Postural control of arm and fingers through integration of movement commands

  1. Scott T Albert  Is a corresponding author
  2. Alkis M Hadjiosif
  3. Jihoon Jang
  4. Andrew J Zimnik
  5. Demetris S Soteropoulos
  6. Stuart N Baker
  7. Mark M Churchland
  8. John W Krakauer
  9. Reza Shadmehr  Is a corresponding author
  1. Johns Hopkins School of Medicine, United States
  2. Columbia University Medical Center, United States
  3. Newcastle University, United Kingdom

Abstract

Every movement ends in a period of stillness. Current models assume that commands that hold the limb at a target location do not depend on the commands that moved the limb to that location. Here, we report a surprising relationship between movement and posture in primates: on a within-trial basis, the commands that hold the arm and finger at a target location depend on the mathematical integration of the commands that moved the limb to that location. Following damage to the corticospinal tract, both the move and hold period commands become more variable. However, the hold period commands retain their dependence on the integral of the move period commands. Thus, our data suggest that the postural controller possesses a feedforward module that uses move commands to calculate a component of hold commands. This computation may arise within an unknown subcortical system that integrates cortical commands to stabilize limb posture.

Data availability

Source data files generated or analyzed during this study are included for Figures 1-7 and have also been deposited in OSF under accession code YC64A.

The following data sets were generated

Article and author information

Author details

  1. Scott T Albert

    Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, United States
    For correspondence
    scottalbert1@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9140-1077
  2. Alkis M Hadjiosif

    Department of Neurology, Johns Hopkins School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jihoon Jang

    Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Andrew J Zimnik

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Demetris S Soteropoulos

    Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Stuart N Baker

    Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Mark M Churchland

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9123-6526
  8. John W Krakauer

    Department of Neurology, Johns Hopkins School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4316-1846
  9. Reza Shadmehr

    Laboratory for Computational Motor Control, Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, United States
    For correspondence
    shadmehr@jhu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7686-2569

Funding

National Institute of Neurological Disorders and Stroke (R01NS078311)

  • Reza Shadmehr

Sheikh Khalifa Stroke Institute

  • John W Krakauer

Medical Research Council (MR/K023012/1)

  • Demetris S Soteropoulos

National Institute of Neurological Disorders and Stroke (1DP2NS083037)

  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (R01NS100066)

  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (1U19NS104649)

  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (F31NS095706)

  • Scott T Albert

National Institute of Neurological Disorders and Stroke (F32NS092350)

  • Mark M Churchland

National Science Foundation (1723967)

  • Reza Shadmehr

Simons Foundation (SCGB#542957)

  • Mark M Churchland

Medical Research Council (MR/P023967)

  • Stuart N Baker

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

Reviewing Editor

  1. Kunlin Wei, Peking University, China

Ethics

Animal experimentation: All animal procedures in the U.S. were conducted in accord with the US National Institutes of Health guidelines and were approved by the Columbia University Institutional Animal Care and Use Committee (AC-AAAQ7409). These data were originally published in Lara, Cunningham, & Churchland (2018) as well as Lara, Elsayed, Zimnik, Cunningham, & Churchland (2018). All procedures in the U.K. were carried out under appropriate UK Home Office licenses in accordance with the Animals (Scientific Procedures) Act 1986, and were approved by the Local Research Ethics Committee of Newcastle University. These data were originally published in Soteropoulos, Williams, & Baker (2012).

Human subjects: Informed consent was obtained from all participants. All human subjects work was approved by the Johns Hopkins School of Medicine Institutional Review Board, protocol number NA_00037510.

Version history

  1. Received: October 6, 2019
  2. Accepted: February 3, 2020
  3. Accepted Manuscript published: February 11, 2020 (version 1)
  4. Version of Record published: March 9, 2020 (version 2)

Copyright

© 2020, Albert 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. Scott T Albert
  2. Alkis M Hadjiosif
  3. Jihoon Jang
  4. Andrew J Zimnik
  5. Demetris S Soteropoulos
  6. Stuart N Baker
  7. Mark M Churchland
  8. John W Krakauer
  9. Reza Shadmehr
(2020)
Postural control of arm and fingers through integration of movement commands
eLife 9:e52507.
https://doi.org/10.7554/eLife.52507

Share this article

https://doi.org/10.7554/eLife.52507

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