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].”

“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].”

“The activation in ACC was significant in women ([9, 18, 27]; P , 0.”

“…of previous experience have recently been confirmed by functional magnetic resonance imaging: Seeing the pain of a cooperative confederate activates painrelated brain areas, but seeing the pain of an unfair confederate activates reward-related brain areas, at least in men (Singer et al. 2006).”

“For example, does the neural representation of another person's undeserved pain differ from the neural representation of morally justified or retributive pain (Decety, Michalska, & Akitsuki, 2008; Singer et al., 2006)? Studies of central nervous system activity also offer the promise of testing some of the predictions…”

“From childhood through adulthood, increasingly complex and domain-specific theories form (Reeder 1993), although this increasing sophistication does not always yield greater accuracy (Gilbert & Malone 1995).”

“…fMRI literature, which has so far demonstrated shared somatosensory activations only in secondary somatosensory cortex (e.g., Jackson et al. 2006a; Singer et al. 2006) or in parts of primary somatosensory cortex that are not somatotopically specific for the affected body part (Lamm et al. 2007b).”

“In studies of empathy, it was found that our perception of other people's fairness (from their behavior in an economic game) modulated how much empathy was felt when they were observed to be given painful electric shock, an effect that correlated with activation of the insula (Singer et al. 2006).”

“…See, e.g., Camerer et al. (2005), Borghans et al. (2005) and Hsu et al. (2005), De Quervain et al. (2004), McCLure et al. (2004), Kuhnen/Knutson (2005), Knutson/Peterson (2005), Fehr et al. (2005a, b), Singer et al. (2006) and for a broader social science perspective, Freese et al. (2003).”

“…in response to primary rewards such as food (McClure et al. 2003; O’Doherty et al. 2003), secondary rewards such as money (Kuhnen & Knutson, 2005), and social rewards such as positive social comparison or one’s rivals experiencing pain (Fliessbach et al. 2007; Hein et al. 2010; Singer et al. 2006).”

“This confirms several recent fMRI studies ( Jackson et al., 2005, 2006; Singer et al., 2004, 2006; Botvinick et al., 2005; Morrison et al., 2004), which indicate that ACC and anterior insula activity during the observation of pain is related to the affective aspects of pain processing rather than…”

“2003) and the feeling of pain in others (Frith and Singer 2008; Singer et al. 2006).”

“In the experiments undertaken so far (Wicker et al., 2003; Keysers et al., 2004; Singer et al., 2004a, 2006; Morrison et al., 2004), subjects were neither required to make any explicit judgment about the feelings of the other person (for an exception see Avenanti et al., 2005, commented on by…”

“fMRI experiments have shown that individuals who score higher in a questionnaire measuring their tendency to place themselves in the other person’s shoes activate their MNS more strongly while listening to other people’s problems.(10,11) These results draw the ‘soft’ concept of empathy into ‘hard’ science, which opens…”

“Singer and colleagues[91] engaged participants in a sequential Prisoner’s dilemma game with confederate targets, who would either play the game in a fair or unfair way.”

“Recently, researchers have begun to investigate whether these empathy processes can be modulated by the implicit context of the empathic experience [8,16].”

“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript played an economic game with cooperative and non-cooperative confederates and then watched the confederates inflicted with pain (Singer et al., 2006).”

“In social contexts, NAcc activation has also been observed when people derive pleasure from themisfortune of others (Singer et al., 2006; Takahashi et al., 2009).”

“From Nemiah 1977 ASD: autism spectrum disorder empathic traits ( Jabbi et al. 2007; Saarela et al. 2007; Singer et al. 2004, 2006).”

“However, the empathic neural responses are modulated by affective link between individuals (Singer et al., 2006) and top-down attention to painful cues in stimuli (Gu and Han, 2007; Fan and Han, 2008).”

“…increased rejection rates by impairing emotion regulation (Crockett 2009) or by decreasing the value of an abstract monetary reward (Moretti et al. 2009) relative to the immediate social reward of successfully punishing the unfair proposer (de Quervain et al. 2004, Singer et al. 2006) (see below).”

