MDN brain descending neurons coordinately activate backward and inhibit forward locomotion

Elife. 2018 Aug 2:7:e38554. doi: 10.7554/eLife.38554.

Abstract

Command-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming (we define 'command-like neuron' as a neuron whose activation elicits or 'commands' a specific behavior). In most animals, it remains unknown how neural circuits switch between antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here, we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of Drosophila larval 'mooncrawler descending neurons' (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by stimulating a backward-active premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct monosynaptic reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals.

Keywords: D. melanogaster; backward crawl; behavior; command neuron; descending neuron; locomotor; neural circuit; neuroscience.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / physiology*
  • Brain / ultrastructure
  • Connectome
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / physiology*
  • Drosophila melanogaster / ultrastructure
  • Larva / physiology
  • Larva / ultrastructure
  • Locomotion / physiology*
  • Models, Biological
  • Motor Neurons / physiology*
  • Motor Neurons / ultrastructure

Substances

  • Drosophila Proteins