Elsevier

Physiology & Behavior

Volume 83, Issue 2, 15 November 2004, Pages 319-328
Physiology & Behavior

Neurochemical regulation of pair bonding in male prairie voles

https://doi.org/10.1016/j.physbeh.2004.08.024Get rights and content

Abstract

Pair bonding represents social attachment between mates and is common among monogamous animals. The prairie vole (Microtus ochrogaster) is a monogamous rodent in which mating facilitates pair bond formation. In this review, we first discuss how prairie voles have been used as an excellent model for neurobiological studies of pair bonding. We then primarily focus on male prairie voles to summarize recent findings from neuroanatomical, neurochemical, cellular, molecular, and behavioral studies implicating vasopressin (AVP), oxytocin (OT), and dopamine (DA) in the regulation of pair bonding. Possible interactions among these neurochemicals in the regulation of pair bonding, the brain areas important for pair bond formation, and potential sexually dimorphic mechanisms underlying pair bonding are also discussed. As analogous social bonds are formed by humans, investigation of the neurochemical regulation of pair bond formation in prairie voles may be beneficial for our understanding of the mechanisms associated with normal and abnormal social behaviors in humans.

Introduction

While several types of social behaviors such as aggression, sex, and social separation have been the focus for many studies in behavioral neuroscience, the neurobiology of pair bonding, a special type of social attachment between mates, has been largely unexplored. The lack of previous research in this area may be partly explained by the complexity of pair bonding, which involves, but is not limited to, sensory processing, memory, motivation, and more subtle aspects of behavior that may be difficult to measure. In addition, neurobiological studies of pair bonding require an animal model demonstrating a reliable behavioral index of pair bond formation. Unfortunately, traditionally studied laboratory rodents, such as rats and mice, generally do not display social attachment between mates and thus cannot be used to study pair bonding. Over the past several years, studies focusing on the development of pair bonds in a microtine rodent, the prairie vole (Microtus ochrogaster), have investigated the hormonal, neuroanatomical, cellular and molecular regulation of pair bonding. In these studies, a pair bond is defined as a stable relationship between a breeding pair of animals that share common territory and parental duties. As analogous social bonds are formed by humans, and the inability to form such bonds is a key diagnostic component in certain psychological disorders [76], these results are important, not only for comprehensive understanding of the neural regulation of pair bonding, but also for our understanding of the mechanisms underlying social disorders in humans. In this review, we will first introduce the prairie vole model, and then primarily focus on studies using male prairie voles to review recent findings on the neurochemical regulation of pair bonding. In this regard, we will focus on the neuropeptides vasopressin (AVP) and oxytocin (OT) and the monoamine neurotransmitter dopamine (DA). However, it is important to note that several other neural [29], hormonal [23], chemical [9], and environmental factors [24] are also involved in the regulation of pair bond formation.

Section snippets

Prairie vole model for pair bonding

The prairie vole belongs to the genus Microtus within the family Muridae (subfamily Arvicolinae) [1], and lives primarily in the grasslands of the central United States. Both field and laboratory studies have indicated that prairie voles are monogamous. In the field, male and female prairie voles form long-term bonds and share a nest throughout the breeding season [30], [31], [39], [40]. Such a breeding pair typically remains together until one dies [38]. In the laboratory, both sexes mate

Neuropeptide regulation of pair bonding

Early studies examining the neurobiological basis of pair bonding were primarily focused on the neuropeptides arginine vasopressin (AVP) and oxytocin (OT). These neuropeptides were chosen because they had been implicated in several social behaviors, including sexual behavior [4], [13], parental care [44], [52], [62], [63], aggression [17], [36], [37], and territory marking [49]. In addition, they were found to be involved in learning/memory and individual recognition—processes important for

Dopamine regulation of pair bonding

Pair bond formation likely involves multiple types of sensory processing, reward, and memory formation. Given the importance of DA in each of these mechanisms [12], [94], we hypothesized that DA would also play an important role in pair bonding. While this hypothesis was first confirmed in early studies in females [42], [86], a detailed analysis of DA regulation of partner preference formation has been achieved in our most recent studies using male prairie voles [2], [3].

Neurochemical interactions in the regulation of pair bonding

It is not surprising that complex social behaviors, such as pair bonding, are under the control of multiple neurochemical systems. Instead of acting independently, these neurochemicals may interact with each other in the regulation of pair bonding. At present, relatively few studies have been performed addressing such interactions; however, these studies have shown that AVP, OT, and DA indeed interact in the regulation of pair bonding.

Conclusion

In summary, the prairie vole model provides an excellent opportunity to study the neurobiology of pair bonding. Recent research has demonstrated that AVP, OT, and DA interact in the regulation of this extremely complex behavior. Monogamous prairie voles possess species specific patterns of neurochemical systems (such as central AVP or OT receptor distributions) that may contribute to pair bond formation. In addition, it has been demonstrated that pair bonding is regulated, in part, by the same

Acknowledgements

We thank Drs. J. Thomas Curtis and Yan Liu as well as Christie D. Fowler and Michael Smeltzer for their critical reading of the manuscript. We also thank Drs. Elaine Hull, Lique Collen, and Stephen Woods for their helpful comments and suggestions. This work was supported by National Institutes of Health grants MH-54554, MH-58616 and MH-66734 (ZXW) and MH-67396 (BJA).

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