Abstract

Social monogamy at its most basic is a group structure in which two adults form a unit and share a territory. However, many socially monogamous pairs display attachment relationships known as pair bonds, in which there is a mutual preference for the partner and distress upon separation. The neural and hormonal basis of this response to separation from the adult pair mate is under-studied. In this project, we examined this response in male titi monkeys (Callicebus cupreus), a socially monogamous New World primate. Males underwent a baseline scan, a short separation (48 h), a long separation (approximately 2 weeks), a reunion with the female pair mate and an encounter with a female stranger (with nine males completing all five conditions). Regional cerebral glucose metabolism was measured via positron emission tomography (PET) imaging using [18F]-fluorodeoxyglucose (FDG) co-registered with structural magnetic resonance imaging (MRI), and region of interest (ROI) analysis was carried out. In addition, plasma was collected and assayed for cortisol, oxytocin (OT), vasopressin (AVP), glucose and insulin concentrations. Cerebrospinal fluid (CSF) was collected and assayed for OT and AVP. We used generalized estimating equations (GEE) to examine significant changes from baseline. Short separations were characterized by decreases in FDG uptake, in comparison to baseline, in the lateral septum (LS), ventral pallidum (VP), paraventricular nucleus of the hypothalamus (PVN), periaqueductal gray (PAG), and cerebellum, as well as increases in CSF OT, and plasma cortisol and insulin. Long separations differed from baseline in reduced FDG uptake in the central amygdala (CeA), reduced whole brain FDG uptake, increased CSF OT and increased plasma insulin. The response on encounter with a stranger female depended on whether or not the male had previously reproduced with his pair mate, suggesting that transitions to fatherhood contribute to the neurobiology underlying response to a novel female. Reunion with the partner appeared to stimulate coordinated release of central and peripheral OT. The observed changes suggest the involvement of OT and AVP systems, as well as limbic and striatal areas, during separation and reunion from the pair mate.

Highlights

  • Social bonds form the foundation of our daily lives, and are widely acknowledged to have far-reaching effects on health and psychological well-being (Uchino, 2006; Cacioppo et al, 2015; Valtorta et al, 2016)

  • Pair bonds are forms of attachment relationships (Hazan and Shaver, 1987); first studied in mothers and offspring (Bowlby, 1969; Ainsworth et al, 1978), these attachment relationships include a strong preference for the familiar partner, distress upon separation from the partner and the ability of the partner to buffer the individual against stress (Mason and Mendoza, 1998)

  • In the short-term separation condition, as compared to baseline, FDG uptake was lower in the ventral pallidum (VP), lateral septum (LS), the PVN, the periaqueductal gray (PAG) and the cerebellum (Cere)

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Summary

INTRODUCTION

Social bonds form the foundation of our daily lives, and are widely acknowledged to have far-reaching effects on health and psychological well-being (Uchino, 2006; Cacioppo et al, 2015; Valtorta et al, 2016). Chronic separation from the pair mate resulted in increased plasma corticosterone and increased OT, AVP and corticotrophin-releasing hormone (CRH) in the PVN of the hypothalamus; plasma OT and AVP did not change (Bosch et al, 2009; McNeal et al, 2014; Sun et al, 2014) This differs from human studies in which challenges to the pair bond or grief at the loss of a loved one, appear to result in sex-specific changes in plasma OT and AVP (Taylor et al, 2000, 2010). Based on evidence from prairie voles that pair bonding may be facilitated by reproduction (Resendez et al, 2016), we compared responses to reunion as a function of whether or not the pair had produced offspring together prior to the separation, predicting increased neural uptake in fathers in the PVN, SON and LS

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