"No creature not endowed with divinatory
power can perform an act voluntarily for the
first time". Voluntary movements must be
preceded, as William James wrote, by "random,
automatic, or reflex movements." These movements
leave a trace formed by kinesthetic impressions
and by their outcome as perceived by the agent
of the action ["remote effects"]. The
idea of an internal sensory copy of the executed
action that in modern time has been reproposed
in computer science [forward internal models
] and in psychology [ideomotor theory of
learning ] has far reaching consequences for
understanding imitation. If the motor
representation of a voluntary action indeed
evokes an internal sensory representation of its
consequences, imitation can be achieved by a
mechanism relating this representation with the
visual representation of the movement to be
imitated and a subsequent re-activation of the
relevant motor representations. Evidence that
the observed actions are mapped directly onto
neurons coding actions has been provided
recently by Rizzolatti and coworkers. They
demonstrated that in the ventral premotor cortex
[area F5 ] and in the parietal area PFk
of the monkey there are neurons that discharge
both when the monkey makes a specific hand
action and when it observes another individual
making a similar action (mirror neurons). The
issue, however, of whether there is a visual
area that codes the observed actions as well as
the remote effects of voluntary movements is
open. Given its reciprocal connections with
parietal area PF (and indirectly with F5), the
superior temporal sulcus (STS) region, a
cortical sector in which there is a large number
of neurons responding to the observation of
biological actions, is one of the most likely
candidates.
The mirror system, given its observation
execution matching properties, very likely
represents the evolutionary precursor of the
human mechanism for imitation, a behavior
fundamental for culture transmission. Evidence
in favor of this hypothesis was provided
recently by an experiment in which we studie
dimitative behavior by using functional magnetic
resonance imaging. Our reasoning was the
following: because mirror neurons are first of
all motor neurons, a"mirror area" should
beactivated during execution of finger hand
movements regard lessof how the movement is
actually triggered. Moreover, given that mirror
neurons, unlike other cortical motor neurons,
are triggeredspecifically by action observation,
mirror areas should show an additional
activation during imitation, compared with a
control motor task. Finally, mirror areas should
be activated by simple observation of the
action. Two areas with these characteristics
were found: area 44 and the rostral most part of
the superior parietal cortex. Note that in terms
of comparative neuroanatomy, area F5, the area
showing mirror properties in the macaque brain,
corresponds to area 44 of the human brain.
Mirror properties appeared to be present also in
a third areal ocated in the STS, thus
anatomically compatible with the STS region of
the macaque brain, as we reported preliminarily
in abstract form.
This finding is rather surprising because
unlike the first two areas, which are located
in cortical sectors where movement-related
activity is a characterizing functional
property,this third area was located in the
cortex mainly dominatedby sensory processing
. Also, the activation was only marginally
significant and given its unexpected location,
additional empirical evidence on its functional
properties was needed.We therefore performed a
new experiment on a new group of volunteers by
using the previously observed area as a search
region of interest and instructing the subjects
to observe and imitate both left and right hand
movements. There is evidence rom psychological
studies that humans tend to imitate
preferentially mirror-image movements (A common
experienceis that when a person touches his
right cheek with his righthand, telling another
person that there is something on her cheek, the
other person touches the left cheek, not the
right cheek, with the left hand.) This
behavioral evidence suggests a similar
privileged neural link between opposite-side
effectors. Thus, when using the right hand to
imitate, observed left hand actions should
produce a stronger activation of the area in
which visual information and reafferent copy of
the imitated action interact than observed right
hand actions. The results corroborated this
prediction, suggesting that this newly
identified region in the human STS has all the
requisites for being a region in which
interactions occur between observed action and
the reafferent motor-related copy of that
action. Both the first experiment that allowed
us to identify the region of interest and the
second experiment in which we tested the
reafferent-copy hypothesis are reported
here.
Discussion The STS-activated area
reported in the present study appears to
correspond in its location to the monkey STS
region. As shown by Perrett et al. this region
is characterized by a large number of neurons
that selectively respond to the observation of
biological stimuli. Previous imaging studies in
which volunteers observed actions such as hand
or eye movements also showed that biological
moving stimuli activate the human STS
region.
It therefore appears that both in humans and
monkeys, the cortex around the STS is a visual
region involved in the analysis of complex
biological stimuli. Given these findings, it is
not surprising that in the present experiments
activation was found in STS during the
observation of finger movements. In previous
studies in humans the STSregion was observed as
activated by biological motion in left,right, or
both hemispheres. This difference in the
laterality of activation of STS is likely caused
by the type of biological actions used as
stimuli.
