkey and humans is shortly reviewed.
Ó 2006 Elsevier Ltd. All rights reserved.
Keywords: Broca’s region; Ventral premotor cortex; Mirror neuron system; Action recognition; Motor resonance; Language processing
1. Introduction
This review consists of two parts. In the first part the
data coming from neurophysiological and brain imaging
studies concerning the role of ventral premotor cortex in
action execution both in monkeys and humans will be
*
Corresponding author. Address: Department of Neurology, University
Hospital Schleswig-Holstein, Campus Luebeck, Ratzeburger Allee 160,
23538 Lübeck, Germany. Tel.: +49 451 500 2499; fax: +49 451 500 2489.
E-mail address: [email protected] (F. Binkofski).
0928-4257/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jphysparis.2006.03.005
reviewed. In the second part, the features of a particular
set of neurons, the so called mirror neurons, first described
in area F5 will be discussed. A major problem when considering the role of ventral premotor cortex in action execution is the difficulty to compare monkey data with human
data: in fact, classically the ventral premotor cortex of
the monkey (area F5) is thought to be endowed with a
motor representation of hand and mouth goal-directed
actions, while the same sector in humans (Broca’s area) is
thought to be devoted to speech production. Recent brain
imaging studies have clearly shown a motor representation
of hand actions also in Broca’s area, thus supporting the
F. Binkofski, G. Buccino / Journal of Physiology - Paris 99 (2006) 396–405
notion of a homology between area F5 in the monkey and
Broca’s area in humans.
Mirror neurons discharge both when the animal performs a goal-directed hand action and when it observes
another individual performing the same or a similar action.
More recently, in the same area mirror neurons responding
to the observation of mouth actions have also been found.
In humans, by means of an fMRI study, it has been shown
that the observation of actions performed with the hand,
the mouth and the foot leads to the activation of different
sectors of Broca’s area and premotor cortex, according to
the effector involved in the observed action. These activations follow a somatotopic pattern which resembles the
classical motor cortex homunculus. These results strongly
support the existence of an observation–execution matching
system in humans (mirror neuron system), similar to that
found in the monkey. Whereas in monkeys mirror neurons
responding to action related sounds have been discovered,
the evidence is growing that in humans mirror neurons
not only code action words, but also contributes to process
action related sentences and this in a somatotopic manner.
Thus, there is evidence that the mirror neuron system plays
a fundamental role in action understanding both in humans
and monkeys and might constitute a bridge between action
and language processing.
2. The role of ventral premotor cortex in action execution
2.1. Motor functions of ventral premotor cortex (area F5)
in the monkey
Based on cytoarchitectural and histochemical data, a
modern parcellation of the agranular frontal cortex has
397
been worked out in the macaque monkey (Matelli et al.,
1985, 1991). Fig. 1 shows this parcellation.
In the terminology proposed by Matelli and co-workers,
area F1 corresponds basically to Brodmann’s area 4 (primary motor cortex), the other areas are mainly subdivisions of Brodmann’s area 6. Areas F2 and F7, which lie
in the superior part of area 6, are referred to collectively
as ‘‘dorsal premotor cortex’’, while areas F4 and F5, which
lie in the inferior area 6, are often referred to as ‘‘ventral
premotor cortex’’ (Matelli and Luppino, 2000).
Neurophysiological studies showed that in area F5,
which occupies the most rostral part of ventral premotor
cortex in the macaque monkey, there is a motor representation of distal hand movements (Rizzolatti et al., 1981,
1988; Kurata and Tanji, 1986; Hepp-Reymond et al.,
1994). The neurons of this area discharge during specific
goal-directed hand movements such as grasping, holding
and tearing. It has been proposed, that area F5 contains
a ‘‘motor vocabulary’’ for hand actions (Rizzolatti et al.,
1988; Murata et al., 1997). This area is directly connected
with the primary motor cortex (F1) and receives rich input
from the second somatosensory area (SII), from parietal
area PF (7b), and from a parietal area located inside the
intraparietal sulcus, the anterior intraparietal area (AIP)
(Matsumura and Kubota, 1979; Muakkassa and Strick,
1979; Godschalk et al., 1984; Matelli et al., 1986; Luppino
et al., 1999). The study of AIP showed that many of its neurons discharge during finger and hand movements, others
respond to specific visual 3-D stimuli and, finally, others
discharge both during active finger movements and in
response to 3-D stimuli congruent in size and shape with
the coded grasping movement (Taira et al., 1990; Sakata
et al., 1995). Taken together, these data suggest that the
Fig. 1. Schematic drawing of the parcellation of the ventral premotor cortex in monkeys (modified after Matelli and Luppino, 1996, with permission).
