An extrasynaptic GABAergic signal modulates a pattern of forward movement in Caenorhabditis elegans

Author:

Shen Yu1,Wen Quan234,Liu He1,Zhong Connie1,Qin Yuqi1,Harris Gareth1,Kawano Taizo5,Wu Min2,Xu Tianqi2,Samuel Aravinthan DT3,Zhang Yun1ORCID

Affiliation:

1. Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, Cambridge, United States

2. Chinese Academy of Sciences Key Laboratory of Brain Function and Disease, School of Life Sciences, University of Science and Technology of China, Hefei, China

3. Department of Physics, Center for Brain Science, Harvard University, Cambridge, United States

4. CAS Center for Excellence in Brain Science and Intelligence Technology, University of Science and Technology of China, Hefei, China

5. Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, University of Toronto, Toronto, Canada

Abstract

As a common neurotransmitter in the nervous system, γ-aminobutyric acid (GABA) modulates locomotory patterns in both vertebrates and invertebrates. However, the signaling mechanisms underlying the behavioral effects of GABAergic modulation are not completely understood. Here, we demonstrate that a GABAergic signal in C. elegans modulates the amplitude of undulatory head bending through extrasynaptic neurotransmission and conserved metabotropic receptors. We show that the GABAergic RME head motor neurons generate undulatory activity patterns that correlate with head bending and the activity of RME causally links with head bending amplitude. The undulatory activity of RME is regulated by a pair of cholinergic head motor neurons SMD, which facilitate head bending, and inhibits SMD to limit head bending. The extrasynaptic neurotransmission between SMD and RME provides a gain control system to set head bending amplitude to a value correlated with optimal efficiency of forward movement.

Funder

National Institute on Deafness and Other Communication Disorders

National Institute of General Medical Sciences

National Natural Science Foundation of China

Canadian Institutes of Health Research

Natural Sciences and Engineering Research Council of Canada

National Science Foundation

John Merck Fund

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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