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 journalArticle

    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

    Fingerprint

    Motor Neurons
    Lab-On-A-Chip Devices
    Locomotion
    Motor Activity
    Optogenetics
    Central Pattern Generators
    Proprioception
    Body Regions
    Sensory Feedback
    Cholinergic Neurons
    Invertebrates
    Reflex
    Vertebrates
    Head
    Calcium
    Drive

    ASJC Scopus subject areas

    • Neuroscience(all)

    Cite this

    Wen, Q., Po, M. D., Hulme, E., Chen, S., Liu, X., Kwok, S. W., ... 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

    Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion. / Wen, Quan; Po, Michelle D.; Hulme, Elizabeth; Chen, Sway; Liu, Xinyu; Kwok, Sen Wai; Gershow, Marc; Leifer, Andrew M.; Butler, Victoria; Fang-Yen, Christopher; Kawano, Taizo; Schafer, William R.; Whitesides, George; Wyart, Matthieu; Chklovskii, Dmitri B.; Zhen, Mei; Samuel, Aravinthan D T.

    In: Neuron, Vol. 76, No. 4, 21.11.2012, p. 750-761.

    Research output: Contribution to journalArticle

    Wen, Q, Po, MD, Hulme, E, Chen, S, Liu, X, Kwok, SW, Gershow, M, Leifer, AM, Butler, V, Fang-Yen, C, Kawano, T, Schafer, WR, Whitesides, G, Wyart, M, Chklovskii, DB, Zhen, M & Samuel, ADT 2012, 'Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion', Neuron, vol. 76, no. 4, pp. 750-761. https://doi.org/10.1016/j.neuron.2012.08.039
    Wen, Quan ; Po, Michelle D. ; Hulme, Elizabeth ; Chen, Sway ; Liu, Xinyu ; Kwok, Sen Wai ; Gershow, Marc ; Leifer, Andrew M. ; Butler, Victoria ; Fang-Yen, Christopher ; Kawano, Taizo ; Schafer, William R. ; Whitesides, George ; Wyart, Matthieu ; Chklovskii, Dmitri B. ; Zhen, Mei ; Samuel, Aravinthan D T. / Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion. In: Neuron. 2012 ; Vol. 76, No. 4. pp. 750-761.
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