Mirror Neurons- From Origin to Function

Mirror neurons: From origin tofunction

Richard CookDepartment of Psychology, City University London, London EC1R 0JD,United Kingdom

[email protected]://www.city.ac.uk/people/academics/richard-cook

Geoffrey BirdMRC Social, Genetic and Developmental Psychiatry Centre, Institute of

Psychiatry, Kings College London, London SE5 8AF, United [email protected]://sites.google.com/site/geoffbirdlab/http://www.iop.kcl.ac.uk/staff/prole/default.aspx?go=13152

Caroline CatmurDepartment of Psychology, University of Surrey, Guildford, Surrey GU2 7XH,

United [email protected]://www.surrey.ac.uk/psychology/people/dr_caroline_catmur/http://sites.google.com/site/carolinecatmur/

Clare PressDepartment of Psychological Sciences, Birkbeck College, University ofLondon, London WC1E 7HX, United Kingdom

[email protected]://www.bbk.ac.uk/psychology/actionlab/http://www.bbk.ac.uk/psychology/our-staff/academic/dr-clare-press

Cecilia HeyesAll Souls College, University of Oxford, Oxford, OX1 4AL, and Department ofExperimental Psychology, University of Oxford, Oxford OX1 3UD, UnitedKingdom

[email protected]://www.all-souls.ox.ac.uk/users/heyesc/

Abstract: This article argues that mirror neurons originate in sensorimotor associative learning and therefore a new approach is needed toinvestigate their functions. Mirror neurons were discovered about 20 years ago in the monkey brain, and there is now evidence that theyare also present in the human brain. The intriguing feature of many mirror neurons is that they re not only when the animal isperforming an action, such as grasping an object using a power grip, but also when the animal passively observes a similar actionperformed by another agent. It is widely believed that mirror neurons are a genetic adaptation for action understanding; that theywere designed by evolution to fulll a specic socio-cognitive function. In contrast, we argue that mirror neurons are forged bydomain-general processes of associative learning in the course of individual development, and, although they may have psychologicalfunctions, they do not necessarily have a specic evolutionary purpose or adaptive function. The evidence supporting this view showsthat (1) mirror neurons do not consistently encode action goals; (2) the contingency- and context-sensitive nature of associativelearning explains the full range of mirror neuron properties; (3) human infants receive enough sensorimotor experience to supportassociative learning of mirror neurons (wealth of the stimulus); and (4) mirror neurons can be changed in radical ways bysensorimotor training. The associative account implies that reliable information about the function of mirror neurons can be obtainedonly by research based on developmental history, system-level theory, and careful experimentation.

Keywords: action understanding; associative learning; contextual modulation; contingency; genetic adaptation; imitation; mirror neuron;poverty of the stimulus; sensorimotor experience.

1. Introduction

Mirror neurons (MNs) were discovered serendipitously in1992 and given their brilliant name four years later (di Pel-legrino et al. 1992; Gallese et al. 1996). The striking feature

of many MNs is that they re not only when a monkey isperforming an action, such as grasping an object using apower grip, but also when the monkey passively observesa similar action performed by another. Neurons with thiscapacity to match observed and executed actions, to code

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both my action and your action, were originally found inarea F5 of the ventral premotor cortex (PMC) (di Pelle-grino et al. 1992; Gallese et al. 1996) and the inferior par-ietal lobule (IPL) (Bonini et al. 2010; Fogassi et al. 2005) of

the monkey brain. There is now a substantial body of evi-dence suggesting that MNs are also present in the humanbrain (Molenberghs et al. 2012).MNs have received a great deal of attention from special-

ists and in the scientic and public media. Hailed as cellsthat read minds (Blakesee 2006), the neurons that shapedcivilization (Ramachandran 2009), and a revolution inunderstanding social behavior (Iacoboni 2008), MNs havebeen ascribed a wide variety of functions. The primary can-didates relate to action understanding (Gallese & Sinigaglia2011; Rizzolatti et al. 1996), imitation (Iacoboni et al.1999), and language processing (Rizzolatti & Arbib 1998).However, signifying the way in which MNs have capturedthe attention and imagination of neuroscientists, psycholo-gists, and philosophers, they have also been implicated in:embodied simulation (Aziz-Zadeh et al. 2006b), empathy(Avenanti et al. 2005), emotion recognition (Enticottet al. 2008), intention-reading (Iacoboni et al. 2005),language acquisition (Theoret & Pascual-Leone 2002),language evolution (Arbib 2005), manual communication(Rizzolatti et al. 1996), sign language processing (Corina& Knapp 2006), speech perception (Glenberg et al.2008), speech production (Kuhn & Brass 2008), music pro-cessing (Gridley & Hoff 2006), sexual orientation (Ponsetiet al. 2006), and aesthetic experience (Cinzia & Gallese2009). In addition, it has been suggested that MN dysfunc-tion contributes to a number of disorders, including autism(Dapretto et al. 2006; Nishitani et al. 2004; J. H. Williamset al. 2001), schizophrenia (Arbib & Mundhenk 2005),Downs syndrome (Virji-Babul et al. 2008), multiple scler-osis (Rocca et al. 2008), cigarette addiction (Pineda &Oberman 2006), and obesity (Cohen 2008).Thus, much of the rst 20 years of MN research has been

devoted to theorizing and speculation about their func-tions. In contrast, the primary focus of this article is theorigin of MNs. Our principal questions are not What doMNs do? or What are they for?, but What is theprocess that gives MNs their mirrorness; their fascinating,cardinal capacity to match observed with executedactions?The standard view of MNs, which we will call the

genetic account, alloys a claim about the origin of MNswith a claim about their function. It suggests that the mir-rorness of MNs is due primarily to heritable genetic factors,and that the genetic predisposition to developMNs evolvedbecause MNs facilitate action understanding. In the senseof an adaptation developed by G. C. Williams, and usedin Evolutionary Psychology, the genetic account castsMNs as an adaptation for action understanding. In contrast,we argue in this article that the balance of evidence cur-rently favors an associative account of MNs, which separ-ates questions about their origin and function. It suggeststhat MNs acquire their capacity to match observed withexecuted actions through domain-general processes of sen-sorimotor associative learning, and that the role of MNs inaction understanding, or any other social cognitive func-tion, is an open empirical question. The associativeaccount is functionally permissive; it allows, but does notassume, that MNs make a positive contribution to socialcognition. Thus, there are three critical differencesbetween the genetic and associative accounts: (1) Theformer combines, and the latter dissociates, questionsabout origin and function. (2) The genetic account sug-gests that natural selection has acted directly on MNs,

RICHARD COOK completed his Ph.D. in the Cognitive,Perceptual and Brain Sciences Department at Univer-sity College London in 2012, and took up a lectureshipat City University London in the same year. Hisresearch, which combines the methods of social cogni-tive neuroscience and visual psychophysics, examinesthe mechanisms of imitation and the perceptual pro-cesses recruited by faces, bodies, and actions. Hiswork has been published in the Journal of ExperimentalPsychology, the Journal of Vision, Proceedings of theRoyal Society, and Psychological Science.

GEOFF BIRD is a Senior Lecturer at the MRC (MedicalResearch Council) Social, Genetic, and DevelopmentalPsychiatry Centre at the Institute of Psychiatry, KingsCollege London. After being taught how to thinkby Cecilia Heyes during his Ph.D. studies at UniversityCollege London, Geoff now studies typical and atypicalsocial cognition in collaboration with (among others) hisexcellent co-authors on this target article.

CAROLINE CATMUR is an ESRC (Economic and SocialResearch Council) Future Research Leader and SeniorLecturer in Cognitive Psychology at the University ofSurrey. She received her B.A. in 2002 from the Univer-sity of Oxford and her Ph.D. in 2009 from UniversityCollege London. Her research investigates the cognitiveand neural mechanisms underlying social cognition. Hercurrent work, which combines behavioural studies withneuroimaging and transcranial magnetic stimulation,focuses on the development and control of social cogni-tive processes, including imitation, perspective-taking,and empathy.

CLARE PRESS is a Lecturer in Psychological Sciences atBirkbeck, University of London, UK. She received herB.Sc. and Ph.D. from University College London, andsubsequently worked as an ESRC/MRC PostdoctoralResearch Fellow at the Wellcome Trust Centre forNeuroimaging. Her research uses behavioural and neu-roimaging techniques, with a focus on electrophysiologi-cal methods, to examine the mechanisms underlyingperception-action mapping for social processes such asimitation and action perception, as well as action selec-tion and control functions.

CECILIA HEYES is a Senior Research Fellow in Theor-etical Life Sciences and full Professor of Psychology atAll Souls College, University of Oxford, and a Fellowof the British Academy. Her work concerns the evol-ution of cognition. It explores the ways in whichnatural selection, learning, and developmental and cul-tural processes combine to produce the mature cogni-tive abilities found in adult humans. Her experimentaland theoretical research, initially in animal cognitionand later in human cognitive neuroscience, hasfocused on imitation, social learning, self-recognition,and theory of mind. She is currently asking to whatextent these processes of cultural learning are, like lit-eracy, culturally inherited.

