The neuropeptides oxytocin (OT) and vasopressin (AVP) are critical in the formation of pair bonding in the vole, and potentially in other species. The finding that normally promiscuous male rats display a conditioned ejaculatory preference (CEP) for females that bear an odor paired with the sexual reward state induced by ejaculation prompted us to examine whether similar mechanisms may mediate this rudiment of pair bonding. Sexually naïve Long-Evans male rats were given 9 multi-ejaculatory copulation trials at 4-day intervals with either almond-scented (paired) or unscented (unpaired) sexually receptive females. CEP was examined in an open field, in which each male had unrestricted access to two receptive females, one scented with almond and the other unscented. Males in both groups were given two reconditioning trials and presented with the almond odor on gauze for 1 h prior to sacrifice. Neuronal activation was assessed by immunohistochemical detection of Fos protein within OT or AVP neurons. Exposure to the odor induced significantly greater activation of OT neurons in parvocellular neurons of the paraventricular nucleus (PVN) and of AVP in magnocellular neurons of the supraoptic nucleus (SON) in the paired group compared to the unpaired group. The second experiment examined whether oxytocin or vasopressin could enhance the acquisition of a CEP. Sexually naïve male Long-Evans rats received a subcutaneous injection of OT, AVP, or the saline vehicle, prior to their first sexual experience with an almond-scented female. CEP was examined 4 days later in the open field. Males injected with OT, but not AVP or saline, displayed significant CEP. The selective activation of OT neurons by the conditioned odor in the paired group, and the ability of OT injections to enhance the association of the odor and sexual reward, indicates that enhanced OT transmission is critical in the formation of CEP in male rats.
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