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Social Neuroscience
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Mirror neuron system involvement in empathy: A critical look at the evidence


Amee D. Baird , Ingrid E. Scheffer
a b c a b c

& Sarah J. Wilson

a c

Psychological Sciences, University of Melbourne, Melbourne, Australia Department of Medicine, University of Melbourne, Melbourne, Australia

Epilepsy Research Centre, Austin Health, Melbourne, Australia Published online: 10 Jan 2011.

To cite this article: Amee D. Baird , Ingrid E. Scheffer & Sarah J. Wilson (2011) Mirror neuron system involvement in empathy: A critical look at the evidence, Social Neuroscience, 6:4, 327-335, DOI: 10.1080/17470919.2010.547085 To link to this article: http://dx.doi.org/10.1080/17470919.2010.547085

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SOCIAL NEUROSCIENCE, 2011, 6 (4), 327335

PSNS

Mirror neuron system involvement in empathy: A critical look at the evidence


Amee D. Baird1, Ingrid E. Scheffer2,3, and Sarah J. Wilson1,3
1 2

Mirror Neuron System In Empathy

Psychological Sciences, University of Melbourne, Melbourne, Australia Department of Medicine, University of Melbourne, Melbourne, Australia 3 Epilepsy Research Centre, Austin Health, Melbourne, Australia
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It has been proposed that the human mirror neuron system (MNS) plays an integral role in mediating empathy. In this review, we critically examine evidence from three bodies of research that have been cited as supporting this notion: (1) behavioral studies that have examined the relationship between imitation and empathy, (2) findings from functional neuroimaging studies that report a positive correlation between MNS activation and self-report on an empathy questionnaire, and (3) observations of impaired imitation and empathy in autism spectrum disorders (ASD). In addition, we briefly review lesion studies of the neural correlates of imitation and empathy. Current evidence suggests that the MNS is broadly involved in empathy, but at this stage there has been limited consideration of its various forms, including motor, emotional, and cognitive empathy. There are also various forms of imitation, encompassing emotional and non-emotional, automatic, and voluntary actions. We propose that the relationship between imitation and empathy may vary depending on the specific type of each of these abilities. Furthermore, these abilities may be mediated by partially distinct neural networks, which involve the MNS to a variable degree.

Keywords: Empathy; Mirror neuron system; Imitation; Autism spectrum disorders (ASD).

The initial discovery of the human mirror neuron system (MNS), comprising the inferior frontal gyrus and inferior parietal cortex, has led to a surge of interest in the neural correlates of social cognition, including empathy. The broad notion that empathy involves putting oneself in anothers shoes, by simulating what others do, think, or feel, has been linked to the properties of mirror neurons (Iacoboni & Mazziotta, 2007). Specifically, it has been proposed that the internal simulation or mirror matching of actions and emotions by the MNS occurs automatically and unconsciously, and underlies our ability to empathize (Carr, Iacoboni, Dubeau, Mazziotta, & Lenzi, 2003; Gallese, 2003; Leslie, Johnson-Frey, & Grafton, 2003).

The adoption of mirror neurons as the neural underpinning of empathy, or at least an integral part of the neural network underlying this ability, is partly based on a presumed link between imitation and empathy. Surprisingly, there is limited empirical evidence for this link. In this short review, we critically evaluate studies that have examined the relationship between imitation and empathy and their neural correlates. We have chosen to focus our review on studies published since 2008 to ensure that it is topical and up-to-date. The role of the MNS in motor imitation and action understanding has recently been questioned (e.g., Hicock, 2008; Molenbergh, Cunnington, & Mattingley, 2009), and evidence for its specific involvement in empathic functioning is even less

Correspondence should be addressed to: Sarah J. Wilson, Psychological Sciences, University of Melbourne, Parkville, 3010, Australia. E-mail: sarahw@unimelb.edu.au This work was supported by funding from the Australian National Health and Medical Research Council (Project grant 566759) and a Medical Research Grant from the University of Melbourne.

