Idiosyncratic Olfactory Behavior and its Neural Basis

Abstract

Individuality is a fundamental feature of animal behavior. Such behavioral idiosyncrasy exists across animals responding to an identical stimulus, and even within a single animal from moment-to-moment. Behavioral idiosyncrasy is essential to a number of evolutionary strategies to overcome ecological challenges. Despite this importance, the neural mechanisms by which idiosyncratic behavior arises is still unclear. We have found that isogenic Drosophila melanogaster raised in identical environments exhibit idiosyncratic olfactory preferences that are stable across multiple days, representing something akin to a fly personality. The amount of individuality across animals can be tuned through activity of local neurons within the antennal lobe and selective neuromodulators. The observed individuality is, in part, the result of differences in odor coding within the peripheral nervous system. We paired behavior and two-photon imaging to show that idiosyncratic calcium dynamics in both olfactory receptor neurons and projection neurons predict individual preferences for an aversive odorant, suggesting that variation at the periphery of the olfactory system determines individual preference for an odor’s presence. Lastly, we also show that isogenic animals exhibit individuality in learning responses that generalizes across stimulus modalities, both unconditioned and conditioned. These findings add to our perspective on individuality of behavior, and identify sources of variation in neural circuits that could function as substrates for natural selection or ecological strategies.