Biological Cybernetics

, Volume 98, Issue 4, pp 339–351 | Cite as

Neural control of Caenorhabditis elegans forward locomotion: the role of sensory feedback

Original Paper

Abstract

This paper presents a simple yet biologically-grounded model for the neural control of Caenorhabditis elegans forward locomotion. We identify a minimal circuit within the C. elegans ventral cord that is likely to be sufficient to generate and sustain forward locomotion in vivo. This limited subcircuit appears to contain no obvious central pattern generated control. For that subcircuit, we present a model that relies on a chain of oscillators along the body which are driven by local and proximate mechano-sensory input. Computer simulations were used to study the model under a variety of conditions and to test whether it is behaviourally plausible. Within our model, we find that a minimal circuit of AVB interneurons and B-class motoneurons is sufficient to generate and sustain fictive forward locomotion patterns that are robust to significant environmental perturbations. The model predicts speed and amplitude modulation by the AVB command interneurons. An extended model including D-class motoneurons is included for comparison.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

422_2008_212_MOESM1_ESM.pdf (189 kb)
ESM 1 (PDF 189 kb)
422_2008_212_MOESM2_ESM.tex.
ESM 2 (TEX 19 kb)

References

  1. Bamber BA, Beg AA, Twyman RE and Jorgensen EM (1999). The Caenorhabditis elegans unc-49 locus encodes multiple subunits of a heteromultimeric GABA receptor. J Neurosci 19: 5348–5359 PubMedGoogle Scholar
  2. Berri S, Boyle JH, Tassieri M, Hope IA, Cohen N (2008) The locomotion of nematodes: from swimming to crawling (to be submitted)Google Scholar
  3. Boyle JH, Cohen N (2007) On the role of body wall muscles in C. elegans locomotion. In: Olde-Scheper T, Crook N (eds) Proceedings of IPCAT 2007, pp 363–375Google Scholar
  4. Boyle JH, Bryden JA, Cohen N (2007) Integrated neuro-mechanical model of C. elegans forward locomotion. In: Proceedings of ICONIP 2007Google Scholar
  5. Bryden JA (2003) A simulation model of the locomotion controllers for the nematode Caenorhabditis elegans. Master’s thesis, University of LeedsGoogle Scholar
  6. Bryden JA, Cohen N (2004a) C. elegans at Leeds University, Biosystems Group. http://www.comp.leeds.ac.uk/celegans
  7. Bryden JA, Cohen N (2004b) A simulation model of the locomotion controllers for the nematode Caenorhabditis elegans. In: Schaal S, Ijspeert AJ, Billard A, Vijayakumar S, Hallam J, Meyer JA (eds) Proceedings of the eighth international conference on the simulation of adaptive behavior, MIT Press/Bradford Books, pp 183–192Google Scholar
  8. Bryden JA, Cohen N, Hope IA (2003) Video of C. elegans moving across agar. http://www.comp.leeds.ac.uk/celegans/agar.mov, digital video was taken at Ian Hope’s Laboratory, School of Biology, University of Leeds, LS2 9JT
  9. Chalfie M and White JG (1988). The nervous system. In: Wood, WB (eds) The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory, Cold Spring Harbor Google Scholar
  10. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN and Brenner S (1985). The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5(4): 956–964 PubMedGoogle Scholar
  11. Chen BL, Hall DH and Chklovskii DB (2006). Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci USA 103: 4723–4728 PubMedCrossRefGoogle Scholar
  12. Cinar H, Keles S and Jin Y (2005). Expression profiling of GABAergic motor neurons in Caenorhabditis elegans. Curr Biol 22: 340–346 CrossRefGoogle Scholar