2011 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business www.psypress.com/socialneuroscience DOI: 10.1080/17470919.2010.547085

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BAIRD ET AL. TABLE 1 A schematic overview of the different forms of imitation and empathy and their main neural correlates identified by research to date Function Imitation Emotional Non-emotional Main neural correlates Type of research studies

Automatic Voluntary Automatic Voluntary

Unknown Right inferior frontal gyrus, limbic systema Frontal regions: left frontal operculumb Frontal regions: premotor cortex, inferiorfrontal gyrus Parietal regions: superior and inferiorparietal lobules Sensorimotor MNS Inferior frontal gyrus Ventromedial prefrontal cortex

No studies to date fMRI Lesion, fMRI, TMS Lesion, fMRI, TMS

Empathy Motor Emotional Cognitive


a

TMS Lesion, fMRI Lesion, fMRI

fMRI: functional magnetic resonance imaging; TMS: transcranial magnetic stimulation; MNS: mirror neuron system. See Iacoboni (2009). bSee Bien et al. (2009).

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compelling (Decety, 2010). It is enticing to assert that the MNS underpins empathy, and studies in several different areas support this contention. These include lesion studies of imitation and empathy, functional neuroimaging showing a positive correlation between empathy self-report and MNS activation, and observations of impaired imitation and empathy in autism spectrum disorders (ASD). While valuable, these studies do not as yet provide us with a comprehensive framework for understanding the role of the MNS in empathy, and researchers have recently challenged the extent to which the MNS may be involved (Decety, 2010). As this review will show, research to date suggests that there are various forms of imitation and empathy that are likely to be underpinned by partially independent neural substrates. These forms include emotional and non-emotional, automatic, and voluntary imitation, as well as motor, cognitive, and emotional empathy (see summary in Table 1). Recent neuroimaging and lesion studies demonstrate that distinct neural regions underlie these forms, and each form recruit the MNS to a variable degree (Bien, Roebroeck, Goebel, & Sack, 2009; Shamay-Tsoory, AharonPeretz, & Perry, 2008). Conceivably, the development of a comprehensive account of empathy and its neural underpinnings would need to address the relevance of the relationships between these various forms and the role of the MNS in each.

WHAT IS EMPATHY?
Theodor Lipps is regarded as the father of the concept of einfhlung or empathy (translated from the German by Tichener in 1909). Although Robert Vischer first

used the term in 1873 to describe the projection of human feeling onto the natural world, Lipps (1903) expanded this theory to explain how we understand the mental states of others. He considered it to be an unconscious process based on a natural instinct and inner imitation (Montag, Gallinat, & Heinz, 2008). Since then, empathy has been defined in many ways, and definitional debates have predominated, including whether empathy is a cognitive or an emotional process (Preston & de Waal, 2002). For example, some authors adopt a broad definition of empathy that encompasses emotional contagion or sympathy, while others prefer a narrower definition that distinguishes empathy from these related phenomena (de Vignemont & Singer, 2006). Different forms of empathy have been proposed. Blair (2005) distinguished cognitive, motor, and emotional empathy, and considered each to have a distinct neural correlate. Others acknowledge various forms, such as cognitive and emotional empathy, but argue that in most instances these components co-occur and cannot be disentangled (Baron-Cohen & Wheelwright, 2004). In addressing this issue, Preston and de Waal (2002, p. 3) suggested that the different views of empathy can be cohered into a unified whole if a broad view of the perception action model is taken. They conceived empathy as part of a group of related processes, including imitation, which depend on a perception action mechanism. These mechanisms are thought to be underpinned by the same neural network that mediates the perception and production of a given behavior. This assumption is evident in recent functional neuroimaging studies that have used imitation paradigms as a proxy for an empathy condition (see below). Thus, while differences in defining empathy between studies make it difficult to compare

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findings, they nonetheless allow examination of MNS involvement in various forms of empathy and imitation. In this review, we will define the type of empathy (corresponding with the measure used) that each study investigated, where possible. When it is not specified, the reader can assume that we are referring to emotional empathy.

