Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion

Quan Wen; Michelle D. Po; Elizabeth Hulme; Sway Chen; Xinyu Liu; Sen Wai Kwok; Marc Gershow; Andrew M. Leifer; Victoria Butler; Christopher Fang-Yen; Taizo Kawano; William R. Schafer; George Whitesides; Matthieu Wyart; Dmitri B. Chklovskii; Mei Zhen; Aravinthan D.T. Samuel

doi:10.1016/j.neuron.2012.08.039

Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion

Quan Wen, Michelle D. Po, Elizabeth Hulme, Sway Chen, Xinyu Liu, Sen Wai Kwok, Marc Gershow, Andrew M. Leifer, Victoria Butler, Christopher Fang-Yen, Taizo Kawano, William R. Schafer, George Whitesides, Matthieu Wyart, Dmitri B. Chklovskii, Mei Zhen, Aravinthan D.T. Samuel

Research output: Contribution to journal › Article › peer-review

189 Citations (Scopus)

Abstract

Locomotion requires coordinated motor activity throughout an animal@s body. In both vertebrates and invertebrates, chains of coupled central pattern generators (CPGs) are commonly evoked to explain local rhythmic behaviors. In C. elegans, we report that proprioception within the motor circuit is responsible for propagating and coordinating rhythmic undulatory waves from head to tail during forward movement. Proprioceptive coupling between adjacent body regions transduces rhythmic movement initiated near the head into bending waves driven along the body by a chain of reflexes. Using optogenetics and calcium imaging to manipulate and monitor motor circuit activity of moving C. elegans held in microfluidic devices, we found that the B-type cholinergic motor neurons transduce the proprioceptive signal. In C. elegans, a sensorimotor feedback loop operating within a specific type of motor neuron both drives and organizes body movement.

Original language	English
Pages (from-to)	750-761
Number of pages	12
Journal	Neuron
Volume	76
Issue number	4
DOIs	https://doi.org/10.1016/j.neuron.2012.08.039
Publication status	Published - 2012 Nov 21

Bibliographical note

Funding Information:
We are grateful to Christopher Gabel, Cornelia Bargmann, L. Mahadevan, and Yun Zhang for useful discussions; Gal Haspel and Netta Cohen for reading the manuscript; Mason Klein for the help with spinning disk confocal microscopy; and Edward Pym and Zengcai Guo for sharing their strains. This work was supported by NIH Pioneer Award, NSF, and Harvard-MIT Innovation Fund.

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2012.08.039

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Wen, Q., Po, M. D., Hulme, E., Chen, S., Liu, X., Kwok, S. W., Gershow, M., Leifer, A. M., Butler, V., Fang-Yen, C., Kawano, T., Schafer, W. R., Whitesides, G., Wyart, M., Chklovskii, D. B., Zhen, M., & Samuel, A. D. T. (2012). Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion. Neuron, 76(4), 750-761. https://doi.org/10.1016/j.neuron.2012.08.039

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abstract = "Locomotion requires coordinated motor activity throughout an animal@s body. In both vertebrates and invertebrates, chains of coupled central pattern generators (CPGs) are commonly evoked to explain local rhythmic behaviors. In C. elegans, we report that proprioception within the motor circuit is responsible for propagating and coordinating rhythmic undulatory waves from head to tail during forward movement. Proprioceptive coupling between adjacent body regions transduces rhythmic movement initiated near the head into bending waves driven along the body by a chain of reflexes. Using optogenetics and calcium imaging to manipulate and monitor motor circuit activity of moving C. elegans held in microfluidic devices, we found that the B-type cholinergic motor neurons transduce the proprioceptive signal. In C. elegans, a sensorimotor feedback loop operating within a specific type of motor neuron both drives and organizes body movement.",

author = "Quan Wen and Po, {Michelle D.} and Elizabeth Hulme and Sway Chen and Xinyu Liu and Kwok, {Sen Wai} and Marc Gershow and Leifer, {Andrew M.} and Victoria Butler and Christopher Fang-Yen and Taizo Kawano and Schafer, {William R.} and George Whitesides and Matthieu Wyart and Chklovskii, {Dmitri B.} and Mei Zhen and Samuel, {Aravinthan D.T.}",

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AU - Kwok, Sen Wai

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AU - Chklovskii, Dmitri B.

AU - Zhen, Mei

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Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion

Abstract

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