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

“At the same time, however, such intergroup bias may also create feelings of deprivation and resentment in outgroups, who may respond with hostility toward the discriminating ingroup (De Dreu, 2012; Dovidio & Gaertner, 2010; Fiske, 2002; Wildschut, Pinter, Vevea, Insko, & Schopler, 2003).”

“…conducted in individuals with a history of personal adversity, suggest that in some contexts exogenous oxytocin can have asocial or negative consequences (Bartz et al. 2011), including increasing the perception of threat in the presence of individuals from other social groups (De Dreu 2012).”

“In economic games, intranasal oxytocin also reduces the likelihood of men to cooperate with out-group members when they become a threat to in-group members (De Dreu 2012, De Dreu et al. 2010, De Dreu & Kret 2016).”

“However, the behavioral effects of oxytocin have been questioned by complex findings from those studies, as detailed in many reviews (De Dreu, 2012; Macdonald and Feifel, 2013; Bethlehem et al., 2014; Bernaerts et al., 2017; Hurlemann and Grinevich, 2018).”

“Thus, by some accounts, oxytocin’s facilitation of this response is largely parochial, leading to in-group favoritism and ethnocentric behavior (De Dreu, 2012).”

“This work on how hormone levels are affected by interactions in the laboratory has now been supplemented by exciting work investigating how hormones affect behavior (de Dreu 2012).”

“…(Hurlemann et al., 2010; Kemp and Guastella, 2011; Striepens et al., 2011), although this can be context- and person-dependent (Bartz et al., 2011), since OXT can also promote risk aversion (Declerck et al., 2010) and noncooperation toward individuals perceived as outsiders (De Dreu, 2012).”

“Together, these findings point to a recursive and reinforcing cycle between positive within-group exchange on the one hand and oxytocin release on the other (52).”

“…and this in turn may be driven by the same neurobiological circuitries as other forms of group-serving behaviors such as parochial altruism, social attachment, and parental care (Madden and Clutton-Brock, 2011; De Dreu, 2012a). al., 2005; Ludwig and Leng, 2006; Donaldson and Young, 2008).”

“Oxytocin often increases trust, willingness to cooperate, and prosocial tendencies (De Dreu, 2012), though possibly only for in-group members (De Dreu and Kret, 2016).”

“The anxiolytic effect of oxytocin is proposed to facilitate social cohesion during highly risky situations that might otherwise precipitate defection away from threat (4).”

“…might themselves be directly sensitive to motivational state—for instance, it has been suggested that the amygdala’s sensitivity to the neuromodulator oxytocin will change its responding in the face of social threats or opportunities (De Dreu, 2012), and this could affect dopamine responding.”

“…of either actual Biological Reviews 91 (2016) 390–408 © 2015 Cambridge Philosophical Society families, or ‘psychological kinship’ (Bailey & Wood, 1998) systems of direct and indirect reciprocity (Alexander, 1987; Zak & Barraza, 2013), in each case generating ‘us and them’ dynamics (De Dreu, 2012).”

“Hormones are known to affect and be affected by a variety of social challenges in a range of species, and to be generally important in recognition, territorial aggression, stress, and behavioral interactions (De Dreu 2012; Oliveira and Oliveira 2014).”

“Ingroup favoritism and defense appear to have a neurobiological basis, being enhanced by the neuropeptide oxytocin, which promotes trust by dampening amygdala activity and up-regulates circuitries involved in empathy (De Dreu 2011; De Dreu et al. 2010, 2011).”

“Altogether, these findings are consistent with the in-group vs. out of group OT theory in humans (De Dreu, 2012), with OT’s positive actions toward existing social partners and negative actions toward unfamiliar partners.”

“It has been suggested that oxytocin upregulates behavioral expressions of concern for others more strongly if the other belongs to the in-group (De Dreu, 2012).”

“This result is surprising given that OT typically shows a positive rather than negative association with affiliative behaviors (Crockford et al., 2013; Insel, 2010; Snowdon et al., 2010; but see Bartz et al., 2011; De Dreu, 2012; Mustoe et al., 2015).”

“To investigate whether oxytocin may play a role in IPV inclinations, we adopted an interactionist approach drawn from human research on nonromantic relationships (Bartz, Zaki, et al., 2011; also see De Dreu, 2012).”

