Emotional Empathy in Autism Spectrum Conditions: Weak, Intact, or

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Simon Baron-Cohen. © Springer ... state of the person being observed (Baron-Cohen and. Wheelwright 2004). ..... Does Joe influence Fred's action? Not if Fred ...
J Autism Dev Disord DOI 10.1007/s10803-009-0800-x

LETTER TO THE EDITOR

Response to Smith’s Letter to the Editor ‘Emotional Empathy in Autism Spectrum Conditions: Weak, Intact, or Heightened?’ Ilaria Minio-Paluello Æ Michael V. Lombardo Æ Bhismadev Chakrabarti Æ Sally Wheelwright Æ Simon Baron-Cohen

! Springer Science+Business Media, LLC 2009

Dear Editor, We read with interest the Letter by Smith (2009) suggesting that individuals with Autism Spectrum Conditions (ASC) have heightened emotional empathy (EE). We are pleased to be invited to contribute to the discussion. We do this by commenting on both the evidence cited by Smith, and also the evidence he does not cite. We conceptually reframe the question being posed and argue that, in the light of a broader review of the evidence, empathic responses in people with ASC are in general reduced. However, a basic type of empathic response that would fall into Smith’s definition of EE may indeed be heightened (a self-oriented personal distress response to others’ distress). We end by suggesting additional avenues to be explored. Empathy is a process where another person’s mental state (which include intentions, desires, emotions and proprioceptive states) automatically activates in the observer a representation of the observed state. These representations, unless inhibited, prime associated autonomic and somatic responses in the observer, thus generating a state in the observer that is more appropriate to the state of the person being observed (Baron-Cohen and I. Minio-Paluello (&) Dipartimento di Psicologia La Sapienza, Universita’ di Roma, Via dei Marsi 78, 00185 Rome, Italy e-mail: [email protected] M. V. Lombardo ! B. Chakrabarti ! S. Wheelwright ! S. Baron-Cohen Department of Psychiatry, Autism Research Centre, Cambridge University, Douglas House, 18B Trumpington Rd, Cambridge CB2 8AH, UK B. Chakrabarti School of Psychology and Clinical Language Sciences, University of Reading, Reading, UK

Wheelwright 2004). The empathic process can therefore be considered as a superordinate category that includes many phenomena sharing this same underlying mechanism (Preston and de Waal 2002). Minio-Paluello et al. (2009) addressed the embodied side of empathy in people with ASC by investigating the response to others’ pain using a paradigm that involved watching a hand being penetrated by a needle. Facial or vocal representations of pain were not shown, to avoid any confound due to emotion recognition difficulties (Humphreys et al. 2007; Ashwin et al. 2006; Kuusikko et al. 2009) or atypical face processing (Spezio et al. 2007; Behrmann et al. 2006) in ASC. This study found that when observing another person’s physical pain, unlike controls, participants with ASC did not show a neurophysiological response as if they were experiencing pain themselves, and nor did their neurophysiological response correlate with the imagined pain sensory qualities. Instead, participants with ASC represented others’ pain in relation to the level of self-oriented arousal experienced while watching pain affecting another person. Further, participants with high empathy and a low number of autistic traits showed a stronger embodied empathy response. Thus, embodiment of another person’s state is one possible mechanism underlying the empathic process (Niedenthal 2007; Gallese 2007) and one that seems reduced in ASC (Minio-Paluello et al. 2009; Williams 2008). Reduced embodiment in people with ASC does not directly relate to their level of EE, defined by Smith (2009) as ‘an emotional response in an individual that stems from and parallels the emotional state of another individual’ (italics added). In the study by Minio-Paluello et al. (2009), for example, neither participants with ASC nor controls reported vicariously experiencing any pain while watching the model’s hand being penetrated by the needle.

