Deng, L, Denham, J, Arya, C et al. (3 more authors) (2021) Inhibition Underlies Fast Undulatory Locomotion in Caenorhabditis elegans. eNeuro, 8 (2). 0241-20.20. ISSN 2373-2822
Abstract
Inhibition plays important roles in modulating the neural activities of sensory and motor systems at different levels from synapses to brain regions. To achieve coordinated movement, motor systems produce alternating contractions of antagonist muscles, whether along the body axis or within and among limbs, which often involves direct or indirect cross-inhibitory pathways. In the nematode Caenorhabditis elegans, a small network involving excitatory cholinergic and inhibitory GABAergic motoneurons generates the dorsoventral alternation of body-wall muscles that supports undulatory locomotion. Inhibition has been suggested to be necessary for backward undulation because mutants that are defective in GABA transmission exhibit a shrinking phenotype in response to a harsh touch to the head, whereas wild-type animals produce a backward escape response. Here, we demonstrate that the shrinking phenotype is exhibited by wild-type as well as mutant animals in response to harsh touch to the head or tail, but only GABA transmission mutants show slow locomotion after stimulation. Impairment of GABA transmission, either genetically or optogenetically, induces lower undulation frequency and lower translocation speed during crawling and swimming in both directions. The activity patterns of GABAergic motoneurons are different during low-frequency and high-frequency undulation. During low-frequency undulation, GABAergic VD and DD motoneurons show correlated activity patterns, while during high-frequency undulation, their activity alternates. The experimental results suggest at least three non-mutually exclusive roles for inhibition that could underlie fast undulatory locomotion in C. elegans, which we tested with computational models: cross-inhibition or disinhibition of body-wall muscles, or neuronal reset.
Metadata
Item Type: | Article |
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Authors/Creators: |
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Copyright, Publisher and Additional Information: | © 2021 Deng et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. |
Keywords: | C. elegans; GABA; inhibition; locomotion; model; motoneuron |
Dates: |
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Institution: | The University of Leeds |
Academic Units: | The University of Leeds > Faculty of Engineering & Physical Sciences (Leeds) > School of Computing (Leeds) |
Funding Information: | Funder Grant number EPSRC (Engineering and Physical Sciences Research Council) EP/C011953/1 EPSRC (Engineering and Physical Sciences Research Council) EP/C011961/1 BBSRC (Biotechnology & Biological Sciences Research Council) BB/E008038/1 EPSRC (Engineering and Physical Sciences Research Council) EP/J004057/1 EPSRC (Engineering and Physical Sciences Research Council) EP/S01540X/1 |
Depositing User: | Symplectic Publications |
Date Deposited: | 03 Dec 2020 16:04 |
Last Modified: | 25 Jun 2023 22:31 |
Status: | Published |
Publisher: | Society for Neuroscience |
Identification Number: | 10.1523/ENEURO.0241-20.2020 |
Open Archives Initiative ID (OAI ID): | oai:eprints.whiterose.ac.uk:168655 |