Oxytocin modulates cooperation within and competition between groups: an integrative review and research agenda

The author reviews evidence that hypothalamic release (or infusion) of the neuropeptide oxytocin modulates the regulation of cooperation and conflict among humans because of three reasons. First, oxytocin enables social categorization of others into in-group versus out-group. Second, oxytocin dampens amygdala activity and enables the development of trust. Third, and finally, oxytocin up-regulates neural circuitries (e.g., inferior frontal gyrus, ventromedial prefrontal cortex, caudate nucleus) involved in empathy and other-concern. Consistent with an evolutionary perspective on the functionality of cooperation, it is concluded that oxytocin-motivated cooperation is mostly parochial-it motivates (i) in-group favoritism, (ii) cooperation towards in-group but not out-group members, and (iii) defense-motivated non-cooperation towards threatening outsiders. Thus, in addition to its well-known role in reproduction and pair-bond formation, oxytocin's primary functions include in-group "tend-and-defend." This review concludes with avenues for new research on oxytocin's functions in within-group cooperation and between-group competition. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

Fear or greed? Oxytocin regulates inter-individual conflict by enhancing fear in men

People may choose non-cooperation in social dilemmas either out of fear (if others choose to defect) or out of greed (when others choose to cooperate). Previous studies have shown that exogenous oxytocin motivates a “tend and defend” pattern in inter-group conflict in which oxytocin stimulates in-group cooperation and out-group defense. Using a double-blind placebo-controlled design combined with a modified Prisoner's dilemma game (PDG), we examined the effect of oxytocin on social motivations in inter-individual conflict in men. Results showed that compared with the placebo group, oxytocin-exposed participants were less cooperative in general. Specifically, oxytocin amplified the effect of fear on defection but did not influence the effect of greed. Another non-social control study confirmed participants' decisions were sensitive to social factors. Our findings suggest that even when social group conflict is removed, oxytocin promotes distrust of strangers in “me and you” inter-individual conflict by elevating social fear in men.     

Disease avoidance and ethnocentrism: the effects of disease vulnerability and disgust sensitivity on intergroup attitudes

Extending a model relating xenophobia to disease avoidance [Faulkner, J., Schaller, M., Park, J. H., & Duncan, L. A. (2004). Evolved disease-avoidance mechanisms and contemporary xenophobic attitudes. Group Processes & Intergroup Relations, 7(4), 333–353.], we argue that both inter- and intragroup attitudes can be understood in terms of the costs and benefits of interacting with the in-group versus out-groups. In ancestral environments, interaction with members of the in-group will generally have posed less risk of disease transmission than interaction with members of an out-group, as individuals will have possessed antibodies to many of the pathogens present in the former, in contrast to those prevalent among the latter. Moreover, because coalitions are more likely among in-group members, the in-group would have been a potential source of aid in the event of debilitating illness. We conducted two online studies exploring the relationship between disease threat and intergroup attitudes. Study 1 found that ethnocentric attitudes increase as a function of perceived disease vulnerability. Study 2 found that in-group attraction increases as a function of disgust sensitivity, both when measured as an individual difference variable and when experimentally primed. We discuss these results with attention to the relationships among disease salience, out-group negativity, and in-group attraction.     

Cooperation and conflict: field experiments in Northern Ireland

The idea that cohesive groups, in which individuals help each other, have a competitive advantage over groups composed of selfish individuals has been widely suggested as an explanation for the evolution of cooperation in humans. Recent theoretical models propose the coevolution of parochial altruism and intergroup conflict, when in-group altruism and out-group hostility contribute to the group''s success in these conflicts. However, the few empirical attempts to test this hypothesis do not use natural groups and conflate measures of in-group and unbiased cooperative behaviour. We conducted field experiments based on naturalistic measures of cooperation (school/charity donations and lost letters'' returns) with two religious groups with an on-going history of conflict—Catholics and Protestants in Northern Ireland. Conflict was associated with reduced donations to out-group schools and the return of out-group letters, but we found no evidence that it influences in-group cooperation. Rather, socio-economic status was the major determinant of cooperative behaviour. Our study presents a challenge to dominant perspectives on the origins of human cooperation, and has implications for initiatives aiming to promote conflict resolution and social cohesion.     

