Functionally asymmetric motor neurons contribute to coordinating locomotion of Caenorhabditis elegans
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.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data files are videos from live cell imaging and behavioral experiments. They are several terabytes in size and can therefore be provided upon request to the corresponding author.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (GO1011/4-2)
- Petrus Van der Auwera
- Wagner Steuer Costa
- Alexander Gottschalk
Goethe University (GO-IN)
- Oleg Tolstenkov
European Union Marie Curie Actions (PCOFUND-GA-2011-291776)
- Oleg Tolstenkov
Deutsche Forschungsgemeinschaft (GO1011/8-1)
- Oleg Tolstenkov
- Alexander Gottschalk
Deutsche Forschungsgemeinschaft (EXC115/3)
- Petrus Van der Auwera
- Wagner Steuer Costa
- Alexander Gottschalk
Max-Planck-Research School (IMPReS Membrane Biology)
- Amelie CF Bergs
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States
Version history
- Received: January 11, 2018
- Accepted: September 9, 2018
- Accepted Manuscript published: September 11, 2018 (version 1)
- Version of Record published: October 5, 2018 (version 2)
Copyright
© 2018, Tolstenkov et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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