Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies.

Efrén Álvarez-Salvado,Benjamin Mn King,Jonathan D Victor,Nicholas Stavropoulos,Margaret K Mchugh,Katherine I Nagel,Erin G Connor,John P Crimaldi,Angela M Licata

doi:10.7554/elife.37815

Abstract

Odor attraction in walking Drosophila melanogaster is commonly used to relate neural function to behavior, but the algorithms underlying attraction are unclear. Here, we develop a high-throughput assay to measure olfactory behavior in response to well-controlled sensory stimuli. We show that odor evokes two behaviors: an upwind run during odor (ON response), and a local search at odor offset (OFF response). Wind orientation requires antennal mechanoreceptors, but search is driven solely by odor. Using dynamic odor stimuli, we measure the dependence of these two behaviors on odor intensity and history. Based on these data, we develop a navigation model that recapitulates the behavior of flies in our apparatus, and generates realistic trajectories when run in a turbulent boundary layer plume. The ability to parse olfactory navigation into quantifiable elementary sensori-motor transformations provides a foundation for dissecting neural circuits that govern olfactory behavior.

Highlights

Fruit-flies, like many animals, are adept at using olfactory cues to navigate toward a source of food
Algorithms for olfactory navigation have been studied in a number of species, and can be broadly divided into two classes, depending on whether the organisms typically search in a laminar environment or in a turbulent environment
To investigate the specific responses underlying olfactory navigation, we developed a miniature wind-tunnel apparatus in which we could present well-controlled wind and odor stimuli to walking flies (Figure 1A and B and Materials and methods)

Summary

Introduction

Fruit-flies, like many animals, are adept at using olfactory cues to navigate toward a source of food. The precise algorithms by which walking flies locate an odor source are not clear. Odor concentration provides a smooth directional cue that can be used to locate the odor source. Laminar navigators include bacteria (Brown and Berg, 1974), nematodes (Pierce-Shimomura et al, 1999), and Drosophila larvae (Gomez-Marin et al, 2011; Gershow et al, 2012). In each of these organisms, a key computation is detection of temporal changes in odor concentration, which drives changes in the probability of re-orientation behaviors. Odors are transported by the instantaneous structure of air or water currents, forming plumes with complex spatial and temporal structure

Methods

Results

Conclusion