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Home , Anticipation, Claus Lamm, Compassion, Empathic concern, Pain empathy, Revenge

THE YEAR IN COGNITIVE 2009

The of and University of Zurich, Laboratory for Social and Neural Systems Research, Zurich, Switzerland

The phenomenon of empathy entails the ability to share the affective experiences of others. In recent years social neuroscience made considerable in revealing the mechanisms that enable a person to feel what another is . The present review pro- vides an in-depth and critical discussion of these findings. Consistent evidence shows that sharing the of others is associated with activation in neural structures that are also active during the first-hand experience of that . Part of the neural activation shared between self- and other-related experiences seems to be rather auto- matically activated. However, recent studies also show that empathy is a highly flexible phenomenon, and that vicarious responses are malleable with respect to a number of factors—such as contextual appraisal, the interpersonal relationship between em- pathizer and other, or the perspective adopted during observation of the other. Future investigations are needed to provide more detailed insights into these factors and their neural underpinnings. Questions such as whether individual differences in empathy can be explained by stable personality traits, whether we can train ourselves to be more empathic, and how empathy relates to are of utmost relevance for both science and society.

Key words: empathy; social neuroscience; ; fMRI; anterior insula (AI); anterior (ACC); prosocial behavior; , ; emotion contagion

Introduction ultimately results in a better understanding of the present and future mental states and actions Being able to understand our conspecifics’ of the people around us and possibly promotes mental and affective states is a cornerstone of prosocial behavior. our lives as “social animals.” It enables us to not In recent years, the field of social neuro- only communicate and interact with each other science has begun to shed light on the neural in effective and pleasant ways, but also to pre- underpinnings of the phenomenon of empa- dict the actions, intentions, and of oth- thy. The aim of this review chapter is to give ers. How ordinary the ability to empathize with an overview of this research, to discuss short- others appears to us often only becomes evident comings, and to provide recommendations for when things go wrong, as when we are misun- future research. Since we mostly focus on stud- derstood by someone else and by consequence ies in the domain of empathy for pain, evidence our feelings get hurt. But even in those cases our concerning other emotions is only partially in- immediate affective reaction enables the other corporated (see Decety & Jackson 2004; Decety person to become aware of the misunderstand- & Lamm 2006; Hein & Singer 2008; Singer & ing and the emotional consequences of his or Leiberg 2009; Singer 2006 for more exhaustive her actions. This ability to share others’ feelings coverage of related issues). The present chap- ter is divided into three parts. First, we pro- vide definitions of empathy and related terms Address for correspondence: Tania Singer, Claus Lamm, Univer- such as , emotion contagion, and per- sity of Zurich, Laboratory for Social and Neural Systems Research, sonal distress. This is intended to illustrate that Blumlisalpstrasse¨ 10, CH-8006 Zurich, Switzerland. [email protected], [email protected] sharing the feelings of others, defined here as

The Year in 2009: Ann. N.Y. Acad. Sci. 1156: 81–96 (2009). doi: 10.1111/j.1749-6632.2009.04418.x C 2009 New York Academy of Sciences. ! 81 82 Annals of the New York Academy of Sciences

“empathy,” is only one part of a large spec- nitive mechanisms enable us to “put ourselves trum of a person’s possible vicarious responses into someone else’s shoes.” Surprisingly, it took toward others. In the second part, current ev- quite some time for the field of neuroscience idence from social neuroscience studies of em- and in particular of functional pathy will be selectively reviewed. This re- to dare to make contributions to this challeng- view will focus on a discussion of the shared ing pursuit (Carr et al. 2003; Keysers et al. representations account of empathy, which is 2004; Morrison et al. 2004; Singer et al. 2004; currently the dominant neuroscientifically mo- Wicker et al. 2003). This might be attributed tivated approach to understanding the mech- to the complexities inherent in this multidi- anisms underlying empathy. In addition, we mensional psychological phenomenon as well will reflect on the role of bottom-up and top- as to the methodological challenges of bringing down influences in generating and modulat- such an idiosyncratic and context-dependent ing empathic responses and discuss the dif- phenomenon into a scientific environment ferent motivational consequences carried by that requires well-controlled and reproducible the vicarious responses of empathy versus per- experiments. sonal distress. In the final part, we propose At a basic phenomenological level, empa- research questions and domains that should thy denotes an affective response to the directly be given special by future empathy perceived, imagined, or inferred feeling state researchers. of another being (for an excellent overview of the various “things called empathy,” see Batson 2009). In our own understanding, em- Definition of Terms: Empathy pathy occurs when an observer perceives or and Its Sisters imagines someone else’s (i.e., the target’s) and this triggers a response such that the ob- Despite the word’s linguistic roots in ancient server partially feels what the target is feeling. Greek—from empatheia (), which is com- De Vignemont and Singer (2006, p. 435), for posed of “en” (in) and “” (feeling)—the example, define empathy as follows: We “em- scientific scrutiny of empathy has a relatively pathize” with others when we have (1) an af- short history that can be dated back to its use fective state (2) which is isomorphic to another in philosophical aesthetics. From there the En- person’s affective state, (3) which was elicited glish term originated as a direct translation of by observing or imagining another person’s af- the German