Challenges to the Pair Bond: Neural and Hormonal Effects of Separation and Reunion in a Monogamous Primate

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.

Oxytocin regulates reunion affiliation with a pairmate following social separation in marmosets

“…We found that OT treatments had more prominent effects following a long-separation challenge that was designed to induce biobehavioral distress (Cavanaugh et al, 2016) than following a short-separation challenge that was designed to be minimally stressful (Mustoe et al, 2015, 2016). In male titi monkeys ( Callicebus cupreus ), levels of CSF OT were elevated during both prolonged (48 hr) and long-term (2–3 weeks) separation from a pairmate (Hinde et al, 2016). While CSF OT levels remained elevated during reunion with their pairmate and during exposure to opposite-sex strangers, following separation, reunion with their pairmate stimulated coordinated release of both central and peripheral OT.…”

“…While CSF OT levels remained elevated during reunion with their pairmate and during exposure to opposite-sex strangers, following separation, reunion with their pairmate stimulated coordinated release of both central and peripheral OT. Moreover, males that previously reproduced with their pairmate had lower neural activity in the supraoptic (SON) and paraventricular (PVN) nuclei of the hypothalamus (central hubs of OT production) during exposure to an opposite-sex stranger, than males that had not reproduced with their pairmate (Hinde et al, 2016). This suggests that oxytocinergic activity underlies reunion behavior differently as a function of experiences in the pair (i.e., raising vs. not raising offspring), and that the OT system is sensitive to the level of reproductive success of an individual’s current relationship and implicates fatherhood as bond-enhancing experience.…”

“…Measures across individuals were balanced and order effects were counter-balanced across separations and therefore time or order effects were not analyzed. Independent correlation matrices provided the best model fits and were used for both analyses; though, notably, there were very few significant differences in model effects using exchangeable correlation matrices, which have been utilized previously (Hinde et al, 2016). GEE was preferred over GLMM models due to issues with convergence on the measure of proximity during separation.…”

“…Although the role of OT in the regulation of social behavior upon reunion in marmosets has not yet been addressed, data from the pairliving and socially monogamous titi monkey ( Callicebus moloch ) suggests that changes in endogenous OT release may facilitate reunion in this species, particularly for prolonged social separations. In male titi monkeys, CSF OT is elevated during both prolonged (48 hr) and long-term (2–3 weeks) separations from pairmates (Hinde et al, 2016). Reunion with their pairmate, but not exposure to an opposite-sex stranger, following the separations stimulated coordinated release of both CSF and plasma OT, suggesting that the OT response is induced specifically by the long-term partner, and that the elevated OT response may facilitate social behavior that is specific to long-term partners in monogamous primates.…”

Imaging, Behavior and Endocrine Analysis of “Jealousy” in a Monogamous Primate

“…Subjects, pair mates and young offspring (less than one year old) were relocated to a metabolism room 48 hours prior to their positron emission tomography (PET) scan. As in our previous PET studies (Bales et al, 2007; Hinde et al, 2016; Maninger et al, 2017), animals were relocated prior to the scan in order to reduce the possible effect of novel housing on brain metabolism. Animals were fasted 6–12 h prior to the scan, with water available throughout the pre-scan period.…”