Abstract

Female mammals generally have a superior sense of smell than males, but the biological basis of this difference is unknown. Here, we demonstrate sexually dimorphic neural coding of odorants by olfactory sensory neurons (OSNs), primary sensory neurons that physically contact odor molecules in the nose and provide the initial sensory input to the brain’s olfactory bulb. We performed in vivo optical neurophysiology to visualize odorant-evoked OSN synaptic output into olfactory bub glomeruli in unmanipulated (gonad-intact) adult mice from both sexes, and found that in females odorant presentation evoked more rapid OSN signaling over a broader range of OSNs than in males. These spatiotemporal differences enhanced the contrast between the neural representations of chemically related odorants in females compared to males during stimulus presentation. Removing circulating sex hormones makes these signals slower and less discriminable in females, while in males they become faster and more discriminable, suggesting opposite roles for gonadal hormones in influencing male and female olfactory function. These results demonstrate that the famous sex difference in olfactory abilities likely originates in the primary sensory neurons, and suggest that hormonal modulation of the peripheral olfactory system could underlie differences in how males and females experience the olfactory world.

Highlights

  • Female mammals generally have a superior sense of smell than males, but the biological basis of this difference is unknown

  • Subjects remained anesthetized while the synaptic output of olfactory sensory neurons (OSNs) was visualized by fluorescence microscopy during 4 6-sec presentations of each stimulus in the odor panel, which consisted of 3 separate concentrations of 4 monomolecular odorants

  • Because spH is a cumulative measure of exocytosis from OSNs, these long presentations permit odor-evoked responses to be detected even in weakly activated OSN populations[35]

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Summary

Introduction

Female mammals generally have a superior sense of smell than males, but the biological basis of this difference is unknown. We performed in vivo optical neurophysiology to visualize odorant-evoked OSN synaptic output into olfactory bub glomeruli in unmanipulated (gonad-intact) adult mice from both sexes, and found that in females odorant presentation evoked more rapid OSN signaling over a broader range of OSNs than in males. These spatiotemporal differences enhanced the contrast between the neural representations of chemically related odorants in females compared to males during stimulus presentation. Because each OSN expresses only one out of a large www.nature.com/scientificreports/

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