Oxytocin, Neural Plasticity, and Social Behavior.

Oxytocin regulates parturition, lactation, parental nurturing, and many other social behaviors in both sexes. The circuit mechanisms by which oxytocin modulates social behavior are receiving increasing attention. Here, we review recent studies on oxytocin modulation of neural circuit function and social behavior, largely enabled by new methods of monitoring and manipulating oxytocin or oxytocin receptor neurons in vivo. These studies indicate that oxytocin can enhance the salience of social stimuli and increase signal-to-noise ratios by modulating spiking and synaptic plasticity in the context of circuits and networks. We highlight oxytocin effects on social behavior in nontraditional organisms such as prairie voles and discuss opportunities to enhance the utility of these organisms for studying circuit-level modulation of social behaviors. We then discuss recent insights into oxytocin neuron activity during social interactions. We conclude by discussing some of the major questions and opportunities in the field ahead.

Benefits of an online group dance program for adolescents' social bonding and wellbeing.

INTRODUCTION: The Covid-19 pandemic and its ensuing effects on mental health made it clearer than ever that social bonds are critical for survival, flourishing, and mental wellbeing. Experimental laboratory-based research with children and adults shows that activities involving movement alignment and joint action, such as dance, can facilitate social bonds. METHODS: This study examined whether an online group dance intervention positively affects social bonding and wellbeing using a randomized control design. Participants were 58 UK adolescents aged 11-16 years (N = 52 girls, 75% White, 7% Asian/Asian British, 18% Mixed-Other), randomly assigned to an online intervention or waitlist control group. Participants in the intervention group completed an online 5-week hip-hop dance program during the Covid-19 pandemic in January to February 2021. Measures of social bonding, wellbeing, and future orientation were taken at the beginning and end of the program. RESULTS: Linear mixed model analyses examining group × timepoint interaction showed greater increase in social bonding (p < .0001), and wellbeing (p < .0001) in the intervention vs control group. Moreover, increases in bonding significantly predicted increases in wellbeing (p < .0001), and increases in bonding (p = .03) and wellbeing (p = .0002) significantly predicted increases in the adolescents' hope for the future. CONCLUSIONS: These data, collected at a time of mass social isolation, show that a 5-week-long online dance activity can help adolescents forge stronger social bonds, and improve their wellbeing and future orientation. Our findings suggest that the wellbeing and future orientation benefits of group dance may stem from having stronger social connectedness, opening up avenues for future research and interventions.

Social factors drive vocal exchanges in red-capped mangabeys (Cercocebus torquatus).

Of all the calls made by non-human primates, the function of short-distance contact calls has largely remained to be determined. These calls are the most frequent in the repertoire and are most often exchanged between individuals in a non-random way. To our knowledge, no study has ever examined how vocal exchanges are structured in red-capped mangabeys (Cercocebus torquatus), a semi-terrestrial monkey living in the African forest with a complex semi-tolerant/semi-despotic social system. Our goal was to assess the organization of contact call exchanges in this species and their relationship with individual and social factors such as age, affinity, and hierarchy. Therefore, we observed several captive groups of red-capped mangabeys and collected data on vocal behavior, as well as grooming, agonistic behavior, and spatial proximity. We defined a vocal exchange in this species as a series of contact calls made by two or more individuals within a maximum inter-caller interval of 2 s. At the individual level, the higher the individual's hierarchical rank, the less they initiated exchanges. Furthermore, the most socially integrated individuals had a longer average response time than the less integrated ones. At the dyadic level, preferred exchange partners were individuals often observed near one other or individuals most distant in age. Also, the further apart two individuals were in the dominance hierarchy, the shorter the response time. Our results support both the social bonding hypothesis and a modulating key role of the dominance hierarchy on the social use of contact calls, which is in line with the social style of this species.

Chimpanzee communities differ in their inter- and intrasexual social relationships.

