Opioid Regulation of Pair Bonding in the Socially Monogamous Prairie Vole.

Abstract

The socially monogamous prairie vole is an excellent animal model for studies of the neurobiology of selective social attachment. Here, we have demonstrated that monogamous bonds are formed and maintained by a balance between mu- and kappa-opioid receptor activation within motivational circuitry. We first show that the formation of a pair bond requires the activation of mu-opioid receptors that mediate both motivational and positive hedonic aspects of reward processing. We hypothesize that these two populations of mu-opioid receptors work in parallel to motivate social interactions with a potential mating partner and subsequently encode these interactions as rewarding through the induction of a positive hedonic state. In contrast to pair bond formation, which is associated with affiliative social encounters generally categorized as positive, the maintenance of a pair bond is associated with aversive social encounters, such as the aggressive rejection of novel conspecifics, that acts to both guard the mate and prevent the formation of a subsequent alternate bond. In the present body of work, we demonstrate that selective aggression, an established behavioral indicator of pair bond maintenance, is mediated by interactions between D1-like dopamine receptors and kappa-opioid receptors within the nucleus accumbens shell and that direct activation of kappa-opioid receptors within this region encodes social aversion. These data suggest that the encoding of social stimuli besides the mating partner as aversive and subsequently aggressively rejecting this stimulus is important for the maintenance of the original pair bond. Additionally, we show that the establishment of a pair bond is associated with a dramatic reorganization of the dopamine and kappa-opioid receptor systems, which likely acts to mediate the transition from generally affiliative to selectively aggressive. Together, these data suggest that interactions between valence coding opioid receptors and motivational circuitry are critical for guiding the direction of socially motivated behaviors, such as the motivation to form and maintain bonds. Importantly, an increased understanding of neural mechanisms that mediate social attachment behavior of prairie voles may provide insight into neural mechanisms that regulate attachment behavior in our own species.