Lateral view of the monkey brain showing the cytoarchitectonic parcellation of the motor cortex and the posterior parietal cortex (area VIP, buried inside
IP, is not shown). The motor area F7, receiving its main input from the prefrontal lobe, is indicated in blue. Areas F2 and F7 are often referred to as dPM;
areas F4 and F5 form the vPM. AI, inferior arcuate sulcus; AS, superior arcuate sulcus; C, central sulcus; DLPFd, dorsolateral prefrontal cortex dorsal
part; DLPFv, dorsolateral prefrontal cortex ventral part; IP, intraparietal sulcus; L, lateral fissure; Lu, lunate sulcus; P, principal sulcus; SI, primary
somatosensory cortex; ST, superior temporal sulcus.
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circuit connecting AIP and F5 plays a pivotal role in
controlling the organization of hand/object interactions
(Jeannerod et al., 1995).
2.2. Area F5 in the monkey and Broca’s region in humans
In humans the ventral sector of the premotor cortex is
formed by two areas: the ventral part of area 6a alpha
and BA 44 (Vogt and Vogt, 1919). Brodmann’s areas 44
and 45, occupying the opercular and triangular parts of
the inferior frontal gyrus, form the Broca’s region (Broca,
1864; Amunts et al., 1999).
Brodmann’s areas 44 and 6 share a common basic cytoarchitectonic structure, the main characteristics of which
are the poverty (BA 44) or lack (BA 6) of granular cells
(see Campbell, 1905; von Economo, 1929) and the presence
of large pyramid cells in the third layer. Classically, both
ventral BA 6 and BA 44 were thought of as areas controlling oro-laryngeal movements, but with a different specialization and selectivity. The most lateral part of BA 6 was
considered to be responsible for the motor control of
oro-laryngeal movements, regardless of the movement purpose, while, in contrast, BA 44 was considered to be the
main speech motor area. Because Broca’s region occurred
only in the evolution of the human brain, the search for
homologies between Broca’s region and ventral premotor
areas of non-human primates is somehow difficult. It is
interesting to note, however, that a homology between
BA 44 and area F5 was already suggested by von Bonin
and Bailey (1947) on the basis of their cytoarchitectonic
studies. (In their terminology, F5 was called FCBm.) This
view has been recently fully supported by Petrides and
Pandya (1994); (see also Galaburda and Pandya, 1982; Preuss et al., 1996). A possible weakness of this homology (see
Passingham, 1993) is the richness of the oro-laryngeal representation, including that of speech control, in human
Broca’s area and, on the contrary, the presence of a motor
representation of hand actions in monkey area F5. A series
of recent neuroimaging studies, which will be shortly
reviewed in this article, has clearly demonstrated that the
role of Broca’s area 44 is not restricted to speech production and that in this area there is not only an oro-laryngeal
motor representation, but also a motor representation of
distal hand movements. Obviously, the relative cortical
space for the two representations is not the same. However,
the development of the cortex devoted to oro-laryngeal
representations specifically in BA 44 is probably not a mere
coincidence, but is due to the close evolutionary relation
between action and speech (see Rizzolatti and Arbib,
1998).
that are different from speech. Activation of the right inferior frontal cortex was found during overt and covert production of gestures (Bonda et al., 1995; Parsons et al., 1995;
Decety et al., 1994), especially during mental rotations necessary for hand recognition (Parsons et al., 1995), during
mental imagery of grasping movements (Decety et al.,
1994; Grafton et al., 1996a,b), during preparation of finger
movements on the basis of a copied movement (Krams
et al., 1998), during imagery and performance of visually
guided movements (Binkofski et al., 2000; Toni et al.,
2001). The vPMC was also found to be of importance for
motor tasks with high motor execution demands (Winstein
et al., 1997). Ventral premotor cortex seems to play a crucial role in motor imagery as repeatedly shown in neuroimaging studies (Decety et al., 1994; Stephan et al., 1995;
Binkofski et al., 2000). Common to all these tasks was
the performance of complex motor acts with higher degree
of sensorimotor control.