Male and female human social bonding strategies are culturally shaped, in addition to being genetically rooted. Investigating nonhuman primate bonding strategies across sex groups allows researchers to assess whether, as with humans, they are shaped by the social environment or whether they are genetically predisposed. Studies of wild chimpanzees show that in some communities males have strong bonds with other males, whereas in others, females form particularly strong intrasex bonds, potentially indicative of cultural differences across populations. However, excluding genetic or ecological explanations when comparing different wild populations is difficult. Here, we applied social network analysis to examine male and female social bonds in two neighbouring semiwild chimpanzee groups of comparable ecological conditions and subspecies compositions, but that differ in demographic makeup. Results showed differences in bonding strategies across the two groups. While female-female party co-residence patterns were significantly stronger in Group 1 (which had an even distribution of males and females) than in Group 2 (which had a higher proportion of females than males), there were no such differences for male-male or male-female associations. Conversely, female-female grooming bonds were stronger in Group 2 than in Group 1. We also found that, in line with captive studies but contrasting research with wild chimpanzees, maternal kinship strongly predicted proximity and grooming patterns across the groups. Our findings suggest that, as with humans, male and female chimpanzee social bonds are influenced by the specific social group they live in, rather than predisposed sex-based bonding strategies.

People and place attachment: Exploring compliance in neighborhood health centers.

This article explores the roles of place attachment and social relationships in encouraging clients of a health center to comply with their health providers' directives. We draw on place attachment theory to explore the extent to which emotional bonds between clients and the center promote compliance. Next, we draw on place social bonding to explore whether clients' experiences derived from interactions at the center encourage compliance. Based on data obtained from center clients, we conclude that place attachment and social bonding drive compliance. From a practical perspective, providers and clients must engage in social interaction to promote compliance and engender place attachment.

Testing the effect of oxytocin on social grooming in bonobos.

Oxytocin has attracted research attention due to its role in promoting social bonding. In bonobos and chimpanzees, the two species most closely related to humans, urinary oxytocin is known to correlate with key behaviours related to social bonding such as social grooming in chimpanzees and female-female sexual behaviour in bonobos. However, no study has demonstrated that the administration of oxytocin promotes real-life social interactions in Pan, leaving it unclear whether oxytocin is merely correlated with social behaviors or does affect them in these species. To test this, we administered nebulized oxytocin or saline placebo to a group of female bonobos and subsequently observed changes in their gross behavior during free interaction. We found an overall effect of more frequent grooming in the oxytocin condition. However, on the individual level this effect remained significant for only one participant in our follow-up models, suggesting future work should explore interindividual variation. Our results provide some experimental support for the biobehavioural feedback loop hypothesis, which posits that some functions of the oxytocin system support the formation and maintenance of social bonds through a positive feedback loop; however, further tests with a larger number of individuals are required. Our results, at a minimum, demonstrated that oxytocin affects spontaneous, naturalistic social interactions of at least some female bonobos, adding to accumulating evidence that oxytocin modulates complex social behaviors of Pan.

The development of sex differences in play in wild white-faced capuchins (Cebus capucinus).

Many mammalian species display sex differences in the frequency of play behavior, yet the animal literature includes few longitudinal studies of play, which are important for understanding the developmental timing of sex differences and the evolutionary functions of play. We analyzed social play, solitary play, and grooming using an 18-year data set on 38 wild white-faced capuchin monkeys (Cebus capucinus) followed since infancy. Rates of each behavior were measured as the proportion of point samples taken during focal follows in which the individual engaged in each behavior. To determine sex differences in these rates, we ran a series of generalized linear mixed models, considering both linear and quadratic effects of age, and chose the optimal model for each of the three behavioral outcomes based on information criteria. Rates of both social play and solitary play decreased with age, with the exception of social play in males, which increased in the early juvenile period before decreasing. Male and female capuchins had different developmental patterns of social play, with males playing more than females during most of the juvenile period, but they did not display meaningful sex differences in solitary play rates. Additionally, males and females had different patterns of grooming over the lifespan: males participated in grooming at low rates throughout their lives, while adult females participated in grooming at much higher rates, peaking around age 11 years before declining. We suggest that male and female white-faced capuchins may adopt alternative social bonding strategies, including different developmental timing and different behaviors (social play for males vs. grooming for females). Our results were consistent with two functional hypotheses of play, the practice and bonding hypotheses. This study demonstrates that play behavior may be critical for the development of sex-specific social strategies and emphasizes the importance of developmental perspectives on social behaviors.

