Oxytocin receptor binding in the titi monkey hippocampal formation is associated with parental status and partner affiliation

Abstract

Social cognition is facilitated by oxytocin receptors (OXTR) in the hippocampus, a brain region that changes dynamically with pregnancy, parturition, and parenting experience. We investigated the impact of parenthood on hippocampal OXTR in male and female titi monkeys, a pair-bonding primate species that exhibits biparental care of offspring. We hypothesized that in postmortem brain tissue, OXTR binding in the hippocampal formation would differ between parents and non-parents, and that OXTR density would correlate with frequencies of observed parenting and affiliative behaviors between partners. Subjects were 10 adult titi monkeys. OXTR binding in the hippocampus (CA1, CA2/3, CA4, dentate gyrus, subiculum) and presubiculum layers (PSB1, PSB3) was determined using receptor autoradiography. The average frequency of partner affiliation (Proximity, Contact, and Tail Twining) and infant carrying were determined from longitudinal observations (5–6 per day). Analyses showed that parents exhibited higher OXTR binding than non-parents in PSB1 (t(8) = − 2.33, p = 0.048), and that OXTR binding in the total presubiculm correlated negatively with Proximity (r = − 0.88) and Contact (r = − 0.91), but not Tail Twining or infant carrying. These results suggest that OXTR binding in the presubiculum supports pair bonding and parenting behavior, potentially by mediating changes in hippocampal plasticity.

Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles

“…To our knowledge, this is the first study showing that acute oxytocinergic modulation of excitatory transmission can be different depending on an adult's social history. Altered connectivity within neural networks is usually attributed to synaptic plasticity 45,46 or state-dependent neuromodulation (e.g., release or receptor expression) 16,47 rather than changes in how neurotransmitters themselves work within the network. In fact, most studies of how OXTR agonists facilitate social behavior assume its mechanistic stability over state and time in adults.…”

Neural correlates of mating system diversity: oxytocin and vasopressin receptor distributions in monogamous and non-monogamous Eulemur

“…Oxytocin acting on OXTRs in the NAcc is necessary for pair-bond formation in voles 4 . Precise functions of oxytocin or vasopressin within the hippocampal formation remain to be identified 68 , but there is some evidence that they modulate the encoding and consolidation of socially relevant memories 69,70 . In any event, our divergent results in these regions suggest that neural mechanisms of pair bonding in lemurs may differ substantially from other mammalian groups studied thus far.…”

“…Thus, while receptor distributions can differ widely between species and social systems 18,19,22 , they might also differ substantially within individuals of the same species or mating system. Indeed, Phelps and Young 27 report intraspecific variation in AVPR1a binding among prairie voles often comparable to or greater than interspecific variation (for a recent example of experience-dependent, intraspecific OXTR patterns in a primate model, see 68 ). Nevertheless, these same authors also report less variation in regions regulating social bonding, relative to those unrelated to social bonding-a pattern consistent with natural selection winnowing neuropeptide expression in these former regions.…”

Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles

“…Building social relationships presumably involves neural changes in the steps leading from perception of another to the behavioral action towards that individual. Altered connectivity within neural networks is usually attributed to synaptic plasticity (Rutherford et al 2020; Marlin and Froemke 2017) or state-dependent neuromodulation (e.g., release or receptor expression) (Marlin et al 2015; Baxter et al 2020), rather than changes in how neurotransmitters themselves work within the network. In fact, most studies of how OXT facilitates social behavior assume its mechanistic stability over state and time in adults (Marlin et al 2015; Wei et al 2015; Bartz et al 2011).…”