1 2 A neurobiological association of revenge propensity during intergroup conflict 3 4 Xiaochun Hana, Michele J. Gelfandb, Bing Wuc, Ting Zhanga, Wenxin Lid, Tianyu Gaoa, 5 Chenyu Panga, Taoyu Wua, Yuqing Zhoua, Shuai Zhouc, Xinhuai Wuc,1, Shihui Hana,1 6 7 aSchool of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain 8 Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, 9 China 10 bDepartment of Psychology, University of Maryland, USA c 11 Department of Radiology, The 7th Medical Center of PLA General Hospital, Beijing, China 12 dPeking-Tsinghua Center for Life Sciences, Peking University, Beijing, China 13 14 15 16 Address correspondence to: 17 Shihui Han Ph.D. Prof. 18 School of Psychological and Cognitive Sciences 19 Peking University 20 52 Haidian Road, Beijing 100080, China 21 Phone: (86) 10-6275-9138 22 Email: [email protected] 23 or 24 Xinhuai Wu. M.D. 25 Department of Radiology 26 PLA Army General Hospital 27 5 Nanmencang, Beijing, 100070, China 28 Phone: (86) 10-8400-8368 29 Email: [email protected] 30 1 31 Abstract 32 Revenge during intergroup conflict is a human universal, but its neurobiological 33 underpinnings remain unclear. We address this by integrating functional MRI and 34 measurements of endogenous oxytocin in participants who view an ingroup and an outgroup 35 member's suffering that is caused mutually (Revenge group) or respectively by a computer 36 (Control group). We show that intergroup conflict encountered by the Revenge group is 37 associated with an increased level of oxytocin in saliva compared to in the Control group. 38 Furthermore, the medial prefrontal activity in response to ingroup pain in the Revenge but not 39 Control group mediates the association between endogenous oxytocin and the propensity to 40 give painful electric shocks to outgroup members regardless of whether they were directly 41 involved in the conflict. Our findings highlight an important neurobiological correlate of 42 revenge propensity which may be implicated in conflict contagion across individuals in the 43 context of intergroup conflict. 44 2 45 Revenge, which refers to taking actions of harming someone in retaliation for an 46 injury (Elshout et al., 2015; Jackson et al., 2019), is a global phenomenon and a causal factor 47 in many homicides and transgenerational conflicts (Kopsaj, 2016; Jackson et al., 2019). 48 While revenge is an aggressive act, not all aggressive acts represent vengeance. For example, 49 unsolicited acts of aggression, like deviance, incivility, and bullying, would not count as 50 revenge (Raver and Barling, 2008; Jackson et al., 2019). Revenge often occurs between 51 families or clans when an outgroup member brings harm to an ingroup member which, in 52 turn, induces retaliation upon outgroup members (Ericksen and Horton, 1992). According to 53 early social psychological theories (Allport et al., 1954; Brewer, 1999), a desire to help the 54 ingroup (“ingroup love”) and/or an aggressive motivation to hurt the outgroup (“outgroup 55 hate”) may drive participation in intergroup conflict by taking revenge. Recent behavioral 56 research using economic games indeed suggests that ingroup love plays a key role in driving 57 economic punishment toward outgroup (Halevy et al., 2008; de Dreu, 2010; De Dreu et al., 58 2010; Halevy et al., 2012). Yet despite the severe social consequences of revenge, its 59 neurobiological underpinnings remain unclear. Building upon previous findings (Halevy et al., 60 2008; de Dreu, 2010; De Dreu et al., 2010; Halevy et al., 2012), we suggest that there may 61 be a neurobiological mechanism that links perceived ingroup pain caused by an outgroup and 62 the propensity to seek revenge upon an outgroup during intergroup conflict. The present work 63 specifically examined the hormonal (i.e., oxytocin) and neural responses to ingroup suffering 64 caused by an outgroup that predict revenge propensity against outgroups. 65 Previous brain imaging research has revealed neural responses to ingroup/outgroup 66 members' suffering, yet they have been done in contexts that lack the key character of real- 67 life intergroup conflict, i.e., ingroup and outgroup members causing each others' pain. 68 Functional magnetic resonance imaging (fMRI) studies have identified increased activity in 69 both the empathy network (e.g., the anterior midcingulate (aMCC) and anterior insula (AI)) 3 70 and theory-of-mind network (e.g., the medial prefrontal cortex (mPFC) and temporoparietal 71 junction (TPJ)) in response to ingroup pain (Hein et al., 2010; Cikara et al., 2011; Han, 72 2018). Outgroup pain, on the other hand, is related to enhanced activity in the reward system 73 (e.g., the ventral striatum and nucleus accumbens, Hein et al., 2010; Cikara et al., 2011; Luo 74 et al., 2015). In addition, the mPFC activity in response to perceived pain is associated with 75 decisions to help ingroup members (Hein et al., 2010; Mathur et al., 2010), and the activity 76 in the nucleus accumbens predicts decisions not to help outgroup members (Hein et al., 2010; 77 Luo et