Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans
Open accessAbstract
To navigate different environments, an animal must be able to adapt its locomotory gait to its physical surroundings. The nematode Caenorhabditis elegans , between swimming in water and crawling on surfaces, adapts its locomotory gait to surroundings that impose approximately 10,000-fold differences in mechanical resistance. Here we investigate this feat by studying the undulatory movements of C. elegans in Newtonian fluids spanning nearly five orders of magnitude in viscosity. In these fluids, the worm undulatory gait varies continuously with changes in external load: As load increases, both wavelength and frequency of undulation decrease. We also quantify the internal viscoelastic properties of the worm’s body and their role in locomotory dynamics. We incorporate muscle activity, internal load, and external load into a biomechanical model of locomotion and show that ( i ) muscle power is nearly constant across changes in locomotory gait, and ( ii ) the onset of gait adaptation occurs as external load becomes comparable to internal load. During the swimming gait, which is evoked by small external loads, muscle power is primarily devoted to bending the worm’s elastic body. During the crawling gait, evoked by large external loads, comparable muscle power is used to drive the external load and the elastic body. Our results suggest that C. elegans locomotory gait continuously adapts to external mechanical load in order to maintain propulsive thrust.
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The relative importance of neural coupling through body shape and physical properties depends on the properties of the medium.
“The relative importance of these contributions depends on the properties of the medium (Boyle, 2010; Fang-Yen et al., 2010).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Fang-Yen et al., 2010
The Abstract (page unavailable) reports that the balance between internal body load and external load changes with fluid viscosity, supporting the medium-dependent mechanical part of the claim. It does not establish how the relative importance of neural coupling through body shape changes; the Discussion (page unavailable) says the underlying neuromuscular mechanisms are not yet known. (LLM, conf=0.84)
Experimental — accuracy not yet measuredSwimming behaviour in C. elegans has been well studied biomechanically.
“It has been well studied biomechanically [25].”
From Three-dimensional simulation of the <i>Caenorhabditis elegans</i> body and muscle cells in liquid and gel environments for behavioural analysis (2018) · cites this paper as [25]
C. elegans locomotes in an undulatory fashion, generating thrust by propagating dorsoventral bends along its body.
“C. elegans locomotes in an undulatory fashion, generating thrust by propagating dorsoventral bends along its body with a wavelength of undulation that depends on the properties of the medium through which it moves (Berri, Boyle, Tassieri, Hope, & Cohen, 2009; Fang-Yen et al., 2010; Gray & Lissmann, 1964; Lebois et al., 2012).”
From Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in<i>Caenorhabditis elegans</i> (2018) · cites this paper as Fang-Yen et al., 2010
Forward swimming and crawling in C. elegans are two extremes in a spectrum of behaviors, with intermediate waveforms revealed in appropriate intermediate media.
“Recent results, however, demonstrated that forward swimming and crawling are two extremes in a spectrum of behaviors. Indeed the intermediate waveforms can be revealed by placing worms in appropriate intermediate media (Berri et al., 2009; Fang-Yen et al., 2010; Sznitman et al., 2010; Boyle et al., 2011).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Fang-Yen et al., 2010
A waveform modulation similar to that reported for viscoelastic media has also been reported for increasing viscosities.
“A waveform modulation similar to that reported by Berri et al. (2009) for viscoelastic media was consequently reported also for increasing viscosities (Fang-Yen et al., 2010; Shen and Arratia, 2011).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Fang-Yen et al., 2010
Swimming, crawling, and a continuum of intermediate locomotion waveforms represent different manifestations of the same fundamental behavior in different physical environments.
“The model was motivated by the recent finding that swimming, crawling, and a continuum of intermediate locomotion waveforms represent different manifestations of the same fundamental behavior in different physical environments (Berri et al., 2009; Fang-Yen et al., 2010; Boyle et al., 2011).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Fang-Yen et al., 2010
This discrepancy arises from a purely mechanical perspective, which leads to qualitatively different views of swimming and crawling.
“This discrepancy arises from a purely mechanical perspective, which leads to qualitatively different views of swimming and crawling (Fang-Yen et al., 2010).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Fang-Yen et al., 2010
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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 163 · see citing works
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Distributed rhythm generators underlie Caenorhabditis elegans forward locomotion
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Gait Modulation in C. Elegans: It's Not a Choice, It's a Reflex!
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- Authors
- Fang-Yen, C., Wyart, M., Xie, J., Kawai, R., Kodger, T., Chen, S., Wen, Q., & Samuel, A. D. T.
- Affiliations
- Harvard University (US)
- Howard Hughes Medical Institute (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-11-03
- Volume
- 107
- Issue
- 47
- Pages
- 20323-20328
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2996704
- OpenAlex
- W2116086925
- Cited by
- 200
- References
- 3
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 12 · 2023: 18 · 2022: 7 · 2021: 10 · 2020: 14 · 2019: 10 · 2018: 16 · 2017: 10 · 2016: 10 · 2015: 12 · 2014: 17 · 2013: 15 · 2012: 18
- FWCI
- 25.13
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- 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 Science Foundation
- Harvard University
- National Institutes of Health
- Topics
- Physical Sciences › Engineering › Aerospace Engineering › Biomimetic flight and propulsion mechanisms
- Physical Sciences › Engineering › Biomedical Engineering › Robotic Locomotion and Control
- Physical Sciences › Physics and Astronomy › Condensed Matter Physics › Micro and Nano Robotics
- Keywords
- Caenorhabditis elegans, gait adaptation, locomotion, undulatory swimming, crawling, viscosity, viscoelasticity, muscle power, biomechanical modeling, propulsive thrust, external load, internal load
- MeSH terms
- Adaptation, Biological, Animals, Biomechanical Phenomena, Gait, Locomotion, Models, Biological, Muscles, Viscosity, Caenorhabditis elegans
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