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 three 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 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.Most primate species are highly social, and a number of species form stable, long-term malefemale relationships with strong social attachments, referred to as pair-bonds (Kleiman, 1977;Fuentes, 1999). Pair-bond formation and maintenance are marked by mutual attraction, high rates of selective sociosexual behavior between the pair, and aggression toward unfamiliar conspecifics. Curiously, the neural mechanisms underlying these social relationships in primates have only received limited consideration (Bales et al., 2007) and consequently are not well understood. In this present paper, we used several behavioral assays along with manipulation of oxytocin (OT) activity to examine the underlying neural mechanisms that 1Corresponding author: Adam S. Smith, Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, Florida, C448 PDB, 1107 W. Call Street, Tallahassee, FL, 32306. asmith@neuro.fsu.edu, (850) 645-8716. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors ...

Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird

“…Indeed, although nonapeptides modulate affiliation in virtually every species that has been studied, nonapeptide effects on pair bonding have been demonstrated only in prairie voles and zebra finches [5,29] ( present study). For instance, despite significant effects on other aspects of affiliation, neither OT nor OTA administrations influence the establishment of pair bonds or subsequent partner preference in marmosets [21]. Similarly, injections of a nonapeptide receptor antagonist reduce affiliative behaviours during pair bond formation in the monogamous convict cichlid, but do not impair the ability to form a pair bond [20].…”

“…For instance, in a monogamous cichlid (Amatitlania nigrofasciata), administrations of a nonapeptide antagonist initially reduce affiliative behaviour towards a potential partner and decrease aggression towards neighbours, but do not prevent the formation of pair bonds, and antagonist treatment has no effect on affiliation or mate guarding in established pairs [20]. Similarly, administrations of OT and OT receptor antagonist (OTA) to marmosets (Callithrix penicillata) produce significant effects on partnerdirected affiliative behaviours, but have no effect on the ability to form a pair bond or on subsequent partner preference [21]. A recent study of eight Peromyscus mouse species further shows that the monogamous species lack multiple V1aR characteristics that distinguish prairie voles from their non-monogamous congeners [22], and chronic central infusions of a VP V 1 antagonist cocktail do not impair pair bond formation in male zebra finches [23].…”

A novel form of oxytocin in New World monkeys

“…This substitution could change the overall binding property of the mutated [P8] oxytocin peptide, therefore rendering it more or less able to regulate species-typical reproductive and social behaviours. To date, all pharmacological studies of New World monkey species have involved administration of the conserved oxytocin peptide to species with the P8 mutation [11,12]. Detailed in vitro assays of oxytocin, [P8] oxytocin and arginine vasopressin, as well as their respective receptors, could provide insight on the role of this mutation on binding and activation in these peptide signalling systems, and guide pharmacological studies of the in vivo effects of oxytocin in primate species with and without this mutation.…”

Gene expression correlates of social evolution in coral reef butterflyfishes

“…Indeed, nonapeptide and DA systems appear to regulate pair bonding in other species that span several lineages, and appear to do so through targeting similar brain regions. In male and female marmosets, Callithrix penicillata, OT promotes while an OTR antagonist reduces affiliation during cohabitation with a prospective partner 93 . Similarly, in male and female tamarins, Saquinus Oedipus, urinary OT increases with intra-pair affiliation 94 .…”