Empathic neural responses are modulated by the perceived fairness of others

“Increased pain-related activation (asterisk indicates whole-brain corrected) for women in ACC* [9, 18, 27], left FI* [242, 15,23], right FI* [30, 18,218], left SII* [260,230, 18], right SII* [63,230, 24] and brainstem* [3,218,218]; for men in left FI* [233, 33, 3] right FI [42, 33, 3] and brainstem [3,233,230].”

“…examining individual differences in empathy-related constructs that have primarily examined empathic responses to another person’s physical pain (Singer et al. 2004, 2006; Lamm et al. 2007) or to perceiving basic social signals (i.e., facial displays of emotion, see Chakrabarti et al. 2006;…”

“Previous studies reported that neural responses to social interactions can differ for men and women [38].”

“Parameter estimates extracted at the local maximum activation in the ACC region [x = 8, y = 39, z = 5] neither correlated with pay-off outcomes during the human-computer nor during the human-human interaction (rhuman-computer = .07; p > .05; rhuman-human = .26; p > .05).”

“While it is already known that social relations modulate empathic brain responses (Singer et al .”

“Although there are some sociocultural explanations for these affective differences [68], there is also some evidence to suggest that these differences are driven in part by biological factors, such as hormones [69] or sex-based brain differences [70].”

“The discovery of mirror neurons confirmed that a translation mechanism present in the primate brain is automatically elicited when viewing others' actions ( Singer et al, 2006 ).”

“This reduction is stronger significant activity of the left ventral striatum/nucleus accumbens, a complex of brain region associated with reward processing (Singer et al., 2006).”

“Quervain et al. (2004) show that effective punishment of individuals who behave unkindly produces activity in areas of the brain associated with the processing of rewards (see also Singer et al., 2006 ).”

“A number of similar social cognitive and affective constructs have been studied, including trust and reciprocity (King-Casas et al., 2005), fairness (De Quervain et al., 2004; Sanfey et al., 2003), and empathy (Singer et al., 2004, 2006).”

“In another study, Singer et al. (2004a) allowed subjects to face a series of cooperative and no-cooperative opponents in a sequential PDG.”

“In this regard, Singer et al. (2006) used real-time functional magnetic resonance imaging (fMRI) to observe the brain activity of 16 men and 16 women as they engaged in an economic game, a version of the Prisoner’s Dilemma game.”

“Thus, like for empathy (Singer et al., 2006; Zheng et al., 2016), reputation may modulate vAI responses to advantageous inequality and motivate people to refrain from intentionally violating a social norm.”

“Current Opinion in Neurobiology 2006, 16:1–8 namely those who behaved unfairly in an economic game, be subjected to pain [72].”

“Similar correlations between the anterior insula and self-reported empathy have been observed for empathy of social pain (Masten et al., 2011), and for the observation of other individuals receiving pain (Singer et al., 2004, 2006).”

“Recent research in social neuroscience has shown that psychological questionnaires on social behavior are correlated with neural activity variation between individuals (see for example Fukushima & Hiraki, 2006; Gazzola et al., 2006; Singer et al., 2004, 2006).”

“For example, responses to another’s pain, and to facial expressions indicating pain, locate empathy within the observer’s pain matrix: the anterior cingulate cortex, brainstem, cerebellum, and the anterior insula (Hein and Singer, 2008; Singer et al., 2004, 2006; Decety et al., 1997).”

“According with present results, contextual appraisal and target evaluation in empathy-for-pain paradigms predominantly activate the OFC, among other areas (e.g., Decety et al., 2012; Lamm et al., 2007; Singer et al., 2006).”

“observed in an fMRI study on empathy for pain that in males but not females empathetic reactions were absent for persons who were perceived as behaving unfairly (Singer et al., 2006).”

“There are ample instances of our prosocial failures (Allport, 1954; Cuddy, Rock, & Norton, 2007; Latané & Darley, 1968; Harris & Fiske, 2006; Zaki, 2014), and, in some cases, even enjoyment in others’ suffering (Cikara, Bruneau, & Saxe, 2011; Cikara, Bruneau, Van Bavel, & Saxe, 2014; Singer et al., 2006).”

“This emotional circuitry, in its positive and negative form, has been found not only in humans (Singer et al., 2006; Pfeifer et al., 2008) but also in monkeys (Masserman, Wechkin & Terris, 1964; Palagi et al.”

“According to Steiger (2004), the general rule of thumb to use the CIs to test a statistical hypothesis (H0) is as follows: when testing a two-sided/one-sided hypothesis at the alpha level, use a 100 × (1 − α)%/100 × (1–2α)% CI.”

