1. Neuroscience

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

  1. Koun Onodera
  2. Shumpei Baba
  3. Akira Murakami
  4. Tadashi Uemura
  5. Tadao Usui  Is a corresponding author
  1. Kyoto University, Japan
https://doi.org/10.7554/eLife.29754
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  1. Koun Onodera
  2. Shumpei Baba
  3. Akira Murakami
  4. Tadashi Uemura
  5. Tadao Usui
(2017)
Small conductance Ca2+-activated K+ channels induce the firing pause periods during the activation of Drosophila nociceptive neurons
eLife 6:e29754.
https://doi.org/10.7554/eLife.29754
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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.

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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.

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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  1. Koun Onodera
  2. Shumpei Baba
  3. Akira Murakami
  4. Tadashi Uemura
  5. Tadao Usui
(2017)
Small conductance Ca2+-activated K+ channels induce the firing pause periods during the activation of Drosophila nociceptive neurons
eLife 6:e29754.
https://doi.org/10.7554/eLife.29754

Share this article

https://doi.org/10.7554/eLife.29754

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Further reading

    1. Neuroscience

    Neuronal processing of noxious thermal stimuli mediated by dendritic Ca2+ influx in Drosophila somatosensory neurons

    Shin-Ichiro Terada, Daisuke Matsubara ... Tadao Usui
    Research Article Updated

    Adequate responses to noxious stimuli causing tissue damages are essential for organismal survival. Class IV neurons in Drosophila larvae are polymodal nociceptors responsible for thermal, mechanical, and light sensation. Importantly, activation of Class IV provoked distinct avoidance behaviors, depending on the inputs. We found that noxious thermal stimuli, but not blue light stimulation, caused a unique pattern of Class IV, which were composed of pauses after high-frequency spike trains and a large Ca2+ rise in the dendrite (the Ca2+ transient). Both these responses depended on two TRPA channels and the L-type voltage-gated calcium channel (L-VGCC), showing that the thermosensation provokes Ca2+ influx. The precipitous fluctuation of firing rate in Class IV neurons enhanced the robust heat avoidance. We hypothesize that the Ca2+ influx can be a key signal encoding a specific modality.