Species differences in vasopressin receptor binding are evident early in development: Comparative anatomic studies in prairie and montane voles

Abstract

Monogamous prairie voles (Microtus ochrogaster) and promiscuous montane voles (Microtus montanus) exhibit remarkable differences in the distribution of vasopressin (AVP) receptors in the adult brain. This difference in receptor distribution is associated with species differences in the behaviors, including pair bond formation and paternal care, found selectively in the monogamous vole. To investigate a potential mechanism for this species difference in AVP receptors, the present study examined the ontogeny of receptor binding in the two species to determine whether the adult maps arose from a shared pattern in development. By using 125I-linear-AVP, which is a selective high-affinity ligand for the V1a receptor, we found early appearance and transient expression of AVP receptor binding during postnatal development in both species. However, the ontogenetic patterns of regional AVP receptor binding were species specific. In the diagonal band, the bed nucleus of the stria terminalis, and the central nucleus of the amygdala, prairie voles had higher AVP receptor binding at birth than montane voles, and this difference persisted with little variation into adulthood. In these areas, therefore, species differences in AVP receptor binding appeared to be determined primarily by genetic or prenatal factors. In the lateral septum, both species had low levels of AVP receptor binding at birth. Thereafter, the binding increased rapidly in montane voles, but it remained unchanged in prairie voles. In the cingulate cortex, AVP receptor binding in prairie voles showed a peak in early development with a subsequent decline and reached the adult level at weaning, whereas the binding in montane voles remained unchanged into adulthood. A similar but opposite pattern was found in the frontoparietal cortex, in which AVP receptor binding showed an early peak in montane voles but did not change significantly in prairie voles. These results demonstrate that 1) species differences in regional AVP receptor binding are evident in the early postnatal period and, in several areas, may be determined by genetic or prenatal factors, and 2) AVP may target brain areas differently in infant and adult prairie and montane voles and, thus, could exert differential effects on the organization of the central nervous system in the two species of voles.