“…or gut level emotional experiences (K. D. Craig, 1968) leading to the arousal of empathy in the observer (K. D. Craig, 2009; Goubert et al., 2005; T. Singer et al., 2006) and the activation of pain-related brain regions (Jackson, Meltzoff, & Decety, 2005; Ochsner et al., 2008; Simon, Craig,…”

“Although factors such as the perceived fairness of a target or the oddness of a target’s pain modulate the mean activity within these regions (Singer et al., 2006; Lamm et al., 2010), familiarity with the target seems to modulate the correlation between self and other in ways that are not…”

“1 The notable exceptions are the neural studies of de Quervain et al. (2004) and Singer et al. (2006), which indicate that people receive pleasure from punishing norm violators but even these studies do not tell us what sorts of " misbehavior " trigger punishment.”

“Consistent with previous studies (Berg et al., 1995; de Quervain et al., 2004; Haselhuhn & Mellers, 2005; Singer, Kiebel, Winston, Dolan, & Frith, 2004; Singer et al., 2006), the economic game provided subjects with negative (unfair) and positive (fair) personal experiences with the competitors.”

“This set-up was motivated by previous empathy studies using a similar paradigm (Hein, Silani, Preuschoff, Batson, & Singer, 2010; Rütgen, Seidel, Riečanský, et al., 2015; Singer et al., 2006), with one stimulation train lasting 1500 ms.”

“Other studies have similarly shown strong effects of group assignment on empathy and neuralmirroring processes when groups are defined based on competition (Hein et al., 2010; Singer et al., 2006).”

“A similar definition is also used in domains of emotions (Jabbi et al., 2007; Singer et al., 2004, 2006; Wicker et al., 2003) and sensations (Blakemore et al., 2005; Keysers and Perrett, 2004; Keysers et al., 2004).”

“, 2005) and empathetic responding in men is strongly dependent on the individual perceived (Singer et al., 2006).”

“…in pain increased activity in the insula, inferior frontal (IF) and the secondary somatosensory cortices (SII), similar to previous findings (Han et al., 2009; Jackson et al., 2005; Saarela et al., 2007; Singer et al., 2004, 2006; Carr et al., 2003; Gu et al., 2010; ShamayTsoory et al., 2009).”

“, 2005) and when witnessing disliked ones receiving painful stimulation (Singer et al., 2006), reflecting modulations of human reward activity by emotional”

“…2010; Bolivar et al., 2001; Langford et al., 2006; Wiesenfeld-Hallin, 2005) and women frequently score higher on standard tests of empathy, social sensitivity and emotion recognition than men (Schulte-Ruther et al., 2008; Singer et al., 2006), we attempted to investigate the effect of sex on OFL.”

“Another study reported that watching individuals who had played unfairly in monetary exchange game receive painful electric shocks produced increased activation in the striatum/nucleus accumbens relative to watching individuals who had played fairly (Singer et al., 2006).”

“Indeed, cognition and emotion are fundamental to the evolvement of empathy, which can be defined as a sense of similarity between the feelings one experiences and those expressed by others (refer to people’s emotional state to embodying the experience of that state) (Singer et al., 2006).”

“…direct and observed fear (Whalen et al., 2001), and the dACC and anterior insula are activated by direct and observed physical pain in adults (Singer et al., 2004, 2006; Jackson, Bruney, Meltzoff, & Decety, 2005; Botvinick et al., 2005; Morrison, Lloyd, Di Pellegrino, & Roberts, 2004) and…”

“Finally, participants completed a questionnaire in which they rated the other two players in terms of being fair, likeable, enjoyable, annoying, and attractive [2] on a Likert scale ranging from -3 to +3.”

“, 2012) or administration of electric shocks to norm-violators (Singer et al., 2006; Hein et al., 2010).”

“…or behavior, such as mutually cooperating with other individuals (Rilling et al., 2002, 2004), punishing unfair behavior (De Quervain et al., 2004; Singer et al., 2006), giving charitable donations (Moll et al., 2006; Harbaugh et al., 2007) and receiving a good reputation from others (Izuma et…”

“However, considering the observed empathy–fairness intervention in neural activities, which is found in men who did not feel empathy for the unfair person in pain (Singer et al., 2006), it is plausible that empathy is not always a mere automatic consequence of the passive observation of emotional cues in others, but r…”

“Some relevant brain regions, such as the ACC (with prior links to fairness; e.g., Singer et al., 2006), did not show significant associations to any of the traits examined in this study.”

“A recent brain-imaging study conducted by Singer and colleagues (Singer et al., 2006) reveal the neural correlates of such counter-empathic reactions.”

“Individuals watching others receive electric shocks, for example, had reduced activation in pain-sensitive regions such as the insula and ACC if those others had played unfairly in a prior economic game (Singer et al., 2006).”

“This suggests that women recruit areas containing mirror neurons to a higher degree than men, and therefore, that empathic response of women could be more automatic and less shaped by people’s social behavior [34].”

“Stakeholder interaction allows cross-interest learning and empathy, which are linked to cooperation (Batson et al., 1995; Singer et al., 2006).”

