Based on observed changes in the social context for the display of ultrasonic vocalizations, scent marking, aggression, and mounting behavior by male mice with a null mutation of the transient receptor potential 2 ion channel, it was proposed recently that a primary function of the mouse vomeronasal organ (VNO)/accessory olfactory system is sex discrimination. We tested this hypothesis directly by studying the ability of male mice to discriminate between urinary odors of conspecifics of the two sexes and in different endocrine states using habituation-dishabituation tests. Male mice from which the VNO had been surgically removed (VNOx) resembled sham-operated controls (VNOi) in their ability to discriminate between volatile urinary odors from estrous females versus gonadally intact males, as well as between urinary odors from estrous versus ovariectomized females and from gonadally intact versus castrated males. When physical access to stimuli was permitted, VNOi control males strongly preferred to investigate volatile and nonvolatile urinary odorants from estrous females as opposed to intact males, whereas VNOx males showed no such preference. Mating performance in tests with estrous females was equivalent in VNOi and VNOx subjects. Both groups of males preferred to mount an estrous female instead of a castrated male. Our results suggest that the VNO is not required for sex discrimination but instead detects the nonvolatile components of oppositesex urine that may be used to help prolong contact with individuals that produce these chemosignals.

The main olfactory system, like the accessory olfactory system, responds to pheromones involved in social communication. Whereas pheromones detected by the accessory system are transmitted to the hypothalamus via the medial ('vomeronasal') amygdala, the pathway by which pheromones are detected and transmitted by the main system is not well understood. We examined in female mice whether a direct projection from mitral ⁄ tufted (M ⁄ T) cells in the main olfactory bulb (MOB) to the medial amygdala exists, and whether medial amygdala-projecting M ⁄ T cells are activated by volatile urinary odors from conspecifics or a predator (cat). Simultaneous anterograde tracing using Phaseolus vulgaris leucoagglutinin and Fluoro-Ruby placed in the MOB and accessory olfactory bulb (AOB), respectively, revealed that axons of MOB M ⁄ T cells projected to superficial laminae of layer Ia in anterior and posterodorsal subdivisions of the medial amygdala, whereas projection neurons from the AOB sent axons to non-overlapping, deeper layer Ia laminae of the same subdivisions. Placement of the retrograde tracer cholera toxin B into the medial amygdala labeled M ⁄ T cells that were concentrated in the ventral MOB. Urinary volatiles from male mice, but not from female conspecifics or cat, induced Fos in medial amygdala-projecting MOB M ⁄ T cells of female subjects, suggesting that information about male odors is transmitted directly from the MOB to the 'vomeronasal' amygdala. The presence of a direct MOB-to-medial amygdala pathway in mice and other mammals could enable volatile, opposite-sex pheromones to gain privileged access to diencephalic structures that control mate recognition and reproduction.

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