The frontal opercular cortex of the right hemisphere was
also shown to be critically involved in the learning of explicit and implicit motor sequences (Seitz and Roland, 1992;
Rauch et al., 1995; Hazeltine et al., 1997). The frontal opercular region seems also to be involved in the initial learning
of novel, arbitrary visuo-motor associations (Toni et al.,
2001), while overlearned performance is likely to rely on
dorsal premotor cortex (Toni et al., 2001, 2002). The specific role of area 44 in the execution of goal directed hand
actions could also be demonstrated in another experiment
in which volunteers were asked to manipulate complex
objects, as compared to the manipulation of a sphere (Binkofski et al., 1999). The experiment consisted of two conditions: in one condition the participants were asked to
merely manipulate complex objects and avoid covert naming of them, in the other condition the participants were
explicitly asked to covertly name the explored objects. In
the contrast between both conditions containing manipulation of complex objects and manipulation of a sphere ventral premotor activations were found. The comparison of
the coordinates of the activated foci located around the
opercular and triangular parts of the inferior frontal gyrus
with the coordinates of the probability maps of BAs 44 and
45 (Amunts et al., 1999) demonstrated that the activation
foci located in the pars triangularis related to covert
naming of objects fitted entirely into BA 45. The foci activated during complex object manipulation without naming
and located in vPMC fitted into the borders of BA 44.
These results underline the notion that within Broca’s
region the area 44 is relevant for both grasping and
manipulation.
2.3. Involvement of human ventral premotor cortex in
processing complex actions: evidence from neuroimaging
2.4. Combination of cytoarchitectonic and imaging data
for identification of similarities between human area 44
and monkey area F5
New neuroimaging techniques helped to extend our
understanding of functions of the frontal opercular cortex
While investigating motor imagery under different conditions we found that the posterior, opercular part of the
F. Binkofski, G. Buccino / Journal of Physiology - Paris 99 (2006) 396–405
human inferior frontal cortex became specifically engaged
during imagery of abstract movements (Binkofski et al.,
2000). This imagery of abstract movements was referred
to conditions in which movement had to be imagined from
a third person’s perspective. The imagery of one’s own
movement was associated with activation of the left ventral
opercular cortex, while the imagery of a moving target
caused activation of the right ventral opercular cortex.
After transformation of our data into the standardized reference brain atlas by Roland and Zilles (1994), we superimposed our activation data onto the cytoarchitectonic data
of the Brodmann areas 44 and 45 (Amunts et al., 1999).
The superimposition of our activation data with the probabilistic maps of areas 44 and 45 obtained from cytoarchitectonic data of 10 individual brains allows for exact
localization of the activation foci within one of these areas.
Here, we could clearly demonstrate that during imagery of
one’s own limb motion, from an observer’s perspective,
there was left-hemispheric activation of area 44, whereas
during imagery of spatial target motion in extrapersonal
space, significant activation of the right area 44 became
apparent (Fig. 2).
Moreover, we showed that the centre of gravity of area
44 was significantly caudal to area 45 and rostral to lower
area 6 of premotor cortex. These data support the view that
the left-hemispheric activation of Broca’s region reflected
‘‘pragmatic’’ motor processing, while the right-hemispheric
activation of Broca’s homologue was related to explicit
motor processing of motion. Interestingly, in our study
the inferior frontal cortex was not activated by imagery
of simple finger movements but of more advanced concepts
of motion. Imagery of visually guided finger movements
was associated with activation of more dorsal parts of lateral premotor cortex, possibly in the homologue to monkey
area F4.
