Abstract

An animal’s ability to navigate an olfactory environment is critically dependent on the activities of its first-order olfactory receptor neurons (ORNs). While considerable research has focused on ORN responses to odorants, the mechanisms by which olfactory information is encoded in the activities of ORNs and translated into navigational behavior remain poorly understood. We sought to determine the contributions of most Drosophila melanogaster larval ORNs to navigational behavior. Using odorants to activate ORNs and a larval tracking assay to measure the corresponding behavioral response, we observed that larval ORN activators cluster into four groups based on the behavior responses elicited from larvae. This is significant because it provides new insights into the functional relationship between ORN activity and behavioral response. Subsequent optogenetic analyses of a subset of ORNs revealed previously undescribed properties of larval ORNs. Furthermore, our results indicated that different temporal patterns of ORN activation elicit different behavioral outputs: some ORNs respond to stimulus increments while others respond to stimulus decrements. These results suggest that the ability of ORNs to encode temporal patterns of stimulation increases the coding capacity of the olfactory circuit. Moreover, the ability of ORNs to sense stimulus increments and decrements facilitates instantaneous evaluations of concentration changes in the environment. Together, these ORN properties enable larvae to efficiently navigate a complex olfactory environment. Ultimately, knowledge of how ORN activity patterns and their weighted contributions influence odor coding may eventually reveal how peripheral information is organized and transmitted to subsequent layers of a neural circuit.

Highlights

  • Animals navigate complex olfactory environments in search of food and mates

  • We combined novel methods of olfactory receptor neurons (ORNs) activation with high-resolution behavioral analysis to characterize the functional contributions of ORNs in the Drosophila larval olfactory circuit

  • Our findings provide strong evidence to support the conclusions that, at least for some ORNs, different temporal patterns of activation lead to different behavioral outputs (Figures 3, 4), and that some ORNs impact behavior in response to stimulus increments, while others impact behavior in response to stimulus decrements (Figure 5)

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Summary

Introduction

Animals navigate complex olfactory environments in search of food and mates. While tracking odors in natural environments, the olfactory system must account for odor identity and increases and decreases in odor concentrations that are characteristic of turbulent plumes (ZimmerFaust et al, 1995; Vickers, 2000) and for navigating concentration gradients in non-turbulent situations (Gomez-Marin et al, 2011). The chemical interaction between the odor receptor and odorants is converted into electrical signals (Buck and Axel, 1991; Couto et al, 2005; Fishilevich and Vosshall, 2005; Kreher et al, 2005, 2008; Sato et al, 2008; Smart et al, 2008; Wicher et al, 2008; Yao and Carlson, 2010; Manzini and Korsching, 2011; Dalton and Lomvardas, 2015) These electrical signals are encoded at various levels of the olfactory circuit, eventually eliciting a behavioral response (Wilson et al, 2004; Fishilevich et al, 2005; Chalasani et al, 2007; Gomez-Marin et al, 2011; Turner et al, 2011; Gomez-Marin and Louis, 2014). Despite the accumulating evidence regarding ORN responses to odorants across species, relatively little is known regarding ORN responses in relation to the temporal aspects of odor stimuli or the mechanisms by which sensory information is encoded by activity in ORN clusters

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