The role of mesotocin on social bonding in pinyon jays

The neuropeptide oxytocin influences mammalian social bonding by facilitating the building and maintenance of parental, sexual, and same-sex social relationships. However, we do not know whether the function of the avian homologue mesotocin is evolutionarily conserved across birds. While it does influence avian prosocial behavior, mesotocin's role in avian social bonding remains unclear. Here, we investigated whether mesotocin regulates the formation and maintenance of same-sex social bonding in pinyon jays (Gymnorhinus cyanocephalus), a member of the crow family. We formed squads of four individually housed birds. In the first, “pair-formation” phase of the experiment, we repeatedly placed pairs of birds from within the squad together in a cage for short periods of time. Prior to entering the cage, we intranasally administered one of three hormone solutions to both members of the pair: mesotocin, oxytocin antagonist, or saline. Pairs received repeated sessions with administration of the same hormone. In the second, “pair-maintenance” phase of the experiment, all four members of the squad were placed together in a large cage, and no hormones were administered. For both phases, we measured the physical proximity between pairs as our proxy for social bonding. We found that, compared with saline, administering mesotocin or oxytocin antagonist did not result in different proximities in either the pair-formation or pair-maintenance phase of the experiment. Therefore, at the dosages and time frames used here, exogenously introduced mesotocin did not influence same-sex social bond formation or maintenance. Like oxytocin in mammals, mesotocin regulates avian prosocial behavior; however, unlike oxytocin, we do not have evidence that mesotocin regulates social bonds in birds.     

The neurobiology of social attachment: A comparative approach to behavioral, neuroanatomical, and neurochemical studies

The formation and maintenance of social bonds in adulthood is an essential component of human health. However studies investigating the underlying neurobiology of such behaviors have been scarce. Microtine rodents offer a unique comparative animal model to explore the neural processes responsible for pair bonding and its associated behaviors. Studies using monogamous prairie voles and other related species have recently offered insight into the neuroanatomical, neurobiological, and neurochemical underpinnings of social attachment. In this review, we will discuss the utility of the microtine rodents in comparative studies by exploring their natural history and social behavior in the laboratory. We will then summarize the data implicating vasopressin, oxytocin, and dopamine in the regulation of pair bonding. Finally, we will discuss the ways in which these neurochemical systems may interact to mediate this complex behavior.     

Neuropeptidergic regulation of affiliative behavior and social bonding in animals

Social relationships are essential for maintaining human mental health, yet little is known about the brain mechanisms involved in the development and maintenance of social bonds. Animal models are powerful tools for investigating the neurobiological mechanisms regulating the cognitive processes leading to the development of social relationships and for potentially extending our understanding of the human condition. In this review, we discuss the roles of the neuropeptides oxytocin and vasopressin in the regulation of social bonding as well as related social behaviors which culminate in the formation of social relationships in animal models. The formation of social bonds is a hierarchical process involving social motivation and approach, the processing of social stimuli and formation of social memories, and the social attachment itself. Oxytocin and vasopressin have been implicated in each of these processes. Specifically, these peptides facilitate social affiliation and parental nurturing behavior, are essential for social recognition in rodents, and are involved in the formation of selective mother-infant bonds in sheep and pair bonds in monogamous voles. The convergence of evidence from these animal studies makes oxytocin and vasopressin attractive candidates for the neural modulation of human social relationships as well as potential therapeutic targets for the treatment of psychiatric disorders associated with disruptions in social behavior, including autism.     

社会互作奖赏效应的多巴胺依赖机制

社会性玩耍、配偶联系和母子联系等亲密社会互作会激活中脑-边缘-皮质多巴胺（DA）系统（mesocorticolimbic dopamine system,MCLDS）,促进DA传递。阿片肽、催产素（oxytocin,OT）和加压素（vasopressin,AVP）能够促进亲密的社会互作,并通过调制DA的活动,提高社会互作的奖赏价值。社会互作和滥用药物之间相互影响,阿片肽、OT和AVP系统是两者交互作用的重要枢纽。揭示两者交互作用的神经机制,对于开展精神疾病或成瘾戒断的治疗有重要指导意义。     

