Elsevier

Hormones and Behavior

Volume 50, Issue 4, November 2006, Pages 506-517
Hormones and Behavior

Neuropeptidergic regulation of affiliative behavior and social bonding in animals

https://doi.org/10.1016/j.yhbeh.2006.06.028Get rights and content

Abstract

Social relationships are essential for maintaining human mental health, yet little is known about the brain mechanisms involved in the development and maintenance of social bonds. Animal models are powerful tools for investigating the neurobiological mechanisms regulating the cognitive processes leading to the development of social relationships and for potentially extending our understanding of the human condition. In this review, we discuss the roles of the neuropeptides oxytocin and vasopressin in the regulation of social bonding as well as related social behaviors which culminate in the formation of social relationships in animal models. The formation of social bonds is a hierarchical process involving social motivation and approach, the processing of social stimuli and formation of social memories, and the social attachment itself. Oxytocin and vasopressin have been implicated in each of these processes. Specifically, these peptides facilitate social affiliation and parental nurturing behavior, are essential for social recognition in rodents, and are involved in the formation of selective mother–infant bonds in sheep and pair bonds in monogamous voles. The convergence of evidence from these animal studies makes oxytocin and vasopressin attractive candidates for the neural modulation of human social relationships as well as potential therapeutic targets for the treatment of psychiatric disorders associated with disruptions in social behavior, including autism.

Introduction

Healthy social relationships are essential for proper mental health and many psychiatric disorders are associated with disruptions in social motivation and the ability to maintain social relationships (Bowlby, 1977, House et al., 1988, Kiecolt-Glaser and Newton, 2001, Monroe et al., 1986). Relationships among spouses, family, and friends are universally important across all human societies, yet little is known about the neurobiological mechanisms underlying the development and maintenance of such human relationships. Aside from a handful of postmortem studies and more recent functional imaging approaches, the neurobiology of human social behavior has been difficult to study. Fortunately, research using animal models has begun to provide insights into the social brain and the regulation of social relationships. Although the research in this field is far from complete, these animal models can serve to complement existing data on normal human social behavior and guide investigations of the neurobiology of pathological sociality, such as in autism spectrum disorders (see Bartz and Hollander, in this issue).

The formation and maintenance of social relationships are a complex process that involves several levels of information processing in the brain. For both ease and clarity, animal models of social behavior have generally focused on a single level of processing at a time. Therefore, we have developed a simplified conceptual framework as a useful heuristic tool for understanding the neurobiology of social bonds, and we will follow that framework in this review. First, the organism must be motivated to approach and engage another individual. Next, the animal must be able to identify the individual based on social cues through the formation of social memories. Finally, given the appropriate conditions, a bond can form, leading to preferential interaction with that individual. Each of these conceptual levels engages different brain regions and neural circuits. Thus, neuropathology can occur at any level of this framework, with the resulting phenotype being a global impairment in the development of social relationships. This chapter will discuss the animal models developed for each of the three levels with a focus on the neuropeptides oxytocin and vasopressin as a preface to the following review, which will discuss translational implications relevant to these basic neuroscience discoveries (Bartz and Hollander, in this issue).

Section snippets

Background

The neurohypophyseal hormones oxytocin and vasopressin play central roles in the regulation of affiliative behavior and social bonding in animals. Oxytocin is best known for its reproductive role in the peripheral circulation, particularly in contraction of the uterus during labor and ejection of milk during lactation (Burbach et al., 2006). Oxytocin is synthesized in magnocellular neurons in the paraventricular and supraoptic nuclei of the hypothalamus (PVN and SON, respectively), which

Social approach and motivation

The neurobiology of social approach and motivation can be studied by measuring the latency time to approach another individual and the amount of time spent in social contact. Here we discuss the role of oxytocin and vasopressin in three general animal models of social approach and motivation: parental behavior, infant–mother interactions, and adult affiliation. At this conceptual level, social motivation is primarily non-selective in nature. For example, maternal female rodents direct maternal

Social recognition

The recognition of a familiar individual and the formation of a social memory of that individual is the next major step to forming a social bond. The neurobiology of social recognition and memory in rodent models can be studied in the laboratory by measuring the duration of social investigation during subsequent exposures to the same individual. This behavioral assay is based upon the phenomenon that rodents investigate novel items (or individuals) longer than familiar items (or individuals).

Social bond formation

Social bonding is a complex social behavior that requires the integration of many cognitive processes including social approach, motivation, and memory formation. Once an individual is motivated to approach another individual and forms a memory of that individual, then the stage is set for the formation of a social relationship. Animal models of attachment behavior are different from the general, non-selective maternal or affiliation behaviors described earlier; attachment bonds between

Implications for human bonding

Are there neurobiological correlates of social behavior in humans? Given the roles of oxytocin and vasopressin in social attachment in rodent and sheep models, one might expect to find abnormalities in these neuropeptides in patients with dysfunctional social relationships. Several studies in human patient populations do in fact support this hypothesis. One study found that autistic children had significantly lower levels of plasma oxytocin as compared to age-matched normal subjects (Modahl et

Acknowledgments

This research was supported by NIH MH65050 to M.M.L., MH56897, MH 56539 and MH 64692 to L.J.Y., and NSF STC IBN-9876754 and the Yerkes Center Grant RR00165.

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    Present address: Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA.

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