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 journalArticlepeer-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 languageEnglish
    Pages (from-to)750-761
    Number of pages12
    JournalNeuron
    Volume76
    Issue number4
    DOIs
    Publication statusPublished - 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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