Cellular mechanisms of social attachment

Pharmacological studies in prairie voles have suggested that the neuropeptides oxytocin and vasopressin play important roles in behaviors associated with monogamy, including affiliation, paternal care, and pair bonding. Our laboratory has investigated the cellular and neuroendocrine mechanisms by which these peptides influence affiliative behavior and social attachment in prairie voles. Monogamous prairie voles have a higher density of oxytocin receptors in the nucleus accumbens than do nonmonogamous vole species; blockade of these receptors by site-specific injection of antagonist in the female prairie vole prevents partner preference formation. Prairie voles also have a higher density of vasopressin receptors in the ventral pallidal area, which is the major output of the nucleus accumbens, than montane voles. Both the nucleus accumbens and ventral pallidum are key relay nuclei in the brain circuits implicated in reward, such as the mesolimbic dopamine and opioid systems. Therefore, we hypothesize that oxytocin and vasopressin may be facilitating affiliation and social attachment in monogamous species by modulating these reward pathways.     

From affiliative behaviors to romantic feelings: a role of nanopeptides

Love is one of the most desired experiences. The quest for understanding human bonds, especially love, was traditionally a domain of the humanities. Recent developments in biological sciences yield new insights into the mechanisms underlying the formation and maintenance of human relationships. Animal models of reproductive behaviors, mother-infant attachment and pair bonding complemented by human studies reveal neuroendocrine foundations of prosocial behaviors and emotions. Amongst various identified neurotransmitters and modulators, which control affiliative behaviors, the particular role of nanopeptides has been indicated. New studies suggest that these chemicals are not only involved in regulating bonding processes in animals but also contribute to generating positive social attitudes and feelings in humans.     

Social cues and hormone levels in male Octodon degus (Rodentia): a field test of the Challenge Hypothesis

Social interactions are important factors determining and regulating individual behaviors. Testosterone has been related to agonistic interactions, while glucocorticoids have been related to social stress, especially during interactions of dominance. We compared testosterone and cortisol concentrations in male degus (Octodon degus, Rodentia) under laboratory conditions without male social interactions, with data from wild males in nature. Under natural conditions, males should present higher levels of testosterone during the breeding season due to social interactions (Challenge Hypothesis). Alternatively, intense social instability could act as a stressing environment, raising glucocorticoids, which inhibit testosterone concentrations. Our results show a significant increase in agonistic interactions between males during the breeding season, and disappearance of non-agonistic male interactions during this period. Hormone levels in breeding season show nonsignificant differences between laboratory groups, but testosterone concentrations in field males were significantly higher than in laboratory males. Testosterone levels were similar among pre-breeding and breeding periods, but in field animals the concentration was approximately 30% higher than in laboratory degus. In field animals, we found two different mating strategies: resident males, with territorial behavior, and transient males, displayed an opportunistic approach to females. Finally, cortisol presents a similar pattern in both laboratory and field animals; pre-breeding values of cortisol are higher than during the breeding season. This suggests that social interactions in O. degus activate a rise in testosterone, supporting the Challenge Hypothesis, and could be considered as partial support of the Social Stress Hypothesis.     

Bonds of bros and brothers: Kinship and social bonding in postdispersal male macaques

Group‐living animals often maintain a few very close affiliative relationships—social bonds—that can buffer them against many of the inevitable costs of gregariousness. Kinship plays a central role in the development of such social bonds. The bulk of research on kin biases in sociality has focused on philopatric females, who typically live in deeply kin‐structured systems, with matrilineal dominance rank inheritance and life‐long familiarity between kin. Closely related males, in contrast, are usually not close in rank or familiar, which offers the opportunity to test the importance of kinship per se in the formation of social bonds. So far, however, kin biases in male social bonding have only been tested in philopatric males, where familiarity remains a confounding factor. Here, we studied bonds between male Assamese macaques, a species in which males disperse from their natal groups and in which male bonds are known to affect fitness. Combining extensive behavioural data on 43 adult males over a 10‐year period with DNA microsatellite relatedness analyses, we find that postdispersal males form stronger relationships with the few close kin available in the group than with the average nonkin. However, males form the majority of their bonds with nonkin and may choose nonkin over available close kin to bond with. Our results show that kinship facilitates bond formation, but is not a prerequisite for it, which suggests that strong bonds are not restricted to kin in male mammals and that animals cooperate for both direct and indirect fitness benefits.     

