Developmental Cognitive Neuroscience - Antonia ?· A.F.d.C. Hamilton / Developmental Cognitive Neuroscience…

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<ul><li><p>R</p><p>Ro</p><p>AS</p><p>a</p><p>ARR2A</p><p>KAMIS</p><p>C</p><p>1h</p><p>Developmental Cognitive Neuroscience 3 (2013) 91 105</p><p>Contents lists available at SciVerse ScienceDirect</p><p>Developmental Cognitive Neuroscience</p><p>j ourna l ho me pag e: ht t p: / /www.e lsev ier .com/ locate /dcn</p><p>eview</p><p>eflecting on the mirror neuron system in autism: A systematic reviewf current theories</p><p>ntonia F. de C. Hamiltonchool of Psychology, University of Nottingham, United Kingdom</p><p> r t i c l e i n f o</p><p>rticle history:eceived 20 July 2012eceived in revised form7 September 2012ccepted 28 September 2012</p><p>eywords:utism</p><p>a b s t r a c t</p><p>There is much interest in the claim that dysfunction of the mirror neuron system inindividuals with autism spectrum condition causes difficulties in social interaction andcommunication. This paper systematically reviews all published studies using neurosciencemethods (EEG/MEG/TMS/eyetracking/EMG/fMRI) to examine the integrity of the mirrorsystem in autism. 25 suitable papers are reviewed. The review shows that current data arevery mixed and that studies using weakly localised measures of the integrity of the mirrorsystem are hard to interpret. The only well localised measure of mirror system function is</p><p>irror neuron systemmitationocial cognition</p><p>fMRI. In fMRI studies, those using emotional stimuli have reported group differences, butstudies using non-emotional hand action stimuli do not. Overall, there is little evidence fora global dysfunction of the mirror system in autism. Current data can be better understoodunder an alternative model in which social top-down response modulation is abnormal in</p><p>autism. The implications of this model and future research directions are discussed.</p><p> 2012 Elsevier Ltd. All rights reserved.</p><p>ontents</p><p>1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 912. The mirror system and autism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 923. Methodology of the review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 934. Studies which indirectly measure MNS function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93</p><p>4.1. EEG studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 934.2. MEG studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 964.3. TMS studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 964.4. Eyetracking studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 964.5. EMG studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97</p><p>5. fMRI studies of the MNS in autism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 975.1. Structural MRI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98</p><p>6. Discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 996.1. Evaluating the broken mirror theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1006.2. Social response modulation: an alternative explanation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101</p><p>7. Conclusions and future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102</p><p>Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . </p><p>E-mail address: antonia.hamilton@nottingham.ac.uk</p><p>878-9293/$ see front matter 2012 Elsevier Ltd. All rights reserved.ttp://dx.doi.org/10.1016/j.dcn.2012.09.008</p><p> . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102</p><p>1. Introduction</p><p>Individuals with autism spectrum condition (ASC)struggle with social interaction and communication, both</p><p>dx.doi.org/10.1016/j.dcn.2012.09.008http://www.sciencedirect.com/science/journal/18789293http://www.elsevier.com/locate/dcnmailto:antonia.hamilton@nottingham.ac.ukdx.doi.org/10.1016/j.dcn.2012.09.008</p></li><li><p>l Cognit</p>92 A.F.d.C. Hamilton / Developmenta<p>in formal testing and in their everyday lives. Many differ-ent cognitive and brain-based theories have been proposedto account for these difficulties. Current proposals includedifficulties in theory of mind (Frith, 2001), in social motiva-tion (Chevallier et al., 2012) and in mirror neuron function(Dapretto and Iacoboni, 2006; Gallese et al., 2009; Rizzolattiet al., 2009). The latter is the focus of the present paper,where I examine the human mirror neuron system (MNS)and whether damage to this system might have relevancefor autism.</p><p>The manuscript proceeds in three parts. First, I brieflydescribe the functions of the human mirror system andthe different models of MNS dysfunction which have beenproposed. Second, I systematically review the scientific lit-erature on the MNS in ASC, focusing on studies which haveused neuroscientific methods to assess the function of theMNS. Third, I provide an overall assessment of the field,and make suggestions for future directions in terms of boththeory and experiment.</p><p>2. The mirror system and autism</p><p>The human mirror neuron system (MNS) can be definedas the set of brain regions which are active both whenparticipants perform an action and when they observeanother person performing the same action (Rizzolatti andCraighero, 2004). The core components of the human MNSare inferior frontal gyrus (IFG) and inferior parietal lobule(IPL). In the macaque monkey equivalents of these regions,single neurons have been recorded with mirror properties(Fogassi et al., 2005; Gallese et al., 1996). Though singleunits have not been recorded in the human MNS, detailedpatterns of activation in fMRI studies leave little doubtthat these areas contain mirror neuron populations (Kilneret al., 2009; Oosterhof et al., 2010). The human MNS iswidely assumed to play a key role in action understand-ing and imitation, though this remains debated (Dinsteinet al., 2008; Hickok, 2009). There are also a number offMRI studies, some using emotional stimuli, which suggestthe existence of a broader mirror neuron network (Casperset al., 2010) that incorporates somatosensory and premo-tor cortex (Keysers et al., 2010), and possibly anterior insula(Wicker et al., 2003). The present paper will not considerthis extended mirror network in detail.