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.     

Oxytocin is associated with human trustworthiness

Human beings exhibit substantial interpersonal trust-even with strangers. The neuroactive hormone oxytocin facilitates social recognition in animals, and we examine if oxytocin is related to trustworthiness between humans. This paper reports the results of an experiment to test this hypothesis, where trust and trustworthiness are measured using the sequential anonymous "trust game" with monetary payoffs. We find that oxytocin levels are higher in subjects who receive a monetary transfer that reflects an intention of trust relative to an unintentional monetary transfer of the same amount. In addition, higher oxytocin levels are associated with trustworthy behavior (the reciprocation of trust). Absent intentionality, both the oxytocin and behavioral responses are extinguished. We conclude that perceptions of intentions of trust affect levels of circulating oxytocin.     

Oxytocin Effect on Collective Decision Making: A Randomized Placebo Controlled Study

Collective decision making often benefits both the individuals and the group in a variety of contexts. However, for the group to be successful, individuals should be able to strike a balance between their level of competence and their influence on the collective decisions. The hormone oxytocin has been shown to promote trust, conformism and attention to social cues. We wondered if this hormone may increase participants’ (unwarranted) reliance on their partners’ opinion, resulting in a reduction in collective benefit by disturbing the balance between influence and competence. To test this hypothesis we employed a randomized double-blind placebo-controlled design in which male dyads self-administered intranasal oxytocin or placebo and then performed a visual search task together. Compared to placebo, collective benefit did not decrease under oxytocin. Using an exploratory time dependent analysis, we observed increase in collective benefit over time under oxytocin. Moreover, trial-by-trial analysis showed that under oxytocin the more competent member of each dyad was less likely to change his mind during disagreements, while the less competent member showed a greater willingness to change his mind and conform to the opinion of his more reliable partner. This role-dependent effect may be mediated by enhanced monitoring of own and other’s performance level under oxytocin. Such enhanced social learning could improve the balance between influence and competence and lead to efficient and beneficial collaboration.     

Oxytocin Enhances Social Persuasion during Hypnosis

It has long been argued that hypnosis cannot promote behaviors that people will not otherwise engage in. Oxytocin can enhance trust in others, and may promote the extent to which a hypnotized person complies with the suggestion of a hypnotist. This double-blind placebo study administered oxytocin or placebo to high hypnotizable participants (N = 28), who were then administered hypnotic suggestions for socially unorthodox behaviors, including swearing during the experiment, singing out loud, and dancing in response to a posthypnotic cue. Participants who received oxytocin were significantly more likely to swear and dance than those who received the placebo. This finding may be interpreted in terms of oxytocin increasing social compliance in response as a function of (a) increased trust in the hypnotist, (b) reduced social anxiety, or (c) enhanced sensitivity to cues to respond to experimental expectations. These results point to the potential role of oxytocin in social persuasion.     

Oxytocin promotes attention to social cues regardless of group membership

The social saliency account proposes that oxytocin (OT) plays a major role in modulating attentional shifts toward social cues at early stages of processing. We investigated how OT promotes early attention toward nonsocial and social stimuli and explored differences between in-group- and out-group-related social cues. After participants intranasally self-administered OT or placebo, they were eye-tracked while observing a nonsocial and social cues that were assigned to the in- or out-group by a minimal group paradigm. Participants under placebo did not differ in their fixation durations between stimuli, whereas participants administered OT increased gaze durations toward social but not nonsocial stimuli. In this early stage of processing, no in-group bias occurred: in-group- and out-group-related social cues were fixated equally long. These findings support that OT works by a simple illumination of social cues that seem to be processed regardless of social identity aspects at early stages of attention.     

