doi:10.

1093/brain/awp167

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BRAIN
A JOURNAL OF NEUROLOGY

FROM THE ARCHIVES

Action recognition in the premotor cortex. By Vittorio Gallese, Luciano Fadiga, Leonardo Fogassi and Giacomo
Rizzolatti. Brain 1996: 119; 593609.
Dogmafollowing Karl Brodmanns studies from the early
1900steaches that the agranular cortex of the primate frontal
lobe consists of area 4 containing giant pyramidal neurons and
area 6 which does not; to which can be added a functional classification of primary (area 4 and the lateral part of area 6) and
supplementary motor cortex (the medial component of area 6).
But this is overly simplified and a variety of anatomical methodologies (immunohistochemistry, neurochemistry and hodology,
inter alia) have revealed a mosaic of structures in the agranular
frontal region to which distinct functional properties can
be assigned. The classical view of the premotor cortex as the
orchestrator strictly of motor control is now supplemented by
evidence for its role in cognitive and behavioural functions
coding space, decoding the intrinsic properties of objects and
contributing to associative learning. But special attention should
be paid to F5, lying immediately caudal to the inferior arm of
the arcuate sulcus, and concerned with hand and mouth movements in its dorsal and ventral portions, respectively. The hand
neurons discharge during goal-directed movements, such as
specific types of grasping, tearing, manipulating and holding;
and they become active when 3D objects that are the same size
as those activating that neuron during grip, are seen but not
moved. Now the Italian team describe simian neurons that
discharge not only with movement but also when the monkey
observes meaningful movements made by the experimenter.
They also provide a detailed description of the properties
of these cellsdesignated mirror neuronsand some clinical
implications arising from their discovery.
Their method is to record from the rostral inferior part of area
6 in one or both hemispheres of two monkeys trained to observe
and then reach for food and other objects of differing sizes and
shapesmovements that require precision grip (index finger and
thumb), finger prehension (opposition of the thumb to other
fingers), whole hand prehension (flexion of the fingers around a
large object) or reaching. In a more complex experimental design,
the monkey is rewarded with food but only after first turning the
light switch on in a darkened box and waiting for the door to
open automatically before removing a geometric solid item, with
a further variation of theme in which this sequence is performed
entirely in the dark. The physiological properties associated with

these movements are matched to activity of neurons recorded

whilst the monkey is teased by the experimenter manipulating a
variety of food rewards that are seen and anticipated but not
actually handled; and the responses to a variety of emotionally
charged gestures are also captured. Many other controls are
designed to establish that the information obtained is specific to
real or perceived handobject movements, and with visual input
varying in depth and laterality to the hemisphere from which
recordings are made. After recovery from surgery placing the
monkey in a head chamber suitable for repeated awake single
neuronal physiological recordings, these and video sequences of
the experimenter and the resulting behavioural responses, and
electromyography traces from various muscles, are captured.
Eventually the monkey is sacrificed and histological preparations
made of the site from which neuronal signals had been obtained.
The Italian investigators identify 92 mirror neurons from
amongst 532 providing evidence for activity during behavioural
tasks. Mirror neurons respond most reliably to actions in which
the experimenters hand or mouth interacts with objects of interest
to the monkey wherever these are seen. These grasp (Fig. 1),
placement (Fig. 2) and manipulation (Fig. 3) responses do not
habituate. No physiological response in these same cells is
evoked by viewing the objects themselves, moving them with
tools, mimicking the movement without any object being visible
or presenting emotional gestures. Of the 92 mirror neurons
studied, 51 are specific to one routine whereas 38 are activated
by multiple stimuli and 3 are both hand and mouth responsive.
Amongst 30 grasping neurons, some cease firing once the
hand has taken hold of the object but reactivate with transfer
from the experimenters to the monkeys hand; others continue
to discharge throughout the entire sequence. Some mirror neurons
are more fastidious, only responding to particular types of grasp
differentiated as precision grip, and finger or whole hand
prehension. Others activate when the experimenter places something on a tray but not when the expected sequence involving
food, tray and placement is disrupted or re-ordered. And some
mirror neurons respond only in the brief phase during which an
object is manipulated away from its starting location; by the
movement of one hand passing the object towards the other;
by the act of holding the object; by observing hand actions that

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From the Archives

Figure 1 Visual and motor responses of a grasping mirror neuron. The behavioural conditions are schematically represented in the
upper part of each panel. In the lower part are shown a series of eight consecutive trials (raster display) and the relative response
histogram. (A) A tray with a piece of food was presented to the monkey, the experimenter made the grasping movement towards the
food and the tray towards the monkey who grasped it. The phases when the food was presented and when it was moved towards the
monkey were characterized by the absence of neuronal discharge. In contrast, a strong activation was present during grasping
movements of both the experimenter and the monkey. (B) As above, except that the experimenter grasped the food with pliers. In
both A and B, rasters and histograms are aligned with the moment at which the experimenter touched the food either with his hand or
with the pliers (vertical line). Filled circles indicate the beginning of the trials. Histogram bin width = 20 ms. Ordinates, spikes/bin;
abscissa, time.

