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

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125 Scopus citations

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 languageEnglish (US)
Pages (from-to)750-761
Number of pages12
JournalNeuron
Volume76
Issue number4
DOIs
StatePublished - Nov 21 2012

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

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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