Neurochemical regulation of pair bonding in male prairie voles
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).
References (100)
- et al.
Apomorphine stimulation of male copulatory behavior is prevented by the oxytocin antagonist d(CH2)5Tyr(Me)-Orn8-Vasotocin in rats
Pharmacol. Biochem. Behav.
(1989) - et al.
Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster)
Physiol. Behav.
(1994) - et al.
Lipopolysaccharide facilitates partner preference behaviors in female prairie voles
Physiol. Behav.
(1999) Oxytocin and sexual behavior
Neurosci. Biobehav. Rev.
(1992)- et al.
Differential lateral septal vasopressin innervation in aggressive and nonaggressice male mice
Brain Res. Bull.
(1993) - et al.
Peripheral pulses of oxytocin increase partner preferences in female, but not male, prairie voles
Horm. Behav.
(2000) - et al.
The effects of peptides on partner preference formation are predicted by habitat in prairie voles
Horm. Behav.
(2001) - et al.
The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum
Brain Res.
(1983) The role of dopamine in drug abuse viewed from the perspective of its role in motivation
Drug Alcohol Depend.
(1995)- et al.
Behavioral consequences of intracerebral vasopressin and oxytocin: focus on learning and memory
Neurosci. Biobehav. Rev.
(1996)
Lateral septal vasopressin in rats: role in social and object recognition?
Brain Res.
The neuroendocrine basis of social recognition
Front. Neuroendocrinol.
Vasopressin receptor blockade in the anterior hypothalamus suppresses aggression in hamsters
Physiol. Behav.
Specificity in the projection patterns of accumbal core and shell in the rat
Neuroscience
Mating in the monogamous male: behavioral consequences
Physiol. Behav.
Vasopressin in the septal area of the golden hamster controls scent marking and grooming
Physiol. Behav.
Developmental effects of oxytocin on stress response: single versus repeated exposure
Physiol. Behav.
Centrally injected arginine vasopressin (AVP) facilitates social memory in rats
Neurosci. Lett.
Nucleus accumbens dopamine and oxytocin interact to regulate pair bond formation in female prairie voles
Neuroscience
A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum)
Anim. Behav.
A comparison of paternal behaviour in the meadow vole Microtus pennsylvanicus, the pine vole M. pinetorum and the prairie vole M. ochrogaster
Anim. Behav.
Sexual activity increases dopamine transmission in the nucleus accumbens and striatum of female rats
Brain Res.
Intraspecific variation in the induction of female sexual receptivity in prairie voles
Physiol. Behav.
Cooperative breeding and monogamy in prairie voles: influence of the sire and geographical variation
Anim. Behav.
Comparative neuroanatomy of the sexually dimorphic hypothalamus in monogamous and polygamous voles
Brain Res.
Vasopressin cells in the bed nucleus of the stria terminalis of the rat: sex differences and the influence of androgens
Brain Res.
Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster)
Brain Res.
Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles
Brain Res.
Sex and species differences in the effects of cohabitation on vasopressin messenger RNA expression in the bed nucleus of the stria terminalis in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus)
Brain Res.
Ontogeny of oxytocin and vasopressin receptor binding in the lateral septum in prairie and montane voles
Dev. Brain Res.
Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience
Horm. Behav.
Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience
Horm. Behav.
The social deficits of the oxytocin knockout mouse
Neuropeptides
Neurobiology of addiction
Curr. Opin. Neurobiol.
Cellular mechanisms of social attachment
Horm. Behav.
An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens
Neurosci. Biobehav. Rev.
Taxonomy and systematics
A critical role for nucleus accumbens dopamine in partner preference formation of male prairie voles
J. Neurosci.
Opposite modulation of social attachment by D1- and D2-type dopamine receptor activation in nucleus accumbens shell
Horm. Behav.
Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, Microtus pennsylvanicus
J. Neuroendocrinol.
Neuropharmacological mechanisms of drug reward: beyond dopamine in the nucleus accumbens
Crit. Rev. Neurobiol.
The role of dopamine in the nucleus accumbens and striatum during sexual behavior in the female rat
J. Neurosci.
Hypertonic saline mimics the effects of vasopressin and social recognition in rats
Behav. Pharmacol.
Mating systems and sexual dimorphism in mass in microtines
J. Mammal.
The mesolimbic dopamine system as a model reward system
Physiological substrates of mammalian monogamy: the prairie vole model
Neurosci. Biobehav. Rev.
Monogamy and the prairie vole
Sci. Am.
The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster)
Behav. Neurosci.
Vasopressin innervation of sexually dimorphic structures of the gerbil forebrain under various hormonal conditions
J. Comp. Neurol.
Differential effects of intraspecific interactions on the striatal dopamine system in social and non-social voles
Neuroscience
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