Einfuhlung¨ (“feeling into” some- fective state, and (4) when we know that the thing), a term that was originally proposed as other person’s affective state is the source of a tool for analyzing works of art and nature, our own affective state. However, there are al- but later developed into a more general mech- most as many definitions of empathy as there anism for recognizing each other as “minded are researchers in the field. It is therefore es- creatures” (Stuber¨ 2008). After this initial philo- sential to briefly review and define the rele- sophically motivated period of scrutiny, most vant key concepts and components generally of the research on empathy was performed associated with the broad concept of empathy, by developmental and social (e.g., such as mimicry, , sym- Batson 1991, 2009; Hoffman 2000; Eisenberg pathy, and compassion. Although these con- 2000; Eisenberg & Strayer 1987). Naturally, so- cepts each refer to a different phenomenon, cial psychologists showed particular in they usually occur in concert. In most cases, this inherently social phenomenon (e.g., Batson mimicry or emotional contagion precedes em- 1991; Davis 1994). A great deal of social psy- pathy, which precedes and compas- chological research has been devoted to the sion, which in turn may precede prosocial question which perceptual, affective, and cog- behavior. Singer & Lamm: Social Neuroscience of Empathy 83

The Big and Little Sisters of Empathy communicative rather than for epistemological (Chartrand & Bargh 1999; van Baaren First, we need to distinguish between mimicry et al. 2004). and emotional contagion, which can both con- Emotional contagion is another process that tribute substantially to an empathic response. is related to but distinct from empathy. It Mimicry is defined as the tendency to automat- denotes the tendency to “catch” other peo- ically synchronize affective expressions, vocal- ple’s emotions and has alternately been labeled izations, postures, and movements with those “primitive empathy” (Hatfield et al. 2009). For of another person (Hatfield et al. 1994). Our example, babies start crying when they hear understanding of its role as a low-level mech- other babies crying—long before they develop anism contributing to empathy derives from a a sense of a self separate from others. Re- multitude of studies using facial electromyog- cently, initial evidence for involuntary pupil- raphy. These studies demonstrate that when an lary contagion was found in an fMRI study observer perceives another person’s affective fa- (Harrison et al. 2006). Participants were pre- cial expressions, such as a smile or a frown, sented with photos of sad faces with various corresponding affective expressions result in pupil sizes. Their own pupil size was signifi- the observer (see Dimberg & Oehman 1996, cantly smaller when they viewed sad faces with for a review). Relying on the facial feedback small as compared to larger pupils, and the hypothesis, according to which one appraises Edinger Westphal nucleus in the brainstem, one’s own emotions by perceiving their bodily which controls− pupil size, was specifically en- concomitants, Sonnby-Borgstrom (2002) pro- gaged by this contagious effect. Activation in posed that mimicry enables one to automati- this subcortical structure provides evidence that cally share and understand another’s emotions. pupillary contagion occurs outside of aware- Her proposal also receives support from studies ness and may represent a precursor of empathy. showing a (notably, weak) correlation between This study also demonstrates the strong over- the strength of the mimicry response and trait lap between mimicry and emotional contagion measures of empathy. (e.g., Hatfield et al. 1993). Note, however, that However, facial responses are not only trig- there are cases in which mimicry occurs with- gered when we observe others, but also when out an emotional component and other cases we are exposed to negatively or positively va- in which emotions are automatically elicited by lenced visual stimuli without social relevance observing others’ emotional states without the (Cacioppo et al. 2000, for a review). In addition, involvement of motor mimicry. several investigations demonstrate the influence On a conceptual level, neither emotional of top-down processes on mimicry, such as contagion nor mimicry cannot account for the those associated with the relationship between full-blown experience of empathy. In our un- empathizer and target (Lakin & Chartrand derstanding empathy crucially depends upon 2003), the affective state of the observer (Moody self-awareness and self/other distinction; in et al. 2007; Niedenthal et al. 2001), or the per- other words, on our ability to distinguish be- spective from which pain in others is witnessed tween whether the source of our affective ex- (Lamm et al. 2008). These observations cast perience lies within ourselves or was triggered on the assumption that mimicry repre- by the other (de Vignemont & Singer 2006; sents some sort of automatic or “hard-wired” Decety & Jackson 2004; Decety & Lamm 2006). motor resonance with another person’s affec- Without this ability, witnessing someone else’s tive display. Furthermore, mimicry seems to emotions could, for example, result, purely, in serve a social function in increasing rapport personal distress and a self-centered response in and fondness between self and other, raising the observer. We therefore regard mimicry and the question whether this function evolved for emotional contagion as important, yet distinct 84 Annals of the New York Academy of Sciences and neither necessary nor sufficient processes empathy in order to sense how to increase his for the experience of empathy. victim’s ; in competitive environments On the level of vicariously felt responses, we (from sports to business operations to warfare), have to distinguish between empathy, sympa- successful tactics take into account the negative thy, empathic concern, and compassion. In all affective effects that an action will have on the four cases, affective changes are induced in the opponent; and experiencing too much empa- observer in response to the perceived or imag- thy can lead to an aversive distress response and ined affective state of another person. How- selfish instead of other-oriented