Cook et al.: Mirror neurons: From origin to function

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whereas the associative account suggests that natural selec-tion has played a background role; for example, acting ondomain-general mechanisms of associative learning. (3)The genetic account assigns a relatively minor, facilitativerole to sensory and/or motor experience in the develop-ment of MNs, whereas the associative account suggeststhat sensorimotor experience plays a major, instructiverole in their development.We begin, in section 2, with some basic information

about the ways in which MNs have been dened and inves-tigated in both monkeys and humans.1 In the third sectionwe present the genetic and associative accounts, and intro-duce four kinds of evidence that have the potential to favorone of these hypotheses over the other. Sections 47discuss each of these types of evidence in turn. In section8 we survey recent theories that are, or appear to be,alternatives to the genetic and associative accounts, andsuggest that the associative account is stronger. Finally, insection 9 we argue that the associative account has majormethodological implications for research investigating thefunctions of MNs. Unlike the genetic account, the associat-ive account doesnt claim to tell us what MNs do or whatthey are for, but it does tell us how we can nd out.

2. Mirror neuron basics

2.1. Locations and denitions

MNs have been found in the monkey brain (Macaca nemis-trina and Macaca mulatta), not only in classical areas ventral PMC and IPL but also in non-classical areas,including primary motor cortex (Dushanova & Donoghue2010; Tkach et al. 2007) and dorsal PMC (Tkach et al.2007). There is also evidence of single neurons, orcircumscribed populations of neurons, with sensorimotormatching properties in classical areas of the humanbrain, including posterior regions of the inferior frontalgyrus (IFG; considered the human homologue of themonkey F5) (Kilner et al. 2009) and inferior parietalcortex (Chong et al. 2008), and non-classical areas of thehuman brain, including dorsal PMC, superior parietallobule, and cerebellum (Molenberghs et al. 2012), supple-mentary motor area, and medial temporal lobe (Mukamelet al. 2010).Some researchers apply the term mirror neuron only to

neurons found in classical areas (Brown & Brune 2012;Molenberghs et al. 2012), whereas others, like us, use theterm to refer to neurons in both classical and non-classicalareas (Gallese & Sinigaglia 2011; Keysers & Gazzola 2010).In addition to this variation in anatomical specicity, someresearchers reserve the term mirror neuron for units thatdischarge during the observation and execution of precisely(Dinstein et al. 2008b; Keysers 2009) or broadly similaractions (Kilner et al. 2009), whereas others use the term,at least on occasions, to refer to any neuron that is respon-sive to both the observation and execution of action,regardless of whether the observed and executed actionsare even broadly similar to one another (Gallese et al.1996; Rizzolatti & Craighero 2004). In accord with themajority of researchers in the eld, and the meaning ofthe word mirror, we take it to be a cardinal feature ofMNs that they are responsive to observation and executionof similar actions. However, following common usage, wealso refer to logically related MNs (see sect. 2.2), which

re during observation and execution of dissimilaractions, as mirror neurons.

2.2. Monkeys

Early studies of the eld properties of monkey MNs thesensory and motoric conditions in which they re revealed three basic types: Strictly congruent MNs dis-charge during observation and execution of the sameaction, for example, precision grip. Broadly congruentMNs are typically active during the execution of oneaction (e.g., precision grip) and during the observation ofone or more similar, but not identical, actions (e.g.,power grip alone, or precision grip, power grip, and grasp-ing with the mouth). Logically related MNs respond todifferent actions in observe and execute conditions. Forexample, they re during the observation of an exper-imenter placing food in front of the monkey, and whenthe monkey grasps the food in order to eat it. MNs donot respond to the presentation of objects alone (di Pelle-grino et al. 1992). However, canonical neurons, whichare active during object observation and performance ofan action that is commonly performed on that object,are co-located with MNs both in area F5 (Murata et al.1997) and in the anterior intraparietal sulcus (Murataet al. 2000).To date, monkey MNs have been found that are respon-

sive to the observation and execution of hand and mouthactions. The hand actions include grasping, placing, manip-ulating with the ngers, and holding (di Pellegrino et al.1992; Gallese et al. 1996). The mouth actions include inges-tive behaviors such as breaking food items, chewing andsucking, and communicative gestures such as lip-smacking,lip-protrusion, and tongue-protrusion (Ferrari et al. 2003).

2.3. Humans

Only one study purports to offer direct evidence fromsingle cell recording of MNs in the human brain(Mukamel et al. 2010). However, there is a considerablebody of indirect evidence from neuroimaging, transcra-nial magnetic stimulation (TMS), and behavioral studies suggesting that human brains contain MNs or comparablemirror mechanisms; circumscribed cortical areasinvolved in both action production and observation (Glen-berg 2011).

2.3.1. Neuroimaging. Functional magnetic resonanceimaging (fMRI) has identied regions of PMC (bothclassic BA6 and BA44) and inferior parietal areas that areactive during both action observation and execution(Aziz-Zadeh et al. 2006a; Buccino et al. 2004; Carr et al.2003; Grzes et al. 2003; Iacoboni et al. 1999; Leslieet al. 2004; Tanaka & Inui 2002; Vogt et al. 2007). Overlap-ping responses to action observation and execution havebeen found in single-subject analyses of unsmoothed data(Gazzola & Keysers 2009), conrming that the foregoingreports are not artifacts of group averaging. Most recently,repetition suppression protocols have been used to provideevidence of mirror populations encoding visual and motorrepresentations of the same action. These paradigmsexploit the logic that repeated stimulus presentation oraction execution causes a decrease in neural responses(Grill-Spector et al. 2006). Cross-modal repetition


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suppression effects have been reported, whereby actionobservation followed by execution of the same action, orvice versa, elicits repetition suppression in inferior parietalregions (Chong et al. 2008; Lingnau et al. 2009) and inPMC (Kilner et al. 2009; Lingnau et al. 2009).

2.3.2. Mirror pattern of MEPs. A human mirror mechanismis further suggested by mirror motor evoked potentials(MEPs) elicited during action observation (Fadiga et al.1995). When TMS is applied to M1 during passiveaction observation, the amplitude of the MEPs recordedfrom the muscles required to execute that action isgreater than the amplitude of the MEPs recorded whenobserving a different action. For example, observingindex and little nger abduction movements selectivelyfacilitates the amplitude of MEPs recorded from the rstdorsal interosseus and abductor digiti minimi muscles,responsible for index and little nger movements, res-pectively (Catmur et al. 2011). That action observationselectively increases corticospinal excitability to actionrelevant muscles is suggestive of mirror sensorimotorconnectivity.

2.3.3. Automatic imitation. Automatic imitation is said tooccur when observation of an action involuntarily facilitatesperformance of a topographically similar action (body partsmake the same movements relative, not to external framesof reference, but to one another) and/or interferes withperformance of a topographically dissimilar action (Brasset al. 2001; Strmer et al. 2000). Humans show robust auto-matic imitation when they observe hand, arm, foot, andmouth movements (Heyes 2011). This is regarded bymany researchers as evidence of a human mirror mechan-ism (Blakemore & Frith 2005; Ferrari et al. 2009a; Iaco-boni 2009; Kilner et al. 2003; Longo et al. 2008; vanSchie et al. 2008). Supporting this view, several studieshave shown that application of disruptive TMS to theIFG a classical mirror area interferes with automaticimitation (Catmur et al. 2009; Newman-Norlund et al.2010).

3. The mirrorness of mirror neurons: Genetic orassociative?

This section presents the standard, genetic account of theorigin of MNs and the alternative associative account.

3.1. Genes for mirroring?

The genetic account assumes: (1) Among common ances-tors of extant monkeys and humans, some individuals hada stronger genetic predisposition to develop MNs, and(2) these individuals were more reproductively successfulthan those with a weaker genetic predisposition becausethe development of MNs enhanced their capacity to under-stand the actions of other agents. Consequently, (3) agenetic predisposition to develop MNs became universal,or nearly universal, in monkeys and humans. (4) Motorexperience (the performance of actions) and/or sensoryexperience (the observation of actions) plays a facilitative(Gottlieb 1976) or permissive (Gilbert 2003) role in thedevelopment of MNs, but their matching properties areprimarily due to this genetic predisposition.

