Life in groups: the roles of oxytocin in mammalian sociality

Abstract

In recent decades, scientific understanding of the many roles of oxytocin (OT) in social behavior has advanced tremendously. The focus of this research has been on maternal attachments and reproductive pair-bonds, and much less is known about the substrates of sociality outside of reproductive contexts. It is now apparent that OT influences many aspects of social behavior including recognition, trust, empathy, and other components of the behavioral repertoire of social species. This review provides a comparative perspective on the contributions of OT to life in mammalian social groups. We provide background on the functions of OT in maternal attachments and the early social environment, and give an overview of the role of OT circuitry in support of different mating systems. We then introduce peer relationships in group-living rodents as a means for studying the importance of OT in non-reproductive affiliative behaviors. We review species differences in oxytocin receptor (OTR) distributions in solitary and group-living species of South American tuco-tucos and in African mole-rats, as well as singing mice. We discuss variation in OTR levels with seasonal changes in social behavior in female meadow voles, and the effects of OT manipulations on peer huddling behavior. Finally, we discuss avenues of promise for future investigation, and relate current findings to research in humans and non-human primates. There is growing evidence that OT is involved in social selectivity, including increases in aggression toward social outgroups and decreased huddling with unfamiliar individuals, which may support existing social structures or relationships at the expense of others. OT's effects reach beyond maternal attachment and pair bonds to play a role in affiliative behavior underlying "friendships", organization of broad social structures, and maintenance of established social relationships with individuals or groups.

Keywords: aggression; group living; maternal behavior; oxytocin; pair bond; social behavior; sociality; voles.

Figure 1

Representative variation in OTR distribution in rodent species. Even between closely related rodent species, the density and distribution of OTRs shows striking variation. Top row: schematic diagrams of approximate coronal sections displayed (modified from Paxinos and Franklin, 2012). Left column: labels indicate the nucleus accumbens (NAc), endopiriform nucleus (EN), and islands of Calleja (ICj). Center column: lateral septum (LS). Right column: binding in the hippocampus is seen in some animals, as well as binding in the basolateral and central nuclei of the amygdala (BLA, CeA), and ventromedial hypothalamus (VMH). Brain sections are adapted from figures of I¹²⁵ OVTA autoradiographic assays conducted in meadow voles (Beery and Zucker, 2010), tuco-tucos (Beery et al., 2008a), naked mole-rats (Kalamatianos et al., 2010), and singing mice (Campbell et al., 2009), used with permission of original authors and publishers. Brain sizes are not to scale and image brightness and contrast have been adjusted across species to approximately match background density; comparisons of distribution of binding may be made between species, but comparisons of density should be avoided. Arrows indicate brain regions indicated in the schema.