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The Mirror Neuron System NEUROLOGICAL REVIEW SECTION EDITOR: DAVID E. PLEASURE, MD The Mirror Neuron System Luigi Cattaneo, MD; Giacomo Rizzolatti, MD irror neurons are a class of neurons, originally discovered in the premotor cortex of monkeys, that discharge both when individuals perform a given motor act and when they observe others perform that same motor act. Ample evidence demon- strates the existence of a cortical network with the properties of mirror neurons M(mirror system) in humans. The human mirror system is involved in understanding others’ ac- tions and their intentions behind them, and it underlies mechanisms of observational learning. Herein, we will discuss the clinical implications of the mirror system. Arch Neurol. 2009;66(5):557-560 Mirror neurons were first described in the feature of a motor act but have sufficient F5 sector of the macaque ventral premo- clues to understand its goal6 or when mon- tor cortex.1,2 These neurons, like most neu- keys recognize an action from its sound rons in F5, discharge in association with only.7 These data indicate that premotor movements that have a specific goal (mo- mirror neurons discharge whenever the tor acts). They do not fire when a mon- monkey builds up an internal represen- key executes simple movements, that is, tation of a motor act made by another during active displacement of a body part agent, even if the monkey does not see it. devoid of a specific goal. Recent data on the motor organization of Neurons with the same characteristics as theIPLshowthatmirrorneuronsareinvolved those in area F5 were also found in the in- in more complex functions than motor act feriorparietallobule(IPL)ofmonkeys.These understanding. It was found that most hand- 2 areas form a network that is embedded in related neurons in the IPL differently encode the system of parietofrontal circuits that or- the same motor act when it is embedded in ganize actions.3 Visual information on bio- different actions (eg, grasp to eat and grasp logical motor acts reaches F5 through con- to place). These have been named action- nections with the superior temporal sulcus, constrained neurons.8 Most interestingly, whereactionsperformedbybiologicalagents many of these neurons have mirror proper- are coded.4 In the superior temporal sulcus, ties that are congruent with the action- neurons do not appear to discharge in asso- constrained pattern. Their behavior is illus- ciation with motor behavior. trated in Figure 1. These findings indicate It is generally assumed that the main that action-constrained parietal mirror neu- functional role of parietofrontal mirror rons do not only encode the observed mo- neurons is to understand motor acts per- tor act (eg, grasping), but also the aim of the formed by others in an automatic way, ie, observedaction.Ithasbeenhypothesizedthat by matching them to the monkey’s own this organization provides a neural substrate motor repertoire.5 Evidence in favor of this for understanding the goal of the entire ob- hypothesis came from experiments that served action before it is concluded. showed that F5 mirror neurons also fire when monkeys cannot see the triggering THE MIRROR SYSTEM IN HUMANS Author Affiliations: Dipartimento di Neuroscienze, Università di Parma, Parma, Evidence of the existence of a mirror sys- Italy. tem in humans comes from neuroimaging (REPRINTED) ARCH NEUROL / VOL 66 (NO. 5), MAY 2009 WWW.ARCHNEUROL.COM 557 ©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 manual acts in an intermediate position.10 The localization Motor responses of action-constrained mirror neurons of proximal motor acts, ie, the transport phase of the hand to a particular location, was found in a recent functional mag- Unit 67 Unit 161 neticresonanceimaging(fMRI)studytoberepresentedmore dorsally than grasping acts, in the dorsal premotor cortex.12 These studies and other works have also explored the Grasp to Eat representation of observed motor acts in the parietal cor- tex. Transitive motor acts were found to be represented in the intraparietal sulcus and on the IPL convexity im- mediately adjacent to it.10,11 Additional studies have in- vestigated the organization of the parietal lobe during the observation of actions different from distal goal-directed Grasp to Place acts. Reaching movements were shown to be located in the superior parietal lobule, extending ventrally into the intraparietal sulcus. Intransitive (non–object directed) 1 s Visual responses of action-constrained mirror neurons manual actions have been shown to have their own spe- cific parietal representation located—regardless of the act Unit 87 Unit 39 being symbolic, mimed, or meaningless—in the posterior part of the supramarginal gyrus, extending into