Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole

Abstract

Arginine vasopressin and its V1a receptor subtype (V1aR) are critical for pair bond formation between adult prairie voles. However, it is unclear which brain circuits are involved in this vasopressin-mediated facilitation of pair bond formation. Here, we examined mating-induced Fos expression in several brain regions involved in sociosexual and reward circuitry in male prairie voles. Consistent with studies in other species, Fos expression was induced in several regions known to be involved in sociosexual behavior, namely, the medial amygdala, bed nucleus of the stria terminalis, and medial preoptic area. Fos induction also occurred in limbic and reward regions, including the ventral pallidum, nucleus accumbens, and mediodorsal thalamus (MDthal). Next, we infused a selective V1aR antagonist into three candidate brain regions that seemed most likely involved in vasopressin-mediated pair bond formation: the ventral pallidum, medial amygdala, and MDthal. Blockade of V1aR in the ventral pallidum, but not in the medial amygdala or MDthal, prevented partner preference formation. Lastly, we demonstrated that the mating-induced Fos activation in the ventral pallidum was vasopressin-dependent, since over-expression of V1aR using viral vector gene transfer resulted in a proportionate increase in mating-induced Fos in the same region. This is the first study to show that vasopressin neurotransmission occurs in the ventral pallidum during mating, and that V1aR activation in this region is necessary for pair bond formation in male prairie voles. The results from this study have profound implications for the neural circuitry underlying social attachment and generate novel hypotheses regarding the neural control of social behavior.