“EC has been shown to correlate with insular activation while subjects were aware of other people’s pain [46, 47].”

“Third, although we were not able to compare gender differences in the current meta-analysis, males and females have been shown to use different strategies in emotion paradigms (Baron-Cohen and Wheelwright, 2004; Singer et al., 2006; Schulte-Ruther et al., 2008).”

“For male participants, brain regions associated with experiencing ‘‘reward’’ (i.e., left ventral striatum including nucleus accumbens) show positive activation when a competitor receives a painful electric shock (Singer et al., 2006).”

“More importantly, we extended previous findings that showed modulation of empathic brain responses in insular cortices as a function of contextual appraisal and affective link (Singer et al., 2006; Lamm et al., 2007a, b; Hein and Singer, 2008) to the domain of individual trait characteristics.”

“(215), subjects first played a game with a fair and an unfair partner and saw the game partner receive painful stimuli.”

“, and the affective response in an observer can be modified by contex”

“The current view on the functional role of the neural prediction error signal seems to suggest a threshold for error-related activity (similar to perceptual and motor decision making models, (e.g., Schall et al., 2002) that triggers the adjustment of future behavior ( Schultz, 2006 ).”

“A more recent study [33] with the interactive empathy for pain paradigm showed that empathic brain responses in AI and ACC are not restricted to a beloved partner, but also occur when an unknown, but likable person is in pain.”

“…implicated in studies of empathy and compassion (Immordino-Yang, McColl, Damasio, & Damasio, 2009; Lamm et al., 2011; Lutz, Brefczynski-Lewis, et al., 2008; Singer et al., 2006) and predicts helping behavior (Hein, Silani, Preuschoff, Batson, & Singer, 2010; Masten, Morelli, & Eisenberger, 2011).”

“The IFO is also activated when participants observe facial expressions of pain, know a loved one is in pain or experience pain themselves (Singer et al., 2004, 2006; Decety and Jackson, 2004; Botvinick et al., 2005; Jackson et al., 2006; Lamm et al., in press; Saarela et al., in press), with the…”

“, 2002, 2005; Raine and Yang, 2006), social cooperation (Rilling et al., 2002; Singer et al., 2006; Delgado et al., 2005; King-Casas et al., 2005), and social punishment (Sanfey et al.”

“This study (Singer et al. 2006) showed that empathy-related neural responses in AI and dACC were significantly reduced when participants observed unfair players, but only in the male subsample.”

“2007), previous interaction with or empathizing with the ‘‘victim’’ (Singer et al. 2006; Loggia et al. 2008), compassion (Farrow et al.”

“Singer et al. (2006) observed in a study of empathy for pain of other people that both sexes showed activation of similar brain areas during both the self-experience of pain and the observation of painful stimulation of others.”

“…of pain in others can be modulated by a host of factors including attentional demands (Fan and Han, 2008; Gu and Han, 2007), social relationship between individuals (Singer et al., 2006), cognitive appraisal (Lamm et al., 2007), and a priori attitudes towards others (Decety et al., 2009).”

“Singer et al. (2006) have shown that merely observing the punishment of a cheater also activates important components of the human reward system.”

“We feel less empathy, in terms of subjective report and brain activity, if someone who has just treated us unfairly receives pain, especially if we are male (Singer et al. 2006).”

“…the functional circuits involved in empathy (Farrow et al., 2001; Decety and Chaminade, 2003; Shamay- Tsoory et al., 2005b; Vollm et al., 2005; Singer et al., 2006), only complementary data from human lesion studies can provide information about the relative importance of particular…”

“…Batson, & Decety, 2007; Morrison, Lloyd, di Pellegrino, & Roberts, 2004; This content downloaded from 129.215.19.194 on Fri, 13 Dec 2013 06:55:54 AM All use subject to JSTOR Terms and Conditions Morrison, Peelen, & Downing, 2007; Ochsner et al., 2008; Singer et al., 2004; Singer et al., 2006).”

“…(Botvinick et al., 2005; Decety & Ickes, 2009), respectively; however, more recent research has demonstrated that participants exhibit the opposite neural responses when they witness a competitor’s rewards and punishments (de Bruijn et al., 2009; Singer et al., 2006; Takahashi et al., 2009).”

