The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans

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Abstract

C. elegans is widely used to dissect how neural circuits and genes generate behavior. During locomotion, worms initiate backward movement to change locomotion direction spontaneously or in response to sensory cues; however, the underlying neural circuits are not well defined. We applied a multidisciplinary approach to map neural circuits in freely behaving worms by integrating functional imaging, optogenetic interrogation, genetic manipulation, laser ablation, and electrophysiology. We found that a disinhibitory circuit and a stimulatory circuit together promote initiation of backward movement and that circuitry dynamics is differentially regulated by sensory cues. Both circuits require glutamatergic transmission but depend on distinct glutamate receptors. This dual mode of motor initiation control is found in mammals, suggesting that distantly related organisms with anatomically distinct nervous systems may adopt similar strategies for motor control. Additionally, our studies illustrate how a multidisciplinary approach facilitates dissection of circuit and synaptic mechanisms underlying behavior in a genetic model organism.

Original languageEnglish
Pages (from-to)922-933
Number of pages12
JournalCell
Volume147
Issue number4
DOIs
StatePublished - Nov 11 2011

Funding

We thank J. Gao, W. Li, W. Zhou, and A. Ward for technical assistance; L. Looger for the G-CaMP3.0 plasmid; A. Gottschalk for ChR2 plasmid; K. Deisseroth for NpHR plasmid; J. Dent and L. Avery for avr-14 strains and plasmids; and P. Hu, A. Kumar, and B. Ye for comments on the manuscript. Some strains were obtained from the CGC and Knockout Consortiums in the USA and Japan. B.J.P. was supported by a predoctoral T32 training grant from the NEI (University of Michigan). This work was supported by grants from the NIGMS and Pew scholar program (to X.Z.S.X.).

FundersFunder number
R01DA022316
University of Michigan

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