behavior (see ever, while empathy involves feelings that are below). In general, however, empathy is con- isomorphic to those of the other person, sym- ceived to be a first necessary step in a chain that pathy, empathic concern, and compassion do begins with affect sharing, followed by under- not necessarily involve shared feelings. For ex- standing the other person’s feelings, which then ample, empathizing with a person feeling sad motivates other-related concern and finally en- will result in a feeling of in the self, gagement in helping behavior. Empathy and whereas sympathizing with, being empathically prosocial behavior are thus closely linked on a concerned, or feeling compassion for a sad per- conceptual level. Notably, while consistent ev- son will result in either or compassionate idence for the link between “feeling for” (em- for the person, but not sadness. Also, when pathic concern) and prosocial behavior exists an observer notices that someone is jealous of (e.g., Batson 1991; Eisenberg 2000; Eisenberg him, he will most likely not start feeling jeal- et al. 1989), a clearcut empirical demonstra- ous himself—though he might show sympa- tion of a link between empathy and prosocial thy or compassion for the jealous person (for behavior is still missing. similar arguments, see de Vignemont & Singer 2006). Note also that the terms empathic concern, sympathy, and compassion have sometimes been Empathy Research in the Context treated as synonymous (cf. Batson 2009) and of Social Neuroscience: The Shared that the most widely used psychometric mea- Network Hypothesis sures of empathic concern (see below) involve self-report of compassionate, sympathetic, or Variousscholars have proposed that we come tender feelings. Therefore, the crucial distinc- to understand the actions, sensations, and emo- tion between the term empathy and those like tions of others by the activation of neural sympathy, empathic concern, and compassion is that representations corresponding to those states. empathy denotes that the observer’s emotions Inspired by earlier perception action models reflect affective sharing (“feeling with” the other in the domain of action understanding− (Prinz person) while compassion, sympathy, empathic 2005), Preston and de Waal (2002) proposed concern denote that the observer’s emotions a neuroscientific model of empathy, one which are inherently other oriented (“feeling for” the suggests that observing or imagining another other person). person in a particular emotional state auto- Further, folk psychological accounts usually matically activates a representation of that state relate the occurrence of empathy to proso- in the observer, along with its associated auto- cial and altruistic, other-oriented nomic and somatic responses. Other authors (i.e., a with the goal to increase the have also suggested that shared neural repre- other person’s well-being or welfare). Empathy, sentations play a general role in understand- though, does not necessarily carry such moti- ing other people’s mental states. They claim vations, and real-life examples of how empa- that shared representations provide us with a thy can “go awry” (from a prosocial point of simulation of their corresponding sensorimo- view) abound. For example, a torturer may use tor, affective, or mental states (Gallese 2003a; Singer & Lamm: Social Neuroscience of Empathy 85

Goldman 2006). Such accounts hold that the 2000), which consists of the areas in- capacity to project ourselves imaginatively into volved in the processing of pain, were activated another person’s perspective by simulating their when participants experienced pain themselves mental activity using our own mental appara- as well as when they saw a signal indicating tus lies at the root of our mature mind-reading that their loved one would experience pain. abilities, and the reasoning of these accounts These areas—in particular, bilateral anterior has been extended to the domains of actions insula (AI), the dorsal anterior cingulate cortex and feelings: To understand what another per- (ACC), brain stem, and the —are son is doing we simulate his movements using involved in the processing of the affective com- our own motor program; to understand what ponent of pain; in other words, they encode another person is feeling, we simulate his feel- how unpleasant or aversive the subjectively felt ings using our own affective programs (see also pain is. Thus, both the firsthand experience of Keysers & Gazzola 2006). Indeed, this so-called pain and the knowledge that a beloved partner shared representations account of social inter- is experiencing pain activates the same affective action and intersubjectivity has become the brain circuits—suggesting that our own neural dominant explanation of the hemodynamic ac- response reflects our partner’s negative affect. tivation patterns observed in recent fMRI stud- This initial finding of shared neural activa- ies of empathy. tion between self and other has been replicated The majority of social neuroscience studies and extended using a variety of and on empathy used the observation of pain in oth- methods. While initially evidence was restricted ers as a model to evoke empathic re- to the affective component of pain—as indi- sponses (de Vignemont & Singer 2006; Decety cated by activation restricted to areas involved & Lamm 2006; Singer & Leiberg 2009; see, in coding the affective motivational aspects of e.g., Jabbi et al. 2007 or Wicker et al. 2003, for the feeling of pain—there− is now evidence that examples using other emotional states). One areas associated with somatosensory processing common finding of these investigations is that can also be activated when we witness another vicariously experiencing pain activates part of person’s pain, in particular, when our attention the neural network that is also activated when is directed to the somatosensory aspects of the we are in pain ourselves. For example, Singer pain experience (e.g., Bufalari et al. 2007; and colleagues (2004) recruited couples and Cheng et al. 2008; Lamm & Decety 2008; measured hemodynamic responses triggered by Lamm et al. 2007b). Bufalari and colleagues painful of the female partner via an (2007), for example, demonstrated that the am- electrode attached to her right hand. In another plitude of an