We suggest that these frontal opercular activations in
humans within the cytoarchitectonical borders of Brodmann’s area 44 may correspond to neuronal activations
related to action perception and recognition as reported
399
for a set of neurones in the ventral premotor cortex in
the area F5 of macaques (Rizzolatti et al., 1996a; Gallese
et al., 1996). This notion is strongly supported in a review
by Rizzolatti et al. (2002).
3. The mirror neuron system
3.1. The mirror neuron system in the monkey
Neurophysiological studies have shown that a set of F5
neurons discharges both when the monkey performs specific goal-directed hand actions and when it observes
another monkey or an experimenter performing the same
or a similar action (Gallese et al., 1996; Rizzolatti et al.,
1996a). These neurons are called mirror neurons. The congruence between the action coded by the neuron in motor
terms and that triggering the same neuron visually may
be very strict: in this case only the observation of an action
identical to that coded motorically by the neuron can activate it. More often, this congruence is only broad; in this
case, the observed and the executed action coded by the
neuron share the goal of the action itself rather than the
single movements constituting it. During action observation mirror neurons discharge only when a biological effector (a hand, for example) interacts with an object; if the
action is executed with a tool the neuron is not active. Also
mirror neurons are not active when the observed action is
simply mimicked, that is not acted upon an object. Finally,
mirror neurons do not discharge during the mere visual
presentation of an object. Fig. 3 shows some examples of
mirror neurons. The visual properties of mirror neurons
resemble those of neurons found by Perrett et al. (1989)
in the superior temporal sulcus region. These neurons, like
mirror neurons, respond to the presentation of goal-directed hand actions, but also to walking, turning the head,
moving the hand and bending the torso (for a review see
Carey et al., 1997). Differently from mirror neurons
described in area F5, neurons of STS region do not seem
to have a motor counterpart.
Fig. 2. Activation of the left area 44 during processing of internal motion (A) and of the right area 44 during processing of external motion (B).
Superposition of activation foci (blue, from Binkofski et al., 2000) on the probablilistic cytoarchitectonic map of area 44.
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Fig. 3. Characteristic properties of mirror neurons. (a) Strong activation of a mirror neuron in the macaque ventral premotor area F5 during execution of
a grasping movement by the macaque (right) and during the observation of a similar grasping movement performed by an experimenter (left). (b) During
observation of a grasping movement performed with a tool remains the mirror neuron silent. Adapted from Gallese et al., 1996.
Since their discovery, the hypothesis has been forwarded
that mirror neurons may play an important role both in
action recognition and in motor learning (Jeannerod,
1994). Evidence in favour of the fundamental role of mirror
neurons in action understanding has been provided by
an electrophysiological study (Umilta et al., 2001). In the
experiment, two conditions were considered: in the first
one (vision condition) the animal could see the whole
sequence of a hand goal-directed action, in the second one
(hidden condition) the final part of the action was hidden
from the sight of the monkey by means of a screen. In this
last condition, however, the animal was shown that an
object, for example a piece of food, was placed behind the
screen which prevented the observation of the final part of
the executed action. The results showed that mirror neurons
discharge not only during the observation of the whole
action, but also when the final part of it is hidden. As a
control, a mimicked action was presented in the same conditions. As expected, in this case, the neuron did not discharge,
neither in the full vision condition nor in the hidden
condition.
Actions may be recognized also when presented acoustically, from their typical sound. Besides visual properties, a
recent experiment has demonstrated that about 15% of
mirror neurons also respond to the peculiar sound of an
action. These neurons are called audio–visual mirror neurons (Koehler et al., 2002). Audio–visual mirror neurons
could be used to recognize actions performed by other individuals even if only heard. It has been argued that these
neurons code the action content, which may be triggered
either visually or acoustically, thus representing a possible,
fundamental step for the evolution of language.
The studies reported so far concerned mirror neurons
related to hand actions. More recently it has been demonstrated that in area F5 there are also mirror neurons which
discharge during the execution and observation of mouth
actions. Most of mouth mirror neurons become active during the execution and observation of mouth actions related
to ingestive functions such as grasping, sucking or breaking
food. Some of them respond during the execution and
observation of oral communicative actions such as lipsmacking (Ferrari et al., 2003).
