MNS and social cognition.pdf

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The mirror system and its role in social cognition

Giacomo Rizzolatti 1 and Maddalena Fabbri-Destro 1 , 2

Experiments in monkeys have shown that coding the goal of the

motor acts is a fundamental property of the cortical motor

system. In area F5, goal-coding motor neurons are also

activated by observing motor acts done by others (the

‘classical’ mirror mechanism); in area F2 and area F1, some

motor neurons are activated by the mere observation of goal-

directed movements of a cursor displayed on a computer

screen (a ‘mirror-like’ mechanism). Experiments in humans and

monkeys have shown that the mirror mechanism enables the

observer to understand the intention behind an observed motor

act, in addition to the goal of it. Growing evidence shows that a

deﬁcit in the mirror mechanism underlies some aspects of

autism.

The mirror mechanism is present in various cortical areas

and according to its location mediates different functions.

The mirror mechanism is located in the parieto-frontal

network and underlies the understanding of the goal of

the observed motor acts and the intention behind them.

The mirror mechanism is also located in human Broca’s

area and transforms heard phonemes into the motor

format necessary to produce them. Finally, the mirror

mechanism is present in the insula and anterior cingulate

cortex. It mediates the understanding of emotions of

others. In the present article we will deal only with the

parieto-frontal mirror network (for recent reviews on

other systems endowed with the mirror mechanism see

[ 4,5 ]). Our review will be not exhaustive. Only those

studies that are relevant with the main theme of this

article will be reviewed.

Addresses

1 Dipartimento di Neuroscienze, Sezione Fisiologia, Universit` di Parma,

via Volturno, 39, 43100 Parma, Italy

2 Dipartimento SBTA, Sezione di Fisiologia Umana, Universit` di Ferrara,

via Fossato di Mortara,17-19, 44100 Ferrara, Italy

The mirror mechanism in monkeys

Goal coding in the monkey motor areas

The mirror mechanism is embedded in the motor system

( Figure 1 ). Crucial, therefore, for understanding its func-

tion is to understand which are the motor properties of the

areas where the mirror neurons are located. As far the

parieto-frontal circuit is concerned early experiments

showed that, in F5, many neurons ﬁre regardless of

whether the motor act is done using the right hand,

the left hand or the mouth [ 6 ]. This was interpreted as

evidence that area F5 codes the goal of the motor act

rather than the single movements forming it [ 7 ].

Corresponding author: Rizzolatti, Giacomo ( giacomo.rizzolatti@unipr.it )

and Fabbri-Destro, Maddalena ( fbbmdl@unife.it )

Current Opinion in Neurobiology 2008, 18:179–184

This review comes from a themed issue on

Cognitive neuroscience

Edited by Read Montague and John Assad

Available online 20th August 2008

0959-4388/$ – see front matter

DOI 10.1016/j.conb.2008.08.001

The problem of goal coding in area F5 has been recently

re-examined in a more stringent way. Macaque monkeys

were trained to use two tools: normal pliers and ‘reverse’

pliers (an implement that requires ﬁnger opening, instead

of closing, to grasp an object). Single neurons were

recorded from F5 and the primary motor cortex (F1).

The result showed that all the recorded neurons from F5

and about 40% of neurons recorded from F1 discharged in

relation to the goal of the motor act independent of

whether it was achieved by closing the hand (normal

pliers) or opening it (reverse pliers) [ 8 ].

Introduction

Social cognition is the study of how people interact with

other individuals in social situations. A fundamental

aspect of social interaction is the capacity to understand

what others are doing, their intention and their feelings.

A series of experiments carried out in the last decade

showed that this capacity is mediated, in part, by a

speciﬁc mechanism called the mirror mechanism [ 1,2 ].

This mechanism transforms sensory information

describing actions of others into a motor format

similar to that the observers internally generate

when they imagine themselves doing that action or

when they actually perform it. The similarity between

the motor format generated by observing others and

that internally generated during motor and emotional

behavior allows the observer to understand others’

behavior, without any complex cognitive elaboration

[ 3 ].

The goal representation in the cortical motor system is not

a peculiarity of F5, but has been also described in other

sectors of the premotor cortex and in F1 [ 9–12 ]. However,

because, alternative explanations could not be ruled out,

the claim of goal coding in the cortical motor system was

advanced with caution. The new data just reviewed show

beyond any doubt that the cortical motor system has the

goal of a motor act (grasping, holding, reaching) inbuilt in

its organization. This organization has fundamental con-

ceptual consequences because it indicates that the ﬁring

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Current Opinion in Neurobiology 2008, 18:179 – 184