Designing Man's New Best Friend: Enhancing Human-Robot Dog Interaction through Dog-Like Framing and Appearance.

To understand how to improve interactions with dog-like robots, we evaluated the importance of "dog-like" framing and physical appearance on interaction, hypothesizing multiple interactive benefits of each. We assessed whether framing Aibo as a puppy (i.e., in need of development) versus simply a robot would result in more positive responses and interactions. We also predicted that adding fur to Aibo would make it appear more dog-like, likable, and interactive. Twenty-nine participants engaged with Aibo in a 2 × 2 (framing × appearance) design by issuing commands to the robot. Aibo and participant behaviors were monitored per second, and evaluated via an analysis of commands issued, an analysis of command blocks (i.e., chains of commands), and using a T-pattern analysis of participant behavior. Participants were more likely to issue the "Come Here" command than other types of commands. When framed as a puppy, participants used Aibo's dog name more often, praised it more, and exhibited more unique, interactive, and complex behavior with Aibo. Participants exhibited the most smiling and laughing behaviors with Aibo framed as a puppy without fur. Across conditions, after interacting with Aibo, participants felt Aibo was more trustworthy, intelligent, warm, and connected than at their initial meeting. This study shows the benefits of introducing a socially robotic agent with a particular frame and importance on realism (i.e., introducing the robot dog as a puppy) for more interactive engagement.

Suffer together, bond together: Brain-to-brain synchronization and mutual affective empathy when sharing painful experiences.

Previous behavioral studies have shown that sharing painful experiences can strengthen social bonds and promote mutual prosociality, yet the neural mechanisms underlying this phenomenon remain unclear. We hypothesized that sharing a painful experience induces brain-to-brain synchronization and mutual empathy for each other's pain between pain-takers and pain-observers, which then leads to enhanced social bonding. To test this hypothesis, we adopted an electroencephalographic (EEG) hyper-scanning technique to assess neuronal and behavioral activity during a Pain-Sharing task in which high- or low-intensity pain stimulation was randomly delivered to one participant of a dyad on different experimental trials. Single-brain analysis showed that sensorimotor α-oscillation power was suppressed more when expecting high-intensity pain than when expecting low-intensity pain similarly for self-directed or partner-directed pain. Dual-brain analysis revealed that expecting high-intensity pain induced greater brain-to-brain synchronization of sensorimotor α-oscillation phases between pain-takers and pain-observers than did expecting low-intensity pain. Mediation analysis further revealed that brain-to-brain synchronization of sensorimotor α-oscillations mediated the effects of pain-stimulation intensity on mutual affective sharing for partner-directed pain. This mutual affective empathy during the task predicted the social bonding, as indexed by prosocial inclinations measured after the task. These results support the hypothesis that sharing a painful experience triggers emotional resonance between pairs of individuals through brain-to-brain synchronization of neuronal α-oscillations recorded over the sensorimotor cortex, and this emotional resonance further strengthens social bonds and motivates prosocial behavior within pairs of individuals.

Grooming site preferences in black capuchin monkeys: Hygienic vs. social functions revisited.

