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.

Keywords: attachment; cortisol; oxytocin; separation; stress; vasopressin.

Figure 1

Schematic of research design. Males underwent five conditions. The first two were a baseline scan while with their pair mate, and a short separation of 48 h. These two conditions were counterbalanced. All males then underwent a 2-week long “long separation” from their pair mate. They then underwent two final scans, following an encounter with a stranger female or a reunion with their pair mate (these two scans were also counterbalanced).

Figure 2

Positron emission tomography (PET) image co-registered with structural magnetic resonance imaging (MRI).

Figure 3

Fluorodeoxyglucose (FDG) uptake by condition. Please note that FDG in some areas also demonstrated a time-based effect, which is not shown on the graph (see Table 1). In some cases, this may be the reason that an effect designated as statistically significant may not appear so on the graph. (A) FDG uptake in the nucleus accumbens (NAcc), ventral pallidum (VP) and posterior cingulate cortex (PCC), in comparison to baseline. Conditions included a baseline scan, a short separation (short sep), a long separation (long sep), encounter with a strange female (stranger) and reunion with the partner (partner). *p < 0.05 for comparison to baseline concentrations. (B) FDG uptake in the lateral septum (LS), medial amygdala (MeA), medial preoptic area (MPOA) and central amygdala (CeA), by condition, in comparison to baseline. (C) FDG uptake in the supraoptic nucleus of the hypothalamus (SON), paraventricular nucleus of the hypothalamus (PVN), periaqueductal gray (PAG) and cerebellum (Cere); by condition, in comparison to baseline.

Figure 4

Hormones by condition. (A) Concentrations of oxytocin (OT) and vasopressin (AVP) in cerebrospinal fluid (CSF), in comparison to baseline. Conditions included a baseline scan, a short separation (short sep), a long separation (long sep), encounter with a strange female (stranger) and reunion with the partner (partner). *p < 0.05 for comparison to baseline concentrations. (B) Concentrations of plasma OT and AVP, in comparison to baseline. (C) Concentrations of plasma cortisol and glucose, in comparison to baseline. (D) Concentrations of plasma insulin, in comparison to baseline.

Figure 5

FDG uptake by fatherhood. FDG uptake in the SON (supraoptic nucleus of the hypothalamus) and the PVN (paraventricular nucleus of the hypothalamus) upon encountering a stranger female was higher in males that did not have offspring with their pair mate (non-fathers), than in males that did have offspring with their pair mate (fathers). *p < 0.05.

Figure 6

Hormones by fatherhood. Plasma AVP, CSF OT and plasma glucose were all significantly lower in fathers than non-fathers during a reunion with their pair mate; while plasma cortisol was higher. *p < 0.05.

Figure 7

Summary of effects of each condition.

Figure 8

Proposed relationships of neural and hormonal changes associated with short separation. The parts that are in bold are data from this study; the other relationships are hypothesized.