C. Sue Carter

NEUROENDOCRINE PERSPECTIVES ON SOCIAL ATTACHMENT AND LOVE

The purpose of this paper is to review existing behavioral and neuroendocrine perspectives on social attachment and love. Both love and social attachments function to facilitate reproduction, provide a sense of safety, and reduce anxiety or stress. Because social attachment is an essential component of love, understanding attachment formation is an important step toward identifying the neurobiological substrates of love. Studies of pair bonding in monogamous rodents, such as prairie voles, and maternal attachment in precocial ungulates offer the most accessible animal models for the study of mechanisms underlying selective social attachments and the propensity to develop social bonds. Parental behavior and sexual behavior, even in the absence of selective social behaviors, are associated with the concept of love; the analysis of reproductive behaviors, which is far more extensive than our understanding of social attachment, also suggests neuroendocrine substrates for love. A review of these literatures reveals a recurrent association between high levels of activity in the hypothalamic pituitary adrenal (HPA) axis and the subsequent expression of social behaviors and attachments. Positive social behaviors, including social bonds, may reduce HPA axis activity, while in some cases negative social interactions can have the opposite effect. Central neuropeptides, and especially oxytocin and vasopressin have been implicated both in social bonding and in the central control of the HPA axis. In prairie voles, which show clear evidence of pair bonds, oxytocin is capable of increasing positive social behaviors and both oxytocin and social interactions reduce activity in the HPA axis. Social interactions and attachment involve endocrine systems capable of decreasing HPA reactivity and modulating the autonomic nervous system, perhaps accounting for health benefits that are attributed to loving relationships.

The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster).

This study compared the effects of centrally administered oxytocin (OT) and arginine vasopressin (AVP) on partner preference formation and social contact in male and female prairie voles (Microtus ochrogaster). After 1 hr of cohabitation and pretreatment with either AVP or OT, both males and females exhibited increased social contact and significant preference for the familiar partner. After pretreatment with either an OT receptor antagonist (OTA) or an AVP (V1a) receptor antagonist (AVPA), neither OT nor AVP induced a partner preference. In addition, treatment with OT+OTA or AVP+AVPA was associated with low levels of social contact in both sexes. Either AVP or OT is sufficient to facilitate social contact if either the OT or AVP receptor is available. However, the formation of partner preferences may require access to both AVP and OT receptors.

The Mating System of the Prairie Vole, Microtus ochrogaster: Field and Laboratory Evidence for Pair-Bonding

Summary1.Field and experimental evidence is provided for the existence of pair-bonding or monogamy in prairie voles (Microtus ochrogaster).2.Multiple-capture live-trap data indicated that male and female pairs of M. ochrogaster were repeatedly captured together. (A comparable analysis for data from M. pennsylvanicus revealed no indications of long-term male-female associations.)3.Male-female pair captures of M. ochrogaster were equally likely during either the breeding or nonbreeding seasons, further suggesting a relative stability of pairs.4.In laboratory dyadic encounters, both males and females from breeding pairs tended to show relatively high levels of aggression toward unfamiliar animals of the opposite sex. In contrast, aggression was rarely observed between members of established breeding pairs. Nonpaired animals of either sex infrequently initiated aggressive encounters.5.When pairs were separated for 8 days (during which time the females lived with a new male) the apparent pair-bond with the original male was broken. These females became aggressive toward the male with which they had previously bred, and rarely fought with their new mate. This suggests that the pair-bonding process is reversible.6.Females in postpartum estrus preferentially showed high levels of sexual receptivity and low levels of aggression toward familiar males and were less likely to mate with unfamiliar sexually experienced males. The presence of pups at the time of testing did not appear to influence female-initiated aggression.

Oxytocin Administered Centrally Facilitates Formation of a Partner Preference in Female Prairie Voles (Microtus ochrogaster)

Prairie voles (Microtus ochrogaster) are monogamous mammals that form male‐female pair bonds. Partner preference formation, one component of the pair bond in prairie voles, occurs following male‐female cohabitation and is facilitated by mating. The peptide hormone oxytocin is released during physical contact and particularly following vaginal stimulation. Oxytocin has been implicated in mother‐infant bond formation. The present study tested the hypothesis that oxytocin participates in the partner preference component of pair bond formation in adult prairie voles. Ovariectomized female prairie voles were implanted with osmotic mini‐pumps releasing oxytocin (1–100 ng/h) or artificial cerebrospinal fluid (CSF). Pumps were implanted intracerebroventricularly or subcutaneously and females then were housed for 6 h with a male partner, followed by a preference test in which females could elect to spend time with either the partner or an unfamiliar male. Females in groups that received centrally‐administered oxytocin (10 or 100 ng/h), but not CSF, exhibited a significant preference for the partner present during infusion. The induction of a partner preference after oxytocin administration appeared specific for central oxytocin pathways as peripheral oxytocin administration was ineffective. Moreover, central administration of a selective oxytocin receptor antagonist inhibited the behavioral effect of exogenous oxytocin. These results suggest that oxytocin may be one factor contributing to the development of partner preferences in this monogamous rodent.

