Abstract

Sensory navigation results from coordinated transitions between distinct behavioral programs. During chemotaxis in the Drosophila melanogaster larva, the detection of positive odor gradients extends runs while negative gradients promote stops and turns. This algorithm represents a foundation for the control of sensory navigation across phyla. In the present work, we identified an olfactory descending neuron, PDM-DN, which plays a pivotal role in the organization of stops and turns in response to the detection of graded changes in odor concentrations. Artificial activation of this descending neuron induces deterministic stops followed by the initiation of turning maneuvers through head casts. Using electron microscopy, we reconstructed the main pathway that connects the PDM-DN neuron to the peripheral olfactory system and to the pre-motor circuit responsible for the actuation of forward peristalsis. Our results set the stage for a detailed mechanistic analysis of the sensorimotor conversion of graded olfactory inputs into action selection to perform goal-oriented navigation.

Highlights

  • Animals explore their environment to locate food while avoiding danger

  • Identification of a descending neuron involved in the control of chemotaxis To identify neurons in the larval brain involved in chemotaxis behavior, we conducted a loss-of-function (LoF) screen on a large collection of Split-Gal4 driver lines (Li et al, 2014; Dionne et al, 2018)

  • The larva displays stereotyped behavioral programs that can be decomposed into forward motion (‘run’), locomotor pauses (‘stops’) followed by exploratory lateral-head movements (‘head casts’) and turns (Green et al, 1983; SawinMcCormack et al, 1995; Berni et al, 2012; Gomez-Marin and Louis, 2012)

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Summary

Introduction

Animals explore their environment to locate food while avoiding danger This process is directed by the detection and the integration of multimodal cues, which organize the sequential release of behavioral programs. Evolution has produced a variety of orientation mechanisms responding to the anatomical and physiological constraints of each animal (Fraenkel and Gunn, 1961). These mechanisms share a common algorithmic basis: attractive cues promote motion toward favorable directions while aversive cues suppress it. This algorithm is exemplified in bacterial chemotaxis where bouts of straight motion (‘runs’) alternate with turns (‘tumbles’) that randomize the direction of motion (Berg, 2008; Bi and Sourjik, 2018).

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