180 Cognitive neuroscience

Figure 1

Example of a mirror neuron and anatomy of agranular frontal and posterior parietal cortex of the macaque monkey. (Upper part) F5 mirror neuron. The

neuron discharges when the monkey grasps an object (a) and when it observes the experimenter grasping it (b). (Lower part) the central part of the

figure shows the cytoarchitectonic parcellation of the agranular frontal cortex (areas indicated with F and arabic numbers) and of the parietal lobe

(areas indicated with P and progressive letters). The enlargement of the frontal region (rectangle on the left) shows the parcellation of area F5. The

rectangle on the right shows the areas buried within the intraparietal sulcus. AIP, anterior intraparietal area; IP, intraparietal sulcus; LIP, lateral

intraparietal area; MIP, medial intraparietal area; POs, parieto-occipital sulcus; As, superior arcuate sulcus; Ai inferior arcuate sulcus; C, central sulcus;

Ca, calcarine fissure; CG, cingulate cortex; FEF, frontal eye field; L, lateral sulcus; Lu, lunate sulcus; P, principal sulcus; STS, superior temporal sulcus.

(Modified from [ 5 ]).

elicited in F5 mirror neurons by the observation of a motor

act describes the goal of the observed motor act. This

enables the observer to understand it, without the need to

postulate a dichotomy between putative posterior goal-

understanding areas (e.g. STS) and motor areas.

of two phases: An active movement phase in which the

monkey moved the cursor, and an observation phase in

which the monkey observed the replayed movements

generated in the active phase. The observation phase has

three conditions. In the ﬁrst, both the cursor and the

targets were visible; in the second, the monkey saw only

the replayed targets; in the third, the monkey saw only

the moving cursor, but not the targets. The results

showed that, in both PMd and F1 passive observation

of the task elicited a neural discharge similar to that found

during task execution. The observation of the cursor

without targets and of the targets without cursor gave

either no responses or responses weaker than those found

during the observation of both cursor and targets [ 14 ].

Mirror-like mirror neurons

Typically, the mirror mechanism in the monkey has been

studied in ethological situations. A few years ago evidence

was provided that, in the dorsal premotor cortex (PMd or

F2) there are neurons that discharge both when a monkey

executes a conditioned task (moving a cursor on a com-

puter screen) and when the animal observes the same task

done by the experimenter. Unlike ‘classical’ mirror

neurons these neurons did not require, to be triggered,

the observation of an effector (e.g. a hand) that acts on the

object. The mere observation of goal achievement was

sufﬁcient [ 13 ].

The most likely explanation of these ﬁndings is that these

mirror-like neurons are sensitive to the goal of the motor

act. In fact, the moment in which the cursor reaches the

target corresponds to the goal achievement, normally

obtained using natural effectors. The study does not

report whether these neurons discharge during the obser-

vation of motor act done with natural effectors, yet the

A recent study extended this observation. Monkeys were

trained to move repetitively a cursor to targets that

appeared at random locations. The experiment consisted

Current Opinion in Neurobiology 2008, 18:179 – 184

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The mirror system and its role in social cognition Rizzolatti and Fabbri-Destro 181

mechanism underlying their activation appears to be

similar to that of mirror neurons.

clips showing hand grasping movements activated

neurons in F5 (Caggiano et al., abstract in Society for

Neuroscience, 123.12, 2007).

Another important development in the study of mirror

system has been the demonstration that mirror neurons

do not require the presentation of a real scene to be

activated. First an fMRI study [ 15 ] and recently a single

neuron recording study showed that, in monkeys con-

ditioned to ﬁxate a spot light, the observations of video-

Mirror-mechanism in humans

Goal coding in human mirror system

As in the monkey, human parieto-frontal mirror network

( Figure 2 ) possesses a mirror mechanism for coding the

goal of motor acts. An earlier evidence for this was

Figure 2

Later view of human cortex with an enlarged view the frontal lobe. Cytoarchitectonic subdivision according to Brodmann. The areas in yellow show

areas responding to the observation and execution of hand motor acts. (Upper part) enlarged view of the frontal lobe. The possible homology between

monkey and human premotor cortex are indicated. C: central sulcus; IF: inferior frontal sulcus; FEF: frontal eye field; PMd: dorsal premotor cortex;

PMv: ventral premotor cortex; PrePMd: pre-dorsal premotor cortex; SP: upper part of the superior precentral sulcus. For areas indicated with F see

Figure 1 . (Modified from [ 5 ].)