Oxytocin promotes intuitive rather than deliberated cooperation with the in-group

A contribution to a special issue on Hormones and Human Competition.In intergroup settings, individuals prefer cooperating with their in-group, and sometimes derogate and punish out-groups. Here we replicate earlier work showing that such in-group bounded cooperation is conditioned by oxytocin and extend it by showing that oxytocin-motivated in-group cooperation is intuitive rather than deliberated. Healthy males (N = 65) and females (N = 129) self-administered intranasal placebo or 24 IU oxytocin in a double-blind placebo-controlled between-subjects design, were assigned to a three-person in-group (that faced a 3-person out-group), and given an endowment from which they could contribute to a within-group pool (benefitting the in-group), and/or to a between-group pool (benefitting the in-group and punishing the out-group). Prior to decision-making, participants performed a Stroop Interference task that was either cognitively taxing, or not. Cognitively taxed individuals kept less to themselves and contributed more to the within-group pool. Furthermore, participants receiving placebo contributed more to the within-group pool when they were cognitively taxed rather than not; those receiving oxytocin contributed to the within-group pool regardless of cognitive taxation. Neither taxation nor treatment influenced contributions to the between-group pool, and no significant sex differences were observed. It follows that in intergroup settings (i) oxytocin increases in-group bounded cooperation, (ii) oxytocin neither reduces nor increases out-group directed spite, and (iii) oxytocin-induced in-group cooperation is independent of cognitive taxation and, therefore, likely to be intuitive rather than consciously deliberated.     

Intergroup threat gates social attention in humans

Humans shift their attention to follow another person''s gaze direction, a phenomenon called gaze cueing. This study examined whether a particular social factor, intergroup threat, modulates gaze cueing. As expected, stronger responses of a particular in-group to a threatening out-group were observed when the in-group, conditioned to perceive threat from one of two out-groups, was presented with facial stimuli from the threatening and non-threatening out-groups. These results suggest that intergroup threat plays an important role in shaping social attention. Furthermore, larger gaze-cueing effects were found for threatening out-group faces than for in-group faces only at the 200 ms but not the 800 ms stimulus onset asynchrony (SOA); the specificity of the gaze-cueing effects at the short SOA suggests that threat cues modulate the involuntary component of gaze cueing.     

Positive Feeling,Negative Meaning: Visualizing the Mental Representations of In-Group and Out-Group Smiles

Even though smiles are seen as universal facial expressions, research shows that there exist various kinds of smiles (i.e., affiliative smiles, dominant smiles). Accordingly, we suggest that there also exist various mental representations of smiles. Which representation is employed in cognition may depend on social factors, such as the smiling person’s group membership: Since in-group members are typically seen as more benevolent than out-group members, in-group smiles should be associated with more benevolent social meaning than those conveyed by out-group members. We visualized in-group and out-group smiles with reverse correlation image classification. These visualizations indicated that mental representations of in-group smiles indeed express more benevolent social meaning than those of out-group smiles. The affective meaning of these visualized smiles was not influenced by group membership. Importantly, the effect occurred even though participants were not instructed to attend to the nature of the smile, pointing to an automatic association between group membership and intention.     

Real or Artificial? Intergroup Biases in Mind Perception in a Cross-Cultural Perspective

Recent research suggests that attributions of aliveness and mental capacities to faces are influenced by social group membership. In this article, we investigated group related biases in mind perception in participants from a Western and Eastern culture, employing faces of varying ethnic groups. In Experiment 1, Caucasian faces that ranged on a continuum from real to artificial were evaluated by participants in the UK (in-group) and in India (out-group) on animacy, abilities to plan and to feel pain, and having a mind. Human features were found to be assigned to a greater extent to faces when these belonged to in-group members, whereas out-group faces had to appear more realistic in order to be perceived as human. When participants in India evaluated South Asian (in-group) and Caucasian (out-group) faces in Experiment 2, the results closely mirrored those of the first experiment. For both studies, ratings of out-group faces were significantly predicted by participants’ levels of ethnocultural empathy. The findings highlight the role of intergroup processes (i.e., in-group favoritism, out-group dehumanization) in the perception of human and mental qualities and point to ethnocultural empathy as an important factor in responses to out-groups.     

