1. Neuroscience
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Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva

  1. Csaba Verasztó
  2. Nobuo Ueda
  3. Luis A Bezares-Calderón
  4. Aurora Panzera
  5. Elizabeth A Williams
  6. Réza Shahidi
  7. Gáspár Jékely  Is a corresponding author
  1. Max Planck Institute for Developmental Biology, Germany
  2. Max-Planck-Institute for Developmental Biology, Germany
Research Article
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Cite this article as: eLife 2017;6:e26000 doi: 10.7554/eLife.26000

Abstract

Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.

Article and author information

Author details

  1. Csaba Verasztó

    n/a, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6295-7148
  2. Nobuo Ueda

    n/a, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Luis A Bezares-Calderón

    Max-Planck-Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6678-6876
  4. Aurora Panzera

    n/a, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Elizabeth A Williams

    Max-Planck-Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Réza Shahidi

    Max-Planck-Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Gáspár Jékely

    Max-Planck-Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    gaspar.jekely@tuebingen.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8496-9836

Funding

Deutsche Forschungsgemeinschaft (777/3-1)

  • Gáspár Jékely

Max-Planck-Gesellschaft (Open-access funding)

  • Gáspár Jékely

European Commission (GA 317172)

  • Gáspár Jékely

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

Reviewing Editor

  1. Piali Sengupta, Brandeis University, United States

Publication history

  1. Received: February 13, 2017
  2. Accepted: May 14, 2017
  3. Accepted Manuscript published: May 16, 2017 (version 1)
  4. Version of Record published: July 27, 2017 (version 2)

Copyright

© 2017, Verasztó 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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