Pan-neuronal screening in Caenorhabditis elegans reveals asymmetric dynamics of AWC neurons is critical for thermal avoidance behavior

Abstract

Understanding neural functions inevitably involves arguments traversing multiple levels of hierarchy in biological systems. However, finding new components or mechanisms of such systems is extremely time-consuming due to the low efficiency of currently available functional screening techniques. To overcome such obstacles, we utilize pan-neuronal calcium imaging to broadly screen the activity of the C. elegans nervous system in response to thermal stimuli. A single pass of the screening procedure can identify much of the previously reported thermosensory circuitry as well as identify several unreported thermosensory neurons. Among the newly discovered neural functions, we investigated the role of the AWCOFF neuron in thermal nociception. Combining functional calcium imaging and behavioral assays, we show that AWCOFF is essential for avoidance behavior following noxious heat stimulation by modifying the forward-to-reversal behavioral transition rate. We also show that the AWCOFF signals adapt to repeated noxious thermal stimuli and quantify the corresponding behavioral adaptation.

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Author details

  1. Ippei Kotera

    Donnelly Centre, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Nhat Anh Tran

    Donnelly Centre, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Donald Fu

    Donnelly Centre, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Jimmy HJ Kim

    Department of Physics, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Jarlath D Byrne Rodgers

    Donnelly Centre,, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5395-9950
  6. William S Ryu

    Donnelly Centre, University of Toronto, Toronto, Canada
    For correspondence
    willryu@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0350-7507

Funding

Natural Sciences and Engineering Research Council of Canada

  • Jarlath D Byrne Rodgers
  • William S Ryu

Human Frontier Science Program

  • Ippei Kotera
  • Nhat Anh Tran
  • Donald Fu
  • William S Ryu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2016, Kotera et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Ippei Kotera
  2. Nhat Anh Tran
  3. Donald Fu
  4. Jimmy HJ Kim
  5. Jarlath D Byrne Rodgers
  6. William S Ryu
(2016)
Pan-neuronal screening in Caenorhabditis elegans reveals asymmetric dynamics of AWC neurons is critical for thermal avoidance behavior
eLife 5:e19021.
https://doi.org/10.7554/eLife.19021

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https://doi.org/10.7554/eLife.19021