Measures of individual differences in empathy


Numerous measures of empathy have been previously reviewed by Baron-Cohen and Wheelwright (2004). Here, we briefly review only two self-report questionnaires that are relevant to the discussion of this review. The Interpersonal Reactivity Index (IRI) (Davis, 1983) is the most commonly used questionnaire in empathy research. This measure comprises four scales of seven items each: (1) perspective taking (PT), assessing cognitive empathy or the ability to understand anothers point of view; (2) fantasy scale (FS), measuring the ability to imagine oneself in the place of fictional characters in books or movies; (3) empathic concern (EC), assessing emotional empathy or expressed concern for others; and (4) personal distress (PD), measuring the emotional response induced by observing strong emotions in others. This scale has good internal consistency, with alpha coefficients ranging from .68 to .79 (Davis, 1983). Although it has been criticized as measuring processes broader than empathy, such as self-control and imagination, it is generally considered the most comprehensive measure available (Baron-Cohen & Wheelwright, 2004). The Questionnaire Measure of Emotional Empathy (QMEE) (Mehrabian & Epstein, 1972) contains seven subscales assessing the tendency to react to anothers experience. Its split-half reliability is high (.84), suggesting that it measures a single construct. The authors propose this is emotional arousal to the environment in general, rather than the emotions of others specifically. Thus, while the scale has been used to assess affective empathy, it may be measuring a different but related construct (Baron-Cohen & Wheelwright, 2004).

and Bargh (1999) investigated unconscious motor mimicry, or what they termed the chameleon effect, in participants during social interactions. They described the mechanism underlying this effect as a perception-behavior link, or the tendency to automatically engage in behavior that one has perceived in another. Chartrand and Bargh considered this a passive, cognitive process that is not associated with an affective or emotional state. Correspondingly, they predicted that individual differences in emotional empathy would not modulate the chameleon effect. In support of their prediction, they found a higher frequency of motor imitation (foot shaking, face rubbing, smiling) in individuals with higher cognitive empathy scores (PT scale of the IRI) (Davis, 1983), but no association between motor mimicry and emotional empathy scores (EC scale of the IRI). Sonnby-Borgstrm (2002) subsequently reported findings that appear inconsistent with the work of Chartrand and Bargh (1999). She used electromyography (EMG) to measure the motor mimicry of emotional facial expressions, such as happy and angry. Individuals with high emotional empathy (as measured by the QMEE) showed a higher degree of facial expression mimicry than those with low emotional empathy. This led Sonnby-Borgstrm (2002) to conclude that automatic mimicry is an early automatic element of emotional empathy (p. 439). The findings of these studies suggest that the relationship between imitation and empathy may vary depending on the particular form of each of these abilities. Specifically, facial imitation was associated with emotional empathy (Sonnby-Borgstrm, 2002), while motor imitation was related to cognitive but not emotional empathy (Chartrand & Bargh, 1999). It is noteworthy, however, that Chartrand and Barghs definition of motor imitation included smiling, a form of facial imitation. The inconsistent results in relation to facial imitation may be due to the use of different stimuli (i.e., static photographs versus actors), or the different measures of emotional empathy used in each study. Further research is therefore required to clarify the relationship between these different forms of imitation and empathy, using a range of stimuli.

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THE RELATIONSHIP BETWEEN IMITATION AND EMPATHY


Despite the long-held association between imitation and empathy, there are few empirical studies of individual differences in this relationship. Only two studies have examined both abilities in healthy individuals. Chartrand

Neural correlates of imitation and empathy


Neuroimaging studies of empathy Numerous neuroimaging studies have investigated empathy with a variety of stimuli and paradigms, the majority using observation of pain in others as a