The term action understanding was introduced by Riz-zolatti and colleagues to characterize the function of MNs(Rizzolatti & Fadiga 1998; Rizzolatti et al. 1996). As far aswe are aware, it had not previously been used in researchon animal or human cognition. The term plays a key rolein the genetic account; it describes the adaptive functionof MNs, the effects that made them a target of positiveselection pressure. However, there is still no consensusabout exactly what is meant by action understanding, orhow it differs from cognate functions such as action per-ception, action recognition, and action selection(Gallese et al. 2011). Attempts to clarify have emphasizedthat, in comparison with purely visual processing ofaction, MN activity relates to the meaning of an actionand yields a richer understanding, real understanding,or understanding from within (Gallese et al. 2011; Rizzo-latti & Sinigaglia 2010). As we discuss further in section 8,these descriptions do not provide an operational denitionof action understanding, that is, a denition that wouldallow behavior based on (this kind of) action understandingto be distinguished empirically from behavior based onother processes.Until recently, the genetic account was largely implicit in

discussions of the evolution of MNs (Gallese & Goldman1998; Rizzolatti & Arbib 1998; Rizzolatti & Craighero 2004;M. J. Rochat et al. 2010). For example, it has beensuggested that the mirror neuron mechanism is a mechan-ism of great evolutionary importance through which pri-mates understand actions done by their conspecics(Rizzolatti & Craighero 2004, p. 172) and that in theirbasic properties, MNs constitute a relatively simpleaction-perception mechanism that could have beenexploited several times in the course of animal evolution(Bonini & Ferrari 2011, p. 172). A number of discussionshave also expressed the view that MNs are present atbirth (Ferrari et al. 2009; Gallese et al. 2009; Lepage &Theoret 2007; Rizzolatti & Fadiga 1998), a feature com-monly associated with traits for which there is stronggenetic predisposition (Mameli & Bateson 2006). Forexample, Casile and colleagues have suggested that bothface processing and the mirror neuron system, or at leastthe part involved in facial movements, rely on a brainnetwork that is present already at birth and whose elementsare probably genetically predetermined (Casile et al. 2011,p. 531).In its starkest form, the genetic hypothesis would suggest

that gene-based natural selection has provided each indi-vidual monkey and human with MNs that code themapping between a xed set of observed and executedactions, and that experience plays a minimal role in thedevelopment of the observation-execution matching prop-erties of these neurons. However, the genetic hypothesisdoes not necessarily assume that experience plays aminimal role. For example, in a recent explicit statementof the genetic account, Gallese et al. (2009) suggestedthat links form during gestation between motor regionsand to-become-visual regions that will subsequentlymediate sensorimotor matching abilities in young infants.They implied that these projections are genetically predis-posed to target certain visual areas, and therefore that thematching properties of MNs are produced by informationencoded in the genome. However, they also suggestedthat motor experience plays a part in preparing motorregions to send projections to visual areas, and that visual



experience may also facilitate the maturation of fully func-tioning MNs.

3.2. A product of associative learning

The associative hypothesis assumes that gene-based naturalselection has played a signicant background role withrespect to the development of MNs; for example, inshaping the anatomy of visual and motor cortex for visualguidance of action, and in producing the capacity for associ-ative learning in neural tissue. However, it suggests that thecardinal matching properties of MNs are a product, not of aspecic genetic predisposition, but of domain-general pro-cesses of associative learning the same kind of learningthat produces Pavlovian and instrumental conditioningphenomena (Catmur et al. 2009; Heyes 2010; Ray &Heyes 2011). Associative learning is found in a widerange of vertebrate and invertebrate species, indicatingthat it is an evolutionarily ancient and highly conservedadaptation for tracking predictive relationships betweenevents (Heyes 2012b; Schultz & Dickinson 2000).Figure 1 is a schematic representation of howMNs could

acquire their matching properties through sensorimotorassociative learning. Before associative learning, sensoryneurons in the superior temporal sulcus (STS), responsiveto different high-level visual properties of observed action(Oram & Perrett 1994; 1996), are weakly connected,directly or indirectly, to motor neurons in PMC (Rizzolattiet al. 1988) and parietal cortex (Gallese et al. 2002). Someof these connections may be stronger than others, but thelinks between sensory and motor neurons coding similar

actions are not consistently stronger than other, non-matching links. The kind of learning that produces MNsoccurs when there is correlated (i.e., contiguous and con-tingent) excitation of sensory neurons and motor neuronsthat code similar actions. For example, when an adult imi-tates an infants facial movements, there might be corre-lated excitation of neurons that are responsive to theobservation and execution of lip protrusion. Correlatedexcitation of the sensory and motor neurons increases thestrength of the connection between them, so that sub-sequent excitation of the sensory neuron propagates tothe motor neuron. Thereafter, the motor neuron res,not only during execution of lip protrusion, but also, viaits connection with the sensory neuron, during observationof lip protrusion; what was originally a motor neuron hasbecome a lip protrusion MN. Correlated excitation ofsensory and motor neurons encoding the same propertyof action occurs not only when humans are imitated, butalso when we observe our own actions (directly or usingan optical mirror); observe others during the kind of syn-chronous activities involved in sports and dance training;and as a consequence of acquired equivalence experi-ence, for example, when the same sound (a word, or asound produced by an action) is paired sometimes withobservation of an action and sometimes with its execution(Catmur et al. 2009; Ray & Heyes 2011).There are several important things to note about the

associative hypothesis:

1. Strong experience-dependence It suggests thatcorrelated sensorimotor experience plays an inductive

Figure 1. Mirror neurons from associative learning. (a) Before learning, sensory neurons in STS, encoding visual descriptions ofobserved action, are not systematically connected to motor neurons in premotor and parietal areas involved in the production ofsimilar actions. (b) Through social interaction and self-observation in the course of typical development, agents receive correlatedsensorimotor experience; they see and do the same action at about the same time (contiguity), with one event predicting the other(contingency). This experience produces correlated activation of sensory and motor neurons coding similar actions, and, throughassociative learning, (c) strengthens connections between these neurons. Due to these connections, neurons that were once involvedonly in the execution of action will also discharge during observation of a similar action; motor neurons become MNs (see sect. 3.2).Because the visual system and motor system are organised hierarchically, some types of sensorimotor experience produce correlatedactivation of sensory and motor neurons coding relatively low-level features of action (e.g., left or right hand, power or precisiongrip), and thereby generate strictly congruent, hand- and direction-sensitive MNs. Other types produce correlated activation ofneurons coding relatively high-level features (e.g., grasping) and generate broadly congruent MNs (see sect. 5.1).



(Gottlieb 1976) or instructive (Gilbert 2003) role; withoutthis kind of experience, MNs would not develop at all.2. Social construction It proposes that much of the

sensorimotor experience required for MN developmentcomes from being imitated, synchronous action, andexposure to action words (Ray & Heyes 2011), and there-fore that MNs are to a very large extent built throughsocial interaction.3. Contingency Following contemporary learning

theory, the associative account species that MN develop-ment requires, not just that sensory and motor neuronsre together in a Hebbian way (contiguity), but that theevent provoking ring of one predicts the event provokingring of the other (contingency; Cook et al. 2010).4. Testability The associative account makes novel

predictions about the development and mature propertiesof MNs, many of which have already been tested andsupported by experiments using a variety of methods (seesect. 7).Thus, the associative hypothesis implies that the cha-

racteristic, matching properties of MNs result from agenetically evolved process, associative learning, but thisprocess was not designed by genetic evolution toproduce MNs. Rather, it just happens to produce MNswhen the developing system receives correlated experienceof observing and executing similar actions. When thesystem receives correlated experience of observingobjects and executing actions, the same associativeprocess produces canonical neurons. When the systemreceives correlated experience of observing one actionand executing a different action, the same associativeprocess produces logically related MNs.

3.3. Not nature versus nurture

The contrast between the genetic and associative hypoth-eses does not represent a dichotomous naturenurturedebate. It has been recognized for decades that the devel-opment of all phenotypic characteristics depends on theinteraction of nature and nurture, genes and the environ-ment, evolution and learning (Elman et al. 1996; Oyama1985). Rather, the two accounts differ in the specicroles they assign to genetic evolution and to learning, andin the types of experience they take to be important, in pro-ducing the characteristic matching properties of MNs. Thegenetic hypothesis says that genetic evolution has played aspecic and decisive role, and learning based on sensoryand/or motor experience plays a merely facilitative role,in the development of MNs. In contrast, the associativehypothesis says that genetic evolution has played a non-specic background role, and that the characteristic match-ing properties of MNs are forged by sensorimotor learning.Regarding the function of MNs, the genetic account

assumes that they play a fundamental role in action under-standing, and that this is why a specic genetic predisposi-tion to develop MNs was favored by natural selection. Inother words, it proposes that action understanding is theadaptive function of MNs, or that MNs are an adap-tation for action understanding. In this way, the geneticaccount offers a hypothesis about the function of MNs asan explanation for their origins. In contrast, the associativeaccount separates questions about the origin and functionof MNs. It suggests that MNs develop through associativelearning, and that further research is needed to nd out

how they contribute to social cognition (see sect. 9). Ifthis research reveals that MNs make positive contributionsto social cognition, these would be psychological uses orpsychological functions, but not necessarily adaptivefunctions; they may not have enhanced reproductivetness, nor resulted in the evolution of mechanisms speci-cally designed to foster the development of MNs (see sect.8). Rather, it is possible that MNs are constructed bydomain-general processes of associative learning, and arerecruited in the course of development to contributeto one or more psychological functions, without eitherthe construction or the recruitment processes havingbecome a specic target of gene-based selection (Elmanet al. 1996).In this respect, MNs may be like beak morphology in

Neotropical woodcreepers, which has been selected forforaging and food manipulation (a non-social function, ana-logous to visuomotor capability) but also has effects on songproduction (a social function, analogous to action under-standing; Derryberry et al. 2012). Another more closelyrelated example comes from honeybees, which are ableto use associative learning to discriminate among humanfaces (Dyer et al. 2005). Given the taxonomic- anddomain-generality of associative learning, and the factthat human faces were not part of the environment inwhich honeybee nervous systems evolved, we can be surethat associative learning is not an adaptation for face dis-crimination in honeybees. However, when they are put inan environment where faces are important, honeybeescan use associative learning about faces to optimize theirforaging behavior. Another example, which may beclosely related in a different way, is the area of thehuman occipito-temporal cortex known as the visualword form area (VWFA; Petersen et al. 1990). This areaplays an important role in reading, but, given the recentemergence of literacy in human history, the VWFA isvery unlikely to be a genetic adaptation for reading.Rather, the reading-related properties of the VWFA areforged in the course of development, by literacy training,from a system adapted for generic object recognition.

