Abstract

In most animals, the brain makes behavioral decisions that are transmitted by descending neurons to the nerve cord circuitry that produces behaviors. In insects, only a few descending neurons have been associated with specific behaviors. To explore how descending neurons control an insect's movements, we developed a novel method to systematically assay the behavioral effects of activating individual neurons on freely behaving terrestrial D. melanogaster. We calculated a two-dimensional representation of the entire behavior space explored by these flies, and we associated descending neurons with specific behaviors by identifying regions of this space that were visited with increased frequency during optogenetic activation. Applying this approach across a large collection of descending neurons, we found that (1) activation of most of the descending neurons drove stereotyped behaviors, (2) in many cases multiple descending neurons activated similar behaviors, and (3) optogenetically activated behaviors were often dependent on the behavioral state prior to activation.

Highlights

  • As animals navigate a dynamic environment, their survival depends on their ability to execute specific motor programs and to adjust motor output in response to external stimuli

  • While the brain performs computations essential for behavior, the motor circuits that directly control behavior are located close to the muscles that they control in the vertebrate spinal cord and insect ventral nerve cord

  • In flies, descending commands from the brain to the ventral nerve cord are transmitted through an estimated 250–550 pairs of descending neurons that arborize in 20 highly conserved clusters in the brain involved in sensory processing and motor behavior (Gronenberg and Strausfeld, 1990; Hsu and Bhandawat, 2016)

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Summary

Introduction

As animals navigate a dynamic environment, their survival depends on their ability to execute specific motor programs and to adjust motor output in response to external stimuli. While the brain performs computations essential for behavior, the motor circuits that directly control behavior are located close to the muscles that they control in the vertebrate spinal cord and insect ventral nerve cord. Information to drive motor patterns must be transmitted from the brain to the nerve cord to direct behavior. In flies, descending commands from the brain to the ventral nerve cord are transmitted through an estimated 250–550 pairs of descending neurons that arborize in 20 highly conserved clusters in the brain involved in sensory processing and motor behavior (Gronenberg and Strausfeld, 1990; Hsu and Bhandawat, 2016). Each descending neuron extends a single axon through the neck connective to the ventral nerve cord, where they synapse onto interneurons associated with leg, neck, and wing motor circuitry (Namiki et al, 2018)

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