Social exchange and solidarity: in-group love or out-group hate?

Men exhibit a stronger tendency to favor the in-group over the out-group compared to women. We examined whether this male-specific “coalitional psychology” represents in-group love or out-group hate. One hundred thirty-three college freshmen played a prisoner's dilemma game with a member of their own group and a member of another group. Both groups consisted of same-sex participants. An in-group bias (cooperation with the in-group at a level higher than cooperation with the out-group) based on expectations of cooperation from the in-group was observed for both men and women. When such expectations were experimentally eliminated, women did not show any in-group bias, whereas men still exhibited an in-group bias. This male-specific in-group bias was found to be a product of intragroup cooperation (in-group love) rather than a product of intergroup competition (out-group hate). These findings suggest that the male-specific coalitional psychology caters more toward the promotion of within-group solidarity than aggression against the out-group.     

Social Groups Prioritize Selective Attention to Faces: How Social Identity Shapes Distractor Interference

Human faces automatically attract visual attention and this process appears to be guided by social group memberships. In two experiments, we examined how social groups guide selective attention toward in-group and out-group faces. Black and White participants detected a target letter among letter strings superimposed on faces (Experiment 1). White participants were less accurate on trials with racial out-group (Black) compared to in-group (White) distractor faces. Likewise, Black participants were less accurate on trials with racial out-group (White) compared to in-group (Black) distractor faces. However, this pattern of out-group bias was only evident under high perceptual load—when the task was visually difficult. To examine the malleability of this pattern of racial bias, a separate sample of participants were assigned to mixed-race minimal groups (Experiment 2). Participants assigned to groups were less accurate on trials with their minimal in-group members compared to minimal out-group distractor faces, regardless of race. Again, this pattern of out-group bias was only evident under high perceptual load. Taken together, these results suggest that social identity guides selective attention toward motivationally relevant social groups—shifting from out-group bias in the domain of race to in-group bias in the domain of minimal groups—when perceptual resources are scarce.     

When to diversify,and with whom? Choosing partners among out-group strangers in lowland Bolivia

Evidence from the ethnographic and archaeological records reveals that humans often rely on out-group relationships for access to non-local resources and resource buffering. However, little is known about how actors choose out-group cooperative partners. The existing literature suggests that (in-group) partner choice is based on characteristics associated with greater cooperation (e.g., trustworthiness and productivity). Is out-group partner choice based on the same criteria as in-group? Because out-groups may be unique sources of resource access, we suggest that out-group partner choice should track characteristics of both the candidate partner and the partner's group that are associated with benefits for the actor. To assess partner choice, we employed a non-anonymous, one-shot economic game where participants could allocate money towards in-group and out-group strangers. Participants were from three populations of Bolivian horticulturalists (n = 200) that range in their market integration and their mobility, thus capturing variation in potential benefits to out-group cooperation. We find that individual-level qualities of prospective partners, such as wealth and trustworthiness, affect allocation behavior differently for in-group vs out-group prospective partners. While we find no consistent effects of perceived group qualities on a donor's giving to in-group and out-group members, the relevance of out-group market resource access for Tsimane' donors' allocations suggests that, at least when it comes to dividing a limited resource, qualities associated with a group can affect partner preference. Taken together, results provide insight into patterns of intergroup relationship building that have been crucial in the human lineage.     