lack purposeful properties; by use of the left or right hand only;

by whether cells sense information presented in the ipsilateral or
contralateral field; or by the direction of movement from left to
right or vice versa (most mirror neurons preferring movement

towards the recording hemisphere). The grasping-with-thehand-and-the-mouth neurons that respond to observing one
component or other of an action also discharge with strict congruence (31%), broad congruence (61%) or non-congruence

From the Archives

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Figure 2 Visual responses of a placing mirror neuron. (A) The experimenter placed a piece of food on the tray. Rasters are aligned with
the moment at which the experimenters hand touched the tray surface. The neurons discharge started when the hand approached the
tray and continued for the whole time the hand was in contact with the food. (B) The experimenter grasped a piece of food located on
a tray. A tray was presented to the monkey with a piece of food on it; the experimenter moved his hand towards the food and grasped
it. As in A, the rasters are aligned with the moment at which the experimenters hand touched the tray surface. The responses during
grasping observation were much weaker than during placing observation. Conventions as in Fig. 1.

(8%) when the same movement is actually performed by the

monkey, and with the same specificity for particular components
of that behaviour. The motor activity of mirror neurons is not due
to responses generated in the visual system whilst the monkey
looks at the objectcongruence being present when seeing an
object or manipulating it in the dark; or through the artefact of
concomitant muscle activity. The hand area (F1) does not encode
any mirror neuronal activity. Rather, this is confined to F5 (Fig. 4).
It seems therefore that goal-directed neurons in F5, selectively
activated in response to types of prehension, are closely associated
with others that respond to the sight of the same specific actions
performed by others. Cells having some similar properties but not
the full range of orientations are also to be found in the region of
the superior temporal sulcus. Perhaps these encode the semantic
representation of handobject interactions, registering and
matching perceived actions with the motor-vocabulary before
F5 orchestrates pragmatic aspects of the behavioural response.
The main connections of F5 are with the anterior intraparietal
area. The lack of connectivity between the visual cortex and F5,
and failure both to stimulate mirror neurons through direct visualization of the object provide further evidence for the interaction
of the agent of the action with the object target of the action
as fundamental to the activity of mirror neurons.
As for their function, the authors dislike the interpretation that
mirror neurons provide motor preparation after the animal sees

something coming, since the pattern of discharge is confined

to discrete steps in a given movement. They might generate an
internal representation of the intended movement that links to
motor learning and understanding the meaning of observed
action having resonances in learning by imitation and the need
to appreciate that a purposeful actionas opposed to a random
movementrequiring an appropriate response is imminent; and to
predict its consequences. The selectivity for hand and mouth
movements, and for armhand directional properties preferring
movement towards, not away, from the monkey, might suggest
a primary function related to feeding. But mirror neurons respond
equally to food, inert 3D objects and (generally) those of all sizes
irrespective of distance and hence the level of retinal stimulation.
Transcranial magnetic stimulation and positron emission tomography studies also hint at the existence of mirror neurons in man
but here the evidence is necessarily circumstantial. However,
simian area F5 corresponds to the human inferior frontal
gyrusBrocas area. That, in turn, argues for a complex evolutionary relationship between manual activities and speech, for the
common association between aphasia and loss of recognition for
pantomime and for the formulation that speech perception
depends more on the critical primitives provided by phonetic gestures of the speaker than the sounds emitted. [We are] tempted
to speculate that neurons with properties similar to those of
monkey mirror neurons, but coding phonetic gestures, should

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From the Archives

Figure 3 Visual responses of a manipulating mirror neuron. (A) The experimenter retrieved a piece of food placed in a well in a tray,
using his index finger. This was the only action that activated the neuron. (B) The same action was mimed without food. (C) The food
was retrieved using a tool. Conventions as in Fig. 1.

Figure 4 Location of microelectrode penetrations in one monkey (MK8): visual responses of a manipulating mirror neuron. The lateral
views of the two hemispheres are shown below the enlarged views of the explored cortex. The penetrations performed in areas F5 and
F1 are indicated by dots. Dot size is calibrated according to the number of mirror and mirror-like neurons found in a given penetration.
Arrows indicate the borders between the cortical areas. As = arcuate sulcus; Cs = central sulcus. Calibration bars1mm.

From the Archives

exist in human Brocas area and should represent the neurophysiological substrate for speech perception. Subsequent work
has indeed shown that Brocas area is involved in syntactical
analysis, mathematical calculation, music processing, language
comprehension, understanding actions of others and observing
hand and mouth actionevidence that Patrik Fazio, Luciano

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Fadiga and colleagues now supplement by showing that patients

with frontal aphasia but no apraxia cannot correctly encode
observed human actions (page 1980).
Alastair Compston
Cambridge