Functionally asymmetric motor neurons contribute to coordinating locomotion of Caenorhabditis elegans.

Oleg Tolstenkov,Wagner Steuer Costa,Amelie CF Bergs,Alexander Gottschalk,Tim M Gemeinhardt,Olga Bazhanova,Petrus Van der Auwera

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.

Highlights

Locomotion represents a basic component of many complex behaviors and is regulated by neuronal circuits that share similar properties in a wide variety of species, including humans (Guertin, 2013; Kiehn, 2011; Mullins et al, 2011)
We investigated the role of AS motor neurons (AS Motor neurons (MNs)) in the Ventral nerve cord (VNC) locomotor circuit based on predictions made from the wiring diagram, using optogenetic tools, electrophysiology, behavioral analysis, and Ca2+ imaging in immobilized and moving animals
MNs) and punc-4, we could restrict expression of optogenetic tools to the AS MNs (Fig. 1A, B): Briefly, broad expression from punc-17 was suppressed in the DB, VB, DA, VA and VC neurons by expressing dsRNA constructs targeting the optogenetic tool using pacr-5 and punc-4 promoters (Fig. 1AI)

Summary

Invertebrate nervous systems are valuable models for fundamental principles of the control of behavior. Combining specific expression and selective illumination, we precisely targeted AS MNs by optogenetics and addressed their role in the locomotion circuit. AS MNs induce currents in post-synaptic body wall muscles (BWMs), exhibiting an initial asymmetry of excitatory output. This may facilitate complex regulatory motifs for adjusting direction during navigation. By Ca2+-imaging in AS MNs and in their synaptic partners, we reveal that AS MNs play a role in mediating forward and backward locomotion by integrating activity of premotor interneurons (PINs), as well as in coordination of the dorso-ventral body wave. AS MNs have essential roles in coordinating locomotion, combining several functions, and emphasizing the compressed nature of the C. elegans nervous system in comparison to higher animals

Introduction

RESULTS

DISCUSSION

Conclusions

EXPERIMENTAL PROCEDURES

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