Oxytocin Receptor Gene Polymorphisms Are Associated with Human Directed Social Behavior in Dogs (Canis familiaris)

The oxytocin system has a crucial role in human sociality; several results prove that polymorphisms of the oxytocin receptor gene are related to complex social behaviors in humans. Dogs'' parallel evolution with humans and their adaptation to the human environment has made them a useful species to model human social interactions. Previous research indicates that dogs are eligible models for behavioral genetic research, as well. Based on these previous findings, our research investigated associations between human directed social behaviors and two newly described (−212AG, 19131AG) and one known (rs8679684) single nucleotide polymorphisms (SNPs) in the regulatory regions (5′ and 3′ UTR) of the oxytocin receptor gene in German Shepherd (N = 104) and Border Collie (N = 103) dogs. Dogs'' behavior traits have been estimated in a newly developed test series consisting of five episodes: Greeting by a stranger, Separation from the owner, Problem solving, Threatening approach, Hiding of the owner. Buccal samples were collected and DNA was isolated using standard protocols. SNPs in the 3′ and 5′ UTR regions were analyzed by polymerase chain reaction based techniques followed by subsequent electrophoresis analysis. The gene–behavior association analysis suggests that oxytocin receptor gene polymorphisms have an impact in both breeds on (i) proximity seeking towards an unfamiliar person, as well as their owner, and on (ii) how friendly dogs behave towards strangers, although the mediating molecular regulatory mechanisms are yet unknown. Based on these results, we conclude that similarly to humans, the social behavior of dogs towards humans is influenced by the oxytocin system.     

Oxytocin increases generosity in humans

Human beings routinely help strangers at costs to themselves. Sometimes the help offered is generous-offering more than the other expects. The proximate mechanisms supporting generosity are not well-understood, but several lines of research suggest a role for empathy. In this study, participants were infused with 40 IU oxytocin (OT) or placebo and engaged in a blinded, one-shot decision on how to split a sum of money with a stranger that could be rejected. Those on OT were 80% more generous than those given a placebo. OT had no effect on a unilateral monetary transfer task dissociating generosity from altruism. OT and altruism together predicted almost half the interpersonal variation in generosity. Notably, OT had twofold larger impact on generosity compared to altruism. This indicates that generosity is associated with both altruism as well as an emotional identification with another person.     

Bonobos Share with Strangers

Humans are thought to possess a unique proclivity to share with others – including strangers. This puzzling phenomenon has led many to suggest that sharing with strangers originates from human-unique language, social norms, warfare and/or cooperative breeding. However, bonobos, our closest living relative, are highly tolerant and, in the wild, are capable of having affiliative interactions with strangers. In four experiments, we therefore examined whether bonobos will voluntarily donate food to strangers. We show that bonobos will forego their own food for the benefit of interacting with a stranger. Their prosociality is in part driven by unselfish motivation, because bonobos will even help strangers acquire out-of-reach food when no desirable social interaction is possible. However, this prosociality has its limitations because bonobos will not donate food in their possession when a social interaction is not possible. These results indicate that other-regarding preferences toward strangers are not uniquely human. Moreover, language, social norms, warfare and cooperative breeding are unnecessary for the evolution of xenophilic sharing. Instead, we propose that prosociality toward strangers initially evolves due to selection for social tolerance, allowing the expansion of individual social networks. Human social norms and language may subsequently extend this ape-like social preference to the most costly contexts.     

Song matching in the great tit (Parus major): The effect of similarity and familiarity

Great tits were played recordings of one of their own songs, and a song of the same type from a neighbour and one from a stranger (from more than 500 m away). The birds matched their own songs most often and those of strangers least. We had predicted that strangers would be matched most, because previous work had shown an association between matching and a strong response. An analysis using a difference index showed that the birds matched most often when the stimulus song was very similar in detailed structure to their own rendition of the song. This was confirmed in a second experiment in which we played ‘similar’ and ‘different’ renditions recorded from strangers. However, once the effect of similarity was partialled out there was a residual tendency to match strangers more than neighbours, as we had first predicted. We discuss the implications of these results for perception of song categories by the birds, possible use by the birds of their own songs as ‘standards’ and the functional significance of matching.     