3.2. The mirror neuron system in humans
There is increasing evidence that a mirror neuron system
also exists in humans. Converging data supporting this
notion come from experiments carried out with neurophysiological, behavioural and brain imaging techniques.
An early, indirect evidence in favour of the existence of a
mirror neuron system in humans has been provided by
Fadiga et al. (1995) through a transcranial magnetic stimulation (TMS). During this experiment, single pulse TMS
was delivered while subjects were observing an experimenter performing various distal hand actions in front of
them. As control conditions, single pulse TMS was delivered during object observation, dimming detection and
observation of arm movements. Motor evoked potentials
were recorded from different hand muscles. Results showed
that during hand action observation, but not in the other
conditions, there was an increase of the amplitude of motor
evoked potentials (MEPs) recorded from those hand muscles, normally recruited when the observed action is actually performed by the observer. These results were fully
confirmed by Strafella and Paus (2000). Furthermore,
using the same technique, Gangitano et al. (2001) found
that during hand action observation, MEPs recorded from
muscles involved in the actual execution of the observed
action are modulated in a fashion strictly resembling the
time-course of the observed action. Taken together, these
TMS data support the notion of a mirror neuron system
coupling action execution and action observation in terms
of both the muscles involved and the temporal sequence of
the action.
In keeping with these results are those obtained by
Cochin et al. (1999) using quantified electroencephalogra-
F. Binkofski, G. Buccino / Journal of Physiology - Paris 99 (2006) 396–405
phy (qEEG). In this study l-rhythm activity was blocked,
as compared to rest, during both the observation and
execution of various hand actions. Results similar to those
of Cochin et al. (1999) were obtained by Hari et al. (1998)
using magnetoencephalography (MEG). In this study the
authors found a suppression of 15–25 Hz activity, known
to originate from the precentral motor cortex, during the
execution and, although to a less extent, during the observation of object manipulation. All these studies provide
further evidence that observation and execution of action
share common neural substrates.
Evidence in favour of the existence of a mirror neuron
system derives also from neuropsychological studies, using
behavioural paradigms. Brass et al. (2000) investigated how
the observation of movements can affect movement execution in a stimulus–response compatibility paradigm. To
this purpose they contrasted the role of symbolic cues as
compared to the observation of finger movements in the
execution of finger movements. Subjects were faster when
the relevant cue for the response was the movement as
compared to the condition in which a spatial or a symbolic
cue was relevant for the response. Moreover the degree of
similarity between the observed and executed movement
leads to a further advantage in the execution of the
observed movement. These results provide a strong evidence for an influence of the observed movement on the
execution of that movement. Similar results were obtained
by Craighero et al. (2002) in a study in which subjects were
required to prepare to grasp as fast as possible a bar oriented either clockwise or counter clockwise, after presentation of a picture showing the right hand. Two experiments
were carried out: in the first experiment the picture represented the final required position for the hand to grasp
the bar, as seen through a mirror. In a second experiment,
in addition to stimuli used in experiment one, another two
pictures were presented, obtained by rotating the hand
shown in the pictures used in Experiment 1 by 90°. In both
experiments, responses of the subjects were faster when the
hand orientation of the picture corresponded to that
achieved by the hand at the end of action, when actually
executed. Moreover the responses were globally faster
when the stimuli were not rotated. In the studies reported
here, the observation of an action facilitates the execution
of that action. These results find a clear explanation in
the existence of the mirror neuron system, where by
definition the visual representation of an action and its
motor counterpart are anatomically and functionally
embedded.
