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Small conductance Ca2+-activated K+ channels induce the firing pause periods during the activation of Drosophila nociceptive neurons

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Cite this article as: eLife 2017;6:e29754 doi: 10.7554/eLife.29754

Abstract

In Drosophila larvae, Class IV sensory neurons respond to noxious thermal stimuli and provoke heat avoidance behavior. Previously, we showed that the activated neurons displayed characteristic fluctuations of firing rates which consisted of repetitive high-frequency spike trains and subsequent pause periods, and we proposed that the firing rate fluctuations enhanced the heat avoidance (Terada et al., 2016). Here, we further substantiate this idea by showing that the pause periods and the frequency of fluctuations are regulated by small conductance Ca2+-activated K+ (SK) channels, and the SK knockdown larvae display faster heat avoidance than control larvae. The regulatory mechanism of the fluctuations in the Class IV neurons resembles that in mammalian Purkinje cells, which display complex spikes. Furthermore, our results suggest that such fluctuation coding in Class IV neurons is required to convert noxious thermal inputs into effective stereotyped behavior as well as general rate coding.

Article and author information

Author details

  1. Koun Onodera

    Graduate School of Biostudies, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4203-9865
  2. Shumpei Baba

    Graduate School of Biostudies, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Akira Murakami

    Faculty of Science, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Tadashi Uemura

    Graduate School of Biostudies, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7204-3606
  5. Tadao Usui

    Graduate School of Biostudies, Kyoto University, Kyoto, Japan
    For correspondence
    tadao.usui@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0507-1495

Funding

Japan Society for the Promotion of Science

  • Koun Onodera

Ministry of Education, Culture, Sports, Science, and Technology (Grants-in-Aid for Scientific Research on Innovative Areas 'Mesoscopic Neurocircuitry' 22115006)

  • Tadashi Uemura

Takeda Science Foundation

  • Tadashi Uemura

Ministry of Education, Culture, Sports, Science, and Technology (Grant-in-Aid for Scientific Research (C) 24500410)

  • Tadao Usui

Ministry of Education, Culture, Sports, Science, and Technology (Grants-in-Aid for Scientific Research on Innovative Areas 'Brain Environment' 24111525)

  • Tadao Usui

Toray Industries

  • Tadao Usui

Ministry of Education, Culture, Sports, Science, and Technology (Platform Project for Supporting in Drug Discovery and Life Science Research from AMED)

  • Tadashi Uemura

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

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: June 20, 2017
  2. Accepted: October 14, 2017
  3. Accepted Manuscript published: October 16, 2017 (version 1)
  4. Version of Record published: October 23, 2017 (version 2)

Copyright

© 2017, Onodera 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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