“Singer et al. (2006) found that subjects showed activation in fronto-insular and anterior cingulate cortices toward fair players who were allegedly being hurt.”

“Target perception and evaluation, including (un)fairness perception and blame allocation, are relevant aspects that fall within the contextual appraisal of a situation (Cuff et al., 2016; Singer and Lamm, 2009; Singer et al., 2006).”

“…Stürmer et al., 2006 ; Tarrant et al., 2009 ), historic differences in power and status (Mathur et al., 2010 ), fairness received from the observee (Singer et al., 2006 ), perception of the target’s moral characteristics (Cui et al., 2016 ; Delgado et al., 2005 ), direct or indirect interaction…”

“In a study more squarely focused on warmth comparisons, Singer et al. (2006) had participants react to others' painful experiences after observing their economic-game behavior.”

“This explains why we can get infected by other people’s emotions (Singer et al. 2006).”

“…empathy (Jackson et al., 2005; Singer et al., 2004), expertise (Cheng et al., 2007; Decety et al., 2010), the affective link between individuals (Singer et al., 2006), perceived group membership (Hein et al., 2010) and racial bias (Avenanti et al., 2010; Xu et al., 2009) have been shown to…”

“For example, activation to observed pain is more pronounced for close others and same-group members (Avenanti, Sirigu, & Aglioti, 2010; Cheng, Chen, Lin, Chou, & Decety, 2010; Decety, Echols, & Correll, 2010; Xu, Zuo, Wang, & Han, 2009; Singer et al., 2006), suggesting that interpersonal relationships can moderate the…”

“The males even activated a region of the brain that is involved in processing reward; they literally appeared to enjoy seeing the ‘‘bad guy’’ punished (Keysers 2011; Singer et al. 2006).”

“…of empathic brain responses obtained while subjects were observing other people suffering ! be it their loved ones or people the subjects liked (Singer et al., 2004, 2006) ! have revealed individual differences in activity in empathy-related painsensitive areas (ACC and AI) and that these…”

“These studies provided important clues on some of the possible variables that modulate empathy for pain (Singer et al., 2006; Avenanti et al., 2006; Cheng et al., 2007; Valeriani et al., 2008) and on whether this process impinges upon the affective (Morrison et al., 2004; Singer et al., 2004), the…”

“When empathy is reduced by making the target 13 less sympathetic (e.g. a cheater), there is no reduction in amygdala activity when the 14 target receives a painful electric shock (Singer et al., 2006).”

“displays were presented, either [25][5] or [5][25].”

“…2012; Hogeveen, Inzlicht, & Obhi, 2014; Lamm, Nusbaum, Meltzoff, & Decety, 2007; Liebe & Tutic, 2010; Loggia, Mogil, & Bushnell, 2008; Losin et al., 2015; Reynolds Losin, Iacoboni, & Dapretto, 2014; Reynolds Losin, Iacoboni, Martin, Cross, & Dapretto, 2012; Singer et al., 2006; Zaki et al., 2012).”

“There are still numerous definitions and operationalizations of the concept of empathy in use (e.g., Eisenberg & Lennon, 1983; Hoffman, 1977; Rappaport & Chinsky, 1972; Rogers, 1975; Singer et al., 2006; Truax, 1972; Walton, 1933).”

“In fact, most people tend to feel uncomfortable when witnessing somebody being cheated upon by another person and experience satisfaction from observing or administering punishment to norm-violators (de Quervain et al., 2004; Singer et al., 2006).”

“…individual differences in empathic tendencies (Baron-Cohen & Wheelwright, 2004; Pulos, Elison, & Lennon, 2004) and shows covariation with activity in the anterior cingulate and the anterior insula/fronto-insular cortex (i.e., regions activated when observing pain in others; Singer et al., 2006).”

“Indeed, recent neuropsychological research has demonstrated that the neural activation associated with schadenfreude in response to a rival ’ s misfortune is related to the endorsement of harming behavior (e.g., Singer et al. 2006, Takahashi et al. 2009, Cikara et al. 2011).”

“Moreover, a relationship has been reported between such differences and the presence of higher empathic aptitude in females than males [31,32].”

“In human fMRI experiments, ACC and FI are both activated by paradigms evoking social emotions such as empathy [47], guilt [46], unfairness [ 48 ], humor [60], embarrassing situations or violations of social norms [4], and romantic love [3, 23].”

“, ventral striatum) respond when a competitor receives a painful electric shock (Singer et al., 2006), or when an envied target experiences misfortunes (Takahashi et al.”

“In 12Additionally, Singer et al. (2006) demonstrated that the proposed neural networks subserving empathy indeed represent “true” empathizing with another person, rather than just imagining one’s own emotional experience.”

“For example, affective links (e.g., Singer et al., 2006), perceived similarities (e.g., Perry et al., 2010), and social memberships (e.g., Xu et al., 2009) are likely to modulate the level of empathy experienced by the observer toward agent’s pain.”