Nested mechanosensory feedback actively damps visually guided head movements in Drosophila

  1. Benjamin Cellini
  2. Jean-Michel Mongeau  Is a corresponding author
  1. Pennsylvania State University, United States

Abstract

Executing agile locomotion requires animals to integrate sensory feedback, often from multiple sources. For example, human gaze is mediated by multiple feedback loops that integrate visual and vestibular information. A central challenge in studying biological feedback loops is that they are nested and dynamically coupled. Here, we develop a framework based on control theory for unraveling nested feedback systems and apply it to study gaze stabilization in the fruit fly (Drosophila). By combining experimental and mathematical methods to manipulate control topologies, we uncovered the role of body-generated mechanosensory feedback nested within visual feedback in the control of head movements. We discovered that visual feedback changed the tuning of head movements across visual motion frequencies whereas mechanosensory feedback damped head movements. Head saccades had slower dynamics when the body was free to move, further pointing to the role of damping via mechanosensory feedback. By comparing head responses between self-generated and externally generated body motion, we revealed a nonlinear gating of mechanosensory feedback that is motor-context dependent. Altogether, our findings reveal the role of nested feedback loops in flies and uncover mechanisms that reconcile differences in head kinematics between body-free and body-fixed flies. Our framework is generalizable to biological and robotic systems relying on nested feedback control for guiding locomotion.

Data availability

All code and data is available on Penn State ScholarSphere at this link: https://scholarsphere.psu.edu/resources/7af9b459-4be2-4347-bcb4-6db34cb9cc7e

The following data sets were generated

Article and author information

Author details

  1. Benjamin Cellini

    Department of Mechanical Engineering, Pennsylvania State University, University Park, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0609-7662
  2. Jean-Michel Mongeau

    Department of Mechanical Engineering, Pennsylvania State University, University Park, United States
    For correspondence
    jmmongeau@psu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3292-6911

Funding

Air Force Office of Scientific Research (FA9550-20-1-0084)

  • Jean-Michel Mongeau

Alfred P. Sloan Foundation

  • Jean-Michel Mongeau

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

Reviewing Editor

  1. Stephanie E Palmer, University of Chicago, United States

Version history

  1. Received: June 7, 2022
  2. Preprint posted: June 20, 2022 (view preprint)
  3. Accepted: October 17, 2022
  4. Accepted Manuscript published: October 19, 2022 (version 1)
  5. Version of Record published: November 11, 2022 (version 2)

Copyright

© 2022, Cellini & Mongeau

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. Benjamin Cellini
  2. Jean-Michel Mongeau
(2022)
Nested mechanosensory feedback actively damps visually guided head movements in Drosophila
eLife 11:e80880.
https://doi.org/10.7554/eLife.80880

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https://doi.org/10.7554/eLife.80880

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