  13. Culetto E, Baylis HA, Richmond JE, Jones AK, Fleming JT, Squire MD, Lewis JA and Sattelle DB (2004). The Caenorhabditis elegans unc-63 gene encodes a levamisole-sensitive nicotinic acetylcholine receptor α subunit. J Biol Chem 279: 42479–42483 CrossRefGoogle Scholar
  14. Duerr JS, H-P H, D FS and B RJ (2008). Identification of major classes of cholinergic neurons in the nematode caenorhabditis elegans. J Comp Neurol 506: 398–408 PubMedCrossRefGoogle Scholar
  15. Dunn NA, Lockery SR, Pierce-Shimomura JT and Conery JS (2004). Neural network model of chemotaxis predicts functions of synaptic connections in the nematode Caenorhabditis elegans. J Comput Neurosci 17: 137–147 PubMedCrossRefGoogle Scholar
  16. Estevez M, Estevez AO, Cowie RH and Gardner KL (2004). The voltage-gated calcium channel UNC-2 is involved in stress-mediated regulation of tryptophan hydroxylase. J Neurochem 88: 102–113 PubMedCrossRefGoogle Scholar
  17. Ferrée TC, Lockery SR (1998) Chemotaxis control by linear recurrent networks. J Comput Neurosci Trends Res 373–377Google Scholar
  18. Ferrée TC and Lockery SR (1999). Computational rules for chemotaxis in the nematode C. elegans. J Comput Neurosci 6: 263–277 PubMedCrossRefGoogle Scholar
  19. Ferrée TC, Marcotte BA and Lockery SR (1997). Neural network models of chemotaxis in the nematode Caenorhabditis elegans. Adv Neural Inform Process Systems 9: 55–61 Google Scholar
  20. Fleming JT, Squire MD, Barnes TM, Tornoe C, Matsuda K, Ahnn J, Fire A, Sulston JE, Barnard EA, Sattelle DB and Lewis JA (1997). Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits. J Neurosci 17: 5843–5857 PubMedGoogle Scholar
  21. Francis MM, Mellem JE and Maricq AV (2003). Bridging the gap between genes and behavior: recent advances in the electrophysiological analysis of neural function in Caenorhabditis elegans. TRENDS Neurosci 26: 90–99 PubMedCrossRefGoogle Scholar
  22. Goodman MB, Hall DH, Avery L and Lockery SR (1998). Active currents regulate sensitivity and dynamic range in C. elegans neurons. Neuron 20: 763–772 PubMedCrossRefGoogle Scholar
  23. Gray JM, Hill JJ and Bargmann CI (2005). A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci USA 102: 3184–3191 PubMedCrossRefGoogle Scholar
  24. Hodgkin J (1983). Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics 103: 43–64 PubMedGoogle Scholar
  25. Karbowski J, Cronin CJ, Seah A, Mendel JE, Cleary D and Sternberg PW (2006). Conservation rules, their breakdown, and optimality in Caenorhabditis sinusoidal locomotion. J Theor Biol 242: 652–669 PubMedCrossRefGoogle Scholar
  26. Marder E (2000). Motor pattern generation. Curr Opin Neurobiol 10: 691–698 PubMedCrossRefGoogle Scholar
  27. Marder E and Bucher D (2001). Central pattern generators and the control of rhythmic movements. Curr Biol 11: 986–996 CrossRefGoogle Scholar
  28. Marder E and Calabrese RL (1996). Principles of rhythmic motor pattern generation. Physiol Rev 76(3): 687–717 PubMedGoogle Scholar
  29. Marder E, Bucher D, Schulz DJ and Taylor AL (2005). Invertebrate central pattern generation moves along. Curr Biol 15: 685–699 CrossRefGoogle Scholar
  30. Mathews EA, Garcia E, Santi CM, Mullen GP, Thacker C, Moerman DG and Snutch TP (2003). Critical residues of the Caenorhabditis elegans unc-2 voltage-gated calcium channel that affect behavioral and physiological properties. J Neurosci 23: 6537–6545 PubMedGoogle Scholar
  31. McIntire SL, Jorgensen E and Horvitz HR (1993a). Genes required for GABA function in Caenorhabditis elegans. Nature 364: 334–337 PubMedCrossRefGoogle Scholar
  32. McIntire SL, Jorgensen E, Kaplan J and Horvitz HR (1993b). The GABAergic nervous system of Caenorhabditis elegans. Nature 364: 337–341 PubMedCrossRefGoogle Scholar
