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.     

Oxytocin increases heart rate variability in humans at rest: implications for social approach-related motivation and capacity for social engagement

Context

Oxytocin (OT) plays a key regulatory role in human social behaviour. While prior studies have examined the effects of OT on observable social behaviours, studies have seldom examined the effects of OT on psychophysiological markers such as heart rate variability (HRV), which provides an index of individual’s motivation for social behaviour. Furthermore, no studies have examined the impact of OT on HRV under resting conditions, which provides an index of maximal capacity for social engagement.

Objective

To examine the effects of OT on HRV measures in healthy male participants while at rest. OT was hypothesised to increase HRV, compared to placebo, and that the effects would be greatest for a non-linear measure of HRV (the detrended fluctuation scaling exponent).

Methods

Twenty-one male participants were recruited for this study. Participants were non-smokers, not on any medications and reported no history of psychiatric illness, neurological disorder, or any other serious medical condition (e.g. diabetes, cardiovascular disease). The study employed a randomised, placebo-controlled, within-subject, crossover, experimental design.

Main Outcome Measures

HRV was calculated from electrocardiography under a standardized, 10-minute, resting state condition.

Results

As hypothesised, OT increased HRV and these effects were largest using the detrended fluctuation scaling exponent, a non-linear measure. These changes were observed in the absence of any change in state mood, as measured by the profile of mood states. Importantly, participants were unable to correctly guess which treatment they had been assigned at either of the two assessments.

Conclusions

Together with the broader literature on OT and HRV, findings suggest that acute administration of OT may facilitate a fundamental psychophysiological feature of social behaviour, increasing capacity for social engagement. Findings also suggest that HRV changes may provide a novel biomarker of response to OT nasal spray that can be incorporated into research on response to treatment.     

Oxytocin, vasopressin, and social recognition in mammals

While pheromones may act as social memory signals, oxytocin and vasopressin acting in the brain appear to be critical for the neural processing of olfactory signatures used for social discrimination. Evidence from a variety of laboratories using a range of animal models, as well as an array of molecular and pharmacological techniques, have helped to determine the neuroanatomical and functional roles oxytocin and vasopressin play in social cognition. In this review we discuss the considerable evidence for the roles of oxytocin and vasopressin in social recognition in rats and mice, as well as in offspring recognition in sheep and mate preference in monogamous voles.     

Hormonal systems,human social bonding,and affiliation

Which hormones are implicated in human social bonding and affiliation? And how does field research speak to this issue? We begin by laying out a broad view of how endocrine hormones in general modulate life history allocations of energy and other resources, and the ways in which their neuromodulatory functions must be understood within a broader conceptualization of how they have been shaped to affect allocations. We then turn to four specific hormones or hormone families that have received much attention: oxytocin, opioids, prolactin, and progesterone. Each plays a role in regulating psychological capacities and propensities that underlie individuals' interactions with important social targets. Yet in no case is it clear exactly what regulatory roles these hormones play. We suggest several directions for future research.     

Oxytocin,testosterone, and human social cognition

I describe an integrative social‐evolutionary model for the adaptive significance of the human oxytocinergic system. The model is based on a role for this hormone in the generation and maintenance of social familiarity and affiliation across five homologous, functionally similar, and sequentially co‐opted contexts: mothers with offspring, female and male mates, kin groups, individuals with reciprocity partners, and individuals within cooperating and competing social groups defined by culture. In each situation, oxytocin motivates, mediates and rewards the cognitive and behavioural processes that underlie the formation and dynamics of a more or less stable social group, and promotes a relationship between two or more individuals. Such relationships may be positive (eliciting neurological reward, reducing anxiety and thus indicating fitness‐enhancing effects), or negative (increasing anxiety and distress, and thus motivating attempts to alleviate a problematic, fitness‐reducing social situation). I also present evidence that testosterone exhibits opposite effects from oxytocin on diverse aspects of cognition and behaviour, most generally by favouring self‐oriented, asocial and antisocial behaviours. I apply this model for effects of oxytocin and testosterone to understanding human psychological disorders centrally involving social behaviour. Reduced oxytocin and higher testosterone levels have been associated with under‐developed social cognition, especially in autism. By contrast, some combination of oxytocin increased above normal levels, and lower testosterone, has been reported in a notable number of studies of schizophrenia, bipolar disorder and depression, and, in some cases, higher oxytocin involves maladaptively ‘hyper‐developed’ social cognition in these conditions. This pattern of findings suggests that human social cognition and behaviour are structured, in part, by joint and opposing effects of oxytocin and testosterone, and that extremes of such joint effects partially mediate risks and phenotypes of autism and psychotic‐affective conditions. These considerations have direct implications for the development of therapies for alleviating disorders of social cognition, and for understanding how such disorders are associated with the evolution of human cognitive‐affective architecture.     