The Modulation of Mimicry by Ethnic Group-Membership and Emotional Expressions

Mimicry has been ascribed affiliative functions. In three experiments, we used a newly developed social-affective mimicry task (SAMT) to investigate mimicry´s modulation by emotional facial expressions (happy, angry) and ethnic group-membership (White in-group, Black out-group). Experiment 1 established the main consistent effect across experiments, which was enhanced mimicry to angry out-group faces compared to angry in-group faces. Hence the SAMT was useful for experimentally investigating the modulation of mimicry. Experiment 2 demonstrated that these effects were not confounded by general aspects of response conflict, as a Simon task resulted in different response patterns than the SAMT. Experiment 2 and pooled analysis of Experiments 1 and 2 also corroborated the finding of enhanced mimicry to angry out-group faces. Experiment 3 tested whether this effect was related to perceptions of threat, by framing angry persons as physically threatening, or not. Selective enhancement of mimicry to out-group persons framed as physically threatening confirmed this hypothesis. Further support for the role of threat was derived from implicit measures showing, in all experiments, that black persons were more strongly associated with threat. Furthermore, enhanced mimicry was consistently related to response facilitation in the execution of congruent movements. This suggests that mimicry acted as a social congruency signal. Our findings suggest that mimicry may serve as an appeasement signal in response to negative affiliative intent. This extends previous models of mimicry, which have predominantly focused on its role in reciprocating affiliation. It suggests that mimicry might not only be used to maintain and establish affiliative bonds, but also to ameliorate a negative social situation.     

Cooperation during cultural group formation promotes trust towards members of out-groups

People often cooperate with members of their own group, and discriminate against members of other groups. Previous research establishes that cultural groups can form endogenously, and that these groups demonstrate in-group favouritism. Given the presence of cultural groups, the previous literature argues that cultural evolution selects for groups that exhibit parochial altruism. The source of initial variation in these traits, however, remains uninformed. We show here that a group''s economic production environment may substantially influence parochial tendencies, with groups formed around more cooperative production (CP) displaying less parochialism than groups formed around more independent production (IP) processes. Participants randomized into CP and IP production tasks formed cultural groups, and subsequently played hidden-action trust games with in-group and out-group trustees. We found CP to be associated with significantly greater sharing and exchanging behaviours than IP. In trust games, significant parochial altruism (in-group favouritism combined with out-group discrimination) was displayed by members of IP groups. By contrast, members of CP groups did not engage in either in-group favouritism or out-group discrimination. Further, we found the absence of out-group discrimination in CP to persist even following ‘betrayal’. Finally, belief data suggest that members of CP are not more intrinsically generous than IP members, but rather more likely to believe that out-group trustees will positively reciprocate. Our results have important implications for anyone interested in building cooperative teams, and shed new light on connections between culture and cooperation.     

Altruism toward in-group members as a reputation mechanism

To test the hypothesis that sensitivity to monitoring drives people to act altruistically toward members of their own community, two experiments investigated whether an eye-like painting promotes altruism toward in-group members, but not toward out-group members. Participants played the role of dictator in a dictator game with another participant (a recipient) who was from the minimal in-group or out-group. Participants knew whether their recipient was an in-group member or an out-group member, but were informed that their recipient did not know the group membership of the dictator. In-group favoritism occurred only when participants were facing a computer desktop which displayed a painting of eyes, but did not occur in the absence of eyes. These findings demonstrate that the eye painting displayed on the participant's computer screen worked as a cue for monitoring and thus enhanced the participant's altruistic behavior.     

Neural Correlates of the In-Group Memory Advantage on the Encoding and Recognition of Faces

