Drosophila mechanical nociceptors preferentially sense localized poking

Abstract

Mechanical nociception is an evolutionarily conserved sensory process required for the survival of living organisms. Previous studies have revealed much about the neural circuits and sensory molecules in mechanical nociception, but the cellular mechanisms adopted by nociceptors in force detection remain elusive. To address this issue, we study the mechanosensation of a fly larval nociceptor (class IV da neurons, c4da) using a customized mechanical device. We find that c4da are sensitive to mN-scale forces and make uniform responses to the forces applied at different dendritic regions. Moreover, c4da showed a greater sensitivity to localized forces, consistent with them being able to detect the poking of sharp objects, such as wasp ovipositor. Further analysis reveals that high morphological complexity, mechanosensitivity to lateral tension and possibly also active signal propagation in dendrites contribute to the sensory features of c4da. In particular, we discover that Piezo and Ppk1/Ppk26, two key mechanosensory molecules, make differential but additive contributions to the mechanosensitivity of c4da. In all, our results provide updates into understanding how c4da process mechanical signals at the cellular level and reveal the contributions of key molecules.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. The source data for all plots have been provided as Excel files.

The following previously published data sets were used

Article and author information

Author details

  1. Zhen Liu

    School of Life Sciences, Tsinghua University, Tsinghua, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Meng-Hua Wu

    School of Life Sciences, Tsinghua University, Tsinghua, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Qi-Xuan Wang

    School of Life Sciences, Tsinghua University, Tsinghua, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Shao-Zhen Lin

    Department of Engineering Mechanics, Tsinghua University, Tsinghua, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Xi-Xiao Feng

    Department of Engineering Mechanics, Tsinghua University, Tsinghua, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Bo Li

    Department of Engineering Mechanics, Tsinghua University, Tsinghua, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Xin Liang

    School of Life Sciences, Tsinghua University, Tsinghua, China
    For correspondence
    xinliang@tsinghua.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7915-8094

Funding

National Natural Science Foundation of China (31922018)

  • Xin Liang

National Natural Science Foundation of China (32070704)

  • Xin Liang

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

Reviewing Editor

  1. Matthieu Louis, University of California, Santa Barbara, United States

Publication history

  1. Received: December 21, 2021
  2. Preprint posted: January 5, 2022 (view preprint)
  3. Accepted: October 5, 2022
  4. Accepted Manuscript published: October 6, 2022 (version 1)
  5. Accepted Manuscript updated: October 7, 2022 (version 2)
  6. Version of Record published: November 21, 2022 (version 3)

Copyright

© 2022, Liu 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. Zhen Liu
  2. Meng-Hua Wu
  3. Qi-Xuan Wang
  4. Shao-Zhen Lin
  5. Xi-Xiao Feng
  6. Bo Li
  7. Xin Liang
(2022)
Drosophila mechanical nociceptors preferentially sense localized poking
eLife 11:e76574.
https://doi.org/10.7554/eLife.76574
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