Oxytocin shapes the neural circuitry of trust and trust adaptation in humans

Trust and betrayal of trust are ubiquitous in human societies. Recent behavioral evidence shows that the neuropeptide oxytocin increases trust among humans, thus offering a unique chance of gaining a deeper understanding of the neural mechanisms underlying trust and the adaptation to breach of trust. We examined the neural circuitry of trusting behavior by combining the intranasal, double-blind, administration of oxytocin with fMRI. We find that subjects in the oxytocin group show no change in their trusting behavior after they learned that their trust had been breached several times while subjects receiving placebo decrease their trust. This difference in trust adaptation is associated with a specific reduction in activation in the amygdala, the midbrain regions, and the dorsal striatum in subjects receiving oxytocin, suggesting that neural systems mediating fear processing (amygdala and midbrain regions) and behavioral adaptations to feedback information (dorsal striatum) modulate oxytocin's effect on trust. These findings may help to develop deeper insights into mental disorders such as social phobia and autism, which are characterized by persistent fear or avoidance of social interactions.     

Oxytocin Motivates Non-Cooperation in Intergroup Conflict to Protect Vulnerable In-Group Members

Intergroup conflict is often driven by an individual''s motivation to protect oneself and fellow group members against the threat of out-group aggression, including the tendency to pre-empt out-group threat through a competitive approach. Here we link such defense-motivated competition to oxytocin, a hypothalamic neuropeptide involved in reproduction and social bonding. An intergroup conflict game was developed to disentangle whether oxytocin motivates competitive approach to protect (i) immediate self-interest, (ii) vulnerable in-group members, or (iii) both. Males self-administered oxytocin or placebo (double-blind placebo-controlled) and made decisions with financial consequences to themselves, their fellow in-group members, and a competing out-group. Game payoffs were manipulated between-subjects so that non-cooperation by the out-group had high vs. low impact on personal payoff (personal vulnerability), and high vs. low impact on payoff to fellow in-group members (in-group vulnerability). When personal vulnerability was high, non-cooperation was unaffected by treatment and in-group vulnerability. When personal vulnerability was low, however, in-group vulnerability motivated non-cooperation but only when males received oxytocin. Oxytocin fuels a defense-motivated competitive approach to protect vulnerable group members, even when personal fate is not at stake.     

Microbial Symbionts Accelerate Wound Healing via the Neuropeptide Hormone Oxytocin

Wound healing capability is inextricably linked with diverse aspects of physical fitness ranging from recovery after minor injuries and surgery to diabetes and some types of cancer. Impact of the microbiome upon the mammalian wound healing process is poorly understood. We discover that supplementing the gut microbiome with lactic acid microbes in drinking water accelerates the wound-healing process to occur in half the time required for matched control animals. Further, we find that Lactobacillus reuteri enhances wound-healing properties through up-regulation of the neuropeptide hormone oxytocin, a factor integral in social bonding and reproduction, by a vagus nerve-mediated pathway. Bacteria-triggered oxytocin serves to activate host CD4+Foxp3+CD25+ immune T regulatory cells conveying transplantable wound healing capacity to naive Rag2-deficient animals. This study determined oxytocin to be a novel component of a multi-directional gut microbe-brain-immune axis, with wound-healing capability as a previously unrecognized output of this axis. We also provide experimental evidence to support long-standing medical traditions associating diet, social practices, and the immune system with efficient recovery after injury, sustained good health, and longevity.     

Oxytocin and vasopressin are dysregulated in Williams Syndrome, a genetic disorder affecting social behavior