“…motivates parochial cooperation and empathy with in-group members over out-group members, increases defensive aggression on behalf of in-groups (De Dreu, 2012), and has been implicated in heightened maternal aggression in defense of children (Hahn-Holbrook, Holt-Lunstad, Holbrook, Coyne, &…”

“Importantly, these two functions transcend mammalian species, and have been documented in voles, rats, sheep, and (non)human primates (Carter, 2014; De Dreu, 2012; Donaldson & Young, 2008).”

“IN-OT has been reliably shown to improve facial emotional recognition (e.g. Guastella et al., 2008; Marsh et al., 2010; Domes et al., 2014) and to promote in-group cooperation (e.g. De Dreu et al., 2010, 2011; De Dreu, 2012; Ma et al., 2015a).”

“…(anxiolytic effects; e.g., Kosfeld et al., 2005; Baumgartner et al., 2008; Ditzen et al., 2009; Strathearn et al., 2009; Hurlemann et al., 2010; De Dreu, 2012; Fischer-Shofty et al., 2012; Tops et al., 2013; Bethlehem et al., 2014; Preckel et al., 2014; ShamayTsoory and Abu-Akel, 2016; Feldman,…”

“In nonhuman animals, oxytocin actually promotes aggression toward intruders (Pedersen 2004), and in humans, it increases negative emotions , like envy and gloating, toward competitors (Shamay- Tsoory et al. 2009) and aggressive behavior toward outgroup members (De Dreu 2012).”

“In humans (De Dreu, 2012; Nagasawa et al., 2009) and chimpanzees (Samuni et al., 2017), there is evidence that the OT system has been co-opted outside of maternal and reproductive contexts to facilitate cooperation with a broader range of social partners (reviewed in Trumble et al., 2015).”

“As shown here, and elsewhere [17,36,40,49], oxytocin appears pivotal in up-regulating the human response to (arbitrary) in-group/outgroup distinctions, shifting the focus from protecting and promoting oneself towards protecting and promoting the (members of the) in-group [50].”

“Because group- level cooperation is associated with out- group competition, GCs might trigger increases in social behavior toward group members and aggression/avoidance toward other individuals at the same time (sensu De Dreu, 2012).”

“There is accumulating evidence that OT is associated with detection of and response to socially salient stimuli, fostering behavioral responses that may range from social recognition to social avoidance and bias [69,154].”

“In addition, De Dreu and colleagues have found that oxytocin administration facilitates ingroup favoritism that implicitly disfavors highly threatening outgroups (De Dreu, 2012; De Dreu et al., 2010; Shalvi & De Dreu, 2014).”

“Research in non-human primates as well as in humans (Bartz et al., 2011; De Dreu, 2012; Guastella et al., 2012; Heinrichs and Domes, 2008; Insel, 2010; MacDonald and Feifel, 2013; Meyer- Lindenberg et al., 2011) suggests that OT might be an important component of the neuroendocrinological…”

“…effects on brain regions such as the amygdala, anterior insula, anterior cingulate cortex, inferior frontal gyrus and inferior parietal lobe (De Dreu 2012; Sofroniew 1983; Zink and Meyer-Lindenberg 2012), all of which seem to be involved in emotional contagion in humans (Bastiaansen et al.…”

“Indeed, work in our laboratory, and that of others, has linked in-group biased group psychology to the evolutionary ancient and structurally preserved neuropeptide oxytocin (for reviews see De Dreu, 2012; De Dreu and Kret, 2016).”

“For example, OXT specifically enhances in-group favoritism and parochial cooperation (De Dreu, 2012; Ma et al., 2014) and in-group conformity (Stallen et al., 2012).”

“…been found to modulate social distance between males and females (Scheele et al., 2012), increase memory for facial identity (Savaskan et al., 2008), increase attention to social cues (Leknes et al., 2012), motivate in-group cooperation (De Dreu, 2012), and increase generosity (Zak et al., 2007).”

“Rather, the effect of OXT on modulating social behavior appears to be shaped by the nature of the social context during social interactions, and OXT is likely involved in general processing of social stimuli (Bartz et al., 2011; Bethlehem et al., 2014; De Dreu, 2012).”