event-related potential compo- condition the same painful stimulation was ap- nent known to be generated in primary somato- plied to the male partner who was seated next sensory cortex (P45) is modulated by seeing a to the MRI scanner and whose hand could be needle piercing another person’s hand. In a si- seen via a mirror system by the female part- milar vein, a recent fMRI study showed that ner lying in the scanner. Differently colored (contralateral) right primary somatosensory co- flashes of light on a screen pointed to either rtex was activated when participants wit- the male or the female partner’s hand, indi- nessed another person’s left hand being cating which of them would receive painful pierced (Lamm & Decety 2008; Lamm et al. stimulation. This procedure enabled the mea- 2009). This activation overlapped with indivi- surement of pain-related brain activation when dually determined somatosensory represen- pain was applied either to the scanned subject tations of touch of the hand that had (firsthand experience of pain) or to her part- been determined in a separate localizer run. ner (empathy for pain). The results suggest that The latter finding is an important contri- parts of the so-called pain matrix (Derbyshire bution to the fMRI literature, which has 86 Annals of the New York Academy of Sciences so far demonstrated shared somatosensory serve neural representations of internal bodily activations only in secondary somatosensory states such as about temperature, cortex (e.g., Jackson et al. 2006a; Singer et al. , hunger, bodily states, and informa- 2006) or in parts of primary somatosensory cor- tion from the gut (Craig 2002, 2003; Critchley tex that are not somatotopically specific for the 2005; Critchley et al. 2004; Damasio 1994). affected body part (Lamm et al. 2007b). Fur- Based on anatomical observations in nonhu- thermore, a transcranical magnetic stimulation man species, Craig (2002, 2003) developed a (TMS) study by Avenanti et al. (2006) demon- detailed anatomical model suggesting that an strated that motor-evoked potentials are modu- image of the body’s internal state is first mapped lated when participants observe a needle deeply to the brain by afferents that provide input to penetrate the target’s hand, but not when they thalamic nuclei, sensorimotor cortices, and pos- observe a pinprick. This suggests that it is the terior dorsal insula. Direct activation of both saliency of the somatosensory quality of pain the AI and the ACC may correspond to the si- that determines whether somatosensory areas multaneous generation of both a feeling and an will or will not be involved in empathy for pain. affective motivation with its concomitant au- To investigate the areas involved in affec- tonomic effects. The very same structures (AI tive sharing during pain empathy more pre- and ACC) that play a crucial role in represent- cisely, detailed analyses of activation clusters in ing one’s own subjective feeling states also seem the cingulate and insular cortices have recently to be crucial in processing vicarious feelings. been performed (Decety & Lamm 2009; Jack- Based on this proposal, Singer and colleagues son et al. 2006b; Morrison & Downing 2007). (2004) extended an interoceptive model of emo- These analyses suggest that there is reliable tions to the domain of empathy and suggested overlap when activation in these areas during that cortical re-representations in AI of bod- firsthand and vicarious experience of pain are ily states may have a dual function. First, they compared, but they also show that the majority may allow us to form subjective representations of voxels in the insula and the cingulate cortex of our own feelings. These representations not do not overlap. In particular, a recent meta- only allow us to understand our own feelings analysis compared published localizations for when emotional stimuli are present, but also to the experience of pain to those reported for predict the bodily effects of anticipated emo- empathy for pain. The results suggest a more tional stimuli to our bodies. Second, they may posterior midinsular activation pattern for the serve as the visceral correlate of a prospective firsthand− experience of pain (Decety & Lamm simulation of how something may feel for oth- 2009). While this might have been expected ers. This may then help us to understand the for the hemisphere contralateral to the stim- emotional significance of a particular stimu- ulated body part, it is surprising for the ip- lus and its likely consequences. In accordance silateral (right) hemisphere. The same meta- with this view, it is noteworthy that the an- analysis also suggests overlapping, yet largely ticipation of pain has been found to activate distinct activation patterns in medial and ante- more anterior insular regions, whereas the ac- rior cingulate cortex—a finding that is in line tual experience of pain recruits more posterior with detailed single-subject analyses in native insular regions—confirming the postulated role anatomical space (Morrison & Downing 2007). of more posterior insular regions in modality- What is it, then, that is encoded or processed specific, primary representations of pain and in shared activation areas such as the ante- more anterior regions in the secondary repre- rior insula or the medial and anterior cingu- sentations of the anticipatory negative affect re- late cortex? It has been suggested that these lated to pain (Ploghaus et al. 1999). In line with regions represent a crucial part of the hu- this observation, in pain empathy studies ac- man interoceptive cortex (Craig 2003) and sub- tivity in posterior insular cortices was observed Singer & Lamm: Social Neuroscience of Empathy 87 only when participants were experiencing pain designs (Grill-Spector & Malach 2001; Henson themselves (Lamm et al. 2007a; Singer 2006; & Rugg 2003). Such an approach has already Singer et al. 2004), whereas activity in AI was been used in the domain of action observation observed when participants were experiencing (Dinstein et al. 2007) and mentalizing (Jenkins pain themselves and when vicariously feeling et al. 2008), and similar studies are now under- someone else’s pain. In a similar vein, instruc- way in the domain of empathy research. These tions to imagine pain from a first-person per- studies will