Affiliative relationships and reciprocity among adult male bonnet macaques (Macaca radiata) at Arunachala Hill, India

In captivity, male bonnet macaques (Macaca radiata) frequently express "friendship" toward one another, including affiliative behavior such as huddling, grooming, coalitionary support, and sitting in close proximity. The purpose of this study was to determine whether wild adult male bonnet macaques also express "friendship" by investigating whether or not (1) adult male bonnet macaques have affiliative social relationships with other males, (2) the strength of social relationships varies among dyads, (3) there is time-matched reciprocity in allogrooming among dyads, and if so, whether the level of reciprocity occurs within a bout of grooming, a day, or over 2 months (the limit of this study), and (4) a correlation exists between the strength of social relationships and dominance ranks among adult males. Focal samples totaling 150 hr on all seven adult males in one study group were conducted to record both agonistic and affiliative interactions. Agonistic interactions were used to construct a dominance hierarchy, whereas affiliative interactions (sitting in proximity to within 1 m with and without grooming) were used to quantify the existence and strength of social bonds within dyads. Results show that adult male bonnet macaques had differentiated affiliative relationships with other males in their group. There was little reciprocity of grooming within a bout of grooming or within a day, but greater reciprocity over the study period of 2 months. There was no correlation between dominance ranking distance and the strength of affiliative relationship within dyads; however, within dyads lower-ranking males groomed higher-ranking males more than vice versa. This study suggests that friendships in male bonnet macaques are characterized not by immediate tit-for-tat reciprocal altruism, but by reciprocity over a longer time span, and that affiliative social relationships may be less constrained by agonistic relationships than is the case in more despotic species of macaques.     

Dominance relations in pairs of domestic cats

The dominance relationships in a group of adult male cats were studied by means of paired encounters in an observation arena which was equally familiar to both animals.In order to develop a good operational technique a pilot study was undertaken. Dominance relationships were determined by using criteria based upon approach/withdrawal or threatening postures similar to those described by Leyhausen (1973).During the encounters two conflicting tendencies seemed to appear: efforts to avoid confrontation and agonistic interactions. The intensity of the reaction varied from pair to pair.Some kinds of behaviour, not considered to be agonistic (such as exploration and, to a lesser extent, rubbing and urine marking), were performed more frequently by the dominant male.Furthermore it was shown that in the course of the experiments, the number of encounters in which no dominance could be assessed increased, probably due to increasing familiarity.The results of a pilot study on the effect of castration and testosterone treatment upon dominance relationships are also presented.     

Oxytocin, vasopressin and pair bonding: implications for autism

Understanding the neurobiological substrates regulating normal social behaviours may provide valuable insights in human behaviour, including developmental disorders such as autism that are characterized by pervasive deficits in social behaviour. Here, we review the literature which suggests that the neuropeptides oxytocin and vasopressin play critical roles in modulating social behaviours, with a focus on their role in the regulation of social bonding in monogamous rodents. Oxytocin and vasopressin contribute to a wide variety of social behaviours, including social recognition, communication, parental care, territorial aggression and social bonding. The effects of these two neuropeptides are species-specific and depend on species-specific receptor distributions in the brain. Comparative studies in voles with divergent social structures have revealed some of the neural and genetic mechanisms of social-bonding behaviour. Prairie voles are socially monogamous; males and females form long-term pair bonds, establish a nest site and rear their offspring together. In contrast, montane and meadow voles do not form a bond with a mate and only the females take part in rearing the young. Species differences in the density of receptors for oxytocin and vasopressin in ventral forebrain reward circuitry differentially reinforce social-bonding behaviour in the two species. High levels of oxytocin receptor (OTR) in the nucleus accumbens and high levels of vasopressin 1a receptor (V1aR) in the ventral pallidum contribute to monogamous social structure in the prairie vole. While little is known about the genetic factors contributing to species-differences in OTR distribution, the species-specific distribution pattern of the V1aR is determined in part by a species-specific repetitive element, or 'microsatellite', in the 5' regulatory region of the gene encoding V1aR (avpr1a). This microsatellite is highly expanded in the prairie vole (as well as the monogamous pine vole) compared to a very short version in the promiscuous montane and meadow voles. These species differences in microsatellite sequence are sufficient to change gene expression in cell culture. Within the prairie vole species, intraspecific variation in the microsatellite also modulates gene expression in vitro as well as receptor distribution patterns in vivo and influences the probability of social approach and bonding behaviour. Similar genetic variation in the human AVPR1A may contribute to variations in human social behaviour, including extremes outside the normal range of behaviour and those found in autism spectrum disorders. In sum, comparative studies in pair-bonding rodents have revealed neural and genetic mechanisms contributing to social-bonding behaviour. These studies have generated testable hypotheses regarding the motivational systems and underlying molecular neurobiology involved in social engagement and social bond formation that may have important implications for the core social deficits characterizing autism spectrum disorders.     