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Smith’s proposal that people with ASC might have heightened EE is interesting, but the supporting evidence is not particularly strong. In the following section we consider some of the evidence cited by Smith. Dziobek et al. (2008) found that people with ASC, relative to controls, felt equally concerned about another person’s state. Their results, however, do not address EE, as defined by Smith. Participants were not asked if and to what extent they felt a similar emotion to that observed in another individual (e.g., ‘‘How sad does looking at this (sad) man make you feel?’’). Therefore, although they might have experienced a similar degree of empathic concern, whether they themselves actually felt the emotion being observed is unknown. Shared neural representations for self and other also appear to be involved in empathy. These shared neural representations range from low-level mechanisms such as automatic mirroring during the observation (Other) and execution (Self) of actions (Gazzola and Keysers 2009), observation (Other) and experience (Self) of sensations (Blakemore et al. 2005; Keysers et al. 2004; Bufalari et al. 2007), pain (Singer et al. 2004; Jackson et al. 2006), or emotions (Wicker et al. 2003), to higher-level inference based mentalizing about the self and other (Lombardo et al. 2009; Ochsner et al. 2005; Mitchell et al. 2006; Saxe et al. 2006). While the neural mechanisms underlying these two types of processes appear to be distinct, we recently observed that these two neural systems interact. Neural systems involved in low-level automatic mirroring and/or embodied representations such as frontal operculum/ventral premotor cortex, primary sensorimotor cortex, and the pre-supplementary motor area are functionally connected (e.g., correlated task-specific activation over time between two regions) with neural systems involved in higher level inference-based mentalizing about oneself and another individual (Lombardo et al. 2009). In an altogether different paradigm Zaki et al. (2009), have shown that when engaging in empathic processing, the accuracy of such processing is highly related to both neural systems dealing with low-level and high-level shared representations. Both our observations, as well as those by Zaki and colleagues, suggest that neural mechanisms for EE and cognitive empathy (CE) are not as easily dissociable in the brain as previously thought. Smith cites a recent fMRI study (Nummenmaa et al. 2008) as evidence of a preferential link between EE (rather than CE) and mirror systems in the brain. In the Nummenmaa study, participants were asked to either empathize or watch people interacting in a threatening (EE) or neutral (CE) scenario. The results indicated higher activations of Inferior Parietal Lobule and premotor cortex in the EE condition. This, however, may not have been related to EE

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per se but simply reflecting that the EE threat scenarios had a higher level of implied motion than the neutral scenarios (Urgesi et al. 2006; Proverbio et al. 2009). Additionally, even in instances of CE such as high-level inference based mentalizing, such a process is tightly linked to information processing that is occurring in low-level ‘mirror’ systems (Lombardo et al. 2009). Thus, Smith’s contention of specific links between EE and low-level mirroring mechanisms in the brain do not exclude the fact that CE will also tap processing in such neural systems. According to the proposed relation between EE and mirror systems, Smith cites findings of enhanced motor (Bird et al. 2007) and emotional contagion (Capps et al. 1993; Magnee et al. 2007) in ASC as evidence of increased EE. However, the interpretation of these results again requires extra caution. For example, while Bird et al. (2007) found that actions performed by people with ASC are influenced by the observation of actions performed by others, this motor contagion effect is not more enhanced in ASC than in controls. In fact, there is evidence pointing to the contrary, suggesting that people with ASC have reduced motor and emotional contagion. Following this idea that individuals with ASC show reduced motor and emotional contagion, Smith neglects quite a large body of evidence on this topic. Individuals with ASC show reduced congruent emotional response to others’ emotions (Yirmiya et al. 1992), reduced and delayed automatic electromyographic (EMG) facial mimicry response to others’ emotional facial expressions (McIntosh et al. 2006; Beall et al. 2008; Oberman et al. 2009), reduced overt facial and body mimicry to others’ emotions (Stel et al. 2008), an absence of contagious yawning (Senju et al. 2008), reduced motor contagion from actions (Becchio et al. 2007; Welsh et al. 2009; The´oret et al. 2005; Cattaneo et al. 2007; Pierno et al. 2008) and gaze (Becchio et al. 2007), and reduced emotional contagion (Scambler et al. 2007; Hadjikhani et al. 2009). In keeping with this line of evidence, reduced automatic facial mimicry was also found in neurotypical women with high number of autistic traits (Hermans et al. 2009) and in neurotypical women after administration of testosterone (Hermans et al. 2006). We now turn to the issue of whether people with ASC have a heightened self-oriented personal distress response to others’ distress. Davis (1983, 1996) describes EE (or what he calls ‘affective empathy’) as being a combination of empathic concern (the tendency to experience other-oriented feelings of sympathy and compassion for others’ misfortune), and personal distress (the tendency to experience selforiented feelings of discomfort and anxiety in response to another’s misfortune). Personal distress may be a more rudimentary form of empathy, or it may fall outside of empathy. Throughout typical development, level of personal distress decreases while appropriateness of helping