All the cited studies provide little, if any, insight on the
localization of mirror neuron system in humans. This issue
was addressed by a number of brain imaging studies. In an
early experiment devoted to identify the brain areas active
during action observation, using positron emission tomography (PET), Rizzolatti et al. (1996b) found an activation
of Broca’s area and of the cortex of the middle temporal
gyrus and of the superior temporal sulcus region, when
comparing hand action observation with the observation
401
of an object. Although Broca’s area is classically considered an area devoted to speech production, given the
homology between this area and area F5 in the monkey
(see above), where mirror neurons were originally discovered, this study provided evidence on the anatomical localization of the mirror neuron system in humans, at least for
hand actions. A recent fMRI study showed that in humans
the mirror neuron system is complex and related to different body actions performed not only with the hand, but
also with the foot and the mouth. Buccino et al. (2001)
asked normal volunteers to observe video sequences presenting different actions performed with the mouth, the
hand and the foot, respectively. The actions shown could
be either transitive (the action was acted upon an object)
or intransitive (the same action previously acted upon an
object, was mimicked). The following actions were presented: biting an apple, grasping a cup and a ball, kicking
a ball and pushing a brake. As a control, subjects were
asked to observe a static frame of each action.
The observation of both transitive and intransitive
actions, compared to the observation of a static frame of
the same action, led to the activation of different sectors
in the premotor cortex and in Broca’s area, according to
the effector involved in the observed action. The different
sectors largely overlapped with those where classical studies (Penfield and Rasmussen, 1950) had shown a motor representation of the different effectors. Moreover, during the
observation of transitive actions, distinct sectors in the
inferior parietal lobule, including areas inside the intraparietal sulcus and adjacent to it, were active, according to the
effector involved in the observed action. Fig. 4 shows the
results of the experiment.
On the whole, this study strongly supports the claim
that, as in the actual execution of actions, different,
somatotopically organized frontoparietal circuits (Jeannerod et al., 1995; Rizzolatti et al., 1998) are recruited during
action observation. In this context, it is worth noting that
mirror neurons, similar to those described in area F5, have
also been described by Fogassi et al. (1998) and Gallese
et al. (2002) in the inferior parietal lobule of the monkey
(area PF).
The study of Buccino et al. (2001) show an involvement
of the mirror neuron system during a mere observation
task, thus suggesting that this system is indeed operating
whatever the cognitive strategy of the observer.
As previously stated, in the monkey the mirror neuron
system is activated also when the animal observes a nonconspecific (an experimenter, for example) performing the
same or a similar action coded by the neuron motorically.
In a recent study the issue was addressed whether we recognize action performed by non-conspecifics using the same
neural structures involved in the recognition of action performed by our conspecifics (Buccino et al., 2004). In an
fMRI experiment normal subjects were asked to carefully
observe different mouth actions performed by a man, a
monkey and a dog, respectively. Two kinds of mouth
actions were visually presented: biting a piece of food
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and oral communicative actions (human silent speech,
monkey lip-smacking, and dog silent barking). The results
showed that during the observation of biting, there is a
clear activation of the pars opercularis of the inferior frontal gyrus and of the inferior parietal lobule, with no regards
for the species doing the action. During the observation of
oral communicative mouth actions, a different pattern
of activation was observed according to the individual of
the species performing the action. During the observation
of silent speech there was a clear activation of Broca’s area
in both hemispheres, with a marked prevalence in the left
one, during the observation of lip smacking there was only
a bilateral small activation in the pars opercularis of Broca’s area, with no clear asymmetry between the two hemispheres. Finally, during the observation of barking no
activation was found in the Broca’s area, but activation
was present only in the right superior temporal sulcus
region. The results of the experiment strongly suggest that
action performed by other individuals, including non-conspecifics, may be recognized in two different ways: for
actions like biting or silent speech reading, there is a motor
resonance of the cortical circuits involved in the actual
execution of the observed actions; in other words their
recognition relies on the mirror neuron system. For
actions like barking this resonance is lacking. In the first
case there is a ‘‘personal’’ knowledge of the action
observed, in the sense that it is mapped on the observer’s
motor repertoire and therefore the observer has a direct,
personal experience in motor terms of it (I recognize it
because I am able to do the same action I am looking
at); in the second case, although still recognized as a biological action, as demonstrated by the activation of the
STS region, this personal knowledge is lacking because
the observer has no direct experience of the observed action
in motor terms (I can approximately imitate a dog barking,
but, as a matter of fact, I am not able to do it) (Buccino
et al., 2004).
