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.

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.

Metrics

  • 1,719
    views
  • 213
    downloads
  • 30
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.53908

Further reading

    1. Neuroscience
    Toshiki Kobayashi, Daichi Nozaki
    Research Article

    The remarkable ability of the motor system to adapt to novel environments has traditionally been investigated using kinematically non-redundant tasks, such as planar reaching movements. This limitation prevents the study of how the motor system achieves adaptation by altering the movement patterns of our redundant body. To address this issue, we developed a redundant motor task in which participants reached for targets with the tip of a virtual stick held with both hands. Despite the redundancy of the task, participants consistently employed a stereotypical strategy of flexibly changing the tilt angle of the stick depending on the direction of tip movement. Thus, this baseline relationship between tip-movement direction and stick-tilt angle constrained both the physical and visual movement patterns of the redundant system. Our task allowed us to systematically investigate how the motor system implicitly changed both the tip-movement direction and the stick-tilt angle in response to imposed visual perturbations. Both types of perturbations, whether directly affecting the task (tip-movement direction) or not (stick-tilt angle around the tip), drove adaptation, and the patterns of implicit adaptation were guided by the baseline relationship. Consequently, tip-movement adaptation was associated with changes in stick-tilt angle, and intriguingly, even seemingly ignorable stick-tilt perturbations significantly influenced tip-movement adaptation, leading to tip-movement direction errors. These findings provide a new understanding that the baseline relationship plays a crucial role not only in how the motor system controls movement of the redundant system, but also in how it implicitly adapts to modify movement patterns.

    1. Neuroscience
    Sudhanvan Iyer, Kathryn Maxson Jones ... Mary A Majumder
    Review Article

    In this paper, we provide an overview and analysis of the BRAIN Initiative data-sharing ecosystem. First, we compare and contrast the characteristics of the seven BRAIN Initiative data archives germane to data sharing and reuse, namely data submission and access procedures and aspects of interoperability. Second, we discuss challenges, benefits, and future opportunities, focusing on issues largely specific to sharing human data and drawing on N = 34 interviews with diverse stakeholders. The BRAIN Initiative-funded archive ecosystem faces interoperability and data stewardship challenges, such as achieving and maintaining interoperability of data and archives and harmonizing research participants’ informed consents for tiers of access for human data across multiple archives. Yet, a benefit of this distributed archive ecosystem is the ability of more specialized archives to adapt to the needs of particular research communities. Finally, the multiple archives offer ample raw material for network evolution in response to the needs of neuroscientists over time. Our first objective in this paper is to provide a guide to the BRAIN Initiative data-sharing ecosystem for readers interested in sharing and reusing neuroscience data. Second, our analysis supports the development of empirically informed policy and practice aimed at making neuroscience data more findable, accessible, interoperable, and reusable.