Theory of the locomotion of nematodes
Open accessAbstract
We develop a model of the undulatory locomotion of nematodes, in particular that of Caenorhabditis elegans, based on mechanics. The model takes into account the most important forces acting on a moving worm and allows the computer simulation of a creeping nematode. These forces are produced by the interior pressure in the liquid-filled body cavity, the elasticity of the cuticle, the excitation of certain sets of muscles and the friction between the body and its support.We propose that muscle excitation patterns can be generated by stretch receptor control. By solving numerically the equations of motion of the model of the nematode, we demonstrate that these muscle excitation patterns are suitable for the propulsion of the animal.
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For agar, the tangential drag coefficient C||,agar is 3.2 × 10−3 kg·s−1, as estimated by Niebur and Erdös (1991) from Wallace's measurement.
“For agar, Wallace estimated the tangential drag coefficients C||,agar by directly measuring the force required to pull glass fibers of similar dimension to C. elegans across the surface (Wallace, 1969). Based on this measurement, Niebur and Erdös (1991) estimated C||,agar = 3.2 × 10−3 kg·s−1.”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Niebur and Erdös (1991)
The Forces exerted by the environment section (p. 8) reports Wallace’s glass-fiber measurements on agar, but gives them as a range of forces, not as a tangential drag coefficient. In Initialization and numerical solution procedure (p. 11), Niebur and Erdös say they chose the tangential friction coefficient to give the simulated worm a typical creeping speed; Table 2 lists cL as 1.6 × 10⁻³/N kg/s, not 3.2 × 10⁻³ kg/s estimated from Wallace’s measurement. (LLM, conf=0.86)
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Experimental — accuracy not yet measuredPrevious models of locomotion have typically assumed graded potential neurons, in line with available data at the time.
“Previous models of locomotion have typically assumed graded potential neurons (Niebur and Erdös, 1991; Karbowski et al., 2006; Bryden and Cohen, 2008), in line with available data at the time (Goodman et al., 1998; Nickell et al., 2002; Francis et al., 2003; O’Hagan et al., 2005).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Niebur and Erdös, 1991
The normal drag coefficient for agar C⊥,agar is 128 × 10−3 kg·s−1, obtained by taking Kagar = 40 and Niebur and Erdös' estimate for C||,agar.
“We previously estimated the normal drag coefficient C⊥,agar from recordings of wild type worms using our motion simulator (Berri et al., 2009). Briefly, we found the ratio of drag coefficients to be in the range Kagar ≈ 30–40; taking a value of Kagar = 40 and Niebur and Erdös’ estimate for C||,agar gives C⊥,agar = 128 × 10−3 kg·s−1, which will be used in what follows.”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Niebur and Erdös (1991)
The model requires integration of proprioceptive inputs over up to half a body length.
“Previously, the necessary extent of proprioceptive receptive fields has been considered only for crawling-like motor patterns (Niebur and Erdös, 1991; Bryden and Cohen, 2008), but we find that our model requires integration of proprioceptive inputs over up to half a body length.”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Niebur and Erdös, 1991
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Cites
The structure of the nervous system of the nematode <i>Caenorhabditis elegans</i>
White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1986.0056 · Cited by 5,589 · see citing works
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Research works printed but not linked: 11
- Bird, F. B. 1971. The Structure of Nematodes. Academic Press, New York.
- Crofton, H. D. 1971. Form,. function and behavior. In Plant parasitic Nematodes. B. M. Zuckermann, W. F. Mai, and R. A. Rohde, editors. Academic Press, New York. 83–113.
- Erdös, P., and E. Niebur. 1990. The Neural basis of the locomotion of nematodes. In Lecture Notes in Physics. Vol. 368. L. Garrido, editor. Springer Verlag, Berlin. 253–267.
- Johnson, C. D., and A. O. W. Stretton. 1980. Neural control of behavior in nematodes: anatomy, electrophysiology, and biochemistry. In Nematodes as Biological Models. Vol. 1. B. M. Zuckermann, editor. Academic Press, New York, 159–195.
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- Nachtigall, W. 1983. The biophysics of locomotion in water. In Biophysics. W. Hoppe, W. Lohmann, H. Markl, and H. Ziegler, editors. Springer-Verlag, Berlin.