When primates groom each other, they tend to concentrate on those parts of the body they cannot efficiently self-groom (i.e., not visually accessible), and prefer to intensify grooming in areas with high hair density, thus suggesting a hygienic function. However, preferences for some body sites over others during social grooming may also result from different degrees of social bonding and relative dominance. To assess the relative importance of physical (hygienic) and social factors, we examined grooming interactions in two groups of wild black capuchin monkeys (Sapajus nigritus) during 15 nonconsecutive months. We evaluated the distribution of social grooming across body sites according to their accessibility by self-grooming and hair density. At the same time, we assessed whether the degree of dyadic social bonding affects the relative body orientation between groomer and groomee and the access to vulnerable body sites (e.g., face, throat, groin) during grooming. As expected, capuchins preferentially groomed inaccessible body sites (e.g., back and head), with a disproportionate effort directed to the tufts of their partners. We found that dyadic social bond strength, together with rank distance, significantly affected the proportion of grooming in ventro-ventral body relative orientation only in dominant-subordinate groomer-groomee dyads. This may indicate that, when two individuals differ in rank but are strongly bonded, the level of uncertainty related to the social context is already resolved and thus grooming per se is no longer perceived by the subordinate as an uncertain/risky situation. We found no effect of social bonding on grooming vulnerable body sites for any type of dyad. Our findings suggest that grooming site preferences in black capuchin monkeys simultaneously reflect hygienic and social functions.

Blocking mu-opioid receptors inhibits social bonding in rituals.

Religious rituals are universal human practices that play a seminal role in community bonding. In two experiments, we tested the role of mu-opioids as the active factor fostering social bonding. We used a mu-opioid blocker (naltrexone) in two double-blind studies of rituals from different religious traditions. We found the same effect across both studies, with naltrexone leading to significantly lower social bonding compared with placebo. These studies suggest that mu-opioids play a significant role in experiences of social bonding within ritual contexts.

A novel theory on the predictive value of variation in the ß-endorphin system on the risk and severity of PTSD.

Despite growing interest in genetic and psychosocial indicators of heightened susceptibility to posttraumatic stress disorder (PTSD), a predictive model, which explains why some individuals develop PTSD in response to life-threatening traumatic events, while others, when faced with the same or similar experiences, do not, has thus far remained out of reach. In this paper, we review the literature on gene-environment interactions in ß-endorphin system functioning with regard to PTSD and suggest that variation, both genetic and with regard to environmental stimuli, in systems which, like the ß-endorphin system, distort human perception of life-threatening traumatic experiences may account for some of the variance in resilience to the disorder. Given the role of ß-endorphin in both social connections and physical exercise, this becomes especially relevant with regard to military selection, training, and leadership processes.

Rewritable fidelity: How repeated pairings and age influence subsequent pair-bond formation in male prairie voles.

The prairie vole has proven a valuable animal model for the neurobiological study of social monogamy and pair bonding. Previous research has focused almost exclusively on virgin prairie voles forming pair-bonds for the first time - a paradigm with limited relevance to human social behavior. In the present study, we used stud males to assess the impact of repeated pair-bond formation and dissolution on the behaviors and neurobiology relevant to subsequent pair-bond formation. Stud males were tested for behavioral and neurobiological effects of repeated pair-bonding after the 1st, 5th, and 10th pairing. Aged breeder males that experienced minimal pair-bond dissolution were included to control for the effects of aging. Results showed that male prairie voles readily form new pair-bonds after repeated pair-bond dissolution. In terms of social monogamy, old age was associated with males spending less time in close social contact with unfamiliar females. There were no effects of age nor number of lifetime pairings on depressive-like behavior or paternal behavior toward pups. Within the brain, the patterns of oxytocin (OTR) and vasopressin type 1a (V1aR) receptors were largely unaffected, with the following exceptions: 1) males with only a single pairing had higher OTR densities in the paraventricular thalamus and bed nucleus of the stria terminalis; 2) there was an age-related increase in the density of OTR in the caudate putamen and an age-related decline in the density of V1aR in the cortical amygdala. The present findings have translational relevance to human social behavior in the context of aging and social experience.

Identifying distinct sets of predictors of specific functions of autobiographical memory.

