1. Developmental Biology
  2. Neuroscience

Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

  1. André Ferreira Castro  Is a corresponding author
  2. Lothar Baltruschat
  3. Tomke Stürner
  4. Amirhoushang Bahrami
  5. Peter Jedlicka
  6. Gaia Tavosanis  Is a corresponding author
  7. Hermann Cuntz  Is a corresponding author
  1. Ernst Strüngmann Institut (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany
  2. Center for Neurodegenerative Diseases (DZNE), Germany
  3. University of Cambridge, United Kingdom
  4. Max Planck Institute for Dynamics and Self Organization, Germany
  5. JLU Giessen, Germany
https://doi.org/10.7554/eLife.60920
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  1. André Ferreira Castro
  2. Lothar Baltruschat
  3. Tomke Stürner
  4. Amirhoushang Bahrami
  5. Peter Jedlicka
  6. Gaia Tavosanis
  7. Hermann Cuntz
(2020)
Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction
eLife 9:e60920.
https://doi.org/10.7554/eLife.60920
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Abstract

Class I ventral posterior dendritic arborisation (c1vpda) proprioceptive sensory neurons respond to contractions in the Drosophila larval body wall during crawling. Their dendritic branches run along the direction of contraction, possibly a functional requirement to maximise membrane curvature during crawling contractions. Although the molecular machinery of dendritic patterning in c1vpda has been extensively studied, the process leading to the precise elaboration of their comb-like shapes remains elusive. Here, to link dendrite shape with its proprioceptive role, we performed long-term, non-invasive, in vivo time-lapse imaging of c1vpda embryonic and larval morphogenesis to reveal a sequence of differentiation stages. We combined computer models and dendritic branch dynamics tracking to propose that distinct sequential phases of stochastic growth and retraction achieve efficient dendritic trees both in terms of wire and function. Our study shows how dendrite growth balances structure–function requirements, shedding new light on general principles of self-organisation in functionally specialised dendrites.

Data availability

All data and all code is available on Zenodo https://doi.org/10.5281/zenodo.4290200

The following data sets were generated

Article and author information

Author details

  1. André Ferreira Castro

    Ernst Strüngmann Institut (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt am Main, Germany
    For correspondence
    acastro@mrc-lmb.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.

  2. Lothar Baltruschat

    Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Tomke Stürner

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  4. Amirhoushang Bahrami

    Max Planck Institute for Dynamics and Self Organization, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5841-2516

  5. Peter Jedlicka

    Institute of Clinical Neuroanatomy, JLU Giessen, Giessen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6571-5742

  6. Gaia Tavosanis

    Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
    For correspondence
    Gaia.Tavosanis@dzne.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8679-5515

  7. Hermann Cuntz

    Ernst Strüngmann Institut (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt am Main, Germany
    For correspondence
    cuntz@fias.uni-frankfurt.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5445-0507

Funding

Bundesministerium für Bildung und Forschung (01GQ1406)

  • Hermann Cuntz

Deutsche Forschungsgemeinschaft (SPP 1464)

  • Gaia Tavosanis

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

Copyright

© 2020, Ferreira Castro 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. André Ferreira Castro
  2. Lothar Baltruschat
  3. Tomke Stürner
  4. Amirhoushang Bahrami
  5. Peter Jedlicka
  6. Gaia Tavosanis
  7. Hermann Cuntz
(2020)
Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction
eLife 9:e60920.
https://doi.org/10.7554/eLife.60920

Share this article

https://doi.org/10.7554/eLife.60920

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