Olfactory Sex Discrimination Persists, Whereas the Preference for Urinary Odorants from Estrous Females Disappears in Male Mice after Vomeronasal Organ Removal

Abstract

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 and the accessory olfactory systems interact in the control of mate recognition and sexual behavior

“…Complimentary to the results detailed previously, surgical lesions of the VNO clearly showed that this treatment is not effective in disrupting mate recognition in both male and female mice [44,45,82,83]. Indeed, VNO-lesions did not impair the discrimination of body or urinary volatile odorants in a habituation/dishabituation test as well as the preference for opposite-sex-derived volatile odors measured in Y-maze choicetests.…”

“…In the male, the involvement of VNO in copulatory behavior seems to vary according to the species. In male mice, lesioning the VNO is without any impact on male sexual behavior [82] and Trp2-KO male mice also show normal levels of copulation [105]. These results point to a possible role for the main olfactory system in the expression of male sexual behavior [45].…”

Genetic dissection of pheromone processing reveals main olfactory system-mediated social behaviors in mice

“…Male mice show a preference for female urine over male urine (29). We tested whether this sexual preference is maintained in ΔD mice.…”

Ventromedial hypothalamic nucleus lesions disrupt olfactory mate recognition and receptivity in female ferrets

“…Numerous studies (reviewed in Pankevich et al, 2004) suggest that sex discrimination and resultant heterosexual mate recognition in many non-primate mammals rely on the detection and processing of body odors by the main olfactory system. For example, in the ferret, the induction of anosmia by occlusion of the main olfactory epithelium eliminated the preference of both male and female subjects to approach tethered opposite-sex conspecifics in Y-maze tests (Kelliher and Baum, 2001).…”