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A circuit mechanism for the propagation of waves of muscle contraction in Drosophila

  1. Akira Fushiki
  2. Maarten F Zwart
  3. Hiroshi Kohsaka
  4. Richard D Fetter
  5. Albert Cardona
  6. Akinao Nose  Is a corresponding author
  1. University of Tokyo, Japan
  2. Janelia Research Campus, Howard Hughes Medical Institute, United States
Research Article
  • Cited 73
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Cite this article as: eLife 2016;5:e13253 doi: 10.7554/eLife.13253

Abstract

Animals move by adaptively coordinating the sequential activation of muscles. The circuit mechanisms underlying coordinated locomotion are poorly understood. Here, we report on a novel circuit for propagation of waves of muscle contraction, using the peristaltic locomotion of Drosophila larvae as a model system. We found an intersegmental chain of synaptically connected neurons, alternating excitatory and inhibitory, necessary for wave propagation and active in phase with the wave. The excitatory neurons (A27h) are premotor and necessary only for forward locomotion, and are modulated by stretch receptors and descending inputs. The inhibitory neurons (GDL) are necessary for both forward and backward locomotion, suggestive of different yet coupled central pattern generators, and its inhibition is necessary for wave propagation. The circuit structure and functional imaging indicated that the commands to contract one segment promote the relaxation of the next segment, revealing a mechanism for wave propagation in peristaltic locomotion.

Article and author information

Author details

  1. Akira Fushiki

    Department of Complexity Science and Engineering, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Maarten F Zwart

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Hiroshi Kohsaka

    Department of Complexity Science and Engineering, University of Tokyo, Kashiwa, Chiba, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Richard D Fetter

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Albert Cardona

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Akinao Nose

    Department of Complexity Science and Engineering, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan
    For correspondence
    nose@k.u-tokyo.ac.jp
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Leslie C Griffith, Brandeis University, United States

Publication history

  1. Received: November 22, 2015
  2. Accepted: February 14, 2016
  3. Accepted Manuscript published: February 15, 2016 (version 1)
  4. Version of Record published: March 31, 2016 (version 2)

Copyright

© 2016, Fushiki 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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