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

Alexander Baxter,A M Seelke,M Anderson,S M Freeman,K L Bales,E L Kinnally

doi:10.1038/s41598-020-74243-1

Alexander Baxter, A M Seelke + Show 4 more

Open Access

https://doi.org/10.1038/s41598-020-74243-1

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Journal: Scientific Reports	Publication Date: Oct 14, 2020
Citations: 17	License type: open-access

Affiliation: University of California, Davis

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.

Highlights

Social cognition is facilitated by oxytocin receptors (OXTR) in the hippocampus, a brain region that changes dynamically with pregnancy, parturition, and parenting experience
A MANOVA showed a main effect of parental status on OXTR binding density across presubiculum [including layers 1 (PSB1) and presubiculum layer 3 (PSB3) (F(1, 8) = 5.70, p = 0.034, Pillai’s trace = 0.62)
There was no effect of parental status on OXTR binding across the total presubiculum (i.e., when OXTR binding was quantified across PSB1 and PSB3 together; t(8) = − 1.72, p = 0.12, d = − 1.11), and there was no effect of parental status in a MANOVA with OXTR binding in the hippocampus subregions (CA1, CA2/3, CA4, dentate gyrus, and the subiculum) as dependent variables (F(1, 8) = 0.78, p = 0.61, Pillai’s trace = 0.49)

Summary

Introduction

Social cognition is facilitated by oxytocin receptors (OXTR) in the hippocampus, a brain region that changes dynamically with pregnancy, parturition, and parenting experience. Virgin female rats typically avoid or attack pups, changes occur in the maternal brain after they give birth to their first litter that increase approach behavior and inhibit avoidance behavior, leading to maternal care of offspring ( see[1]) This pathway is well-characterized and is regulated by the hormones oxytocin, estrogen, and progesterone acting in the medial preoptic area, which leads to top-down modulation of mesolimbic dopaminergic structures, including the nucleus accumbens shell, ventral tegmental area, and ventral p allidum[1,2,3]. Through these and other mechanisms, oxytocin plays an important role in regulating hippocampal neuroplasticity, which renders it an excellent candidate system for the neural mechanisms underlying parenting-related changes in the hippocampus[8] In support of this premise, some rodent studies suggest that hippocampal OXTR binding changes in response to pup exposure[22] and during pregnancy[23]. The evidence is mixed, and some studies have found no differences in females’ hippocampal OXTR binding at different stages of pregnancy, parturition, and the post-partum[24,25,26]

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