Grounded in the ecological approach, research has charted several adaptive functions of autobiographical remembering. Each represents a rather different psychosocial domain (i.e., self, social, directive). The goal of this research was to determine the contributions of each of a set of variables, controlling for all others, in predicting use of autobiographical memory to serve each specific function. In two studies, participants (N = 100; N = 195) rated frequency of functional use of specific event memories and completed a brief battery of memory-related measures. Most Study One results were replicated in Study Two. Self-relevance of memories was related to their functional use regardless of domain. Each function was also, however, predicted by a unique set of variables consistent with its use in a given psychosocial domain. Findings emphasise how a combination of factors come into play to allow humans to use autobiographical memory to serve various different functions in navigating daily life.

Urinary oxytocin in capuchin monkeys: Validation and the influence of social behavior.

In highly social species, like primates, oxytocin plays an important role in cooperation, and in the formation and maintenance of social relationships. Despite recent interest in the relationship between oxytocin and social behavior in nonhuman primates, relatively little is known about endogenous oxytocin in social New World Monkeys. In this paper, we investigate the relationship between oxytocin and affiliative behaviors in socially-housed captive capuchin monkeys (Sapajus [Cebus] apella) by first validating methods of analysis of urinary oxytocin in this species and, second, examining the effects of grooming and fur-rubbing behavior on oxytocin concentrations and further affiliative behavior. In the validation, we found that intranasal exogenous oxytocin significantly increased urinary oxytocin 15-60 min post-administration. Oxytocin was also implicated in both grooming and fur-rubbing behaviors. We found that oxytocin concentrations increased after subjects engaged in grooming or fur-rubbing. In addition, we found that fur-rubbing influenced affiliative behaviors, both during and after a social fur-rubbing bout. While individuals spent more time in contact and proximity while fur-rubbing, immediately following the fur-rubbing event (15-30 min afterwards) all affiliative behaviors decreased. This supports previous research that oxytocin may, in fact, initially be related to increased social distance in this species. Yet, an increase in all affiliative behaviors 30-45 min after the onset of fur-rubbing suggests that fur-rubbing, like grooming, may ultimately function to strengthen social relationships. Overall, these results support a critical role for oxytocin in affiliative behaviors that maintain and strengthen social relationships in capuchin monkeys, and highlight the complexity of the interactions among oxytocin, affiliative behaviors, and social bonding.

A Role for Oxytocin-Like Receptor in Social Habituation in a Teleost.

Oxytocin (OT) mediates social habituation in rodent model systems, but its role in mediating this effect in other vertebrates is unknown. We used males of the African cichlid fish, Astatotilapia burtoni, to investigate two aspects of isotocin (IT; an OT homolog) signaling in social habituation. First, we examined the expression of IT receptor 2 (ITR2) as well as two immediate early genes in brain regions implicated in social recognition. Next, we examined IT neuron activity using immunohistochemistry. Patterns of gene expression in homologs of the amygdala and hippocampus implicate IT signaling in these regions in social habituation to a territorial neighbor. In the preoptic area, the expression of the ITR2 subtype and IT neuron activity respond to the presence of a male, independent of familiarity. Our results implicate IT in mediating social habituation in a teleost.

Group music performance causes elevated pain thresholds and social bonding in small and large groups of singers.

Over our evolutionary history, humans have faced the problem of how to create and maintain social bonds in progressively larger groups compared to those of our primate ancestors. Evidence from historical and anthropological records suggests that group music-making might act as a mechanism by which this large-scale social bonding could occur. While previous research has shown effects of music making on social bonds in small group contexts, the question of whether this effect 'scales up' to larger groups is particularly important when considering the potential role of music for large-scale social bonding. The current study recruited individuals from a community choir that met in both small (n = 20 - 80) and large (a 'megachoir' combining individuals from the smaller subchoirs n = 232) group contexts. Participants gave self-report measures (via a survey) of social bonding and had pain threshold measurements taken (as a proxy for endorphin release) before and after 90 minutes of singing. Results showed that feelings of inclusion, connectivity, positive affect, and measures of endorphin release all increased across singing rehearsals and that the influence of group singing was comparable for pain thresholds in the large versus small group context. Levels of social closeness were found to be greater at pre- and post-levels for the small choir condition. However, the large choir condition experienced a greater change in social closeness as compared to the small condition. The finding that singing together fosters social closeness - even in large contexts where individuals are not known to each other - is consistent with evolutionary accounts that emphasize the role of music in social bonding, particularly in the context of creating larger cohesive groups than other primates are able to manage.

