Advertisement

Biological Cybernetics

, Volume 106, Issue 6–7, pp 373–387 | Cite as

A model of chemotaxis and associative learning in C. elegans

  • Peter A. ApplebyEmail author
Original Paper

Abstract

The nematode C. elegans has attracted a great deal of interest from the neuroscience community due to the simplicity of its nervous system, which in the hermaphrodite is composed of just 302 neurons. C. elegans is known to engage in a number of sophisticated behaviours such as chemo- and thermotaxis. Experimental work has shown that these behaviours can be modified by experience and that C. elegans is capable of associative learning. In this paper, we focus on the chemotactic response of C. elegans to sodium chloride mediated by the ASE sensory neurons. We construct a biophysical model of the ASEL and ASER neurons that captures the time course of the ASE responses in response to up- and down-steps in NaCl concentration. We use this model to show that the time course of the ASE responses provide sufficient temporal resolution to successfully drive chemotaxis in C. elegans via steering, pirouettes and control of final turn angle. We show that these different locomotion strategies are individually capable of driving chemotaxis and that by working together they produce the best chemotactic response. We find that there is a separation into upward and downward drives mediated by the left and right ASE neurons. We show that the connectivity from ASEL and ASER must be of opposite polarity and that ASER, and the concomitant ability to sense when the worm is moving down the gradient, is more important for chemotaxis than ASEL, findings that are consistent with existing modelling studies in the literature. Finally, we examine associative learning in the network and show that experimental data can be explained by changes that occur at either the synaptic or sensory neuron level, the choice of which has distinct consequences for network function.