</p><p>The dominant theory of MNS function is based ona direct-matching model in which observed actions aredirectly mapped onto the observers own motor system(Rizzolatti and Sinigaglia, 2010). This framework stressesthe idea that the MNS encodes the goal of an action, notjust the basic motor features, and that this direct goalencoding provides a primary mechanism both for under-standing other people and for imitating them. It is claimedthat the MNS is critical for performing and understandingaction sequences (Fogassi et al., 2005). The MNS might alsomake a contribution to theory of mind (Gallese, 2007) or tolanguage (Gallese, 2008) but these claims are more spec-</p><p>ulative. Many other models of the MNS are possible andmay even be more plausible (Michael, 2011), but the direct-matching model gives the basis for most theories linkingthe MNS to autism.</p><p>ive Neuroscience 3 (2013) 91 105</p><p>The claim that dysfunction of the MNS is a causal factorin poor social cognition in ASC is commonly called the bro-ken mirror theory (BMT) of autism. Here I distinguish threevariants of the BMT which make slightly different claims.First, extensive behavioural evidence of weak imitationskills in ASC (Williams et al., 2004) combined with the puta-tive role of the MNS in imitation (Buccino et al., 2004) ledto the idea that MNS dysfunction is the cause of poor imita-tion in ASC (Williams et al., 2001). The theory put forwardby Williams explicitly links the MNS to the self-other map-ping function described by Rogers and Pennington (1991)and suggests that failure of a basic self-other mapping inASC could cause difficulties in both imitation and otheraspects of social cognition such as theory of mind. A similarposition is endorsed by Gallese et al. (2009), and I call thisthe imitation version of the BMT.</p><p>Second, the simulation version of the BMT is built onthe idea that the MNS provides a basis for simulating otherpeople. Such simulation could apply to actions, but also toemotions and to mental states. The simulation BMT claimsthat a failure of a basic simulation system in the MNS inautism would cause very widespread difficulties in theoryof mind, language and empathy (Dapretto and Iacoboni,2006; Oberman and Ramachandran, 2007). This theory pre-dicts that comprehension of actions and emotions in thebroader MNS should all be abnormal in ASC.</p><p>Third, the chaining version of the BMT is a more subtletheory which only on the claim that some mirror neuronsrepresent action chains or sequences (Fogassi et al., 2005).These chaining mirror neurons are active only when themonkey sees or performs an action embedded in a par-ticular sequence, for example, grasping-to-eat rather thangrasping-to-place. Activation of chaining mirror neuronsat the beginning of a sequence could potentially allow themonkey to predict how the sequence will unfold, and thusunderstand the intention of the actor (Fogassi et al., 2005).Rizzolatti and Fabbri-Destro (2010) suggest that only theseaction chaining mirror neurons are abnormal in ASC, andthat dysfunction of these particular neurons leads to dif-ficulties in other areas of social cognition. The chainingversion of the broken mirror theory does not make directclaims about language or emotion comprehension impair-ment.</p><p>These three versions of the BMT share the claim thatdysfunction of the MNS is a primary cause of poor socialinteraction in individuals with ASC. This claim is intu-itively appealing and has received widespread attention,including in the popular press. Several studies suggestthat brain-based explanations of behaviour are consideredmore convincing than psychological explanations (McCabeand Castel, 2008; Weisberg et al., 2008). This may explainwhy links between a seductively named brain system (theMNS) and a developmental disorder are appealing. Fund-ing has been invested in this area and therapies basedon improving MNS function have been proposed (Perkinset al., 2010; Wan et al., 2010). However, the evidence thatthe MNS is actually abnormal in individuals with ASC is not</p><p>always clear.</p><p>Suitable evidence for abnormalities of the MNS in ASCcould come from a variety of sources, both behaviouraland brain-imaging studies. Behavioural studies are the</p></li><li><p>l Cognit</p><p>matc2tio(atiitittoofosls</p><p>pteBoilwoa</p><p>3</p><p>GcsAmeodbpwamfas</p><p>tnNii</p><p>A.F.d.C. Hamilton / Developmenta</p><p>ost plentiful, and many have examined imitation andction comprehension in an effort to measure MNS func-ion. Papers have reported abnormal imitation behaviour inhildren and adults with ASC (reviewed in Williams et al.,004), with both reduced frequency of spontaneous imi-ation (Charman et al., 1997; Ingersoll, 2007) and reducedmitation accuracy (Rogers et al., 1996; Vivanti et al., 2008)bserved. These have been reviewed in detail elsewhereHamilton, 2008; Kana et al., 2010; Williams et al., 2001)nd overall provide mixed evidence for imitation difficul-ies. In particular, performance is worse on spontaneousmitation and imitation of non-object directed actions buts normal on goal-directed imitation and reaction-timeasks. A major difficulty in interpreting behavioural stud-es of imitation or action comprehension in ASC concernshe specificity of the result. Poor performance on an imita-ion could be caused by failure of the MNS, or by failure ofther brain systems involved in visual processing, controlf responding or motor performance. Similarly, good per-ormance on a particular task could indicate an intact MNSr could re...</p></li></ul>

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