Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata

Abstract

The establishment and maintenance of stable, long-term male-female relationships, or pair-bonds, are marked by high levels of mutual attraction, selective preference for the partner, and high rates of sociosexual behavior. Central oxytocin (OT) affects social preference and partner-directed social behavior in rodents, but the role of this neuropeptide has yet to be studied in heterosexual primate relationships. The present study evaluated whether the OT system plays a role in the dynamics of social behavior and partner preference during the first 3 weeks of cohabitation in male and female marmosets, Callithrix penicillata. OT activity was stimulated by intranasal administration of OT, and inhibited by oral administration of a non-peptide OT-receptor antagonist (L-368,899; Merck). Social behavior throughout the pairing varied as a function of OT treatment. Compared to controls, marmosets initiated huddling with their social partner more often after OT treatments but reduced proximity and huddling after OT antagonist treatments. OT antagonist treatment also eliminated food sharing between partners. During the 24-h preference test, all marmosets interacted more with an opposite-sex stranger than with the partner. By the third-week preference test, marmosets interacted with the partner and stranger equally with the exception that intranasal-OT treatments facilitated initial partner-seeking behavior over initial contact with the stranger. Our findings demonstrate that pharmacological manipulations of OT activity alter partner-directed social behavior during pair interactions, suggesting that central OT may facilitate the process of pair-bond formation and social relationships in marmoset monkeys.

Fig. 1

Social behavior during the first three weeks of pairing as a function of OT treatment. (a) The mean frequency (± s.e.m.) of initiations of close proximity with the partner per observation as a function of the treatment condition. (b) The mean frequency (± s.e.m.) of initiations of huddling with the partner per observation as a function of the treatment condition. (c) The mean number (± s.e.m.) of food shares with the partner throughout the pairing as a function of the treatment condition. White bar indicates intranasal OT treatment (OT+), grey bars indicate control treatment (Control), and black bars indicate the oral OT antagonist treatment (OT−). * p’s < 0.05.

Fig. 2

Social behavior during the 24-h and 3-week partner preference tests. The behaviors include (a) the mean duration (± s.e.m.) of time spent in close proximity, (b) the latency to first contact the social stimuli, and (c) the mean number (± s.e.m.) of approaches or initiations of close proximity during the 20 min preference test. White bar indicates interactions with the partner, grey bars indicate interactions with the opposite-sex stranger, and black bars indicate behavior while alone near the neutral, empty cage.

Fig. 3

The latency to first approach each social stimuli during the 3-week preference test controlling for OT manipulation (OT treatment (OT+), control treatment (Control), and OT antagonist treatment (OT−)). White bar indicates interactions with the partner, grey bars indicate interactions with the opposite-sex stranger, and black bars indicate behavior while alone near the neutral, empty cage.

Fig 4

The mean number (± s.e.m.) of approaches to the neutral cage during the three week preference test. White bar indicates intranasal OT treatment (OT+), grey bars indicate control treatment (Control), and black bars indicate the oral OT antagonist treatment (OT−).