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Current Opinion in Neurobiology 2008, 18:179 – 184

182 Cognitive neuroscience

provided by a TMS experiment in which motor-cortex

excitability was tested during the observation of hand

movements directed to a speciﬁc goal (predictable move-

ments) and in trials in which the hand moved in a

different unpredictable way. The data showed that the

observation of unpredictable movements did not elicit

the expected change in the excitability of the motor

cortex corresponding to the observed movements. During

the observation of the unpredictable movements, the

excitability pattern was that found during the observation

of the predicted ones. This indicates that the observed

motor acts were coded from their very beginning in terms

of the ﬁnal goal of the action and not in terms of the

movements forming them [ 16 ].

without grasping objects. The reaching movements were

actually executed, observed, or imagined. An overlap

between executed, observed and imagined reaching acti-

vation was found in dorsal premotor cortex and in the

superior parietal lobule (SPL) extending into IPS. There-

fore, the human brain possesses a reaching mirror system,

and its location is distinct from that for grasping [ 20 ].

Mirror system and intention understanding

When we observe a motor act like grasping a cup of coffee

we understand not only what the agent is doing but,

typically, also why he/she is doing it. The agent’s intention

can be inferred from the way the object is grasped or from

the context in which the action is executed. Some years

ago, an fMRI experiment showed that when individuals

had to infer the intention of the agent from the context,

there was a selective activation of the right frontal node of

the mirror-system [ 21 ]. The importance of the mirror

system in understanding intention has been recently

conﬁrmed by an fMRI experiment based on the repeti-

tion–suppression paradigm. Participants were asked to

observe repeated movies showing either the same move-

ment or the same outcome independent of the executed

movement. The result showed activity suppression in the

right inferior parietal and in the right IFG when the

outcome was the same [ 22 ].

Further evidence that human parieto-frontal mirror sys-

tem codes the goal of motor act has been provided by

fMRI studies. Gazzola et al. [ 17 ] instructed volunteers to

observe movies where either a human or a robot arm

grasped objects. In spite of differences in shape and

kinematics between the human and robot arms, the

parieto-frontal mirror-system was activated in both con-

ditions [ 17 ]. Hamilton et al [ 18 ] addressed the goal

coding issue using the repetition–suppression technique,

a technique based on the trial-by-trial reduction of a

physiological response to repeated stimuli. Participants

observed a series of movies showing goal-directed motor

acts with the sequence controlled so that some goals were

novel and others repeated relative to the previous move-

ments. Repeated presentation of the same goal, caused

the suppression of the response in the left intraparietal

sulcus (IPS) while this region was not sensitive to the

trajectory of the actor’s hand.

It has been suggested that, in complex situations, infer-

ential processing may complement the mirror mechanism

in intention understanding [ 3 ]. Experimental evidence

for this was provided by Brass et al. [ 23 ] in an fMRI

experiment in which volunteers were required to infer

intention in an unusual situation. Areas that became

active in mentalizing [ 24 ] were found to be active in this

condition.

A motor act performed by a robotic arm is recognized by

the hand mirror system. Can the goal of a hand movement

be also recognized in the absence of any experience of

hand movements? To answer this question two aplasic

individuals, born without arms and hands, were studied.

While being scanned they were asked to watch videos

showing hand actions and their brain activations were

compared with those of control volunteers. All partici-

pants also made actions with different effectors (feet,

mouth and, for normal volunteers, hands). The results

showed that the mirror-system of aplasic individuals is

activated by the observation of hand motor acts. This

demonstrates that the brain of aplasics can mirror motor

acts that they never had executed. The goal is recognized

by recruiting areas involved in the execution of motor acts

having the same goal but using different effectors [ 19 ].

While we know virtually nothing about the neurophysio-

logical mechanisms underlying inferential processing,

data in monkeys suggest a neurophysiological mechanism

that may account for mirror-based intention understand-

ing [ 25 ]. These data show that, in monkey IPL, motor acts

are organized in chains that code speciﬁc intentional

actions (i.e. grasp-for-eating, grasp-for-placing). Most

interestingly, these chains may be also activated by the

mere observation of the ﬁrst motor act of a chain, thus

providing the observer of an internal copy of the whole

future action of the agent before its execution, that is the

agent’s intention.

An EMG study provided evidence for the existence of a

similar mechanism in humans. When ‘typically develop-

ing’ children observe an action formed by several motor

acts, the muscles that are involved in the last motor act

become already active during the observation of the ﬁrst

one. This activation is absent in children with autism.

These data indicate that the mirror system provides the

observers with a copy of the entire action that the agent

A motor goal implies the capacity to reach and grasp an

item. However, virtually all studies on mirror system in

humans were concerned with grasping. Only recently the

problem of a mirror mechanism for reaching movements

was addressed. In an fMRI study volunteers were asked to

transport their hand to a particular location in space

Current Opinion in Neurobiology 2008, 18:179 – 184

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The mirror system and its role in social cognition Rizzolatti and Fabbri-Destro 183

intends to do at the start of it, thus enabling the observer

to understand agent’s intention. Children with autism

appear to lack this motor understanding [ 26 ].