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model (Jackson, Rainville, & Decety, 2006). In general, these studies have shown shared neural activation for observing and experiencing pain that includes the bilateral anterior insula, dorsal anterior cingulate, and sensorimotor cortices. Although these findings appear to support the notion that empathy for pain involves an automatically activated sensorimotor resonance between self and other, Decety and colleagues (Decety, 2010; Yamada & Decety, 2009) have recently argued that the involvement of these brain regions may simply reflect a general aversive response and activation of the threat detection and defensive preparation system. Furthermore, studies of disgust (Wicker et al., 2003) and taste (Jabbi, Swart, & Keysers, 2007) demonstrate the integral role of the insula in empathy, and thus highlight the importance of regions outside the MNS in empathy for pain and other specific emotions. MNS involvement in empathy has been suggested by four functional neuroimaging studies reporting a positive correlation between MNS activation and empathy scores derived from the IRI (Gazzola, AzizZadeh, & Keysers, 2006; Jabbi et al., 2007; Kaplan & Iacoboni, 2006; Pfeifer, Iacoboni, Mazziotta, & Dapretto, 2007). These studies are summarized in Table 2 and show differing associations between specific IRI scales (and their corresponding forms of empathy) and localized regions of MNS activation. Three of the four studies found that MNS activation correlated with emotional empathy (EC or PD scales) (Jabbi et al., 2007; Kaplan & Iacoboni, 2006; Pfeifer et al., 2007). These studies varied according to passive observation versus active imitation of the inscanner task, and included both auditory and visual paradigms. The direction of the correlation was negative in one study (Kaplan & Iacoboni, 2006) and positive in two (Jabbi et al., 2007; Pfeifer et al., 2007). In contrast, Gazzola et al. (2006) found a positive correlation between cognitive empathy (PT scale) and the MNS, specifically left parietal lobule activation. Taken together, these studies are generally considered to support MNS involvement in emotional empathy, most commonly seen as increased activation of the inferior frontal gyrus either unilaterally or bilaterally. It is noteworthy, however, that all the studies used out-of-scanner correlations, the significant pitfalls of which have been outlined by Yarkoni (2009), as well as by Vul, Harris, Winkielman, and Pashler (2009). Methodological differences between these studies also question the strength of the conclusions. Although all the studies used the same out-of-scanner measure of empathy, the in-scanner paradigms, type of stimuli, and age of the participants varied widely (Table 2).

Moreover, prefrontal brain regions, such as the inferior frontal gyrus, may be activated for reasons other than an individuals empathic abilities. As noted by Cabeza and Nyberg (2000), this brain region is consistently activated during a wide range of tasks, and its engagement may reflect attention or linguistic processes rather than empathic functioning per se. Mirror neurons account for only a minority of the cell population in this area in the monkey, yet, despite this, Decety (2010) has noted a bias in human neuroimaging research to attribute a hemodynamic response in the inferior frontal gyrus to MNS activity. Nevertheless, a recent lesion study (Shamay-Tsoory et al., 2008) supports the preliminary neuroimaging findings of Table 2. This study demonstrated dissociable neuroanatomical substrates for cognitive and emotional empathy, with emotional empathy deficits occurring after damage to the inferior frontal gyrus, while impaired cognitive empathy was manifested after ventromedial prefrontal cortical damage (see section below). This finding again highlights the need for a more comprehensive framework that identifies the roles of specific brain regions in the various forms of empathy. Other functional neuroimaging studies have used imitation paradigms as a proxy for empathy (e.g., Carr et al., 2003); however, this approach is problematic. Currently, there is limited empirical evidence of an association between imitation and empathy. Given that the MNS has been found to play a role in imitation, these studies inevitably conclude that the MNS is involved in empathy. As noted by Decety and Michalska (2010, p. 896), there is a problem with equating empathy with motor resonance because the latter does not convey insight into anothers internal state and does not account for any other-oriented motivational state that characterises sympathy. A distinction has also been typically made between voluntary (conscious) and automatic (unconscious) imitation, with the latter assumed to underlie empathic functioning (Leslie et al., 2003). Voluntary imitation typically requires the experimenter to ask the participant to copy an action or expression. Performance on such tasks may be influenced by nonspecific factors such as executive function (Bird, Leighton, Press, & Heyes, 2007). Automatic imitation requires a participant to observe an action or expression, either passively or accompanied by a simple movement, while the experimenter measures involuntary movements or the performance speed of the simple movement. In this way, automatic imitation is considered a purer measure of imitative ability. Despite this, to date there have been no functional neuroimaging studies investigating empathy that use an automatic imitation task. This is a significant gap

