Introduction : How does imitation
occur? How can the motor plans necessary for
imitating an action derive from the observation
of that action? Imitation may be based on a
mechanism directly matching the observed action
onto an internai motor representation of that
action ("direct matching hypothesis"). To test
this hypothesis, normal human participants were
asked to observe and imitate a finger movement
and to perform the same movement after spatial
or symbotic cues. Brain activity was measured
with functional magnetic resonance imaging. If
the direct matching hypothesis is correct, there
should be areas that become active during finger
movement, regardless of how it is evoked, and
their activation should increase when the same
movement is elicited by the observation of an
identical movement made by another individuat.
Two areas with these properties were found in
the left inferior frontal cortex (opercular
region) and the rostral-most region of the right
superior parietal lobule.
Imitation has a central role in human
development and leaming of motor, communicative,
and social skills (1, 2). However, the neural
basis of imitation and its functional mechanisms
are poorly understood. Data from patients with
brain lesions suggest that frontal and parietal
regions may be critical for human imitation (3)
but do not provide insights on the mechanisms
underlying it.
Models of imitation based on instrumental
leaming, associative learning, and more complex
cognitive processes have been proposed (1, 4).
Because imitation is not a unitary phenomenon
(2), it is possible that different imitative
behaviors, subsumed under this name, result from
different mechanisms. The ability to copy
elementary actions, however, should be based on
simple neural mechanisms. In keeping with this
concept, the ability to imitate facial and
manual gestures can be demonstrated in infants
even a few days or hours old (5). The basis of
this type of imitation might involve a "resonance"
mechanism (6) that directly maps a pictorial or
kinematic description of the observed action
onto an intemal motor representation of the same
action. This proposal is supported by the recent
discovery in the premotor cortex of the macaque
monkey (area F5) of neurons that fire both when
the monkey performs an action and when it
observes an individual making a similar action
(7). Thus, a comparable direct matching
mechanism between the observed and executed
action is a reasonable candidate for human
imitation.
The direct matching hypothesis predicts that
the areas where matching occurs must contain
neurons that discharge during action execution
regardless of how action is elicited and that at
least a subset of them should receive input
representing the action they encode. Cortical
areas endowed with a matching mechanism should,
therefore, have motor properties, and, more
importantly, they should become more active when
the action to be executed is elicited by the
observation of that action.
To assess whether such a mechanism exists, we
used functional magnetic resonance imaging
(fMRI), which allows the in vivo study of human
brain functions. The paradigm involved three
observation conditions and three
observation-execution conditions. In the
observation-execution conditions, imitative and
nonimitative behavior of simple finger movements
was compared. In an imitative condition,
participants had to execute the observed finger
movement. In the two nonimitative conditions,
participants had to execute the same movement in
response to spatial or symbolic cues (8).
The imitation task (9, 10) produced reliably
larger signal intensity (df = 66, t = 5.08 ' P
< 0.0125, corrected for multiple spatial
comparisons) when contrasted, either
individually or together, with the other two
observation execution tasks. This effect was
observed in three areas: the left frontal
operculum, the right anterior parietal region,
and the right parietal operculum (Fig. 2). In
the first two areas, activation was also present
during all three observation tasks. During all
scans the participants knew that the task was
either to move a finger or to refrain from
moving it. Thus, the mental imagery of their
finger (or of the finger movement) should have
been present even during simple observation.
This background activity was potentiated when
the stimulus to be imitated was presented. These
findings indicate, therefore, that the left
frontal operculum (area 44) and the right
anterior parietal cortex (PE/PC) have an
imitation mechanism as postulated by the direct
mapping hypothesis.
There are several reasons to expect that, if
a direct mapping for manual imitation does
exist, it should involve Broca's area (area 44).
First, area 44 is one of the relatively few
cortical areas where distal movements (the type
of movements imitated in this experiment) are
represented in humans (11). Second, area 44 is
considered the human homolog of monkey area F5
(12), in which an action observation-execution
matching system exists (7). Third, Broca's area
is the motor area for speech, and learning by
imitation plays a crucial role in language
acquisition. Fourth, as argued previously (13),
language perception should be based on a direct
matching between linguistic material and the
motor actions responsible for their production.
Broca's area is the most likely, place where
this matching mechanisin might occur.
Activation in the PE/PC area in monkeys is
essentially related to the elaboration of
proprioceptive information. Neurons from area PE
are active during passive joint rotation, deep
tissue pressure, and active arm movements (14,
15). In humans, positron emission tomography
(PET) experiments have demonstrated that there
are different activation patterns when
participants observe pantomimes of complex
actions to understand their meaning as opposed
to memorizing and repeating them. In the first
case, there is an activation of the left
inferior frontal lobe, mostly area 45 (16, 17),
but in the latter, the activation is
predominantly parietal, more prominent on the
right (16). On the basis of the physiological
properties of area PE/PC neurons and these last
data, a plausible interpretation of the parietal
activation during imitation is that a
kinesthetic copy of the movement is formed in
the right parietal lobe during movement
observation. This copy, indicating the final and
possibly intermediate joint positions is then
used during action execution.
If this is so, why are two areas involved in
imitation, and what is the difference between
the activation in the parietal and Broca's
areas? We propose that the inferior frontal area
describes the observed action in terms of its
motor goal (for example, lift the finger)
without defining the precise details of the
movement. In contrast, the parietal lobe area
codes the precise kinesthetic aspects of the
movement (for example, how much the finger
should be lifted). This hypothesis is based on
data showing that F5 neurons code the general
goal of a movement and not the precise movement
details (7), whereas PE neurons code a
proprioceptive storage of limb position (14).
Thus, although both areas will collaborate in
action imitation, the more prevalent influence
will be of the left frontal cortex (to perform
the task) or of the right parietal cortex (to
repeat the exact movement), according to the
task request.
An immediate question that the direct
matching mechanism of imitation raises is how an
individual may preserve the sense of self during
action observation, given the shared motor
representation between the "actor" of the
movement and the "imitater." The activation in
the parietal operculurn is probably relevant to
this question. The parietal operculuin is a
sensory area, and its activity here most likely
reflects reafferent signals associated with
action. Note also that the activation is mostly
lateralized to the right hemisphere and that
lesions to the right inferior parietal lobule
are typically associated with body schema
disorders (18). Enhancing brain activity of this
area during action production can be a
computationally simple way to preserve body
identity ("it is my body that is moving") during
imitation (19).