show whether activation overlaps in spective or to specifically assess the somatosen- the observer result from the activation of the sory consequences of vicariously perceived pain same neural resources. revealed more posterior activation clusters in Finally, a word of caution is required as to the (Jackson et al. 2006a; Lamm whether the observed involvement of AI or et al. 2007a,b). ACC is specifically related to empathy or to The important role of anterior insular cor- emotional contagion (or both). One indication tex for empathy has also been demonstrated that shared activations during empathy for pain in other domains. AI is known to be crucially are not simply related to emotional contagion involved in processing sensations and emo- is provided by studies of Singer et al. (2004, tions such as taste or . Similar neu- 2006). Here, arbitrary visual cues rather than ral responses were elicited when participants explicit affective displays or other potentially viewed movies of disgusted faces and when they contagious stimuli such as depictions of painful smelled disgusting odors themselves (Wicker events were used to assess empathic responses. et al. 2003) as well as when they viewed videos In addition, a recent fMRI study by Lamm showing people sampling pleasant or unpleas- et al. (2009) detected substantial responses in ant tastes and when they sampled the different AI and ACC when participants were presented tastes themselves (Jabbi et al. 2007). Interest- with visual stimuli depicting situations that were ingly, the latter study also revealed that brain clearly nonpainful for them (touch of another responses in anterior insular cortex were posi- person’s hand by a Q-tip), but known to be tively correlated with individual differences in painful for the target. Together, these studies empathy measured by empathy questionnaires. render it less plausible that their neural re- The observation of similar neural activations sponses were directly triggered by the percep- during the firsthand vs. the vicarious experi- tion of overt (and emotionally contagious) cor- ence of various sensations and emotions (e.g., relates of the other person’s emotional state. disgust, taste, pain) raises the question whether Nevertheless, additional studies are required to these activations can indeed be interpreted as investigate how the brain actually differentiates shared representations. Shared activations are between self- and other-related feelings and to certainly a indicator of shared represen- dissociate the respective contributions of the tations. However, apart from the fact that we two related phenomena. do not know how observations on one level In sum, while substantial empirical evidence (the psychological/representational level) are suggests that shared neural activations are at mapped to those on another (the neural one), the root of sharing feelings, sensations, and ac- none of the currently available neu- tions of others, additional research is required roimaging methods directly measures activity to clarify whether these activations are actu- of single neurons or neural networks (how- ally shared on the neural level, to what extent ever, see Hutchison et al. 1999). Therefore, two we share both the somatosensory antecedents fMRI activation maps with overlapping clus- or only the affective consequences of another’s ters might still result from differing neural ac- affective state, what constitutes the functional tivity. One way to resolve this problem is the significance of these shared activations, and use of repetition-priming or fMRI-adaptation how we can distinguish between emotional 88 Annals of the New York Academy of Sciences contagion vs. empathy on the neural level. tributed to attention, inhibitory, and other ex- More sophisticated experimental designs, an- ecutive control processes also documents that alytical approaches, as well as closer col- empathy is not a purely sensory-driven process laborations between philosophers of mind, in which affective states are induced in the ob- neurophysiologists, introspection-based con- server solely by means of bottom-up processes. templatives, cognitive scientists, and social neu- On the contrary, it has long been argued that roscientists are required to yield more detailed contextual appraisal, cognitive processes, and answers to these questions. top-down control are important constituents of human empathy.Forexample, in the eighteenth Empathy—Bottom-Up vs. Top-Down century, the philosopher and economist Adam Processes Smith proposed that imagination enables us to project ourselves into the place of other persons, An important aspect of most neuroscien- experiencing sensations that are generally sim- tifically motivated models of empathy is that ilar to, although typically weaker than, those of the activation of shared representations in the the other person (Smith 1759/1976). Most con- observer is initiated mostly automatically and temporary neuroscientific models of empathy without conscious awareness. For example, in endorse this view and the importance of most studies of empathy in the domains of top-down control and contextual appraisal for pain, touch, and disgust, participants are not either the generation of an empathic response informed that the goal of the study is to investi- or for modulating an existing one induced by gate empathy-related neural responses. Rather, the above-mentioned bottom-up processes (de they are instructed to passively watch a scene or Vignemont & Singer 2006; Decety & Lamm movie depicting a person expressing an emo- 2006; Hein & Singer 2008; Singer 2006). tion or being touched (Blakemore et al. 2005; Decety and Lamm (2006), for example, pro- Keysers et al. 2004; Singer et al. 2004, 2006; posed a model in which bottom-up (i.e., direct Wicker et al. 2003). Nevertheless, this situa- matching between perception and action) and tion alone is sufficient to engage brain networks top-down (i.e., regulation, contextual appraisal, representing the firsthand experience of affect and control) information processes are fun- or touch. Some authors have therefore sug- damentally intertwined in the generation and gested that we automatically share other peo- modulation of empathy. In this model, bottom- ple’s feelings, a hypothesis in line with earlier up processes account for