Empathy plays a fundamental social role,
allowing the sharing of experiences, needs, and
goals across individuals. Its functional aspects
and corresponding neural mechanisms, however,
are poorly understood. When Theodore Lipps (as
cited in ref. 1) introduced the concept of
empathy (Einfühlung), he theorized the
critical role of inner imitation of the actions
of others in generating empathy. In keeping with
this concept, empathic individuals exhibit
nonconscious mimicry of the postures,
mannerisms, and facial expressions of others
(the chameleon effect) to a greater extent than
nonempathic individuals (2). Thus, empathy may
occur via a mechanism of action representation
that modulates and shapes emotional contents.
In the primate brain, relatively well-defined
and separate neural systems are associated with
emotions (3) and action representation
(4Ð7). The limbic system is critical for
emotional processing and behavior, and the
circuit of frontoparietal networks interacting
with the superior temporal cortex is critical
for action representation. This latter circuit
is composed of inferior frontal and posterior
parietal neurons that discharge during the
execution and also the observation of an action
(mirror neurons; ref. 7), and of superior
temporal neurons that discharge only during the
observation of an action (6, 8, 9). Anatomical
and neurophysiological data in the nonhuman
primate brain (see review in ref. 7) and imaging
human data (10Ð13) suggest that this circuit
is critical for imitation and that within this
circuit, information processing would flow as
follows. (i) The superior temporal cortex codes
an early visual description of the action (6, 8,
9) and sends this information to posterior
parietal mirror neurons (this privileged flow of
information from superior temporal to posterior
parietal is supported by the robust anatomical
connections between superior temporal and
posterior parietal cortex) (14). (ii) The
posterior parietal cortex codes the precise
kinesthetic aspect of the movement (15Ð18)
and sends this information to inferior frontal
mirror neurons (anatomical connections between
these two regions are well documented in the
monkey) (19). (iii) The inferior frontal cortex
codes the goal of the action [both
neurophysiological (5, 20, 21) and imaging data
(22) support this role for inferior frontal
mirror neurons]. (iv) Efferent copies of
motor plans are sent from parietal and frontal
mirror areas back to the superior temporal
cortex (12), such that a matching mechanism
between the visual description of the observed
action and the predicted sensory consequences of
the planned imitative action can occur. (v) Once
the visual description of the observed action
and the predicted sensory consequences of the
planned imitative action are matched, imitation
can be initiated.
How is this moderately recursive circuit
connected to the limbic system? Anatomical data
suggest that a sector of the insular lobe, the
dysgranular field, is connected with the limbic
system as well as with posterior parietal,
inferior frontal, and superior temporal cortex
(23). This connectivity pattern makes the insula
a plausible candidate for relaying action
representation information to limbic areas
processing emotional content. To test this
model, we used functional MRI (fMRI) while
subjects were either observing or imitating
emotional facial expressions. The predictions
were straightforward: If action representation
mediation is critical to empathy and the
understanding of the emotions of others, then
even the mere observation of emotional facial
expression should activate the same brain
regions of motor significance that are activated
during the imitation of the emotional face
expressions. Moreover, a modulation of the
action representation circuit onto limbic areas
via the insula predicts greater activity during
imitation, compared with observation of emotion,
throughout the whole network outlined above. In
fact, mirror areas would be more active during
imitation than observation because of the
simultaneous encoding of sensory input and
planning of motor output (13). Within mirror
areas, the inferior frontal cortex seems
particularly important here, given that
understanding goals is an important component of
empathy. The superior temporal cortex would be
more active during imitation than observation,
as it receives efferent copies of motor commands
from mirror areas (12). The insula would be more
active during imitation because its relay role
would become more important during imitation,
compared with mere observation. Finally, limbic
areas would also increase their activity because
of the modulatory role of motor areas with
increased activity. Thus, observation and
imitation of emotions should yield substantially
similar patterns of activated brain areas, with
greater activity during imitation in premotor
areas, in inferior frontal cortex, in superior
temporal cortex, insula, and limbic
areas.[...]
Results
Preliminary ANOV as revealed no differences
in activation among the three imitation tasks,
and no differences in activations among the
three observation tasks. Thus, main effects of
imitation, observation, and imitation minus
observation are reported here. As Table 1 shows,
there was a substantially similar network of
activated areas for both imitation and
observation of emotion. Among the areas commonly
activated by imitation and observation of facial
emotional expressions, the premotor face area,
the dorsal sector of pars opercularis of the
inferior frontal gyrus, the superior temporal
sulcus, the insula, and the amygdala had greater
activity during imitation than observation of
emotion. To give a sense of the good overlap
between the network described in this study and
previously reported peaks of activation, Table 2
compares peak of activations in the right
hemisphere observed in this study with
previously published peaks in meta-analyses or
individual studies in regions relevant to the
hypothesis tested in this study. Figs. 1 and 2
show, respectively, the location and time-series
of the right primary motor face area and of the
premotor face area. The peaks of these
activations correspond well with published data,
as discussed below. Task-related activity is
seen not only during imitation, but also during
observation. This observation-related activity
is very clear in premotor cortex but also
visible in primary motor cortex (although not
reaching significance in primary motor cortex).
Fig. 3 shows the activations in inferior frontal
cortex and anterior insula, with their
corresponding time-series. The activity of these
three regions is evidently correlated. Fig. 4
shows the significantly increased activity in
the right amygdala during imitation, compared
with observation of emotional facial
expressions
Discussion
The results of this study support our
hypothesis on the role of action representation
for understanding the emotions of others.