People have a memory advantage for faces that belong to the same group, for example, that attend the same university or have the same personality type. Faces from such in-group members are assumed to receive more attention during memory encoding and are therefore recognized more accurately. Here we use event-related potentials related to memory encoding and retrieval to investigate the neural correlates of the in-group memory advantage. Using the minimal group procedure, subjects were classified based on a bogus personality test as belonging to one of two personality types. While the electroencephalogram was recorded, subjects studied and recognized faces supposedly belonging to the subject’s own and the other personality type. Subjects recognized in-group faces more accurately than out-group faces but the effect size was small. Using the individual behavioral in-group memory advantage in multivariate analyses of covariance, we determined neural correlates of the in-group advantage. During memory encoding (300 to 1000 ms after stimulus onset), subjects with a high in-group memory advantage elicited more positive amplitudes for subsequently remembered in-group than out-group faces, showing that in-group faces received more attention and elicited more neural activity during initial encoding. Early during memory retrieval (300 to 500 ms), frontal brain areas were more activated for remembered in-group faces indicating an early detection of group membership. Surprisingly, the parietal old/new effect (600 to 900 ms) thought to indicate recollection processes differed between in-group and out-group faces independent from the behavioral in-group memory advantage. This finding suggests that group membership affects memory retrieval independent of memory performance. Comparisons with a previous study on the other-race effect, another memory phenomenon influenced by social classification of faces, suggested that the in-group memory advantage is dominated by top-down processing whereas the other-race effect is also influenced by extensive perceptual experience.     

Exaggerated Intergroup Bias in Economical Decision Making Games: Differential Effects of Primary and Secondary Psychopathic Traits

Psychopathic personality traits are linked with selfish and non-cooperative responses during economical decision making games. However, the possibility that these responses may vary when responding to members of the in-group and the out-group has not yet been explored. We aimed to examine the effects of primary (selfish, uncaring) and secondary (impulsive, irresponsible) psychopathic personality traits on the responses of non-offending participants to the in-group and the out-group (defined in terms of affiliation to a UK University) across a series of economical decision making games. We asked a total of 60 participants to act as the proposer in both the dictator game and the ultimatum game. We found that across both tasks, those who scored highly for secondary psychopathic traits showed an elevated intergroup bias, making more generous offers toward members of the in-group relative to the out-group. An exaggerated intergroup bias may therefore represent a motivational factor for the antisocial behavior of those with elevated secondary psychopathic traits.     

Oxytocin modulates selection of allies in intergroup conflict

In intergroup competition and conflict, humans benefit from coalitions with strong partners who help them to protect their in-group and prevail over competing out-groups. Here, we link oxytocin, a neuropeptide produced in the hypothalamus, to ally selection in intergroup competition. In a double-blind placebo-controlled experiment, males self-administered oxytocin or placebo, and made selection decisions about six high-threat and six low-threat targets as potential allies in intergroup competition. Males given oxytocin rather than placebo viewed high-threat targets as more useful allies and more frequently selected them into their team than low-threat targets.     

Implicit Trust between the Uyghur and the Han in Xinjiang,China

Trust is a vital lubricant that increases the sense of security in social interactions. In this study, we investigated the intergroup trust between the Uyghur and the Han, the two largest ethnic groups in Xinjiang, China, with a Go/No-Go Association Task. Specifically, we instructed Uyghur and Han participants to respond to ethnic faces (Uyghur vs. Han) and trust/distrust words and measured the strength of the automatic associations between the faces and words for both in-group and out-group pairs. As expected, both ethnic groups showed implicit in-group trust and out-group distrust, but the Han group demonstrated stronger in-group trust and out-group distrust toward the Uyghur than the Uyghur group toward the Han. However, the magnitude of distrust of the Han toward the Uyghur was small to medium as compared with that reported by other intergroup relationship research. In addition, participant geographic location was associated with out-group distrust. These findings offer implications for developing effective strategies to encourage trust between conflicting groups.     

The Effects of Within- and Between-Group Competition on Trust and Trustworthiness among Acquaintances

Several studies have indicated that between-group competition is a key stimulator of trust and trustworthiness. Another important but neglected type of competition may also affect trust and trustworthiness: within-group competition, especially competition among acquaintances. The present study investigated the effects of both within- and between-group competition on trust and trustworthiness, which were measured using an investment game played by acquaintances. We found that, compared to the participants'' performance in the non-competition condition, when individuals were motivated to compete with their in-group members or the other groups for financial rewards, they demonstrated more trust. When individuals were motivated to compete with their in-group members, they exhibited lower trustworthiness than in non-competition and between-group competition. In addition, within-group competition decreased the trustor''s payoff while both within- and between- group competition increased the trustee''s payoff. Finally, we found that males trusted their group members more than females.