Silent disco: dancing in synchrony leads to elevated pain thresholds and social closeness.

Moving in synchrony leads to cooperative behaviour and feelings of social closeness, and dance (involving synchronisation to others and music) may cause social bonding, possibly as a consequence of released endorphins. This study uses an experimental paradigm to determine which aspects of synchrony in dance are associated with changes in pain threshold (a proxy for endorphin release) and social bonding between strangers. Those who danced in synchrony experienced elevated pain thresholds, whereas those in the partial and asynchrony conditions experienced no analgesic effects. Similarly, those in the synchrony condition reported being more socially bonded, although they did not perform more cooperatively in an economic game. This experiment suggests that dance encourages social bonding amongst co-actors by stimulating the production of endorphins, but may not make people more altruistic. We conclude that dance may have been an important human behaviour evolved to encourage social closeness between strangers.

Oxytocin reverses amphetamine-induced deficits in social bonding: evidence for an interaction with nucleus accumbens dopamine.

Drug addiction has devastating consequences on social behaviors and can lead to the impairment of social bonding. Accumulating evidence indicates that alterations in oxytocin (OT) and dopamine (DA) neurotransmission within brain reward circuitry may be involved. We investigated this possibility, as well as the therapeutic potential of OT for drug-induced social deficits, using the prairie vole (Microtus ochrogaster)-a socially monogamous rodent that forms enduring pair bonds between adult mates. We demonstrate that repeated exposure to the commonly abused psychostimulant amphetamine (AMPH) inhibits the formation of partner preferences (an index of pair bonding) in female prairie voles. AMPH exposure also altered OT and DA neurotransmission in regions that mediate partner preference formation: it decreased OT and DA D2 receptor immunoreactivity in the medial prefrontal cortex (mPFC) and nucleus accumbens (NAcc), respectively, and increased NAcc DA levels. Administration of OT directly into the mPFC of AMPH-exposed voles restored partner preferences, and altered NAcc DA levels, and this effect was dependent on OT receptor activation. Together, these data suggest that repeated AMPH exposure impairs pair bonding through an OT-mediated mechanism, and that OT and DA systems within brain reward circuitry may interact to mediate the complex relationship between drug abuse and social bonding. Further, these results provide empirical support for the idea that the central OT system may represent an important target for the treatment of social deficits in addiction.

Neuropeptidergic regulation of pair-bonding and stress buffering: Lessons from voles.

This article is part of a Special Issue "SBN 2014". Interpersonal attachment is a critical component of the human experience. Pair-bonding ameliorates the severity of several mental and physical diseases. Thus, a better understanding of how the central nervous system responds to and encodes social-buffering during stress is a valuable research enterprise. The prairie vole (Microtus ochrogaster), as a laboratory animal model, provides the gold standard for the investigation of the neurobiology underlying attachment. Furthermore, emerging research in voles, additional laboratory rodents, transgenic mice, primates, and humans has provided novel insight into the neurochemical mechanisms underlying the therapeutic effects of social bonds reducing anxiety, depression, and drug abuse liability. In the present review, we highlight the work from this burgeoning field and focus on the role(s) of the neuropeptides oxytocin (OT), vasopressin (AVP), and corticotrophin releasing hormone (CRH) mediating stress buffering. Together, the data suggest that OT underlies social bonding to reduce stress-induced psychological illness while AVP and CRH facilitate arousal to enhance autonomic reactivity, increasing susceptibility to adverse mental and physical health.