A size principle for recruitment of Drosophila leg motor neurons

  1. Anthony W Azevedo
  2. Evyn S Dickinson
  3. Pralaksha Gurung
  4. Lalanti Venkatasubramanian
  5. Richard S Mann
  6. John C Tuthill  Is a corresponding author
  1. University of Washington, United States
  2. Columbia University, United States

Abstract

To move the body, the brain must precisely coordinate patterns of activity among diverse populations of motor neurons. Here, we use in vivo calcium imaging, electrophysiology, and behavior to understand how genetically-identified motor neurons control flexion of the fruit fly tibia. We find that leg motor neurons exhibit a coordinated gradient of anatomical, physiological, and functional properties. Large, fast motor neurons control high force, ballistic movements while small, slow motor neurons control low force, postural movements. Intermediate neurons fall between these two extremes. This hierarchical organization resembles the size principle, first proposed as a mechanism for establishing recruitment order among vertebrate motor neurons. Recordings in behaving flies confirmed that motor neurons are typically recruited in order from slow to fast. However, we also find that fast, intermediate, and slow motor neurons receive distinct proprioceptive feedback signals, suggesting that the size principle is not the only mechanism that dictates motor neuron recruitment. Overall, this work reveals the functional organization of the fly leg motor system and establishes Drosophila as a tractable system for investigating neural mechanisms of limb motor control.

Data availability

All data is publicly available on Dryad doi:10.5061/dryad.76hdr7stb

The following data sets were generated

Article and author information

Author details

  1. Anthony W Azevedo

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Evyn S Dickinson

    Dept of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Pralaksha Gurung

    Dept of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Lalanti Venkatasubramanian

    Department of Biochemistry and Molecular Biophysics, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9280-8335
  5. Richard S Mann

    Department of Biochemistry and Molecular Biophysics, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4749-2765
  6. John C Tuthill

    Dept of Physiology and Biophysics, University of Washington, Seattle, United States
    For correspondence
    johnctuthill@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5689-5806

Funding

NIH (U19NS104655)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • Lalanti Venkatasubramanian
  • Richard S Mann
  • John C Tuthill

Searle Foundation (Scholar Award)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • John C Tuthill

McKnight Foundation (Scholar Award)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • John C Tuthill

Pew Biomedical Trust (Scholar Award)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • John C Tuthill

Sloan Foundation (Research Fellowship)

  • Anthony W Azevedo
  • Evyn S Dickinson
  • Pralaksha Gurung
  • John C Tuthill

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

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Received: March 9, 2020
  2. Accepted: June 1, 2020
  3. Accepted Manuscript published: June 3, 2020 (version 1)
  4. Version of Record published: July 9, 2020 (version 2)

Copyright

© 2020, Azevedo 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. Anthony W Azevedo
  2. Evyn S Dickinson
  3. Pralaksha Gurung
  4. Lalanti Venkatasubramanian
  5. Richard S Mann
  6. John C Tuthill
(2020)
A size principle for recruitment of Drosophila leg motor neurons
eLife 9:e56754.
https://doi.org/10.7554/eLife.56754

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