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behaviour increases (Zahn-Waxler et al. 1983). Infants initially respond to the distress of others with their own distressed cries (Sagi and Hoffman 1976; Ungerer 1990; Zahn-Waxler and Radke-Yarrow 1982), and only around 2 years of age do they start to respond in an other-oriented affective and prosocial way by helping, comforting, and sharing (Rheingold et al. 1976; Zahn-Waxler et al. 1992). Individuals with ASC self-report lower levels of empathic concern (Dziobek et al. 2008; Rogers et al. 2007; Lombardo et al. 2007; Minio-Paluello et al. 2009) and show reduced or absent comforting responses toward a distressed other (Bacon et al. 1998; Charman et al. 1997; Dawson et al. 1998, 2004; Sigman et al. 1992; Corona et al. 1998). However, individuals with ASC also report higher (Dziobek et al. 2008; Rogers et al. 2007; Lombardo et al. 2007) or equal (Minio-Paluello et al. 2009) levels of personal distress compared to controls. High levels of selforiented personal distress can be considered in the light of ASC high egocentrism (Frith 2004; Frith and de Vignemont 2005). The co-occurrence of both reduced empathic concern and increased personal distress in ASC may interact and culminate in the overall reduction of empathy in ASC. Social psychological research demonstrates this interaction in observations regarding comforting or helping behaviour. If an observer is overwhelmed by his or her own emotional experience when observing a person in need of help, he/she is unlikely to engage in comforting or helping behaviours (Batson 1991; Eisenberg 2007). Interestingly, the idea that empathic difficulties of people with ASC might be in part related to their high levels of personal distress is also supported by research with infants at risk for developing autism. High-risk infants later diagnosed with ASC show higher levels of personal distress (Brian et al. 2008; Bryson et al. 2007; Zwaigenbaum et al. 2005) and greater difficulty to disengage their attention (Zwaigenbaum et al. 2005) and regulate their emotions (Bryson et al. 2007; Garon et al. 2009), relative to high-risk infants who do not receive a diagnosis of ASC or low-risk infants. The ability to disengage one’s attention, away from oneself or from distressing stimuli, is thought to be an effective emotion regulation strategy (Rothbart and Ahadi 1994; Posner and Rothbart 1998; Sheese et al. 2008) and is impaired in young children with autism (Landry and Bryson 2004). According to this account, which highlights the difficulty of people with ASC in emotion regulation, attentional disengagement, and increased levels of personal distress, one would expect individuals with ASC to show increased autonomic reactivity when witnessing others’ distress, and when confronted with social stimuli that might be perceived as aversive and/or that are actively avoided. Studies on autonomic reactivity in ASC are characterized by mixed results. When observing distressed others, children with ASC either show no change in autonomic

response (Corona et al. 1998), or do not differ from controls (Blair 1999). The latter is true when they are exposed to arousing pictures (Bernier et al. 2005; Ben Shalom et al. 2006) or are separated from their mother (WillemsenSwinkels et al. 2000). However, their autonomic response is higher when looking at direct versus averted gaze (Kyllia¨inen and Hietanen 2006) and in relation to neutral stimuli which might be related to higher baseline levels of anxiety. Bo¨lte et al. 2008 found that individuals with ASC, compared to controls, experienced less arousal when viewing sad pictures but higher arousal while processing neutral stimuli. Children with ASC had higher baseline GSR than controls that dropped when they engaged in a stereotypical behaviour (Hirstein et al. 2001). Additional neurophysiological studies are therefore needed to investigate autonomic reactivity in ASC and the links between empathic difficulties, high personal distress and effortful emotion regulation. Future studies could also benefit from considering the role of alexithymia in ASC (Tani et al. 2004; Hill et al. 2004; Berthoz and Hill 2005; Lombardo et al. 2007; Szatmari et al. 2008; Minio-Paluello et al. 2009). Alexithymia pertains to difficulty in self-referential emotion understanding. High levels of alexithymia are likely to selectively influence self-report measures of state affect (in contrast to trait self-report measures). State self-report measures of affect rely/require on-line emotional self-appraisal and on-line interoceptive awareness. Recent evidence points out that the neural substrates of emotional self-appraisal, such as the dorsomedial prefrontal cortex (Lane et al. 1997; Ochsner et al. 2004) are hypoactive in ASC (Silani et al. 2008). However, it is unknown whether interoceptive signals and their awareness are atypical in ASC. These processes possibly affected by alexithymia are likely to be crucial components in the empathizing process. In conclusion, we agree that the study of the empathic processes is of central importance to understanding ASC. While we welcome the Letter by Smith, we suggest caution in evaluating some of the selective evidence he provides in support of his thesis, especially in light of the abundant evidence to the contrary. We propose that investigating personal distress, emotion regulation, disengagement of attention, and self-referential emotion processes in an embodied cognition perspective will provide fruitful venues for future research.

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