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.     

Phylogenetic affiliation of ancient and contemporary humans inferred from mitochondrial DNA.

Nucleotide sequence analysis of the major non-coding region of human mitochondrial DNA (mtDNA) from three major races was extended with data from 27 contemporary Mongoloids (20 from southeast Asia, seven from America) and 11 Ancient Japanese bones (five from Jomon Age; 3000-6000 years BP, six from the early modern Ainu; 200-300 years BP). In both cases, the sequence was determined directly from the polymerase chain reaction products. Based on a comparison of the 482 base pair sequences from a total of 128 contemporary humans, the nucleotide diversity is estimated to be 1.46%, which is three times higher than the corresponding value estimated from restriction-enzyme analysis of the whole mtDNA genome. The phylogenetic tree revealed that all lineages are classified into at least five clusters designated as C1-C5. C1 consists exclusively of Africans, and most Asians and Europeans formed C2, C3, C5 and C4, respectively. Phylogenetic analysis also indicated that part of the Asians, including the Japanese, subsequently diverged from the majority of Africans, and that Asians can therefore be separated into two distinct groups. Native Americans, however, appeared only in C3 and C5, suggesting that the size of the founder population was not so large during the peopling of American. Nucleotide sequences derived from ancient bones in a highly polymorphic region were also compared with those of contemporary humans. The nucleotide diversity among the 139 sequences in the region was estimated to be 2.26%. A group of ancient Japanese, including both Jomon peoples and the Ainu, showed a close phylogenetic affiliation with one group of contemporary Japanese and southeast Asians.(ABSTRACT TRUNCATED AT 250 WORDS)     

Reflexive social attention in monkeys and humans

For humans, social cues often guide the focus of attention. Although many nonhuman primates, like humans, live in large, complex social groups, the extent to which human and nonhuman primates share fundamental mechanisms of social attention remains unexplored. Here, we show that, when viewing a rhesus macaque looking in a particular direction, both rhesus macaques and humans reflexively and covertly orient their attention in the same direction. Specifically, when performing a peripheral visual target detection task, viewing a monkey with either its eyes alone or with both its head and eyes averted to one side facilitated the detection of peripheral targets when they randomly appeared on the same side. Moreover, viewing images of a monkey with averted gaze evoked small but systematic shifts in eye position in the direction of gaze in the image. The similar magnitude and temporal dynamics of response facilitation and eye deviation in monkeys and humans suggest shared neural circuitry mediating social attention.     

Neighbor effects in marmosets: social contagion of agonism and affiliation in captive Callithrix jacchus

Researchers have demonstrated the neighbor effect for affiliative and agonistic neighbor vocalizations in captive chimpanzees. We extend the investigation of the neighbor effect to New World monkeys, Callithrix jacchus. We collected data on vocalizations and behaviors of 31 focal individuals and concurrent neighbor vocalization within three behavioral categories: intragroup and intergroup aggression and intragroup affiliation. We investigated whether there was an influence of neighbor vocalizations on focal behavior within the same behavioral category. For data analysis we used approximate randomization of paired‐sample t‐tests. We found that marmosets performed intergroup aggressive behavior (bristle, anogenital present for neighbor loud shrill only) for significantly longer, and emitted significantly more intergroup agonistic vocalizations (twitter, loud shrill), at a high frequency of intergroup agonistic neighbor vocalizations (twitter, loud shrill) than at low. The marmosets were also significantly more likely to engage in bristle behavior immediately after hearing a neighbor intergroup aggressive call (twitter, loud shrill) than directly beforehand. High neighbor intragroup agonistic calls (chatter) were associated with significantly longer spent in related behavior (composite of: attack, chase, steal food). Affiliative behaviors (share food, grooming invite) were engaged in by marmosets for significantly longer at higher frequencies of affiliative neighbor chirp calls than at low. Marmosets were also significantly more likely to perform food sharing and active affiliative contact immediately after rather than before hearing a neighbor chirp call. Our findings suggest that neighbor vocalizations influence marmoset behavior through social contagion and indicate that the neighbor effect for affiliation and aggression generalizes to the marmoset. Am. J. Primatol. 72:549–558, 2010. © 2010 Wiley‐Liss, Inc.     