Keywords

C. elegans Chemotaxis Plasticity Learning 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adachi R, Wakabayashi T, Oda N, Shingai R (2008) Modulation of Caenorhabditis elegans chemotaxis by cultivation and assay temperatures. Neurosci Res 3: 300–306CrossRefGoogle Scholar
  2. Bargmann C, Horvitz H (1991) Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7: 729–742PubMedCrossRefGoogle Scholar
  3. Chao M, Komatsu H, Fukuto H, Dionne H, Hart A (2004) Feeding status and serotonin rapidly and reversibly modulate a Caenorhabditis elegans chemosensory circuit. Proc Natl Acad Sci USA 101: 15512–15517PubMedCrossRefGoogle Scholar
  4. Chen B, Hall D, Chklovskii D (2006) Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci USA 103: 4723–4728PubMedCrossRefGoogle Scholar
  5. Chi C, Clark D, Lee S, Biron D, Luo L, Gabel C, Brown J, Sengupta P, Samuel A (2007) Temperature and food mediate long-term thermotactic behavioral plasticity by association-independent mechanisms in C. elegans. J Exp Biol 210: 4043–4052PubMedCrossRefGoogle Scholar
  6. Dayan P, Abbott L (2001) Theoretical neuroscience: computational and mathematical modeling of neural systems. MIT Press, CambridgeGoogle Scholar
  7. Dunn N, Lockery S, Pierce-Shimomura J, Conery J (2004) A neural network model of chemotaxis predicts functions of synaptic connections in the nematode Caenorhabditis elegans. J Comput Neurosci 17: 137–147PubMedCrossRefGoogle Scholar
  8. Ferree T, Lockery S (1999) Computational rules for chemotaxis in the nematode C. elegans. J Comput Neurosci 6: 263–277PubMedCrossRefGoogle Scholar
  9. Gray J, Hill J, Bargmann C (2005) A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci USA 102: 3184–3191PubMedCrossRefGoogle Scholar
  10. Hills T, Brockie P, Maricq A (2004) Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J Neurosci 24: 1217–1225PubMedCrossRefGoogle Scholar
  11. Iino Y, Yoshida K (2009) Parallel use of two behavioural mechanisms for chemotaxis in Caenorhabditis elegans. J Neurosci 29: 5370–5380PubMedCrossRefGoogle Scholar
  12. Izquierdo E, Lockery S (2010) Evolution and analysis of minimal neural circuits for klinotaxis in Caenorhabditis elegans. J Neurosci 30: 12908–12917PubMedCrossRefGoogle Scholar
  13. Kimura K, Miyawaki A, Matsumoto K, Mori I (2004) The C. elegans thermosensory neuron AFD responds to warming. Curr Biol 14: 1291–1295PubMedCrossRefGoogle Scholar
  14. Kuhara A, Mori I (2006) Molecular physiology of the neural circuit for calcineurin-dependent associative learning in Caenorhabditis elegans. J Neurosci 26: 9355–9364PubMedCrossRefGoogle Scholar
  15. Mellem J, Brockie P, Madsen D, Maricq A (2008) Action potentials contribute to neuronal signaling in C. elegans. Nat Neurosci 11: 865–867PubMedCrossRefGoogle Scholar
  16. Miller A, Thiele T, Faumont S, Moravec M, Lockery S (2005) Step-response analysis of chemotaxis in Caenorhabditis elegans. J Neurosci 25: 3369–3378PubMedCrossRefGoogle Scholar
  17. Mori I (1999) Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. Annu Rev Genet 33: 399–422PubMedCrossRefGoogle Scholar
  18. Nuttley W, Atkinson-Leadbeater K, van der Kooy D (2002) Serotonin mediates food-odor associative learning in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 99: 12449–12454PubMedCrossRefGoogle Scholar
  19. Pierce-Shimomura J, Morse T, Lockery S (1999) The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J Neurosci 19: 9557–9569PubMedGoogle Scholar
  20. Pierce-Shimomura JT, Faumont S, Gaston M, Pearson BJ, Lockery SR (2001) The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans. Nature 410: 694–698PubMedCrossRefGoogle Scholar
  21. Pierce-Shimomura J, Dores M, Lockery S (2005) Analysis of the effects of turning bias on chemotaxis in C. elegans. J Exp Biol 208: 4727–4733PubMedCrossRefGoogle Scholar
  22. Saeki S, Yamamoto M, Iino Y (2001) Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. Exp Biol 204: 1757–1764Google Scholar
  23. Sambongi Y, Nagae T, Liu Y, Yoshimizu T, Takeda K, Wada Y, Futai M (1999) Sensing of cadmium and copper ions by externally exposed ADL, ASE, and ASH neurons elicits avoidance response in Caenorhabditis elegans. NeuroReport 10: 753–757PubMedCrossRefGoogle Scholar
  24. Sawin E, Ranganathan R, Horvitz H (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26: 619–631PubMedCrossRefGoogle Scholar
  25. Stetak A, Horndli F, Maricq A, van den Heuvel S, Hajnal A (2009) Neuron-specific regulation of associative learning and memory by MAGI-1 in C. elegans. PLoS One 4: e6019PubMedCrossRefGoogle Scholar
  26. Suzuki H, Thiele T, Faumont S, Ezcurra M, Lockery S, Schafer W (2008) Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature 454: 114–117PubMedCrossRefGoogle Scholar
  27. Thiele T, Faumont S, Lockery S (2009) The neural network for chemotaxis to tastants in Caenorhabditis elegans is specialized for temporal differentiation. J Neurosci 29: 11904–11911PubMedCrossRefGoogle Scholar
  28. Torayama I, Ishihara T, Katsura I (2007) Caenorhabditis elegans integrates the signals of butanone and food to enhance chemotaxis to butanone. J Neurosci 27: 741–750PubMedCrossRefGoogle Scholar
  29. Ward S (1973) Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by use of mutants. Proc Natl Acad Sci USA 70: 817–821PubMedCrossRefGoogle Scholar
  30. Ward S, Thomson N, White JG, Brenner S (1975) Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J Comp Neurol 160: 313–337PubMedCrossRefGoogle Scholar
  31. Ware R, Clark D, Crossland K, Russell R (1975) The nerve ring of the nematode Caenorhabditis elegans: sensory input and motor output. J Comp Neurol 162: 71–110CrossRefGoogle Scholar
  32. White J, Southgate E, Thomson J, Brenner S (1986) The structure of the nervous system of the nematode C. elegans. Philos Trans R Soc Lond B 314: 1–340CrossRefGoogle Scholar
  33. Zhao B, Khare P, Feldman L, Dent J (2003) Reversal frequency in Caenorhabditis elegans represents an integrated response to the state of the animal and its environment. J Neurosci 23: 5319–5328PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Kroto Research InstituteUniversity of SheffieldSheffieldUK

Personalised recommendations