  33. Nickell WT, Pun RY, Bargmann CI and Kleene SJ (2002). Single ionic channels of two Caenorhabditis elegans chemosensory neurons in native membrane. J Membrane Biol 189: 55–66 CrossRefGoogle Scholar
  34. Niebur E and Erdös P (1991). Theory of the locomotion of nematodes. Biophys J 60: 1132–1146 CrossRefPubMedGoogle Scholar
  35. Niebur E and Erdös P (1993). Modeling locomotion and its neural control in nematodes. Comments Theor Biol 3(2): 109–139 Google Scholar
  36. Niebur E and Erdös P (1993). Theory of the locomotion of nematodes: control of the somatic motor neurons by interneurons. Mathe Biosci 118: 51–82 CrossRefGoogle Scholar
  37. O’Hagan R, Chalfie M and Goodman MB (2005). The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nature Neurosci 8: 43–50 PubMedCrossRefGoogle Scholar
  38. Pearson K (2000). Motor systems. Curr Opin Neurobiol 10: 649–654 PubMedCrossRefGoogle Scholar
  39. Richmond JE and Jorgensen EM (1999). One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nature Neurosci 2: 791–797 PubMedCrossRefGoogle Scholar
  40. Sakata K and Shingai R (2004). Neural network model to generate head swing in locomotion of Caenorhabditis elegans. Netw Comput Neural Systems 15: 199–216 CrossRefGoogle Scholar
  41. Stein PSG, Grillner S, Selverston AI and Stuart DG (1999). Neurons, networks, and motor behavior. MIT Press, Cambridge Google Scholar
  42. Suzuki H, Kerr R, Bianchi L, Frøkjær-Jensen C, Slone D, Xue J, Gerstbrein B, Driscoll M and Schafer WR (2003). In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron 39: 1005–1017 PubMedCrossRefGoogle Scholar
  43. Tam T, Mathews E, Snutch TP and Schafer W (2000). Voltage-gated calcium channels direct neuronal migration in Caenorhabditis elegans. Develop Biol 226: 104–117 PubMedCrossRefGoogle Scholar
  44. Tavernarakis N, Shreffler W, Wang SL and Driscoll M (1997). unc-8, a DEG/ENaC family member, encodes a subunit of a candidate mechanically gated channel that modulates C. elegans locomotion. Neuron 18(1): 107–119 PubMedCrossRefGoogle Scholar
  45. Towers PR, Edwards B, Richmond JE and Sattelle DB (2005). The Caenorhabditis elegans lev-8 gene encodes a novel type of nicotinic acetylcholine receptor α subunit. J Neurochem 93: 1–9 PubMedCrossRefGoogle Scholar
  46. Tsalik EL and Hobert O (2003). Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. J Neurobiol 56: 178–197 PubMedCrossRefGoogle Scholar
  47. Von Stetina SE, Treinin M and Miller III DM (2005). The motor circuit. Intl Rev Neurobiol 69: 125–167 CrossRefGoogle Scholar
  48. White JG, Southgate E, Thomson JN, Brenner S (1986a) Members: Vb1 to vb11. Online: http://www.wormatlas.org/MoW_built0.92/cells/vbn.html, viewed December 4, 2007
  49. White JG, Southgate E, Thomson JN and Brenner S (1986). The structure of the nervous system of the nematode C. elegans (the mind of a worm). Philos Trans R Soc Lond Series B Biol Sci 314(1165): 1–34 CrossRefGoogle Scholar
  50. Wicks SR, Roehrig CJ and Rankin CH (1996). A dynamic network simulation of the nematode tap withdrawal circuit: predictions concerning synaptic function using behavioral criteria. J Neurosci 16: 4017–4031 PubMedGoogle Scholar
  51. Wood WB (1988). Introduction to C. elegans biology. In: Wood, WB (eds) The Nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory, Cold Spring Harbor Google Scholar
  52. Yanik MF, Cinarm H, Cinarm HN, Chisholm AD, Jin Y and Ben-Yakar A (2004). Neurosurgery: functional regeneration after laser axotomy. Nature 432: 822 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.School of ComputingUniversity of LeedsLeedsUK

Personalised recommendations