the angu- lar gyrus.13 Finally, the observation of actions made with tools, besides activating the hand-manipulating region, Grasp to Eat specifically activates the most rostral part of the supra- marginal gyrus, ventral to the area of representation of hand grasping.14 CONGRUENCE BETWEEN OBSERVED MOVEMENTS AND MOTOR ACTIVATION Grasp to Place IN THE OBSERVER In healthy adults, observation of others’ motor behavior 1 s does not induce overt motor activity in the observer. How- ever, several studies have discovered a subliminal mo- Figure 1. Peristimulus histograms of 4 action-constrained neurons recorded tor activation that is associated with action observation from the monkey inferior parietal lobule. The 2 neurons on the left (units 67 by applying TMS over the primary motor cortex,15 which and 87) discharged when grasping was embedded in a grasp-to-eat action also showed a strong congruence between the observed but would not fire when grasping was the first step of a grasp-to-place 16 action, though these 2 actions are identical. The opposite behavior was motor behavior and the evoked motor output. An in- observed in the 2 neurons on the right side (units 161 and 39).8 crease in the observer’s motor evoked potentials is found when recording from the same muscles that are re- studies and noninvasive neurophysiological investigations cruited in movement execution and with the same acti- (electroencephalography, magnetoencephalography, and vation timing. This phenomenon occurs mostly at the cor- transcranial magnetic stimulation [TMS]).9 Neuroimag- tical level as shown by TMS paired-pulse paradigms.17 ing demonstrated the existence of 2 main networks with Transcranial magnetic stimulation experiments have mirror properties: one residing in the parietal lobe and the provided strong evidence that the human mirror system premotor cortex plus the caudal part of the inferior fron- also codes simple movements. However, in agreement tal gyrus (parietofrontal mirror system) (Figure 1), and the with fMRI and monkey data, TMS can also reveal mirror other formed by the insula and the anterior mesial frontal activation related to the goal of the observed motor act. cortex (limbic mirror system). The parietofrontal mirror A TMS study showed that while observing a reaching and system is involved in recognition of voluntary behavior, grasping act that is suddenly modified by an unpredict- while the limbic mirror system is devoted to the recogni- able movement, motor evoked potential facilitation mir- tion of affective behavior. In the present review, we will rors the time course of the predicted motor act rather than describe only the first system. adjusting to its incongruent variant in real time.18 REPRESENTATION OF OBSERVED MOTOR ACTS MOTOR EXPERIENCE AND MOTOR LEARNING IN THE PREMOTOR AND PARIETAL CORTICES There is evidence that only motor acts that are present A series of experiments have addressed the issue of the ana- in the motor repertoire of the observer are effective in tomicalandfunctionalorganizationoftheparietofrontalmir- activating the mirror system. This was shown in an fMRI ror system. Most of them investigated transitive (goal-di- experiment in which oral actions made by humans, mon- rected), distal motor acts. These studies showed that these keys, and dogs were presented to normal human volun- acts are coded in the ventral premotor cortex according to teers. The data demonstrated that the left hemisphere IPL a rough somatotopic organization,10,11 with motor acts in the and inferior frontal gyrus responded to actions made by legs being located dorsally, oral acts located ventrally, and a human and a nonhuman performer, as long as the ac- (REPRINTED) ARCH NEUROL / VOL 66 (NO. 5), MAY 2009 WWW.ARCHNEUROL.COM 558 ©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 tion was part of the motor repertoire of the human ob- server (eg, biting for eating). The mirror system failed to be activated when the action belonged to another spe- 19 cies (eg, barking). PMDPMD Activation of the mirror system is also related to the SPLSPL observer’s motor experience of a given action. This has IPSIPS been clearly demonstrated in experiments that use dance steps as observed stimuli. First, it was shown that, in the IPLIPL V M observer, the amount of mirror activation correlated with PMVP the degree of his or her motor skill for that action.20 An- IFGIFG other experiment ruled out the possibility that this effect could be due to mere visual familiarity with the stimuli. STSSTS Observing steps particular to male dancers produced a stronger mirror activation in professional male dancers than those performed by female dancers and vice versa.21 An additional prospective study showed that
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