Unraveling nested feedback loops in insect gaze stabilization: Mechanosensory feedback actively damps visually guided head movements in fly flight

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Mongeau, Jean-Michel; Cellini, Benjamin (2022). Unraveling nested feedback loops in insect gaze stabilization: Mechanosensory feedback actively damps visually guided head movements in fly flight [Data set]. Scholarsphere.

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Work Title Unraveling nested feedback loops in insect gaze stabilization: Mechanosensory feedback actively damps visually guided head movements in fly flight
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Open Access
Creators
  1. Jean-Michel Mongeau
  2. Benjamin Cellini
License In Copyright (Rights Reserved)
Work Type Dataset
Publication Date 2022
DOI doi:10.26207/qpxv-5v60
Deposited April 30, 2022

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Version 1
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  • Created
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  • Added Creator Jean-Michel Mongeau
  • Added Creator Benjamin Cellini
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    • https://creativecommons.org/licenses/by/4.0/
  • Added repo.zip
  • Updated Description Show Changes
    Description
    • 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 outer-loop visual sensory feedback and inner-loop mechanosensory feedback in the control of head movements. We discovered that visual feedback changes the tuning of head movements across visual motion frequencies whereas mechanosensory feedback damps 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 to self-generated and externally generated body motion, we revealed a nonlinear gating of mechanosensory feedback. Altogether, our findings clarify the role of nested feedback loops in flies and uncover mechanisms that reconcile differences in flight kinematics between body-fixed and body-free flies. Our framework is generalizable to biological and robotic systems relying on nested feedback control for guiding locomotion.
    • Data for manuscript
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    License
    • https://creativecommons.org/licenses/by/4.0/
    • https://rightsstatements.org/page/NoC-US/1.0/
  • Updated License Show Changes
    License
    • https://rightsstatements.org/page/NoC-US/1.0/
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    • https://www.gnu.org/licenses/gpl.html
    • https://rightsstatements.org/page/InC/1.0/
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Version 2
published

  • Created
  • Updated License Show Changes
    License
    • https://rightsstatements.org/page/InC/1.0/
    • https://creativecommons.org/licenses/by/4.0/
  • Updated License Show Changes
    License
    • https://creativecommons.org/licenses/by/4.0/
    • http://creativecommons.org/publicdomain/zero/1.0/
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    License
    • http://creativecommons.org/publicdomain/zero/1.0/
    • https://rightsstatements.org/page/InC/1.0/
  • Updated License Show Changes
    License
    • https://rightsstatements.org/page/InC/1.0/
    • https://creativecommons.org/licenses/by/4.0/
  • Updated Work Title Show Changes
    Work Title
    • Unraveling nested feedback loops in insect gaze stabilization: Mechanosensory feedback actively damps visually guided head movements in fly flight
    • Unraveling nested feedback loops in insect gaze stabilization
  • Published
  • Updated Work Title, Description, Related URLs Show Changes
    Work Title
    • Unraveling nested feedback loops in insect gaze stabilization
    • Unraveling nested feedback loops in insect gaze stabilization (Data for manuscript)
    Description
    • Data for manuscript
    • Data for "Nested mechanosensory feedback actively damps visually guided head movements in Drosophila."
    • Paper 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.
    Related URLs
    • https://doi.org/10.7554/eLife.80880
  • Updated Creator Jean-Michel Mongeau
  • Updated Creator Benjamin Cellini