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Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis

Nature volume 454, pages 114117 (03 July 2008) | Download Citation

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Abstract

Chemotaxis in Caenorhabditis elegans, like chemotaxis in bacteria1, involves a random walk biased by the time derivative of attractant concentration2,3, but how the derivative is computed is unknown. Laser ablations have shown that the strongest deficits in chemotaxis to salts are obtained when the ASE chemosensory neurons (ASEL and ASER) are ablated, indicating that this pair has a dominant role4. Although these neurons are left–right homologues anatomically, they exhibit marked asymmetries in gene expression and ion preference5,6,7. Here, using optical recordings of calcium concentration in ASE neurons in intact animals, we demonstrate an additional asymmetry: ASEL is an ON-cell, stimulated by increases in NaCl concentration, whereas ASER is an OFF-cell, stimulated by decreases in NaCl concentration. Both responses are reliable yet transient, indicating that ASE neurons report changes in concentration rather than absolute levels. Recordings from synaptic and sensory transduction mutants show that the ON–OFF asymmetry is the result of intrinsic differences between ASE neurons. Unilateral activation experiments indicate that the asymmetry extends to the level of behavioural output: ASEL lengthens bouts of forward locomotion (runs) whereas ASER promotes direction changes (turns). Notably, the input and output asymmetries of ASE neurons are precisely those of a simple yet novel neuronal motif for computing the time derivative of chemosensory information, which is the fundamental computation of C. elegans chemotaxis3,8. Evidence for ON and OFF cells in other chemosensory networks9,10,11,12 suggests that this motif may be common in animals that navigate by taste and smell.

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Acknowledgements

We thank the Caenorhabditis Genetics Center for strains, C. Frøkjœr-Jensen for strain integration and D. Julius for the TRPV1 complementary DNA. Support was provided by grants from the National Institutes of Health (MH051383 to S.R.L.; DA016445 to W.R.S.), National Science Foundation (IOB-0543643 to S.R.L.) and Human Frontier Science Program (to W.R.S.).

Author Contributions H.S. planned and performed the experiments first revealing the ASE ON–OFF function and the effects of transduction and synaptic mutants, made imaging and direct activation reagents, acquired supplementary ion-sensitivity data and drafted the manuscript. T.R.T. planned and performed ON–OFF, dose-response, genetics, direct activation and ablation experiments in the text and Supplementary Information, made imaging reagents, generated figures, and co-wrote the final manuscript. S.F. planned and performed ion selectivity and synaptic mutant imaging in the text and Supplementary Information. M.E. developed dose-response methodologies. S.R.L. planned imaging and behavioural experiments, devised the derivative model, and co-wrote the final manuscript. W.R.S. planned imaging and genetics experiments, and drafted the manuscript.

Author information

Author notes

    • Hiroshi Suzuki
    • , Tod R. Thiele
    •  & Shawn R. Lockery

    These authors contributed equally to this work.

    • Hiroshi Suzuki
    •  & William R. Schafer

    Present addresses: Center for Research in Neurodegenerative Diseases, University of Toronto, Toronto, Ontario M5S 3H2, Canada (H.S.); MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK (W.R.S.).

Affiliations

  1. Division of Biological Sciences, University of California, San Diego, La Jolla, California 92093, USA

    • Hiroshi Suzuki
    •  & William R. Schafer
  2. Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403, USA

    • Tod R. Thiele
    • , Serge Faumont
    •  & Shawn R. Lockery
  3. MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK

    • Marina Ezcurra
    •  & William R. Schafer

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Corresponding author

Correspondence to Shawn R. Lockery.

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    Supplementary information

    The file contains Supplementary Notes with experimental procedures and Supplementary Figures 1-6 with Legends

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https://doi.org/10.1038/nature06927

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