The molecular and neural mechanisms regulating human social-emotional behaviors are fundamentally important but largely unknown; unraveling these requires a genetic systems neuroscience analysis of human models. Williams Syndrome (WS), a condition caused by deletion of ~28 genes, is associated with a gregarious personality, strong drive to approach strangers, difficult peer interactions, and attraction to music. WS provides a unique opportunity to identify endogenous human gene-behavior mechanisms. Social neuropeptides including oxytocin (OT) and arginine vasopressin (AVP) regulate reproductive and social behaviors in mammals, and we reasoned that these might mediate the features of WS. Here we established blood levels of OT and AVP in WS and controls at baseline, and at multiple timepoints following a positive emotional intervention (music), and a negative physical stressor (cold). We also related these levels to standardized indices of social behavior. Results revealed significantly higher median levels of OT in WS versus controls at baseline, with a less marked increase in AVP. Further, in WS, OT and AVP increased in response to music and to cold, with greater variability and an amplified peak release compared to controls. In WS, baseline OT but not AVP, was correlated positively with approach, but negatively with adaptive social behaviors. These results indicate that WS deleted genes perturb hypothalamic-pituitary release not only of OT but also of AVP, implicating more complex neuropeptide circuitry for WS features and providing evidence for their roles in endogenous regulation of human social behavior. The data suggest a possible biological basis for amygdalar involvement, for increased anxiety, and for the paradox of increased approach but poor social relationships in WS. They also offer insight for translating genetic and neuroendocrine knowledge into treatments for disorders of social behavior.     

'Nasty neighbours' rather than 'dear enemies' in a social carnivore

Territorial animals typically respond less aggressively to neighbours than to strangers. This 'dear enemy effect' has been explained by differing familiarity or by different threat levels posed by neighbours and strangers. In most species, both the familiarity and the threat-level hypotheses predict a stronger response to strangers than to neighbours. In contrast, the threat-level hypothesis predicts a stronger response to neighbours than to strangers in species with intense competition between neighbours and with residents outnumbering strangers, as commonly found in social mammals such as the banded mongoose (Mungos mungo). The familiarity hypothesis predicts reduced aggression towards neighbours also in these species. We exposed free-living banded mongoose groups to translocated scent marks of neighbouring groups and strangers. Groups vocalized more and inspected more samples in response to olfactory cues of the neighbours than to the strangers. Our results support the threat-level hypothesis and contradict the familiarity hypothesis. We suggest that increased aggression towards neighbours is more common in social species with intense competition between neighbours, as opposed to reduced aggression towards neighbours typical for most solitary species.     

The role of tracking and tolerance in relationship among friends

Friendship is a core aspect of human social life. Friends form long-term, cooperative relationships, and provide material and emotional support for one another. Previous research in social psychology suggests that people prefer balanced relationships over unbalanced relationship with friends, but at the same time, friendship is defined by an absence of direct reciprocity and careful tracking of favors given and received. The goal of this study was to distinguish between differences in tracking and tolerance of imbalances among friends and strangers. We conducted parallel behavioral economic experiments in three different urban cultural settings, USA, Japan and China, in an effort to expand our understanding of the dynamics of human friendship. Across all sites, we found that subjects monitored their friends less carefully than they monitored strangers, were more generous to friends than to strangers and that friends were more tolerant of imbalances in payoffs than strangers were. Although there were differences in the extent of tracking among friends and strangers, tracking did occur among friends. Our study extends the understanding on the dynamics of human friendship and emphasizes the need for further investigation on how friends balance vigilance and tolerance in real-life interactions.     

Assessing the effects of social environment on blood pressure and heart rates of baboons

The objective of this publication is to report on the feasibility of using a tether system for obtaining data on blood pressure and heart rates of socially housed primates and to evaluate the extent to which housing environment alters cardiovascular responses (mean arterial blood pressure and heart rate). Blood pressure and heart rates of adult male baboons (Papio cynocephalus hamadryas) were evaluated over a 6 week period under three different housing conditions: social companion, individual, and socially unfamiliar. Social environment was manipulated in a specially designed cage that incorporated removable panels of either woven wire or solid sheet metal. The design of the cage permitted nonhuman primates to engage in species-typical social behaviors such as grooming and aggression. Using a tether and catheter system, we monitored cardiovascular physiology. We tested the hypothesis that individual housing, housing with social companions, and housing with social strangers would produce different mean arterial blood pressure and heart rate responses. Individual housing and housing with strangers produced resting mean arterial blood pressures that were elevated relative to blood pressure responses with social companions. Individual housing and housing with social strangers produced different patterns of cardiovascular response. Individual housing resulted in lowered heart rates and elevated blood pressures relative to the social companion condition. Housing with social strangers resulted in both elevated blood pressure and elevated heart rate, relative to the social companion condition. Responses observed during this study demonstrated the sensitivity of blood pressure and heart rates to differences in social environment.     