- NAG 1987. The NAG Fortran Library Manual-Mark 12. The Numerical Algorithms Group Ltd., Oxford, UK.
- Niebur, E. 1988. Théorie du système locomoteur et neuronal des Nématodes. PhD thesis. University of Lausanne, Switzerland.
- Niebur, E., and P. Erdös. 1991. Control of the Undulatory Motion of Vermiform Bodies. In Progress in Robotics and Intelligent Systems. G. Zobrist, editor. Ablex Publishing Company, Norwood, N. J. In press.
- Niebur, E., and P. Erdös. 1988b. Computer simulation of networks of electrotonic neurons. In Computer Simulation in Brain Science. R. M. Cotterill, editor. Cambridge University Press, Cambridge. 148-163.
- Press, W. H., B. F. Flannery, S. A. Teukolsky, and W. T. Vetterling. 1986. Numerical Recipes. Cambridge University Press, Cambridge.
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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
“Previously, the necessary extent of proprioceptive receptive fields has been considered only for crawling-like motor patterns (Niebur and Erdös, 1991; Bryden and Cohen, 2008), but we find that our model requires integration of proprioceptive inputs over up to half a body length.”
BackgroundMethodResultInfluentialSwimming at low Reynolds number: a beginners guide to undulatory locomotion
Cohen, N., & Boyle, J. H. (2010) · Contemporary Physics · doi:10.1080/00107510903268381 · Cited by 110 · see citing works
Backholm, M., Ryu, W. S., & Dalnoki-Veress, K. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219965110 · Cited by 94 · see citing works
Connecting a Connectome to Behavior: An Ensemble of Neuroanatomical Models of C. elegans Klinotaxis
Izquierdo, E. J., & Beer, R. D. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002890 · Cited by 84 · see citing works
“In addition, more realistic models of the body musculature could be employed [86], [87].”
BackgroundThe quest for action potentials in C. elegans neurons hits a plateau
Lockery, S. R., & Goodman, M. B. (2009) · Nature Neuroscience · doi:10.1038/nn0409-377 · Cited by 81 · see citing works
Izquierdo, E. J., & Beer, R. D. (2018) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2017.0374 · Cited by 56 · see citing works
Olivares, E. O., Izquierdo, E. J., & Beer, R. D. (2018) · Network Neuroscience · doi:10.1162/netn_a_00036 · Cited by 38 · see citing works
“They can be broadly divided into those that include a neuronal CPG in the head (Deng, Xu, Wang, Wang, & Chen, 2016; Karbowski et al., 2008; Niebur & Erdös, 1991; Sakata & Shingai, 2004; Wen et al., 2012) and those that rely primarily on sensory feedback mechanisms to generate the rhythmic pattern…”
BackgroundThe whole worm: brain–body–environment models of C. elegans
Izquierdo, E. J., & Beer, R. D. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.06.005 · Cited by 27 · see citing works
Cohen, N., & Ranner, T. (2017) · arXiv · doi:10.48550/arxiv.1702.04988 · Cited by 12 · see citing works
- Authors
- Niebur, E., & Erdös, P.
- Affiliations
- University of Lausanne (CH)
- ORCID
- Niebur, Ernst
- Venue
- Biophysical Journal
- Publisher
- Elsevier BV
- Published
- 1991-11
- Volume
- 60
- Issue
- 5
- Pages
- 1132-1146
- ISSN
- 0006-3495 (ISSN-L)
- PMC
- PMC1260169
- OpenAlex
- W1555732451
- Cited by
- 139
- References
- 1
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 4 · 2023: 8 · 2022: 6 · 2021: 5 · 2020: 7 · 2019: 5 · 2018: 10 · 2017: 7 · 2016: 6 · 2015: 7 · 2014: 7 · 2013: 4 · 2012: 11
- FWCI
- 1.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biophysical Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (20-28846.90, 2000-5.295)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › Robotic Locomotion and Control
- Physical Sciences › Engineering › Aerospace Engineering › Biomimetic flight and propulsion mechanisms
- Physical Sciences › Engineering › Biomedical Engineering › Soft Robotics and Applications
- Keywords
- nematode locomotion, undulatory locomotion, Caenorhabditis elegans, hydrostatic pressure, muscle activation, stretch receptors, propulsion, equations of motion, computer simulation
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