3.4. Four kinds of evidence

Four evidence-based arguments are crucial in decidingbetween the genetic and associative accounts. The rst pro-vided the inspiration and foundation for the genetichypothesis. It suggests that the eld properties of MNsindicate that they were designed for action understanding.The terms design and purpose are used here as theywere by G. C. Williams in his seminal work on Adaptationand Natural Selection (Williams 1966). Williams describedadaptations as designed by natural selection to fulll a par-ticular purpose, and emphasized that the mark of an adap-tation is that it has features making it peculiarly apt toachieve a specic end in a highly efcient way. Forexample, An examination of the legs and feet of the foxforces the conclusion that they are designed for runningand walking, not for the packing or removal of snow (p.13). In a similar way, supporters of the genetic hypothesisargue that examination of the eld properties of MNs and, in particular, their goal coding forces the con-clusion that MNs are designed for action understanding.In section 3 we examine the eld properties of MNs andsuggest that this argument is not compelling.



The second argument is complementary to the rst; ithas a similar form but advocates the associative hypothesis.It suggests that research using conditioning proceduresshows associative learning to be the right kind of learningto produce MNs. Specically, as we discuss in section 5,the ways in which associative learning tracks contingentrelationships, and enables contextual modulation of theseconnections, makes it apt to produceMNs (and non-match-ing visuomotor neurons) in typical developmentalenvironments.The second pair of arguments draws on research examin-

ing the development of MNs and their modicationthrough sensorimotor experience. Section 6 discussesresearch with infants and adults that has been used tosupport a poverty of the stimulus argument (Chomsky1975); to suggest that MNs emerge too early in develop-ment or, more generally, after too little sensorimotorexperience, to have been forged by associative learning.In contrast, we offer a wealth of the stimulus argument.Finally, section 7 focuses on evidence that, even in adult-

hood, the properties of MNs can be changed in radical waysby relatively brief periods of sensorimotor experience. Weargue, against various objections, that this evidence issound and therefore supports the associative hypothesisby showing that it has produced novel, testable predictionswhich have been conrmed by experiment.

4. Designed for action understanding

Supporters of the genetic hypothesis argue that examin-ation of the eld properties of MNs shows that theyencode goals, and this characteristic indicates that theywere designed by genetic evolution to mediate actionunderstanding (Bonini & Ferrari 2011; Rizzolatti & Craigh-ero 2004; Rizzolatti & Sinigaglia 2010). We therefore beginour survey of the evidence by considering how well theneurophysiological data accord with this view. The termgoal affords numerous interpretations (Hickok 2009).We will consider two denitions commonly adopted,assuming that MNs encode goals if they encode object-directed actions (sect. 4.1) or high-level action intentions(sect. 4.2).

4.1. Goals as object-directed actions

Early descriptions of MN eld properties reported thatpantomimed actions (e.g., miming a precision grip in theabsence of an object) and intransitive actions (e.g.,tongue-protrusion) did not elicit MN responses (di Pelle-grino et al. 1992; Gallese et al. 1996). In contrast, robustresponses were reported when monkeys observed object-directed actions. This pattern raised the possibility thatMNs encode goals in the sense that they are responsiveonly to object-directed actions (di Pellegrino et al. 1992;Gallese et al. 1996).However, a close reading of the single-cell data suggests

that only a small subset of MNs appeared to have beendesigned for encoding action goals in these terms. Asubset of the MNs described in the early reports continuedto respond, albeit less strongly, to pantomimed or intransi-tive actions (di Pellegrino et al. 1992; Gallese et al. 1996,Figure 5b), and subsequent studies conrmed that sizableproportions, perhaps the majority, of MNs exhibit robust

responses to the observation of object-free body move-ment. Kraskov et al. (2009) reported that 73% of MNresponses modulated by observation of object-directedgrasping showed similar modulation during observation ofpantomimed grasping. Also, substantial proportions ofMNs respond to intransitive mouth movements such aslip-smacking, lip-protrusion, and tongue-protrusion(Ferrari et al. 2003).Single-unit data also show that, even when they are

responding to object-directed actions, MNs have eldproperties suggesting that they were not tuned to do thisby genetic evolution. For example, after training in whichtools were used to pass food items to monkeys, MNswere discovered that respond to the observation ofactions such as grasping with pliers (Ferrari et al. 2005).Similarly, audiovisual MNs respond to unnatural soundsassociated with actions; for example, the sound of metalstriking metal, plastic crumpling, and paper tearing(Keysers et al. 2003; Kohler et al. 2002). Importantly,large numbers of tool-use and audiovisual MNs respondmore to the sight of tool-actions and to action soundsthan to the sight of gripping or tearing executed with thehands. The fact that these MNs respond maximally to unna-tural stimuli that is, stimuli to which the evolutionaryancestors of contemporary monkeys could not possiblyhave been exposed is hard to reconcile with the genetichypothesis (Cook 2012; see sect. 7).

4.2. Goals as high-level intentions

The term goal has also been used to refer to what, at ahigh level of generality, the actor intends to achievethrough their behavior for example, grasp in order toeat (Fogassi et al. 2005) or taking possession of anobject (M. J. Rochat et al. 2010). Rizzolatti and Sinigaglia(2010, p. 269) state: only those [neurons] that can encodethe goal of the motor behavior of another individual withthe greatest degree of generality can be considered to becrucial for action understanding. The suggestion thatMNs encode high-level action intentions is made plausibleby reports that MN responses to grasping can be modu-lated by the nal outcome of the motor sequence (Boniniet al. 2010; Fogassi et al. 2005). It is also consistent withreports that some broadly congruent MNs respond to theobservation of multiple actions; for example, any graspingaction executed with the hand or mouth (Gallese et al.1996).However, the single-cell data again suggest that relatively

few MNs have the eld properties one would expect of asystem designed by genetic evolution to represent high-level action intentions. For example, Gallese et al. (1996)reported that during action observation 37.5% of MNsresponded differently depending on whether the actionwas executed with the left or right hand, and 64%showed direction sensitivity, preferring either left-to-rightor right-to-left grasping actions. Similarly, many MNs(53%) respond selectively to the observation of actions exe-cuted within (peripersonalMNs) or beyond (extraperso-nal MNs), not the actors, but the observing monkeysreach (Caggiano et al. 2009). The majority (74%) of MNsalso exhibit view-dependent responses; some MNs aretuned to egocentric (rst-person) presentation, whileothers respond maximally to allocentric (third-person) per-spectives (Caggiano et al. 2011). Each of these classes of



MN is sensitive to features of action that fall well belowthe greatest degree of generality of intentions such asgrasping in order to eat or taking possession of anobject.The eld properties of logically related MNs are perhaps

the hardest to reconcile with the idea that MNs weredesigned by genetic evolution to mediate action under-standing by activating in the observer the same goalthat is guiding the actors behavior. Logically relatedMNs re when a monkey observes an action with onegoal (e.g., placing food items on a table, with the intentionof giving food to the monkey) and when the monkey exe-cutes an action with a different goal (e.g., grasping thefood with a precision-grip and bringing it to the mouth,with the intention of eating). Thus, these MNs respondto different object-directed actions, with different inten-tions, in observe and execute conditions.

5. The right kind of learning

The previous section argued that many MNs have eldproperties incompatible with the hypothesis that theywere designed by genetic evolution to mediate actionunderstanding via goal coding. In complementary fashion,this section argues that research on the roles of contingencyand contextual modulation in associative learning enablesthe associative hypothesis to provide a unied account ofall the MN eld properties reported to date.