单配制啮齿动物Pair Bond形成的神经调节机制

单配制啮齿动物社会结构的神经生物学原理可以通过实验室研究Social bonding而获得。在本文中,我们探讨了如何利用单配制的草原田鼠(Microtus ochrogaster)作为研究模型揭示pair bond形成的神经调控机制。我们进而探讨了单配制与多配制田鼠之间神经解剖学的差异以及神经化学物质的调节是怎样影响pair bond的。本篇综述还讨论了与pair bond形成有关的神经化学系统之间的相互影响以及pair bond形成过程中的两性差异。最后,我们预测了这一研究领域的未来研究方向以及研究social bonding的神经调控对人类健康的重要性。     

The coevolution of long‐term pair bonds and cooperation

The evolution of social traits may not only depend on but also change the social structure of the population. In particular, the evolution of pairwise cooperation, such as biparental care, depends on the pair‐matching distribution of the population, and the latter often emerges as a collective outcome of individual pair‐bonding traits, which are also under selection. Here, we develop an analytical model and individual‐based simulations to study the coevolution of long‐term pair bonds and cooperation in parental care, where partners play a Snowdrift game in each breeding season. We illustrate that long‐term pair bonds may coevolve with cooperation when bonding cost is below a threshold. As long‐term pair bonds lead to assortative interactions through pair‐matching dynamics, they may promote the prevalence of cooperation. In addition to the pay‐off matrix of a single game, the evolutionarily stable equilibrium also depends on bonding cost and accidental divorce rate, and it is determined by a form of balancing selection because the benefit from pair‐bond maintenance diminishes as the frequency of cooperators increases. Our findings highlight the importance of ecological factors affecting social bonding cost and stability in understanding the coevolution of social behaviour and social structures, which may lead to the diversity of biological social systems.     

Social Environment Affects Peripheral Oxytocin and Cortisol during Stress Responses in Guinea-Pigs

Numerous studies have demonstrated interactions between oxytocin (OT) secretion, adrenal activity, an animal's social environment, and stress responses. In the present study, we hypothesized that partner preference and pair bonding cause increased peripheral OT, which down‐regulates the adrenal and behavioral response in stress. In addition, we tested whether these interactions depended on sex, the social environment of the individual, or the type of stressor. Experiments were carried out on guinea‐pigs held in sexual‐pairs or stressed by isolation. Among the paired individuals choice tests were carried out to document partner preference. Female preference for a male was expressed by spatial cohesion. Stress responses to abiotic stimuli were examined and compared between isolated and cohabited animals with or without preference. Results show that OT of cohabited animals was significantly higher than during isolation. OT levels were further increased in males preferred by females. Cortisol (CORT) levels were elevated in isolated animals. There were no significant differences between pairs with and without female preference. Behaviorally, partner preferences were expressed by high amounts of tactile contact. The stress‐induced behavioral immobility response after exposure to a noise stressor was significantly reduced in preferred males and to a lesser extent in their female partners. Only females with preferences showed an endocrine stress response. Their levels of OT increased. There was no consistent post‐stressor release of CORT. The data indicate that the social environment of an individual, here expressed as preference or isolation, influences peripheral OT secretion. Behavioral stress responses were similarly affected by social factors without a clear involvement of peripheral CORT or OT.     

Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees

Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent–offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event—food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother–infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.     

Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird

Although many species form socially monogamous pair bonds, relevant neural mechanisms have been described for only a single species, the prairie vole (Microtus ochrogaster). In this species, pair bonding is strongly dependent upon the nonapeptides oxytocin (OT) and vasopressin, in females and males, respectively. Because monogamy has evolved many times in multiple lineages, data from additional species are required to determine whether similar peptide mechanisms modulate bonding when monogamy evolves independently. Here we test the hypothesis that OT-like receptor activation is required for pair bond formation in the socially monogamous zebra finch (Taeniopygia guttata). Males and females were administered chronic intracerebroventricular infusions of saline or an OT receptor antagonist and were observed twice daily for 3 days in a colony environment. A variety of affiliative, aggressive and other behaviours were quantified. The antagonist produced significant and selective effects on pair bonding (latency to pair; number of sessions paired; stable pairing) and the associated behaviour of allopreening. Importantly, findings for males follow the trends of females; this yields main effects of treatment in two-way ANOVAs, although within-sex analyses are significant only for females. These data provide evidence for both convergent evolution and species diversity in the neuroendocrine mechanisms of pair bonding.     