al., 2015). These findings highlight ingroup favoritism in brain responses to others' 78 pain as neural underpinnings of ingroup love but leave open a critical question: Are brain 79 responses to ingroup pain inflicted by outgroup members during intergroup conflict 80 associated with subsequent revenge? Specifically, it is unclear whether activities in the 81 empathy and/or theory-of-mind networks in response to perceived ingroup pain are 82 associated with revenge motives during intergroup conflict. If revenge aims to bring suffering 83 to an outgroup to get reward during intergroup conflict, one may expect the involvement of 84 the reward system in decision making related to outgroup punishment (Hein et al., 2010; 85 Cikara et al., 2011; Han, 2018). However, if the goal of revenge is to help ingroup members 86 who suffer from physical harm caused by an outgroup (Lickel et al., 2006), the mPFC, which 87 responds to ingroup pain and is associated with ingroup help (Hein et al., 2010; Mathur et al., 88 2010), may be associated with tendencies to punish the outgroup. 89 Previous fMRI research has also examined neurobiological correlates of punishment 90 decision-making pertaining to those who have violated social norms in economic games 91 (Seymour et al., 2007; Krueger and Hoffman, 2016). Punishment decisions to prevent social 92 norm violations have been associated with increased activities in both the empathy and 93 theory-of-mind networks including the aMCC, AI, and mPFC (Krueger and Hoffman, 2016). 94 Yet these studies focused on brain activities related to punishment decisions rather than 4 95 neurobiological mechanisms that link perceived ingroup suffering to propensity to seek 96 revenge upon outgroups. Punishment decisions during previously studied economic games 97 were likely motivated by prevention of social norm violations rather than by perceived 98 physical harm to ingroup members caused by outgroup members, which characterizes most 99 of revenge behavior in real-life situations. 100 Finally, at the hormone level, recent research reported increased levels of urinary 101 oxytocin (OT) ù a nine amino acid peptide synthesized in hypothalamic cells ù in 102 Chimpanzees immediately before and during border patrols and intergroup encounters 103 (Samuni et al., 2017). Likewise, intranasal administration of OT (vs. placebo) in humans 104 enhanced empathic neural responses to ingroup pain (Sheng et al., 2013) and individuals’ 105 contributions to ingroup payoffs (De Dreu et al., 2010; de Dreu, 2010). OT administration 106 also promotes motivation to sacrifice outgroup targets (De Dreu et al., 2011) and facilitates 107 within-group coordination for successful outgroup attack during economic games (Zhang et 108 al., 2019). These findings shed light on a functional role of the oxytocinergic system in 109 decision making related to outgroup punishment. However, there has been little direct 110 evidence for modulations of endogenous OT in humans during intergroup conflict (but see 111 Levy et al., 2016). In addition, neural architectures that mediate endogenous OT and revenge 112 propensity during intergroup conflict have been largely unexplored. Among the brain regions 113 in which activities are sensitive to ingroup pain, the mPFC contains OT-sensitive neurons 114 (Ninan, 2011). The mPFC, cingulate, and insula express OT receptors (Gimpl and Fahrenholz, 115 2001; MacDonald and MacDonald, 2010; Boccia et al., 2013) and mPFC/aMCC activities 116 are modulated by administered OT (Sabihi et al., 2014; Eckstein et al., 2015; Liu et al., 2017; 117 Wang et al., 2017). However, to date, whether the neural systems involved in empathy or 118 theory-of-mind link endogenous OT to revenge propensity during intergroup conflict has yet 119 to be examined. 5 120 A key challenge to empirically address these issues is the need for an experimental 121 paradigm of intergroup conflict that can be used in a neuroimaging laboratory setting to 122 measure neurobiological responses to perceived ingroup physical pain caused by an outgroup 123 and revenge propensity to bring physical harm to the outgroup. Another challenge for 124 empirical research on the neurobiological association of revenge propensity during intergroup 125 conflict is to disentangle the effect of the key component of revenge (i.e., to punish outgroup 126 members for their harming to one's ingroup) from other concomitant but nonessential factors, 127 including perceived group identity (Kahn et al., 2017), negative evaluation of the outgroup 128 (Schiller et al., 2014), and decreased empathy for outgroup pain (Hein et al., 2010; Cikara et 129 al., 2011; Han, 2018). These factors themselves may lead to negative treatment of outgroup 130 members based on ingroup biases in social behavior that occur even in the absence of 131 intergroup conflict. It is therefore necessary to examine neurobiological responses in two 132 conditions in which ingroup biases in emotions, attitudes, and behavior are matched but the 133 motive to punish the outgroup is different.