In a recent fMRI study we looked for areas activated by
recognition of tools regardless in which modality they were
presented to the subjects. By using conjunction analysis
between three conditions containing recognition of tools
presented visually, tactically and acoustically (each contrasted with respective modality specific baseline) we found
a common activation of the bilateral infero-temporal and
of bilateral ventral premotor cortex (Binkofski et al.,
2004). Whereas the infero-temporal activation foci represent most probably polymodal object (tool) recognition,
the activation of the bilateral ventral premotor cortex is
bound to polymodal coding of pragmatic properties of
objects and of potential actions on them. This result indicates that polymodal mirror neurons (Koehler et al.,
2002) might also exist in human ventral premotor cortex
(Fig. 5).
As a whole, the studies reviewed so far show an involvement of ventral premotor cortex, including the opercular
part of the inferior frontal gyrus in recognizing actions.
A recent topic of debate is whether, in modern humans,
the mirror neuron system plays also a role in understanding
actions when they are presented through language. Some
experimental evidence and some theoretical approaches
strongly suggest a possible link between the mirror neuron
system and language (for a review see Rizzolatti and Buccino, 2005; Arbib, 2005). Given the homology between the
monkey’s premotor area F5 and Broca’s region, it has been
suggested that the mirror neuron system represents the
neural substrate from which human language evolved
(Arbib, 2005; Rizzolatti and Arbib, 1998; Rizzolatti and
Buccino, 2005). Up to now only few studies have addressed
the issue of a potential involvement of the motor system
during processing of action related sentences. A recent
fMRI study, showed that listening to sentences expressing
actions performed with the mouth, the hand and the foot
causes activation of different sectors of the premotor cortex, depending on the effector used in the action-related
sentence (Tettamanti et al., 2005). Interestingly, these distinct sectors coincide, albeit only approximately, with those
active during the observation of hand, mouth and foot
actions (Buccino et al., 2001). Another recent event-related
fMRI study demonstrated that, during silent reading of
words referring to face, arm or leg actions, different sectors
of the premotor-motor areas are active, depending on the
referential meaning of the read action words (Hauk et al.,
2004). The authors interpreted the results as supportive
of a dynamic view according to which words are processed
in neural substrates reflecting their semantics. Further, a
recent combined TMS and behavioral study showed that
listening to hand action related sentences, as compared
to foot action related and abstract content sentences, specifically modulated the activity of the hand, as revealed
by MEPs recorded from hand muscles or by responses
given with the hand (Buccino et al., 2005). Taken together,
the results from brain imaging studies support those
theories assuming that language understanding relies on
‘‘embodiment’’. According to these theories, the understanding of action-related sentences implies an internal
simulation of the actions expressed by the action-related
verb, mediated by the same motor representations that
are involved in their actual execution (Gallese and Lakoff,
2005).
In conclusion, converging data indicate that we can recognize a large variety of actions performed by other individuals, including those belonging to other species, just
matching the observed actions on our own motor system.
The neural substrate of this direct matching, through which
we recognize actions done by other individuals, is the mirror neuron system. This system could also mediate the processing of actions, when presented through heard and read
sentences expressing a motor content. The possibility to
recognize actions, regardless of the modality through
which they are presented endowed with the mirror neuron
system, makes this system a possible neural substrate not
only for social interactions, but also, as recently proposed,
for empathy with other people and the attribution of intentions to others (Gallese, 2003).
F. Binkofski, G. Buccino / Journal of Physiology - Paris 99 (2006) 396–405
403
Fig. 4. Somatotopy of movement observation. Activation of cortical areas during observation of mouth (red), hand (green) and foot (blue) movements
performed without (a) and with (b) a participating object. Notice the somatotopic pattern of activation in the premotor cortex in both conditions and the
extensive parietal activation during the observation of object related movements (b). Adapted from Buccino et al., 2001.
Fig. 5. Activation of the infero-temporal cortex (fusiform gyrus) and of ventral premotor areas during polymodal tool recognition (conjunction of
activations during recognition of tools presented in visual, tactile and acoustic modalities). Adapted from Binkofski et al., 2004.
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