direct emotion sharing perception action models of motor behavior which is automatically activated (unless inhib- and imitation− and with their extension to the ited) by perceptual input. On the other end, ex- domain of empathy (Gallese 2003b; Preston & ecutive functions implemented in the prefrontal de Waal 2002). Preston and de Waal’s model and cingulate cortex serve to regulate both cog- (2002), for example, stresses the importance of nition and emotion through selective attention automatic and perceptually driven processes and self-regulation. This meta-cognitive level is such as emotional contagion and mimicry. It continuously updated by bottom-up informa- should be noted though that the term automatic tion, and in return controls the lower level by in this case refers to a process that does not providing top-down feedback. Thus, top-down require conscious and effortful processing but regulation, through executive functions, mod- can be inhibited or controlled (cf. Bargh 1994). ulates lower levels and adds flexibility, mak- In addition, attention to the target’s affective ing the individual less dependent on exter- state is required for triggering the postulated nal cues. The meta-cognitive feedback loop cascade of events starting with emotional con- also plays a crucial role in taking into account tagion and, ultimately, resulting in a full-blown one’s own mental competence in order to react empathic experience. The crucial role that is at- (or not) to the affective states of others. This Singer & Lamm: Social Neuroscience of Empathy 89 model should be supplemented by top-down study the same group demonstrated that it is processes that are not classically associated with mainly a late event-related potential compo- executive function and its associated neural nent that differs between the attention and no- structures, in particular those in the medial attention conditions, while an early component and dorsolateral . Mental im- is not affected by the focus of attentional agery, for example, has been shown to result in (Fan & 2008). The early response might shared representations in both the motor and correspond to the postulated automatic activa- the sensory-affective domain without consider- tion of shared representations, representations able prefrontal activation (e.g., Decety & Grezes which might then be interpreted by later neural 2006; Ogino et al. 2007). In addition, con- processes either inhibiting or augmenting the textual appraisal and target evaluation in behavioral relevance of the initial affective res- empathy-for-pain paradigms predominantly onance. Surprisingly, however, only the early activated areas such as the response correlated with subjective reports of or the ventral (e.g., Lamm et al. 2007b; the amount of perceived pain in the other per- Singer et al. 2006), in other words, structures son as well as the unpleasantness experienced involved in affective evaluation, reward, and by the observer. . Recent results also support the assumption Several recent findings provide strong sup- that the contextual appraisal of a situation port for top-down influences on empathy. rather than its sensory input alone determines These findings document the flexibility of the the empathizer’s neural and behavioral re- human mind in responding to others and sponse. In one fMRI study, participants viewed show that empathy is not an all-or-none phe- pictures of needle injections and of tissue biop- nomenon. Here, we want to focus on the role sies performed on human hands—with the lat- of attention, contextual appraisal, perspective- ter consisting of the insertion of a biopsy needle taking, and the relationship between em- into an anesthetized hand (Lamm et al. 2007b). pathizer and target as salient examples of how Hence, the actual painful consequences of two top-down control affects empathic responses basically identical visual stimuli had to be taken (see Hein & Singer 2008 for a more exhaus- into account in order to show appropriate vicar- tive account). ious responses. The neural structures support- Two recent fMRI studies and an event- ing this appraisal process included the medial related potential study demonstrate that the dorsal and orbitofrontal cortex (OFC) and the way we attend to the emotions of others sub- right (rTPJ). Involve- stantially modulates our empathic responses to ment of the OFC was associated with reeval- them. In one study participants were exposed uating the valence of the seemingly aversive, to pictures of painful situations—such as cut- yet actually neutral biopsy stimulus. Activation ting one’s finger or getting one’s hand caught of the rTPJ and dorsal medial prefrontal cor- in the door. When evaluating the painful conse- tex, however, was linked to self/other distinc- quences of those situations, participants showed tion and self-awareness. These capacities en- activation in large parts of the pain matrix— abled the observers to distinguish between a a now typical response given the evidence probably automatically triggered, self-centered reviewed above. However, when participants response to the aversive stimulus and the knowl- were instructed to count the number of hands edge that such a response was actually not shown in a picture—an experimental manipu- appropriate given the contextual information lation that was devised to distract their attention about the biopsy’s affective consequences. No- from the inflicted pain—no activation in insular tably, a recent meta-analysis of neuroimaging or cingulate cortices was observed (Gu & Han studies of attention, , the expe- 2007). In a follow-up electroencephalographic rience of agency, and empathy demonstrated 90 Annals of the New York Academy of Sciences that all these phenomena resulted in largely rior insula, the , as well as various overlapping activations in the rTPJ (Decety & structures involved in action control. Imagining Lamm 2007). This finding also raises awareness oneself in a potentially harmful situation might that, in many cases, so-called high-level phe- therefore trigger a stronger aversive response nomena can be explained more parsimoniously than imagining someone else in the same sit- by underlying low-level processes—such as the uation. In addition, it might engage systems orienting of attention to external cues, or, as that help the