Action Recogntion in the Premotor Cortex

7/23/2019 Action Recogntion in the Premotor Cortex

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BRAINA JOURNAL OF NEUROLOGY

FROM THE ARCHIVES

Action recognition in the premotor cortex. By Vittorio Gallese, Luciano Fadiga, Leonardo Fogassi and GiacomoRizzolatti. 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 classi-

fication 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 methodol-

ogies (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 move-

ments 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 notmoved. 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 isevoked 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 some-

thing on a tray but not when the expected sequence involvingfood, 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

doi:10.1093/brain/awp167 Brain 2009: 132; 16851689 | 1685

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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-the-

hand-and-the-mouth neurons that respond to observing one

component or other of an action also discharge with strict con-

gruence (31%), broad congruence (61%) or non-congruence

Figure 1 Visual and motor responses of a grasping mirror neuron. The behavioural conditions are schematically represented in theupper 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 graspingmovements 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.

1686 | Brain 2009: 132; 16851689 From the Archives


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(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 andmatching 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 visua-

lization 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 tomogra-

phy studies also hint at the existence of mirror neurons in manbut 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 evolu-

tionary 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 ges-

tures 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

Figure 2 Visual responses of a placing mirror neuron. (A) The experimenter placed a piece of food on the tray. Rasters are aligned withthe 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.

From the Archives Brain 2009: 132; 16851689 | 1687


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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 lateralviews 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.

1688 | Brain 2009: 132; 16851689 From the Archives


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exist in human Brocas area and should represent the neuro-

physiological 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

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

From the Archives Brain 2009: 132; 16851689 | 1689

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Action Recogntion in the Premotor Cortex