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Proprioceptive Coupling within Motor Neurons Drives C. elegans Forward Locomotion
Open accessAbstract
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.
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This makes sense given the important role that stretch receptors have been shown to play in propagating the wave posteriorly during forward locomotion.
“This makes sense given the important role that stretch receptors have been shown to play in propagating the wave posteriorly during forward locomotion (Wen et al., 2012).”
From Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans (2018) · cites this paper as Wen et al., 2012
DA and DB motor neurons drive backward and forward locomotion, respectively.
“It has been demonstrated that DA and DB motor neurons drive backward and forward locomotion, respectively (Haspel et al., 2010;Wen et al., 2012).”
From TMEM55B promotes anterograde transport and distal axonal distribution of LAMP1-positive organelles (2026) · cites this paper as Wen et al., 2012
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“The lack of specialized sensory neurons within the motor circuit led Russell and Byerly to speculate that individual motor neurons might themselves have proprioceptive properties (White et al., 1986).”
Gait Modulation in C. elegans: An Integrated Neuromechanical Model
Boyle, J. H., Berri, S., & Cohen, N. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00010 · Cited by 148 · cited 2×
“Biomechanical evidence also implies a role for proprioception in C. elegans locomotion as its gait adapts to the mechanical load imposed by the environment (Berri et al., 2009; Boyle et al., 2012; Fang-Yen et al., 2010).”
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Metadata
- Authors
- 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.
- Affiliations
- Harvard University (US)
- Mount Sinai Hospital (CA)
- Howard Hughes Medical Institute (US)
- MRC Laboratory of Molecular Biology (GB)
- New York University (US)
- Corresponding author
- Wen, Quan
- Samuel, Aravinthan D.T.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2012-11
- Volume
- 76
- Issue
- 4
- Pages
- 750-761
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3508473
- OpenAlex
- W2133351202
- Cited by
- 268
- References
- 3
- Citations by year
- 2026: 13 · 2025: 14 · 2024: 20 · 2023: 15 · 2022: 22 · 2021: 25 · 2020: 17 · 2019: 17 · 2018: 34 · 2017: 24 · 2016: 15 · 2015: 20 · 2014: 15 · 2013: 16 · 2012: 1
- FWCI
- 6.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 385 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Funders
- National Institutes of Health (DP1OD004064)
- National Institute of General Medical Sciences (DP1GM105383)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- proprioception, motor neurons, forward locomotion, Caenorhabditis elegans, central pattern generator, sensorimotor feedback, motor coordination, optogenetics, calcium imaging
- MeSH terms
- Red Fluorescent Protein, Analysis of Variance, Animals, Antiparasitic Agents, Calcium, Color, Ivermectin, Kymography, Light, Locomotion, Luminescent Proteins, Membrane Proteins, Models, Biological, Motor Neurons, Movement, Mutation, Periodicity, Proprioception, Rhodopsin, Video Recording, Caenorhabditis elegans, Homeodomain Proteins, Muscle, Skeletal, Halorhodopsins, Caenorhabditis elegans Proteins, Animals, Genetically Modified, Muscle Cells, Microfluidics, Green Fluorescent Proteins, Laser Therapy, Cholinergic Neurons, GABAergic Neurons, Optogenetics, Central Pattern Generators
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