Oxytocin receptor is not required for social attachment in prairie voles

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Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine

The neuropeptides oxytocin (OXT) and arginine vasopressin (AVP) are evolutionarily highly conserved mediators in the regulation of complex social cognition and behaviour. Recent studies have investigated the effects of OXT and AVP on human social interaction, the genetic mechanisms of inter-individual variation in social neuropeptide signalling and the actions of OXT and AVP in the human brain as revealed by neuroimaging. These data have advanced our understanding of the mechanisms by which these neuropeptides contribute to human social behaviour. OXT and AVP are emerging as targets for novel treatment approaches--particularly in synergistic combination with psychotherapy--for mental disorders characterized by social dysfunction, such as autism, social anxiety disorder, borderline personality disorder and schizophrenia.     

Economic principles motivating social attention in humans

We know little about the processes by which we evaluate the opportunity to look at another person. We propose that behavioural economics provides a powerful approach to understanding this basic aspect of social attention. We hypothesized that the decision process culminating in attention to another person follows the same economic principles that govern choices about rewards such as food, drinks and money. Specifically, such rewards are discounted as a function of time, are tradable for other rewards, and reinforce work. Behavioural and neurobiological evidence suggests that looking at other people can also be described as rewarding, but to what extent these economic principles apply to social orienting remains unknown. Here, we show that the opportunity to view pictures of the opposite sex is discounted by delay to viewing, substitutes for money and reinforces work. The reward value of photos of the opposite sex varied with physical attractiveness and was greater in men, suggesting differential utility of acquiring visual information about the opposite sex in men and women. Together, these results demonstrate that choosing whom to look at follows a general set of economic principles, implicating shared neural mechanisms in both social and non-social decision making.     

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.     

Social status gates social attention in humans

Humans tend to shift attention in response to the averted gaze of a face they are fixating, a phenomenon known as gaze cuing. In the present paper, we aimed to address whether the social status of the cuing face modulates this phenomenon. Participants were asked to look at the faces of 16 individuals and read fictive curriculum vitae associated with each of them that could describe the person as having a high or low social status. The association between each specific face and either high or low social status was counterbalanced between participants. The same faces were then used as stimuli in a gaze-cuing task. The results showed a greater gaze-cuing effect for high-status faces than for low-status faces, independently of the specific identity of the face. These findings confirm previous evidence regarding the important role of social factors in shaping social attention and show that a modulation of gaze cuing can be observed even when knowledge about social status is acquired through episodic learning.     

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 receptors modulate a social salience neural network in male prairie voles

Social behavior is regulated by conserved neural networks across vertebrates. Variation in the organization of neuropeptide systems across these networks is thought to contribute to individual and species diversity in network function during social contexts. For example, oxytocin (OT) is an ancient neuropeptide that binds to OT receptors (OTRs) in the brain and modulates social and reproductive behavior across vertebrate species, including humans. Central OTRs exhibit extraordinarily diverse expression patterns that are associated with individual and species differences in social behavior. In voles, OTR density in the nucleus accumbens (NAc)—a region important for social and reward learning—is associated with individual and species variation in social attachment behavior. Here we test whether OTRs in the NAc modulate a social salience network (SSN)—a network of interconnected brain nuclei thought to encode valence and incentive salience of sociosensory cues—during a social context in the socially monogamous male prairie vole. Using a selective OTR antagonist, we test whether activation of OTRs in the NAc during sociosexual interaction and mating modulates expression of the immediate early gene product Fos across nuclei of the SSN. We show that blockade of endogenous OTR signaling in the NAc during sociosexual interaction and mating does not strongly modulate levels of Fos expression in individual nodes of the network, but strongly modulates patterns of correlated Fos expression between the NAc and other SSN nuclei.