Social factors modulate the effects of hormones on the sexual and aggressive behavior of macaques

We previously reviewed the effects of gonadal hormones on the sexual and aggressive behavior of macaques as observed in field, outdoor colony, and laboratory studies. There were consistent similarities between findings from different observational settings, but there were also noteworthy differences which suggested the importance of social and environmental factors in modulating the effects of hormones. We now examine the role of these factors further and consider the extent to which partner preferences, familiarity between individuals, and also dominance rank can affect the behavior of male-female pairs and thereby modify the influences of hormones. The evidence suggests that all these factors are important. Hormone-dependent short-term partner preferences appear to be critical for the formation of consort bonds and to facilitate mating between unfamiliar partners. Socially based partner preferences tend to dampen hormonal influences and may lead to long-term familiarity. Long-term familiarity decreases sexual interactions and may be a proximate mechanism underlying incest avoidance and periodic male troop transfers. Both males and females exhibit mate competition under certain conditions, and their dominance rank can modify sexual and aggressive behavior by either optimizing or reducing hormone-dependent changes. These interaction effects between social and hormonal variables also have relevance for the design and interpretation of laboratory experiments. © 1996 Wiley-Liss, Inc.     

Effect of testosterone and melatonin on social dominance and agonistic behavior in male Tscheskia triton

Social dominance and agonistic behavior play important roles in animal societies. Melatonin and testosterone are closely related to social dominance and agonistic behavior in rodents, but interactions between both of them remain unknown. In this study we investigated the effects of testosterone and melatonin by manipulating photoperiod and castration on social dominance and agonistic behavior in male Tscheskia triton. Castration significantly decreases social dominance of both short- and long-day males, suggesting that testosterone benefits social dominance of males in both breeding and non-breeding seasons. In intact conditions, long-day males tended to dominate short-day males, suggesting that the effect of testosterone on social dominance was a little stronger than melatonin. However, castrated short-day males became dominant over their castrated long-day opponents meaning that high melatonin levels obviously benefit social dominance in males. Hormone implantation indicated that testosterone had no effect on non-breeding condition, but that melatonin was important during the breeding season. Our results indicate that both testosterone and melatonin are important in determining social dominance in male hamsters, and the effect of testosterone appears to be stronger than melatonin. Testosterone is responsible for aggression and social dominance in male hamsters during the breeding season, while melatonin regulates behavior during non-breeding, probably due to the different seasonal secretory patterns of the hormones.     

Species-specific patterns of nonapeptide brain gene expression relative to pair-bonding behavior in grouping and non-grouping cichlids

Comparative studies have revealed that vasopressin–oxytocin pathways are associated with both pair bonding and grouping behavior. However, the relationship between pair bonding and grouping behavior remains unclear. In this study, our aim was to identify whether two species that differ in grouping behavior display a corresponding difference in their pair bonds, and in the underlying vasopressin–oxytocin hormonal pathways. Using two species of cichlid fishes, the highly social Neolamprologus pulcher and the non-social Telmatochromis temporalis, we measured proximity of pairs during pair bond formation, and then measured social behaviors (proximity, aggression, submission, affiliation) and brain gene expression of isotocin and arginine vasotocin (the teleost homologues of oxytocin and vasopressin, respectively), as well as their receptors, after a temporary separation and subsequent reunion of the bonded pairs. Pairs of the social species spent more time in close proximity relative to the non-social species. Rates of aggression increased in both species following the separation and reunion treatment, relative to controls that were not separated. Overall, whole brain expression of isotocin was higher in the social species relative to the non-social species, and correlated with proximity, submission, and affiliation, but only in the social species. Our results suggest that both a social and a non-social cichlid species have similar behavioral responses to a temporary separation from a mate, and we found no difference in the brain gene expression of measured hormones and receptors based on our separation–reunion treatment. However, our results highlight the importance of isotocin in mediating submissive and affiliative behaviors in cichlid fishes, and demonstrate that isotocin has species-specific correlations with socially relevant behaviors.