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The Neural Basis of Empathy NE35CH01-Singer ARI 12 May 2012 21:32 The Neural Basis of Empathy Boris C. Bernhardt and Tania Singer Department of Social Neuroscience, Max-Planck Institute of Human Cognitive and Brain Sciences, Stephanstraße 1a, 04309 Leipzig, Germany; email: [email protected], [email protected] Annu. Rev. Neurosci. 2012. 35:1–23 Keywords The Annual Review of Neuroscience is online at neuro.annualreviews.org social neuroscience, insula, cingulate cortex, fMRI, emotion This article’s doi: Abstract 10.1146/annurev-neuro-062111-150536 Empathy—the ability to share the feelings of others—is fundamental Copyright c 2012 by Annual Reviews. All rights reserved to our emotional and social lives. Previous human imaging studies fo- cusing on empathy for others’ pain have consistently shown activations by Universidad de Tarapaca on 06/13/14. For personal use only. 0147-006X/12/0721-0001$20.00 in regions also involved in the direct pain experience, particularly ante- rior insula and anterior and midcingulate cortex. These findings suggest Annu. Rev. Neurosci. 2012.35:1-23. Downloaded from www.annualreviews.org that empathy is, in part, based on shared representations for firsthand and vicarious experiences of affective states. Empathic responses are not static but can be modulated by person characteristics, such as degree of alexithymia. It has also been shown that contextual appraisal, includ- ing perceived fairness or group membership of others, may modulate empathic neuronal activations. Empathy often involves coactivations in further networks associated with social cognition, depending on the spe- cific situation and information available in the environment. Empathy- related insular and cingulate activity may reflect domain-general com- putations representing and predicting feeling states in self and others, likely guiding adaptive homeostatic responses and goal-directed behav- ior in dynamic social contexts. 1 NE35CH01-Singer ARI 12 May 2012 21:32 2002). In particular, anterior insula (AI) and Contents dorsal-anterior/anterior-midcingulate cortex (dACC/aMCC) play central roles in vicarious INTRODUCTION.................. 2 responses in the domain of disgust, pleasant or DEFINING EMPATHY . 2 unpleasant tastes, physical and emotional pain, EMPATHY IN THE BRAIN . 3 and other social emotions such as embarrass- EmpathyforPain.................. 4 ment or admiration (for recent meta-analyses, Empathy for Other Emotions see Fan et al. 2011, Kurth et al. 2010, Lamm andSensations.................. 7 et al. 2011; for anatomical orientation, see INSULA AND ACC: Figure 1a). On the basis of their structural and CONNECTIVITY AND functional patterns of connectivity, and their FUNCTIONS.................... 8 involvement in other functional processes at Insula............................. 8 the interface of sensory, affective, and cognitive Cingulate Cortex . 10 domains, regions such as AI and dACC/aMCC Interoceptive Network may generally contribute to the generation of Interactions..................... 10 subjective experiences and adaptive responses MODULATION to actual and predicted states in the self and oth- OFEMPATHY................... 11 ers. These general processes may then subsume PersonCharacteristics.............. 11 empathy as a special case. We also highlight ContextualAppraisal............... 14 evidence that additional networks involved in CONCLUSIONS AND social cognition can be flexibly corecruited dur- OPENQUESTIONS............. 15 ing empathic understanding, depending on the particular situation and information available in the environment. Moreover, we summarize studies that have identified multiple factors that INTRODUCTION modulate or even counteract empathy. For ex- Empathy is a crucial component of human emo- ample, initial evidence suggests that empathic tional experience and social interaction. The responses can be counteracted by opposing mo- ability to share the affective states of our closest tivational systems, such as the desire for revenge ones and complete strangers allows us to predict or Schadenfreude, closely related to activation and understand their feelings, motivations, and in brain areas implicated in reward-processing. actions. Extending previous work from philos- Finally, we outline future research avenues. ophy and behavioral psychology (Batson 2009, by Universidad de Tarapaca on 06/13/14. For personal use only. de Vignemont & Singer 2006, Eisenberg 2000, Hoffman 2000), advances in social neuroscience DEFINING EMPATHY Annu. Rev. Neurosci. 