“Similarly, other fMRI studies documented increases in the activation of pain-related regions during observation of a confederate receiving a painful stimulus, but only if the confederate had played fairly in a previous economic game (Singer et al. 2006).”

“Based on previous work showing that the same regions are involved in both direct and observed experiences of physical pain (dACC, anterior insula; Singer et al., 2004, 2006), we expected that regions associated with the distressing experience of social exclusion (dACC, anterior insula; Eisenberger…”

“The same group (297) showed that the empathic brain responses in the anterior insula and anterior cingulate cortex were not restricted to a beloved partner, but also occurred when an unknown but likable person was in pain, which has obvious implications for the doctor-patient interaction.”

“Our results add to the recent findings that the perception of pain can be modulated by attentional demands [18], as well as by social relations between individuals [17].”

“Advances in neuroscience leading to fuller understanding of brain mechanisms associated with pain have now led to recognition that neurophysiological regulation of pain includes responses to the social environment in which pain is experienced (Singer et al., 2006).”

“Moreover, because social-affective responses are modified with respect to our experience of others (Singer et al., 2006), we conjectured that oxytocin on acquired negative affective ratings related to social stimuli.”

“Singer et al. (2004, 2006) subtracted conditions in which subjects receive an electric shock above the tactile threshold from one above the pain Phil.”

“The importance of the OFC in the regulation of empathic responses is also documented by the fMRI results of [9,24] mentioned above, which both required regulation of one’s own emotional evaluation of an aversive situation.”

“In the past few years, however, research has shown the role of shared representations in the domains of pain (Morrison et al. 2004; Singer et al. 2004, 2006; Avenanti et al. 2005, 2006; Botvinick et al. 2005; Jackson et al. 2005; Minio-Paluello et al. 2006; Saarela et al. 2007) and touch (Keysers…”

“Recent work has greatly advanced our understanding of how the brain evaluates fairness and makes decisions based on the cooperative status and intentions of others during two-party economic exchanges (de Quervain et al., 2004; Delgado et al., 2005; King-Casas et al., 2005; Knoch et al., 2006; Sanfey et al., 2003; Sing…”

“Perception–action-coupling, thus, is essential for a number of forms of interpersonal sensitivity, including emotional contagion, empathy, theory of mind (Singer et al., 2006; Vignemont & Singer, 2006) and action and intention 0022-1031/$ - see front matter 2010 Elsevier Inc.”

“However, a recent study has suggested that at least spontaneous empathetic responses towards disliked versus liked persons are also qualitatively different in males and females (Singer et al., 2006).”

“, 2004), as well as on subjective judgments of targets made by perceivers (Singer et al., 2006).”

“…studies that have reported gender differences in the brain during tasks designed to elicit empathy have suggested than men and women may not differ in overall empathic capacity so much as the types of situations under which empathy is elicited (Fukushima & Hiraki , 2006; Singer et al., 2006).”

“This is in line with results from Singer et al. (2006) who report stronger suppression of automatic mirror reactions in response to pain in unfair situations in males than females.”

“…et al., 2003; Dapretto et al., 2006; Lamm et al., 2007; Leslie et al., 2004; Jabbi et al., 2007; Jackson et al., 2006, 2005; Saarela et al., 2006; Singer et al., 2004, 2006; van der Gaag et al., 2007; Wicker et al., 2003) and the model of emotion understanding via action representation proposed…”

“Because empathic activity is modulated by social relations between individuals (Singer et al., 2006), participants in the experiment of Singer et al. (2004) might pay attention to their loved ones even though no explicit tasks were assigned to their partners’ pain.”

“A further unresolved issue relates to the neural mechanisms supporting these various empathy components and the link to costly altruism (de Vignemont and Singer, 2006).”

“Singer et al. (2006) used a trust and reciprocity game to create good and bad reputations for two previously unknown partners.”

“Those defined using the AAL included the insula and the anterior/mid cingulate (Wicker et al., 2003; Singer et al., 2004, 2006; Jabbi et al., 2007; Bastiaansen et al., 2009; Lamm et al., 2011).”