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

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          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.

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          Most cited references 110

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          Stress, social support, and the buffering hypothesis.

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            Social relationships and health.

            Recent scientific work has established both a theoretical basis and strong empirical evidence for a causal impact of social relationships on health. Prospective studies, which control for baseline health status, consistently show increased risk of death among persons with a low quantity, and sometimes low quality, of social relationships. Experimental and quasi-experimental studies of humans and animals also suggest that social isolation is a major risk factor for mortality from widely varying causes. The mechanisms through which social relationships affect health and the factors that promote or inhibit the development and maintenance of social relationships remain to be explored.
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              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.
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                Author and article information

                Contributors
                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                28 August 2014
                2014
                : 8
                Affiliations
                1California National Primate Research Center, University of California Davis, CA, USA
                2Department of Behavioral Neuroscience, Oregon Health and Science University Portland, OR, USA
                Author notes

                Edited by: Lisa A. Parr, Emory University, USA

                Reviewed by: René Hurlemann, University of Bonn, Germany; Lisa A. Parr, Emory University, USA

                *Correspondence: Tamara A. R. Weinstein, California National Primate Research Center, University of California, One Shields Avenue, Davis, CA 95616, USA e-mail: tarweinstein@ 123456ucdavis.edu

                This article was submitted to the journal Frontiers in Behavioral Neuroscience.

                Article
                10.3389/fnbeh.2014.00295
                4147354
                Copyright © 2014 Weinstein, Bales, Maninger, Hostetler and Capitanio.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 5, Tables: 5, Equations: 0, References: 143, Pages: 13, Words: 12039
                Categories
                Neuroscience
                Original Research Article

                Neurosciences

                affiliation, friendship, oxytocin, rhesus macaque, social behavior, vasopressin

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