5.1. Predictive relationships

It has long been recognized that associative learningdepends, not only on contiguity events occurring closetogether in time but also on contingency the degree towhich one event reliably predicts the other. Where the pre-dictive relationship between two events is weak that is,where one event is equally likely to occur in the presenceand absence of the other event contiguous pairingsproduce little or no learning (Elsner & Hommel 2004;Rescorla 1968; Schultz & Dickinson 2000). The associativeaccount therefore predicts that MNs will acquire sensori-motor matching properties only when an individual experi-ences contingencies between sensory events andperformed actions (Cooper et al. 2013b). This feature ofassociative learning ensures that the matching propertiesof MNs reect, not just chance co-occurrences, but sensor-imotor relationships that occur reliably in the individualsenvironment. Evidence that the human mirror mechanismis modied by contingent but not by non-contingent sen-sorimotor experience has been reported by Cook et al.(2010).Contingency sensitivity explains the mix of strictly con-

gruent MNs, sensitive to the low-level features of observedactions (type of grip, effector used, direction of movement,viewpoint, proximity to the observer), and broadly congru-ent MNs, responsive to multiple related actions irrespec-tive of the manner of their execution. Both visual andmotor systems are known to be organized hierarchically(Felleman & Van Essen 1991; Giese & Poggio 2003; Jean-nerod 1994; Perrett et al. 1989), comprising different popu-lations encoding relatively low-level representations (e.g.,descriptions of particular precision or power grips)and more abstract representations (e.g., descriptions of

grasping). Therefore, contingencies can be experiencedbetween both low- and high-level sensory and motor rep-resentations. When a monkey observes itself performinga precision grip, the excitation of sensory and motor popu-lations encoding a specic grip are correlated. However,during group feeding, a monkey might observe andperform a range of grasping actions, thereby causing corre-lated excitation of higher-level visual and motoric descrip-tions of grasping. Contingency sensitivity thereforeexplains the existence of both strictly congruent MNs,tuned to a particular sensory representation (e.g., a right-to-left precision grip executed with the right hand viewedegocentrically), and broadly congruent MNs, responsiveto the observation of a number of related actions.Contingency sensitivity also explains the existence of

logically related, audiovisual, and tool-use MNs. Accordingto the associative hypothesis, MNs acquire sensorimotorproperties whenever individuals experience a contingencybetween seeing and doing. There is no requirementthat contingencies are between action performance andthe observation of the same action, or indeed of naturalaction-related stimuli, such as the sight of animate motionor sounds that could have been heard by ancestors of con-temporary monkeys. Both monkeys and humans frequentlyexperience non-matching sensorimotor contingencies,where the observation of one action predicts the executionof another; for example, you release and I grasp (Newman-Norlund et al. 2007; Tiedens & Fragale 2003). The associ-ative account therefore explains in a very straightforwardway why logically related MNs respond to differentactions in observe and execute conditions. Equally, theassociative account explains in a simple way why tool-use MNs (Ferrari et al. 2005) develop when action per-formance is reliably predicted by the sight of actionsperformed with tools (e.g., food items being gripped withpliers), and why audiovisual MNs (Keysers et al. 2003;Kohler et al. 2002) develop when action performance pre-dicts characteristic action sounds (e.g., paper tearing orplastic crumpling; Cook 2012).

5.2. Contextual modulation

Studies of conditioning indicate that learned responses areoften subject to contextual control; if a stimulus is associ-ated with two responses, each in a different context, thenthe context determines which response is cued by thestimulus (Bouton 1993; 1994; Peck & Bouton 1990). Forexample, Peck and Bouton (1990) initially placed rats in aconditioning chamber with a distinctive scent (e.g.,coconut) where they learned to expect electric shock fol-lowing a tone. The rats were then transferred to a secondchamber with a different scent (e.g., aniseed) where thesame tone predicted the delivery of food. The ratsquickly learned the new contingency and conditioned fora-ging responses replaced conditioned freezing. However,learning in the second phase was context dependent.When the rats were returned to the rst chamber, or trans-ferred to a third chamber with a novel scent, the tone onceagain elicited freezing. By drawing on the components ofassociative learning theory that explain this kind of effect,the associative account of MNs can explain contextualmodulation of MN ring (Cook et al. 2012a).Many, possibly all, of the ndings cited as evidence that

monkey MNs code action goals can also be interpreted



within an associative framework as evidence that MNs aresubject to contextual control. For example, some MNsshow stronger visual responses to object-directed graspingthan to pantomimed grasping in object-absent contexts(Gallese et al. 1996), and in some cases, the modulatinginuence of the object-context can be seen even whenthe target object is occluded prior to contact with thehand (Umilt et al. 2001). Similarly, MN responsesduring the observation of grasping may be modulated bythe type of object being grasped (Caggiano et al. 2012),with some MNs responding more strongly in the presenceof high-value (food, or non-food objects predictive ofreward), and some in the presence of low-value (non-food objects not associated with reward) stimuli. In theclearest example, the same motor act, grasping with a pre-cision grip, elicits different MN responses dependent onwhether the action is observed in the presence (grasp toplace) or absence (grasp to eat) of a plastic cup(Bonini et al. 2010; Fogassi et al. 2005). Rather than theplastic cup providing a cue to the actors intention, it mayact as a contextual cue modulating the operation of twoassociations. In the same way that the sound of the tone eli-cited different behaviors when presented in the coconutand aniseed contexts (Peck & Bouton 1990), observing aprecision grip may excite different MNs in the cup-present and cup-absent contexts.Thus, many of the eld properties cited as evidence of

goal (intention) coding by MNs can also be explained bycontextual modulation within an associative framework.Under the goal interpretation, these eld properties con-stitute direct evidence that MNs mediate action under-standing. Under the associative interpretation, they arevery interesting but not decisive. The exibility apparentin the eld properties of MNs gives them the potential tomake a useful contribution to social behavior. However,further research, examining the behavior of whole organ-isms, not only of neurons, is needed to nd out how thispotential is realized (see sect. 9).

6. Wealth and poverty of the stimulus

Research involving infants (sect. 6.1) and adults (sect. 6.2)has been used to support a poverty argument suggestingthat MNs emerge too early in development or, more gen-erally, after too little sensorimotor experience, to havebeen forged by associative learning.

6.1. Mirroring in infancy

It has been argued that: (1) imitation is mediated by MNs(or a mirror mechanism); (2) both human and monkeyinfants are able to imitate observed actions when theyhave had minimal opportunity for visuomotor learning;and (3) therefore, the associative account of the origin ofMNs must be wrong (Gallese et al. 2011). The structureof this argument is valid, but the evidence supporting thesecond assumption (e.g., Heimann et al. 1989; Meltzoff& Moore 1977; Nagy et al. 2005) has been challenged intwo respects. Building on previous analyses (e.g., Anisfeld1996), a recent review found evidence that human neo-nates copy only one action tongue-protrusion and thatthis copying does not show the specicity characteristic ofimitation or of MNs (Ray & Heyes 2011). Figure 2

illustrates the rst of these points. For each of the actiontypes tested in young infants, it shows the number of pub-lished studies reporting positive evidence of imitation andthe number reporting negative evidence. This is a highlyconservative measure of how often young infants havefailed imitation tests, because it is much harder to publishnegative than positive results (Fanelli 2012). Nonetheless,Figure 2 shows that the number of positive reports subs-tantially exceeds the number of negative reports onlyfor tongue-protrusion. Evidence that even the tongue-protrusion effect lacks the specicity characteristic of imita-tion and MNs that it is an exploratory response, ratherthan an effect in which action observation is met with per-formance only of a similar action comes from researchshowing that tongue-protrusion can be elicited by a rangeof arousing stimuli, including ashing lights and livelymusic (Jones 1996; 2006), and that it is greater wheninfants observe a mechanical tongue or disembodiedmouth (Soussignan et al. 2011).2 More broadly, evidencethat the development of imitation is crucially dependenton learning is provided by a study of 2-year-old twinsshowing that individual differences in imitation were aresult predominantly of environmental rather than geneticfactors (McEwen et al. 2007), and by a recent study ofinfants indicating that individual differences in associativelearning ability at 1-month predicted imitative performanceeight months later (Reeb-Sutherland et al. 2012).Turning from human to monkey infants, Ferrari et al.

(2006) reported immediate imitation of tongue-protrusionand lip-smacking in 3-days-old monkeys. However, theeffects were not present on days 1, 7, and 14 postpartum,and it is not clear whether they were replicated in a sub-sequent study using a similar procedure (Paukner et al.2011). The later study did report imitation of lip-smackingin monkeys less than one week old, but this effect seems tohave been due to a low frequency of lip-smacking in thecontrol condition, when infants were observing a staticneutral face, rather than to an elevated frequency of lip-smacking when the infants were observing lip-smacking.Therefore, in common with the data from human infants,studies of imitation in newborn monkeys do not currentlysupport a poverty argument.

Figure 2. Summary of experiments seeking evidence of gestureimitation in human infants (adapted from Ray & Heyes 2011).Gesture type refers to the target or modelled movement.Positive frequencies (lighter bars) indicate the number ofpublished experiments reporting positive cross-target comparisons(i.e., infants performed the target action more often afterobserving the target action than after observing an alternativeaction). Negative frequencies (darker bars) indicate the numberof experiments reporting failure to nd a signicant difference incross-target comparison.



