Tuning of feedforward control enables stable muscle force-length dynamics after loss of autogenic proprioceptive feedback

  1. Joanne C Gordon
  2. Natalie C Holt
  3. Andrew A Biewener
  4. Monica A Daley  Is a corresponding author
  1. University of London, United Kingdom
  2. University of California, Riverside, United States
  3. Harvard University, United States
  4. University of California, Irvine, United States

Abstract

Animals must integrate feedforward, feedback and intrinsic mechanical control mechanisms to maintain stable locomotion. Recent studies of guinea fowl (Numida meleagris) revealed that the distal leg muscles rapidly modulate force and work output to minimize perturbations in uneven terrain. Here we probe the role of reflexes in the rapid perturbation responses of muscle by studying the effects of proprioceptive loss. We induced bilateral loss of autogenic proprioception in the lateral gastrocnemius muscle (LG) using self-reinnervation. We compared in vivo muscle dynamics and ankle kinematics in birds with reinnervated and intact LG. Reinnervated and intact LG exhibit similar steady state mechanical function and similar work modulation in response to obstacle encounters. Reinnervated LG exhibits 23ms earlier steady-state activation, consistent with feedforward tuning of activation phase to compensate for lost proprioception. Modulation of activity duration is impaired in rLG, confirming the role of reflex feedback in regulating force duration in intact muscle.

Data availability

The full dataset including raw data, metadata files and processing code have been deposited to DataDryad.org: DOI (doi:10.7280/D11H49).

The following data sets were generated

Article and author information

Author details

  1. Joanne C Gordon

    Comparative Biomedical Sciences, Royal Veterinary College, University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Natalie C Holt

    Evolution, Ecology and Organismal Biology, University of California, Riverside, Riverside, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Andrew A Biewener

    Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3303-8737
  4. Monica A Daley

    Ecology and Evolutionary Biology, University of California, Irvine, Irvine, United States
    For correspondence
    madaley@uci.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8584-2052

Funding

National Institutes of Health (NIAMS 5R01AR055648)

  • Andrew A Biewener

Biotechnology and Biological Sciences Research Council (BB/H005838/1)

  • Monica A Daley

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

Ethics

Animal experimentation: All experiments were undertaken at the Concord Field Station of Harvard University, in Boston (MA, USA), and all procedures were licensed and approved by the Harvard Institutional Animal Care and Use Committee (AEP #20-09) in accordance with the guidelines of the National Institutes of Health and the regulations of the United States Department of Agriculture. Surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: November 24, 2019
  2. Accepted: June 12, 2020
  3. Accepted Manuscript published: June 23, 2020 (version 1)
  4. Version of Record published: July 3, 2020 (version 2)

Copyright

© 2020, Gordon 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. Joanne C Gordon
  2. Natalie C Holt
  3. Andrew A Biewener
  4. Monica A Daley
(2020)
Tuning of feedforward control enables stable muscle force-length dynamics after loss of autogenic proprioceptive feedback
eLife 9:e53908.
https://doi.org/10.7554/eLife.53908
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