References and recommended reading

Papers of particular interest, published within the period of the review,

have been highlighted as:

The mirror system for coding movements

The property of the parieto-frontal mirror system we

stressed in this review is that of coding goals. However,

from the very beginning of mirror system studies, TMS

experiments showed that human motor system, unlike

that of monkeys, also responds to the observation of

movements apparently devoid of a goal (e.g. [ 27–29 ]).

of special interest

of outstanding interest

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the premotor cortex. Brain 1996, 119:593-609.

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the recognition of motor actions. Cogn Brain Res 1996,

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3. Rizzolatti G, Fogassi L, Gallese V: Neurophysiological

mechanisms underlying the understanding and imitation of

action. Nat Rev Neurosci 2001, 2:661-670.

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systems in monkeys and humans. Physiology 2008,

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A recent fMRI study elegantly demonstrated that this

‘movement mirror mechanism’ is extremely sensitive to

movement kinematics. Dayan et al. [ 30 ] examined brain

responses to the observation of drawing and curved

hand movements obeying or not the 2/3- power law,

i.e the law describing the coupling between movement

curvature and velocity. Mirror hand areas were more

strongly activated during the observation of movement

obeying this law than in response the any other type of

motion.

Conclusions

In spite of the explosion of studies on mirror mechanism,

there are two issues of great interest for social cognition

that are not yet solved. The ﬁrst is whether the mirror

mechanism is innate or acquired through experience.

There is ample evidence that mirror system is extremely

plastic and speciﬁc motor experience modiﬁes its respon-

siveness [ 31 ,32,33 ]. We also know that the formation of

motor memories is strongly facilitated when the partici-

pants both observe and perform the same movement

[ 34,35 ] and that the mirror responses triggered by a

corresponding movement can be modiﬁed by repetitively

coupling the performed movement with the observation

of a non-congruent movement [ 36 ]. The extent, however,

of mirror activity at birth and in the ﬁrst months is still an

open question [ 37 ].

Caruana F, Jezzini A, Gallese V, Rizzolatti G: When pliers become

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2008, 105:2209-2213.

A single-unit study showing that hand grasping premotor neurons (area

F5) and several hand motor neurons (area F1) discharge both when the

monkey grasps objects using normal pliers and ‘reverse pliers’ – an

implement that requires ﬁnger opening instead of closing to grasp an

object. This study presents crucial evidence that the goals of motor acts

and not just the movements forming them are coded in the monkey

cortical motor system.

9. Crutcher MD, Alexander GE: Movement-related neuronal

activity selectively coding either direction or muscle pattern in

three motor areas of the monkey. J Neurophysiol 1990,

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target (goal) of visually guided arm movements in three motor

areas of the monkey. J Neurophysiol 1990, 64:164-178.

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representations in the primary motor cortex. Science 1999,

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represented in the ventral premotor cortex. Nat Neurosci 2001,

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dorsal premotor cortex: speciﬁcation of multiple direction

choices and ﬁnal selection of action. Neuron 2005, 45:801-814.

Another fundamental issue concerns the presence of

mirror system in species other than primates. Recently,

mirror mechanism has been elegantly demonstrated in

birds [ 38 ]. What about mammals? Is mirror mechanism a

peculiarity of social cognition of primates, or do other

mammals possess it? Although this is not an easy exper-

imental task, the discovery of a mirror mechanism in

mammals such as rodents would allow a better under-

standing of mirror mechanism at the cellular level and

could help to elucidate the neural basis of pathological

syndromes, such as autism, possibly consequent to

damage of the mirror mechanism [ 39–41 ].

action and action observation inmotor cortex. J Neurosci 2007,

27:13241-13250.

This study shows that single-neuron responses in monkey primary motor

(F1) and dorsal premotor (F2) cortices are present during observation and

execution of a familiar task in the absence of the vision of the performing

effector. It is the ﬁrst demonstration of the presence of mirror-like activity

in the primary motor cortex.

15. Nelissen K, Luppino G, Vanduffel W, Rizzolatti G, Orban GA:

Observing others: multiple action representation in the frontal

lobe. Science 2005, 310:332-336.

16. Gangitano M, Mottaghy FM, Pascual-Leone A: Modulation of

premotor mirror neuron activity during observation of

unpredictable grasping movements. Eur J Neurosci 2004,

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Acknowledgements

This work was supported by, a grant from Ministero dell’Istruzione,

dell’Universita e della Ricerca to GR, EU project Neurocom, and

Interuniversity Attraction Poles (IAP). M.F-D. was supported by

Fondazione Cassa di Risparmio di Ferrara.

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Current Opinion in Neurobiology 2008, 18:179 – 184

Umilt ` MA, Escola L, Intskirveli I, Grammont F, Rochat M,

14.

Tkach D, Reimer J, Hatsopoulos NG: Congruent activity during

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