A similar poverty argument suggests that the associativeaccount must be wrong because (1) suppression of alphaband (613 Hz) oscillations over central scalp locationsduring action observation (and execution) reects the oper-ation of MNs or a mirror mechanism, and (2) electroence-phalographic (EEG) studies indicate that both human andmonkey infants show alpha suppression when they havehad minimal opportunity for sensorimotor learning(Gallese et al. 2011; Nystrm et al. 2011). In this case,both of the assumptions are questionable. First, the func-tional signicance of alpha band oscillatory activity ispoorly understood even in human adults, and is yet moredifcult to interpret in human and monkey infants where,for example, less information is available about the source(Marshall & Meltzoff 2011). Second, human adult studieshave traced the likely source of central alpha suppressionduring action execution to the somatosensory cortex (Hari& Salmelin 1997), suggesting that it may not index motorprocessing at all.3 Third, even if alpha suppression doesindex motor processing, it does not show that the motoractivation matches or mirrors the actions observed (Mar-shall & Meltzoff 2011; Pfurtscheller et al. 2000). Forexample, alpha suppression during observation of lip-smacking, which has been reported in neonatal monkeys(Ferrari et al. 2012), may reect a generalized readinessto act, or arousal-related motor activation of tongue-protru-sion, rather than motor activation of lip-smacking, andthereby the occurrence of MN or mirror mechanismactivity. Furthermore, studies of human infants, whichprovide superior source information, have not shown thatcentral alpha suppression occurs when infants have hadinsufcient correlated sensorimotor experience to build amirror mechanism through associative learning. Indeed,studies of human infants suggest an age-related trend con-sistent with the associative hypothesis (see Marshall et al.[2011] for a review).Sound evidence of MN activity in newborns which,

we suggest, has not been provided by research to date onimitation and alpha suppression would be inconsistentwith the associative model. However, it is important tonote that the associative account is predicated on awealth of the stimulus argument and therefore antici-pates MN activity in young infants (Ray & Heyes 2011).This wealth argument points out that human developmen-tal environments typically contain multiple sources of thekind of correlated sensorimotor experience necessary tobuild MNs; each of these sources is rich; and the mechan-isms of associative learning can make swift and efcient useof these sources. The range of sources available to younghuman infants includes self-observation, being imitatedby adults, being rewarded by adults for imitation, and thekind of experience in which, for example, lip movementsmake the same smacking or popping sound when observedand executed. Evidence of the richness of these sourcescomes from studies showing that infants spend a high pro-portion of their waking hours observing their own hands inmotion (P. Rochat 1998; White et al. 1964); in face-to-faceinteraction with a caregiver, they are imitated on averageonce every minute (Jones 2009; Pawlby 1977; Uzgiriset al. 1989); and noisy actions, which provide an earlysource of acquired equivalence experience, are amongthe rst that infants imitate (Jones 2009). A common mis-conception about associative learning is that it alwaysoccurs slowly. Directly relevant evidence that this is not

the case comes from studies showing that, when the contin-gency is high, infants can learn action-effect associations injust a few trials (Paulus et al. 2012; Verschoor et al. 2010).

6.2. Motor training in adulthood

It has been claimed that the associative account cannotexplain why motor experience obtained without visual feed-back can affect perception of human biological motionrelated to that experience (Gallese et al. 2011, p. 383).This claim assumes that the perception of human biologicalmotion is mediated by MNs or a mirror mechanism, andappeals to a subtle poverty argument; it suggests that thefundamental properties of MNs the way in which theymap observed with executed actions can be changed bymotor experience alone, that is, in the absence of correlatedsensorimotor experience.Two types of evidence, from studies that were not

designed to investigate MNs, have been cited in supportof this subtle poverty argument (Gallese et al. 2011).First, when observing point-light displays of whole bodymovements such as walking, from a third party perspective,people are better able to recognize themselves than torecognize their friends (Beardsworth & Buckner 1981;Loula et al. 2005). Second, practice in executing actionscan improve visual discrimination of those actions, evenwhen actors are prevented from observing their move-ments during execution (Casile & Giese 2006; Hechtet al. 2001). These motor training effects, and the self-recognition advantage, are interesting and importantphenomena in their own right. If they were mediated bya mirror mechanism that is, a mechanism in which thereis a direct, unmediated connection between visual andmotor representations of action they would also supporta poverty argument. However, a recent study provides evi-dence that these effects depend on an indirect mechanismrepresenting temporal cues. It shows, using avatar facialmotion stimuli, that the self-recognition advantage is main-tained despite gross distortion of the kind of spatial cuesthat characterize biological motion, but is abolished byeven relatively minor disturbance of domain-general tem-poral cues (Cook et al. 2012b). In the absence of appropri-ate visual experience, actors appear to be able to use theirconsiderable knowledge of the rhythmic characteristics oftheir own actions to recognize and better represent allo-centric movement displays. Thus, motor training effectsand the self-recognition advantage are of independentinterest, but they do not support a poverty argumentbecause current evidence suggests that they do notdepend on a mirror mechanism.

7. Sensorimotor learning changes mirror neurons

7.1. Testing the predictions of the associative account

The associative account has been explicitly tested in exper-iments examining the effects of laboratory-based sensori-motor training on mirror mechanisms in human adults.Building on the results of more naturalistic studies (Calvo-Merino et al. 2005; 2006; Cross et al. 2006; Ferrari et al.2005; Haslinger et al. 2005; Jackson et al. 2006; Keyserset al. 2003; Kohler et al. 2002; Margulis et al. 2009; Vogtet al. 2007), these experiments have isolated the effects ofsensorimotor experience from those of purely visual and



purely motor experience. Using all of the measures ofmirror mechanism activity commonly applied to humans(sect. 2.3), they have shown that relatively brief periods ofsensorimotor experience can enhance (Press et al. 2007;Wiggett et al. 2012), abolish (Cook et al. 2010; 2012a; Gill-meister et al. 2008; Heyes et al. 2005; Wiggett et al. 2011),reverse (Catmur et al. 2007; 2008; 2011), and induce (Land-mann et al. 2011; Petroni et al. 2010; Press et al. 2012a)mirror mechanism activity. Each of these ndings conrmsa novel prediction of the associative account: it reveals exi-bility of exactly the kind one would expect if MNs/mechan-isms are forged by sensorimotor associative learning. Incontrast, this kind of exibility does not provide anysupport for the genetic hypothesis. Indeed, if MNs were agenetic adaptation, some evolutionary frameworks wouldpredict that the development of MNs would be protectedor buffered against environmental perturbations thatcould interfere with their adaptive function (Cosmides &Tooby 1994; Pinker 1997). In the case of a genetic adap-tation for action understanding, this would include pertur-bations with the potential to divert MNs from codingproperties of action, rather than of inanimate stimuli, andfrom coding similar, rather than dissimilar, observed andexecuted actions.Evidence that MNs/mechanisms are not resistant to

coding inanimate stimuli comes from studies showingthat arbitrary sound, color, and shape stimuli can inducemirror MEP (DAusilio et al. 2006; Petroni et al. 2010),fMRI (Cross et al. 2009; Landmann et al. 2011; Presset al. 2012a) and behavioral effects (Press et al. 2007) fol-lowing sensorimotor training (Press 2011). For example,Press and colleagues gave participants approximately 50minutes of sensorimotor training in which they repeatedlyopened their hand when seeing a robotic pincer open,and closed their hand when seeing the robotic pincerclose (Press et al. 2007). Prior to this training, the pincermovement elicited less automatic imitation (see sect. 2.3)than human hand movement, but 24 hours after training,the automatic imitation effect was as strong for the pincermovement as for the human hand.Evidence that MNs/mechanisms are not resistant to

coding dissimilar actions comes from studies showing thatnon-matching (or counter-mirror) sensorimotor trainingabolishes automatic imitation (Cook et al. 2010; 2012a;Gillmeister et al. 2008; Heyes et al. 2005; Wiggett et al.2011), and reverses both fMRI (Catmur et al. 2008) andMEP mirror responses (Catmur et al. 2007). Forexample, Catmur and colleagues gave participants approxi-mately 90 minutes of non-matching sensorimotor trainingin which they repeatedly made an index nger movementwhile observing a little nger movement, and vice versa(Catmur et al. 2007). Before this training the participantsshowed mirror MEP responses, for example, observationof index nger movement elicited more activity in anindex nger muscle than observation of little nger move-ment, and vice versa for the little nger muscle. After train-ing, this pattern was reversed, for example, observation ofindex nger movement elicited more activity in the littlenger muscle than observation of little nger movement.

7.2. Objections to sensorimotor training evidence

Objections to this evidence suggest, in various ways, that itdoes not show that sensorimotor experience can change

MNs/mechanisms. For example, it has been suggestedthat the evidence comes only from studies of object-freeactions and yet MNs code only object-directed actions (Riz-zolatti & Sinigaglia 2010). However, a study of pianists hasshown that experience modulates mirror responses toobject-directed actions (Haslinger et al. 2005) and, as dis-cussed in sect. 4.1, monkey studies of communicative ges-tures (Ferrari et al. 2003) and pantomimed reachingmovements (Kraskov et al. 2009) have identied MNsthat code object-free actions.A related concern is that, because they use indirect

measures (fMRI, MEPs, and automatic imitation), ratherthan single-cell recording, sensorimotor learning exper-iments may not be measuring MN responses. Section 2.3reviewed the evidence for human MNs from a range ofexperimental techniques. These include conjunction ofneural responses during action observation and perform-ance (Gazzola & Keysers 2009; Iacoboni et al. 1999; Vogtet al. 2007), suppression of neural responses to cross-modally (perceptual-motor or motor-perceptual) repeatedactions (Kilner et al. 2009; Press et al. 2012b), muscle-specic MEPs (Catmur et al. 2011; Fadiga et al. 1995),and automatic imitation (Brass et al. 2001; Strmer et al.2000). In isolation, each of these measures is imperfect(Caggiano et al. 2013), but together they provide strongconverging evidence for human MNs. Sensorimotor learn-ing effects have been demonstrated for all these measuresof mirror responses: fMRI conjunction (Catmur et al. 2008;Landmann et al. 2011); repetition suppression (Press et al.2012a); MEPs (Catmur et al. 2007; 2011; DAusilio et al.2006; Petroni et al. 2010); and automatic imitation (Cooket al. 2010; 2012a; Gillmeister et al. 2008; Heyes et al.2005; Press et al. 2007; Wiggett et al. 2011). Thus, conver-ging evidence using multiple techniques strongly suggeststhat sensorimotor learning experiments are measuring and changing MN responses. Furthermore, althoughexperiments specically testing sensorimotor learning (inwhich sensory, motor, and sensorimotor experience arecompared and/or controlled) have not been performedusing single-unit recording, this conclusion is supportedby single-unit data showing that experience with toolscreates MN responses to observed tool use (Ferrari et al.2005; M. J. Rochat et al. 2010; see sect. 4).Considerations regarding anatomical specicity raise