Operant conditioning of skin resistance tonic levels

The purpose of the current investigation was to determine whether increases and decreases in skin resistance tonic level could be controlled by individuals given discrete visual feedback of such activity. Thirty-six male undergraduate students served as subjects. They were assigned randomly in equal numbers to four groups; two of the groups received accurate feedback of skin resistance level changes and two received inaccurate feedback. The two accurate-feedback groups differed with respect to the order in which increases and decreases in skin resistance level were reinforced. Each noncontingent group was matched with one of the contingent groups in terms of reinforcement density. The results indicated that accurate feedback produced skin resistance level changes consistent with the type of reinforcement employed. However, operant control was not clearly sustained subsequent to a reversal in the type of tonic level change reinforced. Some problems related to the clinical application of skin resistance level training are discussed.Portions of this paper were presented at the meeting of the Midwestern Psychological Association, Chicago, 1973.     

Oxytocin Increases the Influence of Public Service Advertisements

This paper presents a neurophysiologic model of effective public service advertisements (PSAs) and reports two experiments that test the model. In Experiment 1, we show that after watching 16 PSAs participants who received oxytocin, compared to those given a placebo, donated to 57% more causes, donated 56% more money, and reported 17% greater concern for those in the ads. In Experiment 2, we measured adrenocorticotropin hormone (ACTH) and oxytocin levels in blood before and after participants watched a PSA. As predicted by the model, donations occurred when participants had increases in both ACTH and oxytocin. Our results indicate that PSAs with social content that cause OT release will be more effective than those that do not. Our results also explain why some individuals do not respond to PSAs.     

The UNSIN project: exploring the molecular physiology of sins

Although active learning works, promoting it in large undergraduate science classes is difficult. Here, three students (F. Naji, L. Salci, and G. Hoit) join their teacher (P. K. Rangachari) in describing one such attempt. Two cohorts in a first-year undergraduate biology course explored the molecular underpinnings of human misbehavior. Students were divided into 18 groups and randomly allotted to deal with one of the four deadly sins: sloth, gluttony, lust, and wrath. Students were expected to read primary sources to devise molecular ways to counter these sins. Group progress was monitored over the 12-wk period by the preceptor (P. K. Rangachari) at scheduled intervals. A single randomly selected student was questioned about the work done, and future directions were provided by the preceptor. At the end of the term, randomly selected students defended their group's approaches to the entire class. A final written report was graded. The following multiple target molecules were considered for each sin: gluttony (cholecystokinin, ghrelin, GABA, leptin, peptide YY, neuropeptide Y, and the melanocortin 4 receptor); sloth (dopamine, glutamate, GABA, and orexin); wrath (serotonin, GABA, glutamate, and corticotropin-releasing hormone receptor 2); and lust (prolactin, testosterone, oxytocin, dopamine, and estrogen). Students noted that the project provided a valuable learning experience, and the random selection approach gave students a greater sense of responsibility to their group. The project helped students hone their skills at searching, synthesizing, sharing, and presenting information, fostered group interactions, and provided a solid knowledge base for subsequent courses.     

Operant conditioning of skin resistance tonic levels

The purpose of the current investigation was to determine whether increases and decreases in skin resistance tonic level could be controlled by individuals given discrete visual feedback of such activity. Thirty-six male undergraduate students served as subjects. They were assigned randomly in equal numbers to four groups; two of the groups received accurate feedback of skin resistance level changes and two received inaccurate feedback. The two accurate-feedback groups differed with respect to the order in which increases and decreases in skin resistance level were reinforced. Each noncontingent group was matched with one of the contingent groups in terms of reinforcement density. The results indicated that accurate feedback produced skin resistance level changes consistent with the type of reinforcement employed. However, operant control was not clearly sustained subsequent to a reversal in the type of tonic level change reinforced. Some problems related to the clinical application of skin resistance level training are discussed.