1. Neuroscience

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

  1. Shin-Ichiro Terada
  2. Daisuke Matsubara
  3. Koun Onodera
  4. Masanori Matsuzaki
  5. Tadashi Uemura
  6. Tadao Usui  Is a corresponding author
  1. Kyoto University, Japan
  2. National Institute for Basic Biology, Japan
https://doi.org/10.7554/eLife.12959
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Cite this article
  1. Shin-Ichiro Terada
  2. Daisuke Matsubara
  3. Koun Onodera
  4. Masanori Matsuzaki
  5. Tadashi Uemura
  6. Tadao Usui
(2016)
Neuronal processing of noxious thermal stimuli mediated by dendritic Ca2+ influx in Drosophila somatosensory neurons
eLife 5:e12959.
https://doi.org/10.7554/eLife.12959
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Abstract

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 of 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.

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  1. Shin-Ichiro Terada

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

  2. Daisuke Matsubara

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

  3. Koun Onodera

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

  4. Masanori Matsuzaki

    Division of Brain Circuits, National Institute for Basic Biology, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.

  5. Tadashi Uemura

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

  6. 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.

Copyright

© 2016, Terada 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. Shin-Ichiro Terada
  2. Daisuke Matsubara
  3. Koun Onodera
  4. Masanori Matsuzaki
  5. Tadashi Uemura
  6. Tadao Usui
(2016)
Neuronal processing of noxious thermal stimuli mediated by dendritic Ca2+ influx in Drosophila somatosensory neurons
eLife 5:e12959.
https://doi.org/10.7554/eLife.12959

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https://doi.org/10.7554/eLife.12959

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Further reading

    1. Neuroscience

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

    Koun Onodera, Shumpei Baba ... Tadao Usui
    Research Advance Updated

    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.