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

114 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
Externally publishedYes

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.
@article{09c79d3c3fd9475a93b233fb2fbf795c,
title = "Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion",
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}",
year = "2012",
month = "11",
day = "21",
doi = "10.1016/j.neuron.2012.08.039",
language = "English",
volume = "76",
pages = "750--761",
journal = "Neuron",
issn = "0896-6273",
publisher = "Cell Press",
number = "4",

}

TY - JOUR

T1 - Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion

AU - Wen, Quan

AU - Po, Michelle D.

AU - Hulme, Elizabeth

AU - Chen, Sway

AU - Liu, Xinyu

AU - Kwok, Sen Wai

AU - Gershow, Marc

AU - Leifer, Andrew M.

AU - Butler, Victoria

AU - Fang-Yen, Christopher

AU - Kawano, Taizo

AU - Schafer, William R.

AU - Whitesides, George

AU - Wyart, Matthieu

AU - Chklovskii, Dmitri B.

AU - Zhen, Mei

AU - Samuel, Aravinthan D T

PY - 2012/11/21

Y1 - 2012/11/21

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84869773058&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84869773058&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2012.08.039

DO - 10.1016/j.neuron.2012.08.039

M3 - Article

C2 - 23177960

AN - SCOPUS:84869773058

VL - 76

SP - 750

EP - 761

JO - Neuron

JF - Neuron

SN - 0896-6273

IS - 4

ER -