another possible objection to the sensorimotor training evi-dence: Sensorimotor experience may only affect neurons innon-classical mirror areas (e.g., dorsal PMC). However,while recordings of monkey MNs have mostly been con-ned to ventral PMC and IPL, measurements in humansusing single-unit recording and fMRI conjunction suggestthat MNs are more widespread (e.g., Arnstein et al. 2011;Gazzola & Keysers 2009; Landmann et al. 2011; Mukamelet al. 2010; Vogt et al. 2007). Furthermore, paired-pulseTMS indicates that functional connections from dorsal (aswell as ventral) PMC to primary motor cortex enhancemuscle-specic MEP responses to action observation(Catmur et al. 2011). Thus, several sources of evidencesuggest that MNs are not restricted to classical mirrorareas. Therefore, even if sensorimotor experience werealtering neuronal responses only outside ventral PMC andinferior parietal cortex, it could still be affecting MNs.However, there is also evidence that sensorimotor learningaffects classical mirror areas. Many studies have demon-strated effects of sensorimotor experience on classical



mirror areas (Cross et al. 2009; Haslinger et al. 2005; Land-mann et al. 2011; Margulis et al. 2009; Vogt et al. 2007);counter-mirror sensorimotor learning reverses ventralPMC and inferior parietal cortex responses to observedactions (Catmur et al. 2008); and such learning is supportedby ventral PMC-M1 connections (Catmur et al. 2011). Fur-thermore, localizing the effects of sensorimotor learning tospecic neural populations using repetition suppressionsuggested that sensorimotor experience affects MNs in clas-sical mirror areas (Press et al. 2012a). Therefore, it appearsthat MNs are not restricted to classical mirror areas and thatsensorimotor experience has effects both on classical mirrorareas and elsewhere.A nal possibility is that counter-mirror training changes

relatively late neural responses to action observation,leaving earlier responses, mediated by MNs, intact (Barch-iesi & Cattaneo 2013). Such a nding might indicate thatcounter-mirror responses result from a more indirectroute (e.g., via prefrontal areas for rule retrieval) thanmirror responses. Barchiesi and Cattaneo (2013) testedthis hypothesis using a task that is likely to have provokedcoding of domain-general spatial cues, rather than action-specic topographic cues, and therefore to have failed toindex mirror responses at any time-point. A more recentstudy, using a more specic test of mirror responses,found effects of counter-mirror training on MEPs from200 msec, the earliest time-point at which mirror responseshave been observed in monkeys and humans (Cavallo et al.2013; see also Catmur et al. 2011).4 Thus, effects ofcounter-mirror training occur at the time when complexinformation about the observed action has just reachedPMC, making it improbable that mirror and counter-mirror effects occur at different times. It is likely that a pre-frontal route is involved during the training session, whenparticipants retrieve a rule in order to implement taskinstructions (e.g., if index, do little). However, thending that after counter-mirror training, effects of trainingare present in MEPs from 200 msec suggests that suchrule-based responding merely initiates associative learning:after learning, action observation activates counter-mirrorresponses as quickly as the original mirror responses.In summary: Although there are currently no studies sys-

tematically testing the effects of sensorimotor learning onMN responses in monkeys, a substantial body of evidencefrom studies of training and expertise in humans has con-rmed the predictions of the associative account, showingthat mirror responses can be changed in radical ways by sen-sorimotor learning. Furthermore, these studies have pro-vided no evidence that MNs/mechanisms are buffered orprotected against sensorimotor experience of a kind thatmakes them code inanimate stimuli and dissimilar actions.

8. Other models: Canalization and exaptation

This article focuses on the genetic and associative accountsof the origins of MNs because these were the rst modelsto be proposed, and the associative hypothesis is themost fully developed alternative to the standard, geneticview. For example, unlike other alternatives, it has beenused to generate and test novel empirical predictions.However, two other alternatives, which have been motiv-ated in part by the data generated in these tests (seesect. 7) should be considered. One raises the possibility

that the development of MNs is canalized, and the otherthat it represents an exaptation for action understanding.These are interesting possibilities but, we argue, they arenot supported by the evidence reviewed in sections 47.

8.1. Canalization

It has been suggested that MNs are acquired throughHebbian learning (Keysers & Perrett 2004) and thattheir development is supported or canalized by geneti-cally predisposed features of the perceptual-motorsystem, including the tendency of infants to look at theirown hands in motion (Del Giudice et al. 2009). On onereading, this canalization hypothesis is identical in sub-stance to the associative hypothesis; it is helpful in provid-ing a more detailed neuronal model of how sensorimotorexperience makes MNs out of motor neurons, and, in con-trast with the associative hypothesis, it emphasizes self-observation over social interaction as a source of relevantsensorimotor experience in development, but otherwisethe canalization hypothesis is identical to the associativeaccount. On this reading, the term Hebbian learning isunderstood to be a synonym for associative learning,and the canalization hypothesis suggests that if theinfants tendency to look at their own hands in motion isan adaptation (Clifton et al. 1994; Meer et al. 1996) ifthis attentional bias evolved for anything it was topromote the development of precise visuomotor control,rather than MNs and action understanding.On another reading, which we think is less likely to rep-

resent the authors intentions, Hebbian learning differsfrom associative learning in depending on contiguityalone, rather than both contiguity and contingency (seesect. 3.2), and the infant preference for manual self-obser-vation evolved specically to promote the development ofMNs and action understanding. If this reading is correct,the canalization hypothesis is a hybrid of the associative andgenetic accounts; it claims that MNs develop through(Hebbian) sensorimotor learning and constitute a geneticadaptation for action understanding. However, this hybridmodel would not be supported by current evidence forthree reasons. First, there is no evidence that the tendencyof infants to look at their own hands evolved to promotethe development of MNs or action understanding ratherthan visuomotor control (Del Giudice et al. 2009). Second,experimental data and modeling work have indicated thatthe sensorimotor learning which changes MNs depends oncontingency as well as on contiguity (Cook et al. 2010;Cooper et al. 2013b). Third, if MNs are forged by contin-gency-based sensorimotor learning, there is no problem forevolution (or scientists) to solve through canalization forMN development. If it was based on contiguity alone, thereis a risk that sensorimotor learning would produce lots ofjunk associations visuomotor neurons mapping observedand executed actions that happen to have co-occurred bychance. However, contingency-based (i.e., associative) learn-ing could produce the observed distribution of strictly congru-ent, broadly congruent, and non-matching MNs all by itself,without MN-specic canalization (see sect. 5.1).

8.2. Exaptation

Another interesting hybrid of the genetic and associativehypotheses has been developed by Arbib and colleagues



(e.g., Arbib 2005; Oztop et al. 2006). They propose thatMNs are produced, not by domain-general mechanismsof Hebbian or associative sensorimotor learning, but bya special kind of sensorimotor learning which receivesinput from self-observation of hand motion. This specialkind of learning is an exaptation for action understand-ing: It evolved from more domain-general mechanisms,such as those producing canonical neurons, specicallyto promote action understanding through the productionof MNs. This exaptation hypothesis does not specify, inpsychological or neurological terms, exactly what is dis-tinctive about the kind of sensorimotor learning that pro-duces MNs. However, it suggests that some extrastructure is required, both to constrain the variables rel-evant for the system, and to track trajectories of thoserelevant variables, and that the function of this extrastructure is to ensure coding of goals or hand-objectrelationships (Oztop et al. 2006, p. 269). Bonini andFerrari (2011) recently advanced a similar exaptationhypothesis, also motivated by the need to explain whyMNs consistently encode goals. However, as we haveargued in section 4, the evidence from single-unit record-ing in monkeys suggests that MNs do not consistentlyencode goals. Therefore, the primary motivation forinvoking exaptation is not compelling. Furthermore,there is no evidence that the sensorimotor learninginvolved in MN development is modied or constrainedrelative to the associative learning that occurs in standardconditioning experiments. On the contrary, there isexperimental evidence that it is sensitive to contingency,subject to contextual modulation, and open to the encod-ing of both animate and inanimate stimuli in exactly thesame way as standard associative learning (see sects. 5and 7).A recent article (Casile et al. 2011) adds another element

to the hybrid model advanced by Arbib and colleagues. Itsuggests that a special, exapted form of sensorimotor learn-ing underwrites the development of hand-relatedMNs, butthe development of facial MNs is minimally dependent onexperience. This suggestion is designed to accommodateevidence from studies of imitation and EEG suppressionin newborns, which some authors have interpreted asshowing that facial MNs are present at or shortly afterbirth. As we reported in section 6, this evidence has beenchallenged on a number of counts. Independent motivationand support for the idea that hand and faceMNs have differ-ent origins would be provided by evidence that faceMNs areless susceptible than hand MNs to modication by sensori-motor experience. However, as far as we are aware, thisnovel prediction of the hand/face hybrid model has notbeen tested, and a recent study of improvement in facial imi-tation suggests that face MNs are as susceptible to modi-cation by sensorimotor experience as hand MNs (Cooket al. 2013). Thus, until it is used to generate and testnovel predictions, the hand/face hybrid model stands as anintriguing but essentially ad hoc hypothesis.Hybrid modelling is a promising direction for future

research. However, to preserve predictive power, it isessential to check not only that hybrid models are consist-ent with existing data, but also that they have indepen-dent support. We have argued that both of theseconditions are met by the associative account, and thatneither is currently fullled by canalization and exaptationmodels.