“For example, stronger oxytocin effects have been found toward in-group than out-group members (Chen et al., 2011; De Dreu, 2012; De Dreu et al., 2012).”

“This finding is in line with research showing paradoxical oxytocin effects, with beneficial effects in safe and supportive settings, but defensive responding and anxiety-enhancing effects in the context of threat (De Dreu, 2012; Grillon et al., 2012).”

“…as manifested in high pro-sociality, is inherently parochial and rooted in intergroup conflict, which gains theoretical support from evolutionary models and simulations (Bowles, 2008; Choi and Bowles, 2007), as well as empirical support from hormonal studies (De Dreu, 2012; De Dreu et al., 2011).”

“Humans are apparently prone to behaving with more affiliation, generosity and trust towards in-group than out-group members, whether they are of the same nationality, tribe, school or sport team (De Dreu, 2012).”

“…to identify key cognitive and neurobiological mechanisms underlying parochialism, including perceptions of threat (Reik et al., 2006) and the role of oxytocin and brain circuits in modulating behavior toward in-and out-178 group members (De Dreu et al., 2010;Baumgartner et al., 2011;De Dreu, 2012).”

“The prosocial effects of OT may be context dependent and may depend on individual characteristics as well as the group status (ingroup vs. outgroup) of an interaction partner (De Dreu, 2012; Marsh et al., 2017).”

“Beyond its role in close relationships, the oxytocinergic system also appears to pattern intergroup behaviour and processes to some extent (De Dreu, 2012).”

“Also, participants typically invest more money when partners look trustworthy, with this trustworthiness assessed by an independent group of raters, indicating that participants believed that certain facial cues were predictive of the reciprocation of trust (Chang and others 2010; van’t Wout and…”

“Additionally, intergroup situations are often characterised by competition between the members of the two groups (e.g., Campbell, 1965; De Dreu, 2012; Deutsch, 1949; Sassenberg, Moskowitz, Jacoby, & Hansen, 2007; Tajfel, Billig, Bundy, & Flament, 1971; Tajfel & Turner, 1979), as well as…”

“In the past five years, various systematic reviews have summarized findings on OT and general social behavior,(46,47) social cognition,(48) behavior and affect,(49) and cooperation.(50)”

“In humans, intranasal oxytocin administration enhances in-group cooperation against an out-group (De Dreu 2012), suggesting that in-group cooperation in the face of an out-group is mediated by the oxytocin system.”

“The results (at least for girls) are generically consistent with current theories, suggesting that OT may be involved in human in-group favouritism (De Dreu et al., 2011; De Dreu et al., 2010; De Dreu, 2012), an association that seems to be present already during childhood.”

“ORIGINAL RESEARCH ARTICLE published: 05 August 2014 doi: 10.3389/fnbeh.2014.00266 Oxytocin increases liking for a country’s people and national flag but not for other cultural symbols or consumer products”

“…empathy and promotes prosocial behaviors, including CA (for other similar reviews of the human oxytocin literature see Bartz et al., 2011; De Dreu, 2012; Feldman, 2012; Guastella and MacLeod, 2012; Kumsta and Heinrichs, 2012; Van IJzendoorn and BakermansKranenburg, 2012; Carter, 2013; for…”

“We do so by manipulating exposure to oxytocin, which was shown to increase pro-social behavior (De Dreu, 2012; Marsh et al., 2015).”

“These studies in humans strongly reinforce the view that the relationship between OXT and prosociality is highly sensitive to social context, especially with regard to the relationship quality between social partners (De Dreu, 2012; Everett, Faber, Crockett, & De Dreu, 2015).”

“In light of potential treatment applications, these observations highlight the importance of combining oxytocin administration with social stimulation (e.g. psychosocial therapy) to perpe-tuate the endogenous oxytocin feedforward-loop 27 .”

“A preference for members from subjects' own-group was found in studies investigating the effect of oxytocin on social behavior and moral decision making (De Dreu et al., 2011; Van IJzendoorn and Bakermans-Kranenburg, 2012).”

“…Guastella, 2011, De Dreu et al., 2014), including pro-social behavior such as cooperation, while (ii) allows to adaptively respond to aversive stimuli and threat by, for example, flight, seeking shelter or, if needed, lashing out to neutralize the threat (De Dreu, 2012b; Striepens et al., 2012).”