Largely overlapping networks were activated by
both observation and imitation of facial
emotional expressions. Moreover, the observation
of emotional expressions robustly activated
premotor areas. Further, fronto-temporal areas
relevant to action representation, the amygdala,
and the anterior insula had significant signal
increase during imitation compared with
observation of facial emotional expression. The
peak of activation reported here in primary
motor cortex during imitation of facial
emotional expressions corresponds well with the
location of the primary motor mouth area as
determined by a meta-analysis of published
positron-emission tomography (PET) studies, by a
meta-analysis of original data in 30 subjects
studied with PET, and by a consensus
probabilistic description of the location of the
primary motor mouth area obtained merging the
results of the two previously described
meta-analyses (38). This convergence confirms
the robustness and reliability of the findings,
despite the presence of facial motion during
imitation. In fact, residual motion artifacts
that were still present at individual level
after motion correction were eliminated by the
group analysis. This result is likely due to the
fact that each subject had different kinds of
motion artifacts and, when all of the data were
considered, only common patterns of activity
emerged. The data also clearly show peaks of
activity in the presupplementary motor area
(pre-SMA) face area and the face area of the
posterior portion of the rostral cingulate zone
(RCZp) that correspond well with the pre-SMA and
RCZp face locations as determined by a separate
meta-analysis of PET studies focusing on motor
areas in the medial wall of the frontal lobe
(39). Thus, our dataset represents an fMRI
demonstration of human primary motor and rostral
cingulate face area. With regard to premotor
regions, the peaks that we observe correspond
well with premotor mouth peaks described by
action observation studies (40). As Fig. 2
shows, robust pre-motor responses during
observation of facial emotional expressions were
observed, in line with the hypothesis that
action representation mediates the recognition
of emotions in others even during simple
observation.
The activity in pars opercularis shows two
separate foci during imitation, a ventral and a
dorsal peak. Only the dorsal peak remained
activated, although at significantly lower
intensity, during observation of emotion (Table
1). This pattern, with very similar peaks of
activation, was also observed in a recent fMRI
meta-analysis comprising more than 50 subjects
performing hand action imitation and observation
in our lab.fi Pars opercularis maps
probabilistically onto Brodmann area 44 (41,
42), which is considered the human homologue of
monkey area F5 (43-46) in which mirror neurons
were described. In the monkey, F5 neurons coding
arm and mouth movements are not spatially
segregated, and the human imaging data are
consistent with this observation. The imaging
data suggest that the dorsal sector represents
the mirror sector of pars opercularis, whereas
the ventral sector may be simply a premotor area
for hand and face movements.
The superior temporal sulcus (STS) area shows
greater activity for imitation than for
observation of emotional facial expressions, as
predicted by the action representation mediation
to empathy hypothesis. This area aiso
corresponds anatomically well with an STS area
specifically responding to the observation of
mouth movements observed in different studies
from different labs (47-50).
The anterior sector of the insula was active
during both imitation and observation of
emotion, but more so during imitation (Fig. 3),
fulfilling one of the predictions of our
hypothesis that action representation is a
cognitive step toward empathy. Ibis finding is
in line with two kinds of evidence available on
this sector of the insular lobe. First, the
anterior insula receives slow-conducting
unmyelinated fibers that respond to light
caress-like touch and may be important for
emotional and affiliative behavior between
individuals (51). Second, imaging data suggest
that the anterior insular sector is important
for the monitoring of agency (52), that is, the
sense of ownership of actions, which is a
fundamental aspect of action representation.
This finding confîrms a strong input onto
the anterior insular sector from areas of motor
significance.
The increased activity in the amygdala during
imitation compared with observation of emotional
facial expression (Fig. 4) ref lects the
modulation of the action representation circuit
onto limbic activity. It has been long
hypothesized (dating back to Darwin; refs.
53-55) that facial muscular activity influences
people's affective responses. We demonstrate
here that activity in the amygdala, a critical
structure in emotional behaviors and in the
recognition of facial emotional expressions of
others (56-59), increases while subjects imitate
the facial emotional expressions of others,
compared with mere observation.
Previous and current literature on observing
and processing facial emotional expression
provides a rich context in which to consider the
nature of the empathic resonance induced by our
imitation paradigin. In general, our findings
fit well with previously published imaging data
on observation of facial expressions that report
activation in both amygdala and anterior insula
for emotional facial expressions (for a review,
see ref. 57 and references therein). A study on
conscious and unconscious processing of
emotional facial expression (58) bas suggested
that the left but not the right amygdala is
associated with explicit representational
content of the observed emotion. Our data,
showing a right lateralized activation of the
amygdala during imitation of facial emotional
expression, suggest that the type of empathie
resonance induced by imitation does not require
explicit representational content and may be a
form of "niirroring" that grounds empathy via an
experiential mechanism.
In this study, we treated emotion as a
single, unified entity. Recent literature bas
clearly shown that different emotions seem
related to different neural systents. For
instance, disgust seems to activate
preferentially the anterior insula (60), whereas
fear seems to activate preferentially the
amygdala (56, 57). We adopted this approach
because our main goal was to investigate the
relationships between action representation and
emotion via an imitation paradigm. Future
studies may successûdly employ imitative
paradigm to further explore the
différential neural correlates of
emotions.
Taken together, these data suggest that we
understand the feelings of others via a
mechanism of action representation shaping
emotional content, such that we ground our
empathie resonance in the experience of our
acting body and the emotions associated with
specific moivements. As Lipps noted, "When I
observe a circus performer on a hanging wire, I
feel I am inside him" (1). To empathize, we need
to invoke the representation of the actions
associated with the emotions we are witnessing.
In the human brain, this empathie resonance
occurs via communication between action
representation networks and limbic areas
provided by the insula. Lesions in this circuit
may determine an impairment in understanding the
emotions of others and the inability to
"empathize" with them.
