Inhibition underlies fast undulatory locomotion in caenorhabditis elegans
Document Type
Article
Publication Date
1-1-2021
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 in-volves 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-mutu-ally 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.
Identifier
85102132885 (Scopus)
Publication Title
Eneuro
External Full Text Location
https://doi.org/10.1523/ENEURO.0241-20.2020
e-ISSN
23732822
PubMed ID
33361147
First Page
1
Last Page
23
Issue
2
Volume
8
Grant
P40OD010440
Fund Ref
NIH Office of the Director
Recommended Citation
Deng, Lan; Denham, Jack E.; Arya, Charu; Yuval, Omer; Cohen, Netta; and Haspel, Gal, "Inhibition underlies fast undulatory locomotion in caenorhabditis elegans" (2021). Faculty Publications. 4535.
https://digitalcommons.njit.edu/fac_pubs/4535