Prior activity of olfactory receptor neurons is required for proper sensory processing and behavior in Drosophila larvae

Nao Utashiro,Claire R Williams,Kazuo Emoto,Jay Z Parrish

doi:10.1038/s41598-018-26825-3

Abstract

Animal responses to their environment rely on activation of sensory neurons by external stimuli. In many sensory systems, however, neurons display basal activity prior to the external stimuli. This prior activity is thought to modulate neural functions, yet its impact on animal behavior remains elusive. Here, we reveal a potential role for prior activity in olfactory receptor neurons (ORNs) in shaping larval olfactory behavior. We show that prior activity in larval ORNs is mediated by the olfactory receptor complex (OR complex). Mutations of Orco, an odorant co-receptor required for OR complex function, cause reduced attractive behavior in response to optogenetic activation of ORNs. Calcium imaging reveals that Orco mutant ORNs fully respond to optogenetic stimulation but exhibit altered temporal patterns of neural responses. These findings together suggest a critical role for prior activity in information processing upon ORN activation in Drosophila larvae, which in turn contributes to olfactory behavior control.

Highlights

Animals rely on their sensory neurons to detect external stimuli and change their behavior in response to the external world
Video recordings of Ca2+ responses in olfactory receptor neurons (ORNs) demonstrated that the frequency of prior activity in each ORN is different from one another (Supplementary Movie S1)
In order to investigate potential roles for the prior activity in larval behavior, we examined whether Orco mutant larvae might have defects in olfactory behavior evoked by ORN activation

Summary

Introduction

Animals rely on their sensory neurons to detect external stimuli and change their behavior in response to the external world. Mitral cells in the mammalian olfactory bulb show patterned spontaneous activity in the absence of odor stimuli[2,3]. This spontaneous activity could be regarded as a type of prior activity. While Orco expression may extend to tissues involved in other sensory modalities in some insects[20,21], Drosophila Orco expression is apparently restricted to OR-expressing ORNs, Orco mutation provides a tool to potently and block evoked and spontaneous activity in ORNs. In this study, we aim to investigate potential roles for prior activity in the olfactory system by using Drosophila larval ORNs as the model system. Our findings suggest a role for prior neural activity of ORNs in sensory processing and olfactory behavior control

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