Early involvement in friendships predicts later plasma concentrations of oxytocin and vasopressin in juvenile rhesus macaques (Macaca mulatta).

Tamara A R Weinstein,John P Capitanio,Nicole Maninger,Caroline M Hostetler,Karen L Bales

doi:10.3389/fnbeh.2014.00295

Abstract

The neuropeptides oxytocin (OT) and arginine vasopressin (AVP) are involved in social bonding in attachment relationships, but their role in friendship is poorly understood. We investigated whether rhesus macaques’ (Macaca mulatta) friendships at age one predicted plasma OT and AVP at two later time points. Subjects were 54 rhesus macaques at the California National Primate Research Center (CNPRC). Blood was drawn during a brief capture-and-release in the home cage, and plasma assayed for OT and AVP using an enzyme immunoassay (EIA). Separate linear mixed models for each sex tested the effects of dominance rank, age, sampling time point, housing condition, parturition status, two blood draw timing measures, and five friendship types: proximity friendships, play friendships, reciprocal friendships (a preference for a peer that also preferred the subject), multiplex friendships (friendships displayed in more than one behavioral domain), and total number of friendships. Females’ number of reciprocal and play friendships at age one significantly predicted later OT; additionally, these two friendship types interacted with rank, such that high-ranking females with the fewest friendships had the highest OT concentrations. Friendship did not predict later OT levels in males, however proximity, play, reciprocal, and total number of friendships predicted males’ plasma AVP. Play and total number of friendships also tended to predict AVP in females. Our results show that peripheral measures of neuroendocrine functioning in juvenile rhesus monkeys are influenced by early involvement in friendships. Friendships have an especially strong impact on an individual’s psychosocial development, and our data suggest OT and AVP as potential underlying mechanisms. Moreover, sex differences in the functioning of the OT and AVP systems, and their relation to friendship, may have important clinical implications for the use of OT as a therapeutic, as well as informing the social context in which it is administered.

Highlights

Friendships are critically important for healthy development throughout the lifespan, and a lack of friends increases vulnerability to mental disorders such as depression, physical illnesses such as cardiovascular disease, and mortality (Cohen and Wills, 1985; House et al, 1988; Uchino et al, 1996; Thorsteinsson and James, 1999)
Our study revealed that the number and quality of friendships experienced early in development by young rhesus monkeys predict the future functioning of their OT and arginine vasopressin (AVP) systems
Reciprocal friendships are significant in young rhesus monkeys, as they are among the highest quality friendships, and are most likely to persist over time (Weinstein and Capitanio, 2012); similar results have been found in humans (Gershman and Hayes, 1983; Bukowski et al, 1994)

Summary

Introduction

Friendships are critically important for healthy development throughout the lifespan, and a lack of friends increases vulnerability to mental disorders such as depression, physical illnesses such as cardiovascular disease, and mortality (Cohen and Wills, 1985; House et al, 1988; Uchino et al, 1996; Thorsteinsson and James, 1999). Preadolescence may be an especially critical time period for the successful development of adult social skills and ties (Fullerton and Ursano, 1994), and the consequences of friendship formation during this period may be far reaching; for example, friended preadolescents report higher levels of self-worth in adulthood when measured 12 years later, while the absence of friendship is associated with psychopathological symptoms in adulthood (Bagwell et al, 1998). Rhesus macaques have long been regarded as a valuable model system in which to examine socioemotional development, due to the cognitive abilities, physiological and neuroanatomical characteristics, and socioemotional complexity which they share with humans (Suomi, 2005; Capitanio and Emborg, 2008; Weinstein et al, 2008; Nelson and Winslow, 2009; Weiss et al, 2011), and may be uniquely capable of filling the large gap that exists between human and rodent research on the neurobiological basis of affiliative relationships (Weinstein and Capitanio, 2005). The few studies far that have attempted to close this gap suggest that the neuropeptides oxytocin (OT) and arginine vasopressin (AVP) play a key role

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