observer to evaluate the affective recently proposed, the switching between ex- meaning of similar situations, rendering these ternally and internally oriented modes of infor- representations a basis for future projections mation processing (Corbetta et al. 2008). into another person’s situation. Avenanti et al. Perspective taking is another prominent (2006) used similar perspective-taking manip- example of how top-down processes shape ulations to assess their effects on motor inhi- empathic responses and social understanding bition. In line with fMRI findings, TMS re- (Avenanti et al. 2006; Jackson et al. 2006a; sults suggest that perspective-taking effects do Lamm et al. 2007a, 2008; Ruby & Decety 2004; not operate on the level of primary sensorimo- Stotland 1969). There is long-standing interest tor representations. Together with the absence in how placing of oneself into another’s shoes of activation differences in visual areas in the affects one’s vicarious response to the other,and fMRI study by Lamm et al. (2007a), this sug- whether this differentially affects altruistic and gests that information about the other person prosocial behavior (Batson et al. 1997; Batson “enters” the neural system in a similar way for et al. 1987; Underwood & Moore 1982). So- both perspectives but is then processed and ap- cial studies suggest that adopting praised differently (but see also Avenanti et al. a so-called imagine-other perspective (focusing 2008). on the feelings and thoughts of the other) pro- As anyone knows from personal experience, motes empathic concern and an other-oriented our attitudes toward others vary greatly and (altruistic) motivation while explicitly imagin- therefore can affect empathic responses to ing oneself (“imagine-self”) to be in the target’s them. Lanzetta’s group provided the first in- distressful situation results in heightened per- vestigations of the psychophysiological corre- sonal distress and an egoistic motivation to re- lates of how our relationship to someone else duce that distress (via withdrawal or an aversive affects our response to their emotions (Englis response). et al. 1982; Lanzetta & Englis 1989). Facial Recent fMRI and TMS studies investi- EMG and other measures of autonomic ner- gated the neural correlates of this phenomenon vous system activity demonstrated that being (Avenanti et al. 2006; Jackson et al. 2005; in a competitive gaming relationship results in Lamm et al. 2007a). In the study by Lamm counterempathetic responses—in other words, et al. (2007a), participants watched videos joyful affect when the competitor loses and neg- of undergoing painful auditory treat- ative affect when he or she wins. In a similar ment either by imagining that they were in vein, a recent fMRI study (Singer et al. 2006) the ’s place (imagine-self) or by fo- assessed the modulation of empathic brain re- cusing on the patient’s feelings and affective sponses to another person’s pain as a function expressions (imagine-other). The results indi- of the perceived fairness of the other person and cated higher personal distress and less em- the gender of the observer.As in previous empa- pathic concern during the imagine-self per- thy studies, empathy-related activation in ACC spective, which was associated with stronger and AI was observed for both genders when a hemodynamic responses in brain regions cod- fair, liked player was in pain. However, men, ing the motivational affective dimensions of but not women, showed an absence of such pain, such as the bilateral− medial and ante- empathy-related activity when seeing an Singer & Lamm: Social Neuroscience of Empathy 91 unfair and disliked player in pain. Instead, men other’s state in the absence of any bottom-up showed increased activation in areas associ- stimulation. ated with reward (), with As for the former, based on available evi- activation in these areas correlating positively dence, we speculate that cortical areas asso- with their for (as assessed by ciated with executive function, contextual ap- self-report after MRI scanning). These results praisal, and attention play a major role. This suggest that, at least in men, a desire for re- would include cortical structures such as the venge won over empathic motivation when dorsolateral prefrontal cortex, medial and an- they were confronted with someone experi- terior cingulate cortex, right ventral premo- encing pain who they believed deserved to be tor cortex, inferior and superior parietal cor- punished. tex, and orbitofrontal cortex (e.g., Aron et al. These results also point to gender as another 2004; Corbetta et al. 2008; Duncan & Owen important variable in the investigation of em- 2000; Ridderinkhof et al. 2004; Rolls 2004). pathetic responses. In fact, there has been a These areas interact with structures encoding longstanding debate about whether women ac- the bottom-up driven affective responses, such tually possess more empathy, as expressed by as the anterior insula, amygdala, and possibly higher scores in various self-report measures, also parts of the ventral striatum. The latter or whether the different questionnaire scores way in which top-down processes affect empa- can be explained by social desirability and de- thy through mental imagery and top-down gen- mand effects (Davis 1994; Eisenberg & Lennon eration of feelings becomes particularly impor- 1983). While social neuroscience should be able tant when minimal sensory information about to make a valid contribution to this question the other is available, requiring the use of con- soon (see Han et al. 2008 for preliminary evi- text information, affective memory, and self-to- dence), the same amount of caution as in behav- other projection to infer the affective condition ioral studies has to be applied with respect to of the other person. Depending on the situa- experimental demand and social desirability ef- tion and the information available to the em- fects. It will be a major challenge to disentangle pathizer, these processes might be implemented neural responses that can be attributed to inter- in distributed networks that are recruited dur- nal (“true”) or external (“socially desirable,” de- ing the imagery of action, sensation, and affect. mand characteristics) empathetic motivations. In line with this reasoning, a recent fMRI study In