Functionally asymmetric motor neurons contribute to coordinating locomotion of Caenorhabditis elegans

Elife. 2018 Sep 11:7:e34997. doi: 10.7554/eLife.34997.

Abstract

Locomotion circuits developed in simple animals, and circuit motifs further evolved in higher animals. To understand locomotion circuit motifs, they must be characterized in many models. The nematode Caenorhabditis elegans possesses one of the best-studied circuits for undulatory movement. Yet, for 1/6th of the cholinergic motor neurons (MNs), the AS MNs, functional information is unavailable. Ventral nerve cord (VNC) MNs coordinate undulations, in small circuits of complementary neurons innervating opposing muscles. AS MNs differ, as they innervate muscles and other MNs asymmetrically, without complementary partners. We characterized AS MNs by optogenetic, behavioral and imaging analyses. They generate asymmetric muscle activation, enabling navigation, and contribute to coordination of dorso-ventral undulation as well as anterio-posterior bending wave propagation. AS MN activity correlated with forward and backward locomotion, and they functionally connect to premotor interneurons (PINs) for both locomotion regimes. Electrical feedback from AS MNs via gap junctions may affect only backward PINs.

Keywords: C. elegans; Ca2+ imaging; behavioral analysis; gap junctions; locomotor circuit; neuroscience; optogenetics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / growth & development
  • Cholinergic Neurons / physiology*
  • Interneurons / physiology
  • Locomotion / physiology*
  • Motor Neurons / physiology*
  • Muscles / innervation
  • Muscles / physiology
  • Optogenetics*