Oxytocin and sexual behavior.

The neurohypophyseal hormone oxytocin has been implicated in many aspects of reproduction including sexual behavior. This review considers the hypotheses that oxytocin and/or the neural events surrounding the release of oxytocin may have behavioral effects during sexual arousal, orgasm, sexual satiety and other aspects of sociosexual interactions.

Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?

Autism spectrum disorders (ASD) are male-biased and characterized by deficits in social behavior and social communication, excessive anxiety or hyperreactivity to stressful experiences, and a tendency toward repetitiveness. The purpose of this review is to consider evidence for a role for two sexually dimorphic neuropeptides, oxytocin (OT) and arginine vasopressin (VP), in these features of ASD. Both VP and OT play a role in normal development. VP is androgen-dependent and of particular importance to male behavior. Excess VP or disruptions in the VP system could contribute to the male vulnerability to ASD. Alternatively, protective processes mediated via OT or the OT receptor might help to explain the relatively rare occurrence of ASD in females. Disruptions in either OT or VP or their receptors could result from genetic variation or epigenetic modifications of gene expression, especially during early development. Deficits in other developmental growth factors, such as reelin, which may in turn regulate or be regulated by OT or VP, are additional candidates for a role in ASD.

Development of partner preferences in female prairie voles (Microtus ochrogaster): The role of social and sexual experience.

Prairie voles (Microtus ochrogaster) exhibit a monogamous mating system characterized by long-term pair bonds between mates. The purpose of this study was to examine the effect of cohabitation time and sexual experience on the development of pair bond formation in female prairie voles. Females that were allowed to cohabit for 24 hr or more, with or without mating, exhibited a strong social preference for a familiar partner versus a strange male. Females that cohabited and mated for 6 hr showed strong preferences for a familiar partner, while cohabitation for less than 24 hr, without mating, did not result in preferences for the familiar male. These results indicate that mating was not essential for partner preference formation; however, preferences developed more rapidly when mating occurred.

Developmental consequences of oxytocin.

This paper examines the developmental effects of the mammalian neuropeptide, oxytocin (OT). In adults, OT is the most abundant neuropeptide in the hypothalamus and serves integrative functions, coordinating behavioral and physiological processes. For example, OT has been implicated in parturition, lactation, maternal behavior and pair bond formation. In addition, OT is capable of moderating behavioral responses to various stressors as well as the reactivity of the hypothalamic-pituitary-adrenal (HPA) axis. Neonates may be exposed to hormones of maternal origin, possibly including peptides administered to the mother in the perinatal period to hasten or delay birth and in milk; however, whether peptide hormones from the mother influence the developing infant remains to be determined. In rodents, endogenous OT is first synthesized during the early postnatal period, although its functions at this time are not well known. Experiments in neonatal prairie voles have documented the capacity of OT and OT receptor antagonists to have immediate and lifelong consequences for social behaviors, including adult pair bonding and parental behaviors, as well as the reactivity of the HPA axis; most of these effects are sexually dimorphic. Possible mechanisms for such effects, including long-lasting changes in OT and vasopressin, are summarized.

Oxytocin, vasopressin and sociality

The neurobiology of social behaviour is interwoven with autonomic, endocrine and other homoeostatic processes responsible for the adaptive functions of reproduction and survival. Young mammals are dependent on their mothers for nourishment, and the interaction between the mother and infant may be a physiological and neuroendocrine prototype for mammalian sociality. Although these adaptive functions of the mother-infant social behavioural dyad are obvious, adult social interactions, including social bonds, also are important to health and survival. Two neuropeptides, oxytocin (OXT) and arginine vasopressin (AVP), have been repeatedly implicated in mammalian social behaviours and emotional states that support sociality. Although best known for their roles in reproduction and homoeostasis, these peptides play a central role in the activation and expression of social behaviours and emotional states. Recent studies from our work with the prairie vole (Microtus ochrogaster), reviewed here, reveal a role for both OXT and AVP in behavioural and endocrine changes during social interactions, and also changes that are associated with the absence of social interactions (i.e. social isolation).

Oxytocin pathways and the evolution of human behavior.

This review examines the hypothesis that oxytocin pathways--which include the neuropeptide oxytocin, the related peptide vasopressin, and their receptors--are at the center of physiological and genetic systems that permitted the evolution of the human nervous system and allowed the expression of contemporary human sociality. Unique actions of oxytocin, including the facilitation of birth, lactation, maternal behavior, genetic regulation of the growth of the neocortex, and the maintenance of the blood supply to the cortex, may have been necessary for encephalization. Peptide-facilitated attachment also allows the extended periods of nurture necessary for the emergence of human intellectual development. In general, oxytocin acts to allow the high levels of social sensitivity and attunement necessary for human sociality and for rearing a human child. Under optimal conditions oxytocin may create an emotional sense of safety. Oxytocin dynamically moderates the autonomic nervous system, and effects of oxytocin on vagal pathways, as well as the antioxidant and anti-inflammatory effects of this peptide, help to explain the pervasive adaptive consequences of social behavior for emotional and physical health.