Left hemisphere activation was reported
frequently in the case of object-oriented
actions. In our experiments the observed action
was an intransitive action and required,
presumably, a more fine-grained spatial
processing, hence the right hemisphere
prevalence. Regard less of the activation side,
however, what is particularly interesting in our
findings is that STS was activated during the
execution of finger movements and that this
activation was highest when there was a matching
between the action that was prepared and the
action that was
observed.There is
general agreement that the temporal lobe
processes visual information to give a semantic
description of the external word.
According to this view, the temporal lobe is the
place where the "what" of a visual object is
coded, as distinct from the "pragmatic" analysis
of the "where" and "how" performed in the
parietal lobe.
A similar semantic role may be postulated
for the STS region but with a specialization for
biologically relevant stimuli including body and
body-part movements. If this general distinction
between temporal and parietal lobe functions is
accepted, then the activation of the temporal
lobe during action execution can hardly be
interpreted as a command to move or, more
generally, as an activation causally related to
action. Similarly, it is difficult to postulate
that the STS activation may represent an
intention to move, as it has been suggested
forsome sectors of the posterior parietal lobe.
It seems much more likely that the STS
activation reported here representsa reflection
of motor-related activity occurring in the
frontoparietal circuits during action execution.
The possible anatomical circuitry subserving
this functional mechanism may be the connections
from the inferior parietal lobe to STS.It is
interesting to note that the STS activation of
the present study appears to be functionally
different from the classical corollary
discharges, the aim of which is typically that
of canceling or modifying sensory information to
maintain stableperception. On the contrary, the
present data indicate that the activation in STS
is maximal during imitation, i.e., in the
condition under which there is a congruency
between the observed action and the action to be
executed. In other words,the visual
representation of action coded in STS is
potentiated during action execution, not
canceled. This potentiation is notlikely to be
caused by unspecific attentional
mechanisms.
Attentional demands are generally higher for
less "natural" tasks.Behavioral studies have
demonstrated that in the case of imitation of
hand movements, the movement that is imitated
naturally is that of the hand of the actor
facing the hand used by the imitator. That is,
the motor activity evoked by the observation of
left hand movement produces a tendency to move
the right hand and vice versa. These
considerations predict that an increase in
attention is more likely to occur when subjects
imitate in the less natural condition, which is
the opposite of what we observed.It is likely
that the phenomenon of imitating in a
mirror-like fashion occurs for a natural
tendency to interact with other people by using
a sector of space common to both actor and
imitator. In contrast, there is no reason for
this tendency to be present when the observer
simply looks at another individual. Exactly this
dissociation was found in the STS area reported
in the present study.
During observation tasks the activity in
STS was greater when the right hand was the
visual stimulus, comparedwith the left hand.
During imitation, the activity in the STS
area was greater when the imitators observed the
hand mirror image of the hand they used
(left hand as visual stimulus and right hand as
motor effector). This reversal is likely caused
by a modulatory role of the imitative behavior
on STS visual activity that, in the absence of
imitation requirements, reflects animplicit
categorization of the moving hand as referred to
thebody of the observer. Although the hand used
by subjects to imitate the actions is
ipsilateral to the STS region reported here,the
motor control at the parietal and premotor level
is largelybilateral even for distal movements.
It is interesting to note that in our previous
report on imitation we described a left inferior
frontal area and a right posterior parietal area
as endowed with mirror properties.
At slightly lower statistical thresholds,
however, we observed mirror-like activations
also inthe right inferior frontal and left
posterior parietal cortex.What we believe
happens between the STS, inferior frontal, and
posterior parietal cortices in terms of
information processingis that STS neurons
provide an early description of the action to
parietal mirror neurons. These neurons add
additional somatosensory information to the
movement to be imitated. This more complex
information is sent to the inferior frontal
cortex,which in turn codes the goal of the
action to be imitated. Sensory copies of the
imitated actions are then sent back to the STS
area for monitoring purposes ("my actions are
like the actions I haveseen").
In conclusion, returning to the James
proposal that movements leave a trace formed not
only by kinesthetic impression but also by their
visual effects, our data indicate that this
functional mechanism indeed may occur in the STS
region. During action
execution, and in particular during action
imitation,the visual representation of
biological motion located in STS is activated,
and this activation has precisely those
properties that an imitation mechanism must
posses. It codes actions made by others and
stores the remote effects of the movements made
by the imitator.
