Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors

Elife. 2022 Oct 26:11:e81527. doi: 10.7554/eLife.81527.

Abstract

Deciphering how the brain regulates motor circuits to control complex behaviors is an important, long-standing challenge in neuroscience. In the fly, Drosophila melanogaster, this is coordinated by a population of ~ 1100 descending neurons (DNs). Activating only a few DNs is known to be sufficient to drive complex behaviors like walking and grooming. However, what additional role the larger population of DNs plays during natural behaviors remains largely unknown. For example, they may modulate core behavioral commands or comprise parallel pathways that are engaged depending on sensory context. We evaluated these possibilities by recording populations of nearly 100 DNs in individual tethered flies while they generated limb-dependent behaviors, including walking and grooming. We found that the largest fraction of recorded DNs encode walking while fewer are active during head grooming and resting. A large fraction of walk-encoding DNs encode turning and far fewer weakly encode speed. Although odor context does not determine which behavior-encoding DNs are recruited, a few DNs encode odors rather than behaviors. Lastly, we illustrate how one can identify individual neurons from DN population recordings by using their spatial, functional, and morphological properties. These results set the stage for a comprehensive, population-level understanding of how the brain's descending signals regulate complex motor actions.

Keywords: D. melanogaster; descending neuron; grooming; limb; neuroscience; population imaging; two-photon microscopy; walking.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila melanogaster* / physiology
  • Extremities
  • Neurons / physiology
  • Odorants*
  • Population Dynamics

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.