addition, gender-specific physiological dif- showed that the first-person imagery of pain ferences such as head size, skull thickness, but activates structures also involved in empathy also individual differences in hormonal state at for pain as well as in the direct experience of the time of investigation have to be considered pain (Ogino et al. 2007). Similar evidence is as potential confounds. reported by Jabbi et al. (2008), whose analyses To summarize, there is considerable evi- demonstrate that it is not only the activation of a dence that empathy is substantially modulated brain region, but also its interaction with other by top-down processes such as attention or the brain areas which should be taken into account contextual appraisal of a situation. Notably, when one interprets there seem to be at least two different ways data (see also Jabbi et al. 2008; Zaki et al. 2007). in which top-down processes can affect the em- The existence of different pathways for top- pathic response. One way is to either inhibit down control is an important factor that should or amplify representations that have been acti- be taken into account when assessing individual vated via sensory channels and mechanisms as- differences in empathy as well as their link to sociated with perception-action coupling. The prosocial behavior. For example, the responses second way is to generate empathic responses of more “sensory-driven” persons might differ by means of imagination or of the from those with better imaginative capacities. 92 Annals of the New York Academy of Sciences

These different processing styles might be as- attachment style or extraversion/introversion sessed using emotional contagion question- affect the neural correlates of empathy and naires or by assessing personality traits such prosocial behavior. Finally, the question of as extraversion/introversion. whether the phenomenon of empathy itself rep- resents a trait rather than a situation-specific Future Directions state variable is of great interest. Further, empathy researchers need to de- The emergence of the field of social neu- velop new methods and approaches to assess roscience has enabled substantial insight into the functional significance of shared activa- the neural underpinnings of empathy in the tions. Are these representations valid indicators past few years. Nevertheless, we are just start- of simulation processes and what exactly is sim- ing to understand the neuronal and behavioral ulated by the observer? How domain-specific foundations of this complex psychological phe- or domain-general are the observed empathic nomenon. In this final section we will outline brain responses in anterior insula with respect those domains and questions we believe should to coding the qualities of pain, disgust, taste, or be the focus of future research efforts. general aversion, respectively? Does the shared Even though empathy has been studied ex- representations account hold for all emotions, tensively by developmental psychologists in the including positive ones? Initial evidence sug- past few decades (Eisenberg & Strayer 1987; gests that it does (see the studies of pleasant Hoffman 2000; Zahn-Waxler et al. 1992), our tastes discussed above; see also Jabbi et al. 2007; knowledge about the role of the developing van der Gaag et al. 2007, for examples in the brain in the domains of emotions and empathy realm of positive emotions), but future studies is very limited. Little information exists about should investigate the sharing of positive emo- how the above-mentioned bottom-up and top- tions such as , , or elation—which are down processes contribute to the development less directly related to primary sensory triggers of empathy and related concepts such as emo- and less well understood. tional contagion, sympathy, and compassion, In addition, a great deal of the currently how these functions change across the life span, available findings could be largely explained and to what extent these changes depend on the by emotional contagion and self-centered aver- maturation and function of the prefrontal cor- sive responses of the observer, such as personal tex in early childhood, , and later distress or a generalized withdrawal response in life (but see, e.g., Blakemore 2008). triggered by the sight of an aversive object. Social should also invest fur- How do we separate these self-oriented from ther effort in disentangling the mechanisms un- other-oriented responses? Are the observed ac- derlying individual differences in empathy. Are tivations in anterior insula the result of shared these differences attributable to variations in emotions, of personal distress, or rather of sym- sensory-mediated emotion sharing and conta- pathy and compassion? gion, or do they result from differences in cog- Another important question is how empathic nitive control and other top-down influences? brain responses and individual differences in How are they related to genetic variation, and empathy are linked to prosocial behavior. What what role do endocrine differences play in both is the role of personal distress versus sympa- cross-gender and within-gender comparisons? thy in predicting helping and other forms of In a similar vein, it would be particularly in- prosocial behavior? For example, is the absence teresting to learn how stable personality traits of prosocial behavior due to deficits in affec- affect empathic responses. For example, despite tive sharing, insufficient regulation of high per- obvious theoretical connections between these sonal distress, or a combination of the two? phenomena, we do not know how differences in An answer to this question requires a valid Singer & Lamm: Social Neuroscience of Empathy 93 distinction between these two processes and the Conflicts of Interest development of ecologically valid measures of prosocial behavior. The authors declare no conflicts of interest. Finally,and despite the long tradition of plas- ticity research in the field of neuroscience, very References little is known about the malleability of the em- pathic and emotional brain. Can we train peo- Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2004). ple to become more empathic, and which pro- Inhibition and the right inferior frontal cortex. 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