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.

Metrics

  • 1,186
    Page views
  • 159
    Downloads
  • 8
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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

Further reading

    1. Neuroscience
    Liqiang Chen et al.
    Short Report

    The presynaptic protein α-synuclein (αSyn) has been suggested to be involved in the pathogenesis of Parkinson’s disease (PD). In PD, the amygdala is prone to develop insoluble αSyn aggregates, and it has been suggested that circuit dysfunction involving the amygdala contributes to the psychiatric symptoms. Yet, how αSyn aggregates affect amygdala function is unknown. In this study, we examined αSyn in glutamatergic axon terminals and the impact of its aggregation on glutamatergic transmission in the basolateral amygdala (BLA). We found that αSyn is primarily present in the vesicular glutamate transporter 1-expressing (vGluT1+) terminals in mouse BLA, which is consistent with higher levels of αSyn expression in vGluT1+ glutamatergic neurons in the cerebral cortex relative to the vGluT2+ glutamatergic neurons in the thalamus. We found that αSyn aggregation selectively decreased the cortico-BLA, but not the thalamo-BLA, transmission; and that cortico-BLA synapses displayed enhanced short-term depression upon repetitive stimulation. In addition, using confocal microscopy, we found that vGluT1+ axon terminals exhibited decreased levels of soluble αSyn, which suggests that lower levels of soluble αSyn might underlie the enhanced short-term depression of cortico-BLA synapses. In agreement with this idea, we found that cortico-BLA synaptic depression was also enhanced in αSyn knockout mice. In conclusion, both basal and dynamic cortico-BLA transmission were disrupted by abnormal aggregation of αSyn and these changes might be relevant to the perturbed cortical control of the amygdala that has been suggested to play a role in psychiatric symptoms in PD.

    1. Evolutionary Biology
    2. Neuroscience
    Elias T Lunsford et al.
    Research Article Updated

    Animals can evolve dramatic sensory functions in response to environmental constraints, but little is known about the neural mechanisms underlying these changes. The Mexican tetra, Astyanax mexicanus, is a leading model to study genetic, behavioral, and physiological evolution by comparing eyed surface populations and blind cave populations. We compared neurophysiological responses of posterior lateral line afferent neurons and motor neurons across A. mexicanus populations to reveal how shifts in sensory function may shape behavioral diversity. These studies indicate differences in intrinsic afferent signaling and gain control across populations. Elevated endogenous afferent activity identified a lower response threshold in the lateral line of blind cavefish relative to surface fish leading to increased evoked potentials during hair cell deflection in cavefish. We next measured the effect of inhibitory corollary discharges from hindbrain efferent neurons onto afferents during locomotion. We discovered that three independently derived cavefish populations have evolved persistent afferent activity during locomotion, suggesting for the first time that partial loss of function in the efferent system can be an evolutionary mechanism for neural adaptation of a vertebrate sensory system.