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TABLE 2 Summary of neuroimaging studies showing a positive correlation between self-reported empathy and MNS activation Imaging task and stimuli Observation of film clips of drinking cups in different contexts (cleaning, drinking, and no context) and with different hand grips (precision or whole hand) Interpersonal Reactivity Index (IRI)* (Davis, 1983) Empathy measure Main findings Positive correlation between right inferior frontal gyrus activation and empathic concern scale (average across all film clips), and fantasy scale scores (during incongruent and context alone clips) Negative correlation with personal distress scale scores (during congruent actions and action in context clips) Positive correlation between left premotor cortex and inferior parietal lobule activation (during hand and environmental sounds) and perspective-taking scale scores (Note that participants were categorized into high and low empathy groups) Positive correlation between bilateral anterior insula and frontal operculum activation and total IRI score (particularly evident for the personal distress and fantasy scale scores) No correlation between IRI scores and brain activation during tasting Positive correlation between inferior frontal gyrus activation (in addition to right insula, left amygdala, and left fusiform gyrus) and IRI scale scores (except perspective-taking scale) during observation and imitation of facial expressions IRI and Interpersonal Competence Scale (parental report)

Author (year)

Participants (mean age)

Kaplan et al. (2006)

26 adults (26 years)

Gazzola et al. (2006)

16 adults (31 years)

Listening to or performing mouth or hand action sounds (e.g., kissing, ripping paper)

IRI

Jabbi et al. (2007)

18 adults (24 years)

Observation of film clips of actors drinking liquids and displaying pleased, disgusted, and neutral facial expressions, and actual ingestion of pleasant, disgusting, and neutral tasting liquids Imitation and observation of five facial expressions (happy, fearful, sad, angry, neutral)

IRI

Pfeifer et al. (2008)

16 children (10 years)

*See section on measures of empathy for a description of this questionnaire.

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in our current knowledge. Future neuroimaging and lesion studies will need to distinguish between automatic and voluntary imitation involving different body parts (i.e., face, hand, body) and determine how they relate to the various types of empathy and their neural correlates. Lesion-based research While recent neuroimaging research has focused on the neural networks associated with imitation and empathy, only lesion or transcranial magnetic stimulation (TMS) studies can identify brain regions that are necessary for these functions. The majority of neuropsychological studies examining the neural basis of imitation and empathy have involved patients with frontal lobe lesions, who typically show enhanced imitation or impaired empathy (e.g., Brass, Derrfuss, Mathes-von Cramon, & von Cramon, 2003; Eslinger, 1998; Luria, 1980; Shamay-Tsoory et al., 2008). Damage to the left parietal region has also been shown to alter imitation performance (Halsband et al., 2001), while there appear to be no studies reporting impaired emotional processing in these patients. In general, lesion studies suggest a core circuitry of imitation underpinned by the MNS; however, human lesion research has yet to identify more specific areas within frontal and parietal regions. Notably, a recent meta-analysis of 20 functional MRI studies that examined the role of frontal and parietal brain regions in imitation suggested that areas extending beyond the classic MNS are also crucial for imitation (Molenbergh et al., 2009). Two recent TMS studies using self-report questionnaires have demonstrated an association between sensory or motor empathy for pain and MNS function (Avenanti, Bueti, Galati, & Aglioti, 2005; Fecteau, Pascual-Leone, & Theoret, 2008). Both studies measured motor cortex excitability as a marker of sensorimotor MNS function. Although the motor cortex is not typically considered part of the human MNS (Iacoboni & Mazziotta, 2007), mirror neurons have been found in the monkey primary motor cortex (Tkach, Reimer, & Hatsopoulos, 2007). The findings of these two TMS studies provide support for the motor system being involved specifically in awareness of pain.

been hypothesized that the MNS plays a critical role in these deficits (Williams, Whiten, Suddendorf, & Perrett, 2001). Recent studies, however, have challenged the presence of either a global imitation or an empathic deficit in ASD.