9. A new approach to the function of mirrorneurons

We have argued that, at present, there is no positive evi-dence that MNs are a genetic adaptation or exaptation, orthat their development has been canalized, for actionunderstanding. However, the associative hypothesis is func-tionally permissive; it does not deny that MNs make a posi-tive possibly even an adaptive contribution to socialcognition. Rather, the associative hypothesis implies thata new approach is required to nd out what MNs contrib-ute to social behavior.

9.1. From reection to theory-based experimentation

In the 20 years since MNs were discovered, theories relat-ing to their function have been inspired by a method which(if you like a pun) could be called reection. This methodfocuses on the eld properties of the MNs found in asample of laboratory monkeys with unreported develop-mental histories. It asks, usually without reference to pre-existing computational or psychological theory, whatneurons with these eld properties would be good for;that is, what they might enable the animal to do. Forexample, early reports that MNs discharged whenmonkeys saw and produced object-directed actionsinspired the theory that MNs mediate action understand-ing via motor resonance, when neither of these was anestablished category of psychological functioning. Evennow, opposition to the idea that MNs mediate actionunderstanding tends to be answered by stressing theireld properties (Gallese et al. 2011). The associativeaccount suggests that the reection method needs to bechanged and extended in three principal ways.

9.1.1. Developmental history. If MNs were a geneticadaptation, it is likely that their properties would be rela-tively invariant across developmental environments. There-fore, it would be possible to make valid inferences aboutspecies-typical properties of MNs based on a relativelysmall and developmentally atypical sample of individuals.If MNs are instead a product of associative learning, thiskind of inference is not valid. Whether or not an individualhas MNs, which actions are encoded by their MNs, and atwhat level of abstraction, will all depend on the types ofsensorimotor experience received by the individual in thecourse of their development. Therefore, the associativeaccount implies that it is crucial for studies of laboratorymonkeys to report, and ideally to control, the animalsdevelopmental history; that is, the kinds of sensorimotorexperience to which they have been exposed. It alsosuggests that, if we want to know the species-typical prop-erties of monkey MNs, it will be necessary to test monkeysthat have received all and only the types of sensorimotorexperience typically available to them under free-livingconditions. A corollary of this is that we cannot assumethat the mirror mechanisms found in the members of onehuman culture are representative of the whole humanspecies. With its emphasis on the role of social practices such as the imitation of infants by adults, sports and dancetraining, and mirror self-observation in driving the devel-opment of MNs, the associative account provides specic,theory-driven motivation for cross-cultural studies ofmirroring.



9.1.2. System-level theory. If MNs were a genetic adap-tation, one could argue that new categories of psychologicalfunctioning such as action understanding and motorresonance are necessary to characterize what they do.It could be argued that, since they were speciallycreated by evolution, MNs are likely to have a highly dis-tinctive, largely independent, and previously unrecognizedpsychological function. In contrast, by showing that estab-lished psychological theory associative learning theory can cast light on the origin of MNs, the associativeaccount underlines the value of embedding research onMN function within system-level psychological and compu-tational theories of how the brain produces behavior (Giese& Poggio 2003; Kilner 2011; Kilner et al. 2007a). Thisimplies that hypotheses about MN function shouldspecify a part in a process a process that goes all theway from peripheral sensory input to overt motor output that MNs are thought to fulll. The name assigned to thispart is not important in itself. What is important is that thehypothetical function of MNs is distinguished clearly fromother components of the same overall process. Forexample, in this kind of system-level, theory-guidedapproach, action understanding would be distinguishedfrom components that are likely to be more purely percep-tual (which might be called action perception or actionrecognition), more purely motoric (e.g., actionexecution), or to constitute a higher level of understand-ing (e.g., mentalizing). This approach would also make itclear whether the hypothetical function is thought to beoptional or obligatory; whether it can be, or must be,done by MNs. The kind of system-level theoreticalapproach required in research on the functions of MNs isexemplied by studies of their role in speech perception(Lotto et al. 2009; Scott et al. 2009).A system-level theoretical approach would also over-

come a problem that has haunted discussions of theaction understanding hypothesis since MNs were discov-ered: Is this hypothesis claiming that MN activity causes orconstitutes action understanding? The former is anempirically testable hypothesis suggesting that there is adistinctive behavioral competence (the nature of whichhas not yet been specied, see sect. 3.1), called actionunderstanding, to which the activity of MNs contributes.The latter implies that the ring of MNs during actionobservation is, in itself, a form of action understanding;it does not need to have further consequences in order toqualify as action understanding. This claim is notsubject to empirical evaluation; it is true, or otherwise, byvirtue of the meanings of words.

9.1.3. Experimentation. Empirical (rather than constitu-tive) claims about the function of MNs need to be testedby experiments looking for, at minimum, covariationbetween MN activity and behavioral competence, and,ideally, testing for effects on behavioral competence ofinterventions that change MN activity. A brief survey ofrecent research of this kind using fMRI, TMS, and theeffects of focal brain lesions in human participants is pro-vided in the next section. At present, this research faces twomajor challenges. First, because the hypothetical functionsof MNs typically are not dened in the context of a system-level theory, it is difcult to design appropriate controltasks. For example, if an experiment is testing the hypoth-esis that MNs play a causal role in action understanding,

should it control for the possibility that they instead playsome role in action perception? If so, what kind of behav-ioral competence is indicative of action perception ratherthan action understanding?5 To date, only a smallnumber of studies (e.g., Pobric & Hamilton 2006)include control conditions designed to address this issue.The second major challenge is that, with rare exceptions

(Mukamel et al. 2010), MN activity cannot be localized pre-cisely within the human brain. Consequently, many studiesassume that activity in the ventral PMC and IPL areashomologous to those in which MNs have been found inmonkeys is MN activity, and that behavioral changesbrought about through interference with the functioningof these areas are due to interference with MNs. Theresults of such studies are of interest regardless ofwhether they relate to MNs. However, it is unsatisfactoryto assume that they relate to MNs, because, in monkeys,it is likely that fewer than 20% of the neurons in these clas-sical mirror areas are actually MNs, and because there isevidence of MNs in non-classical areas in both monkeysand humans (see sect. 2.1). Techniques such as fMRI rep-etition suppression and TMS adaptation (Cattaneo et al.2011; Silvanto et al. 2007) hold some promise as meansof overcoming the localization problem with human partici-pants, by isolating behavioral effects to specic populationsof neurons. Guided by system-level theory, future studiescould use these techniques with a range of tasks to isolateprocesses in which MNs are involved.Alongside the development of techniques such as fMRI

repetition suppression and TMS adaptation for use withhuman participants, it would be valuable to conductanimal studies that, not only document the eld propertiesof MNs, but also examine how those properties relate tobehavioral competence. For example, are animals withMNs for actions X and Y better than other animals of thesame species at behavioral discrimination of X and Y, orat imitating X and Y? Studies of this kind have been dis-missed as impractical on the assumption that they wouldhave to involve monkeys, which are demanding and expens-ive laboratory animals, and that between-group variation inMN activity would have to be induced via lesions or disrup-tive TMS. However, the associative account suggests that,in the long term, it may be possible to overcome these pro-blems by establishing a rodent model and using sensorimo-tor training to induce between-group variation in thenumber and type of MNs present in rodent brains. Ifthe associative account is correct, rodents are likely to havethe potential to develop MNs because they are capable ofassociative learning. Whether or not they receive in thecourse of typical development the sensorimotor experiencenecessary to realize this potential, it could be provided byvarious regimes of laboratory-based sensorimotor training.

9.2. Early signs

Given the theoretical limitations and methodological chal-lenges faced by research to date on the functions ofMNs, it is very difcult indeed to form a consistent andpotentially reliable picture of where their ndings arepointing. Nonetheless, for completeness, we offer the fol-lowing brief overview of research relating to the two mostcommonly investigated hypotheses MN activity contrib-utes to action understanding and to imitation. We rst sum-marize the results of meta-analyses of functional imaging



data, which, by identifying commonalities across multiplestudies, highlight candidate brain areas involved in thesehypothesized MN functions. Building on the fMRIstudies, patient data and studies using disruptive TMSapplied to classical mirror areas have the potential to ident-ify causal, rather than purely correlational, relationshipsbetween MN activity and behavioral competence.

9.2.1. Action understanding. As discussed in section 3.1,consensus regarding the term action understanding hasyet to be reached. In terms of the involvement of mirrorareas in perceiving others actions, a recent meta-analysisof fMRI data on action observation revealed that obser-vation of hand movements produces respons

Mirror Neurons- From Origin to Function

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