Central processing of leg proprioception in Drosophila

  1. Sweta Agrawal
  2. Evyn S Dickinson
  3. Anne Sustar
  4. Pralaksha Gurung
  5. David Shepherd
  6. James W Truman
  7. John C Tuthill  Is a corresponding author
  1. University of Washington, United States
  2. Bangor University, United Kingdom
  3. Janelia Research Campus, Howard Hughes Medical Institute, United States

Abstract

Proprioception, the sense of self-movement and position, is mediated by mechanosensory neurons that detect diverse features of body kinematics. Although proprioceptive feedback is crucial for accurate motor control, little is known about how downstream circuits transform limb sensory information to guide motor output. Here, we investigate neural circuits in Drosophila that process proprioceptive information from the fly leg. We identify three cell-types from distinct developmental lineages that are positioned to receive input from proprioceptor subtypes encoding tibia position, movement, and vibration. 13Bα neurons encode femur-tibia joint angle and mediate postural changes in tibia position. 9Aα neurons also drive changes in leg posture, but encode a combination of directional movement, high frequency vibration, and joint angle. Activating 10Bα neurons, which encode tibia vibration at specific joint angles, elicits pausing in walking flies. Altogether, our results reveal that central circuits integrate information across proprioceptor subtypes to construct complex sensorimotor representations that mediate diverse behaviors, including reflexive control of limb posture and detection of leg vibration.

Data availability

Data made freely available on Dryad (doi:10.5061/dryad.k3j9kd55t).

The following data sets were generated

Article and author information

Author details

  1. Sweta Agrawal

    Dept 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7518-9512
  3. Anne Sustar

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

    Dept of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. David Shepherd

    School of Natural Sciences, Bangor University, Bangor, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6961-7880
  6. James W Truman

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9209-5435
  7. 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

National Institutes of Health (R01NS102333)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • Pralaksha Gurung
  • John C Tuthill

Howard Hughes Medical Institute

  • David Shepherd
  • James W Truman

Pew Charitable Trusts (Scholar Award)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • Pralaksha Gurung
  • John C Tuthill

Searle Scholars Program (Scholar Award)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • Pralaksha Gurung
  • John C Tuthill

Alfred P. Sloan Foundation (Scholar Award)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • Pralaksha Gurung
  • John C Tuthill

McKnight Endowment Fund for Neuroscience (Scholar Award)

  • Sweta Agrawal
  • Evyn S Dickinson
  • Anne Sustar
  • 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

Version history

  1. Received: June 22, 2020
  2. Accepted: December 1, 2020
  3. Accepted Manuscript published: December 2, 2020 (version 1)
  4. Version of Record published: December 21, 2020 (version 2)

Copyright

© 2020, Agrawal 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. Sweta Agrawal
  2. Evyn S Dickinson
  3. Anne Sustar
  4. Pralaksha Gurung
  5. David Shepherd
  6. James W Truman
  7. John C Tuthill
(2020)
Central processing of leg proprioception in Drosophila
eLife 9:e60299.
https://doi.org/10.7554/eLife.60299

Share this article

https://doi.org/10.7554/eLife.60299

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