Imitation in ASD
The first observation of an imitative deficit in autism was made over 50 years ago (Ritvo & Provence, 1953). Since then, there have been numerous studies of imitation in the ASD population, the majority focusing on motor imitation (meaningful/meaningless gestures or actions). In general, these studies show impaired imitative abilities in ASD compared with controls (Williams, Whiten, & Singh, 2004). More recently, three studies have demonstrated atypical activation of MNS regions during performance of various motor imitation tasks in ASD groups compared with controls (Dapretto et al., 2006; Nishitani, Avikainen, & Hari, 2004; Williams et al., 2006). These findings have been cited as support for MNS dysfunction in ASD. The issue here, however, is that performance of the imitation task by the ASD group was intact (Dapretto et al., 2006; Nishitani et al., 2004; Williams et al., 2006). This suggests that atypical MNS activation does not necessarily reflect MNS dysfunction per se, as imitation was not impaired. Rather, individuals with ASD may simply recruit alternative brain regions or use the MNS differently to perform such tasks. All three studies measured voluntary imitation, which may be dissociated from automatic imitative abilities in ASD (McIntosh, Reichmann-Decker, Winkielman, & Wilbarger, 2006; Tardif, Laine, Rodriguez, & Gepner, 2007). Only a few studies have examined automatic imitation in the ASD population, with inconsistent results. Bird et al. (2007) found intact automatic imitation of robotic and human hand actions in adults with ASD. Moreover, Tardif et al. (2007) found enhanced automatic imitation of facial and vocal stimuli in children with ASD compared with controls. In general, the differing imitation results in ASD probably reflect methodological variations, such as stimulus type (motor or facial/emotional), the age of participants, and the method of measuring automatic imitation (behavioral observations or physiological measures such as EMG). Equally plausible, however, is the suggestion that imitation may not be a unitary construct, but may depend on more than one neural network. Hamilton, Brindley, and Frith (2007), using mirror neuron tasks previously employed in neuroimaging studies, reported intact hand action

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ASD: ARE IMPAIRED IMITATION AND EMPATHY A REFLECTION OF MNS DYSFUNCTION?


From observations of impaired imitation and empathic abilities in individuals with ASD, it has

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imitation in children with ASD. They suggested that different imitation behaviors may be supported by different neural systems. They also reported impaired theory of mind (cognitive empathy) in this sample. Accordingly, various types of empathy may be associated with different forms of imitation, and the integrity of these different forms and their relationships to cognitive and emotional empathy requires systematic investigation in both healthy and ASD populations.

Empathy in ASD
Impaired empathy is considered a hallmark feature of ASD (Baron-Cohen & Wheelwright, 2004; Blair, 2008; Gillberg, 1992). Despite this, there is a paucity of research on the nature of empathic functioning in ASD, particularly in relation to specific forms of empathy. Extant research has primarily focused on one form of empathy, namely cognitive empathy, the majority of studies showing theory of mind deficits. This focus has led to the conclusion that empathy is impaired in ASD. Recent studies, however, have begun to adopt a broader framework, challenging the notion that empathy is a unitary concept by examining different forms of empathy in this population. Three studies have assessed emotional empathy in the ASD population to date. In a case study of two individuals with Asperger syndrome (AS), ShamayTsory, Tomer, Yaniv, and Aharon-Peretz (2002), using the IRI and QMEE, found that both cognitive and emotional empathy were impaired. Two group studies, however, refute this finding. Rogers, Dziobek, Hassenstab, Wolf, and Convit (2007) used the IRI to assess empathy in a sample of individuals with AS and found that while cognitive empathy was impaired, scores on the emotional empathy scale were similar to controls. This finding was replicated by Dziobek et al. (2008). These findings question whether all forms of empathy are impaired in ASD and raise the possibility that cognitive and emotional forms of empathy may be dissociated in this population. This notion is supported by the findings of the lesion study by Shamay-Tsoory et al. (2008) described above. It poses a challenge for the MNS dysfunction hypothesis of ASD, which assumes that empathy is a unitary phenomenon underpinned by the MNS.

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and empathy has contributed to the notion of the MNS as the neural correlate of empathy. There is, however, limited empirical evidence for such an association. Further research is required to clarify the exact nature of this relationship in both healthy and neurologically impaired populations. In our review of functional neuroimaging studies showing positive correlations between MNS activation and empathy scale scores, we found that the results are mixed, despite use of the same behavioral measure of empathic functioning (the IRI). While MNS dysfunction has been demonstrated in ASD, undoubtedly complex links exist between the nature of the imitative or empathic deficit and the network involved. To summarize, we propose that a more comprehensive framework that promotes systematic investigation of the various forms of empathy is needed to guide future research. Development of this framework offers the opportunity to extend our understanding of the neural bases of this complex and fundamental human ability.
Manuscript received 17 February 2010 Manuscript accepted 25 November 2010 First published online 10 January 2011

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In this paper, we have critically examined the current evidence for MNS involvement in empathy. The assumption of an intimate relationship between imitation

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