2012.35:1-23. Downloaded from www.annualreviews.org have provided important new insights into the Despite a long tradition of philosophy and brain basis of empathy. behavioral psychology research (Batson 2009, In this review, we outline the main results Eisenberg 2000, Eisenberg & Fabes 1990, of brain imaging studies that have investigated Hoffman 2000, Wispe 1986), empathy has no the neural underpinnings of human empathy. universally accepted definition, and the differ- fMRI: functional magnetic resonance Using mainly functional magnetic resonance ent phenomena it subsumes remain debatable imaging imaging (fMRI), the majority of studies suggest (Batson 2009, Blair 2005, de Vignemont & AI: anterior insula that observing affective states in others activates Singer 2006, Preston & de Waal 2002). How- brain networks also involved in the firsthand ever, previous conceptual work on empathy has ACC: anterior cingulate cortex experience of these states, confirming the greatly facilitated the design and interpreta- notion that empathy is, in part, based on shared tion of empirical studies that assess empathic MCC: midcingulate cortex networks (de Vignemont & Singer 2006, traits through self-report measures and em- Keysers & Gazzola 2007, Preston & de Waal pathic states through controlled observational 2 Bernhardt · Singer NE35CH01-Singer ARI 12 May 2012 21:32 experiments. Findings from these experiments, prosocial behavior; conversely, contagion and especially those investigating the brain pro- empathy may also induce aversive distress re- cesses underlying the empathic experience, may sponses that can lead to withdrawal behavior Emotional deepen our understanding of this phenomenon motivated by the desire to protect oneself from contagion: tendency at the interface of social interactions and in- negative emotions (Klimecki & Singer 2012). to automatically adopt ternal feeling states and ultimately promise to the emotional state of disentangle the conceptual web surrounding another person empathy. EMPATHY IN THE BRAIN Mimicry: tendency to A relatively specific notion claims that em- In their seminal article on empathy in 2002, synchronize the pathy occurs when the observation or imag- Preston & de Waal suggested that the obser- affective expressions, vocalizations, postures, ination of affective states in another induces vation and imagination of others in a given and movements of shared states in the observer (de Vignemont emotional state automatically activates a corre- another person & Singer 2006, Singer & Lamm 2009). This sponding representation in the observer, along Sympathy: feelings state is also associated with knowledge that with its associated autonomic and somatic for someone, generally the target is the source of the affective state responses (Preston & de Waal 2002). This coupled with the wish in the self. This reading of empathy neces- hypothesis was inspired by accounts that to see them better off sarily involves components of affective shar- suggested a close link between action and or happier ing, self-awareness, and self-other distinction perception through common coding schemes Compassion: an (for other more general notions of empathy (Prinz 1984, 2005). Moreover, the discovery of emotional and motivational state see Baron-Cohen & Wheelwright 2004, Blair mirror neurons, a class of neurons in monkey characterized by 2005). Therefore, empathy differs from ba- premotor and parietal cortices activated during feelings of sic sharing-only phenomena such as emotional execution and observation of actions, provided loving-kindness and a contagion and mimicry. Indeed, neither conta- a neural mechanism for shared representa- genuine wish for the gion nor mimicry requires a distinction about tions in the domain of action understanding well-being of others whether the origin of the affective experience is (Gallese et al. 2004, Keysers & Gazzola 2007, Empathic concern: within the observer or was triggered by another Rizzolatti et al. 2001). Subsequent studies, an emotional and motivational state person. Emotional contagion and empathy, for based predominantly on fMRI, have investi- characterized by the example when watching a friend in distress, can gated empathic brain responses for a variety desire to help and lead to personal distress, a self-centered and of states including pain (Morrison et al. 2004, promote others’ aversive response in the observer (Eisenberg Singer et al. 2004), disgust (Benuzzi et al. 2008, welfare & Fabes 1990). In contrast, during empathic Jabbi et al. 2007, Wicker et al. 2003), fear (de concern, sympathy, or compassion, vicarious Gelder et al. 2004), anxiety (Prehn-Kristensen responses involve a feeling of concern for the et al. 2009), anger (de Greck et al. 2012), by Universidad de Tarapaca on 06/13/14. For personal use only. other’s suffering that induces a motivation to sadness (Harrison et al. 2006), neutral touch alleviate the suffering, but not necessarily any (Blakemore et al. 2005, Ebisch et al. 2008, Annu. Rev. Neurosci. 2012.35:1-23. Downloaded from www.annualreviews.org
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