The roles of the main and accessory olfactory systems in the detection of social odors in mice

Abstract

Our understanding of olfaction has been built on the study of monomolecular (pure) odors, which are easily obtained and well characterized chemically. For most species social odors have far greater biological relevance than typical monomolecular odors, but much less is known about the neural circuits that process them. Three studies were conducted to further explore the neural pathways that process social odors in mice. In Study 1, a Go-No-Go olfactory discrimination task was used to ask whether social odors are more salient stimuli than non-social odors in males and females under different hormonal conditions. Performance (percent correct) was greater in males than females, and poorer in subjects without circulating gonadal hormones when mice were required to discriminate between two social odors (male versus female urine), but not when non-social odors (banana versus peppermint) were used. This suggests that social odors are more salient stimuli than non-social odors but only when gonadal hormones are present. The piriform cortex (PC) is the primary cortical target for volatile odors processed by the main olfactory system (MOS); whether the PC responds to social odor volatiles is not known. In Study 2 I recorded extracellularly from PC pyramidal neurons before and during exposure to urinary volatiles or amyl acetate (banana) in anesthetized males. Neuronal spiking was strongly dependent on testosterone levels. Notably, social odor exposure only weakly induced spiking, which contrasts with the strong behavioral effects these odors are known to induce, so it is likely that other, unknown pathways are more important for their detection. Non-volatile components of social odors are processed by the accessory olfactory system (AOS); however, the role of the AOS during ongoing social interactions is not clear. In Study 3 I used optogenetic activation of the AOB during mating to enhance signaling in the AOS of males; I found that this stimulation significantly increased copulatory behavior efficiency, suggesting that AOB activity during mating facilitates males’ sexual arousal and reproductive performance. Overall these results reveal new properties of social odor processing in mice: sex differences, dependence on gonadal hormones, and a role during ongoing behavioral interactions.