The energetic basis for smooth human arm movements

  1. Jeremy D Wong  Is a corresponding author
  2. Tyler Cluff
  3. Arthur D Kuo
  1. Faculty of Kinesiology, Department of Biomedical Enginee, Canada
  2. University of Calgary, Canada

Abstract

The central nervous system plans human reaching movements with stereotypically smooth kinematic trajectories and fairly consistent durations. Smoothness seems to be explained by accuracy as a primary movement objective, whereas duration seems to economize energy expenditure. But the current understanding of energy expenditure does not explain smoothness, so that two aspects of the same movement are governed by seemingly incompatible objectives. Here we show that smoothness is actually economical, because humans expend more metabolic energy for jerkier motions. The proposed mechanism is an underappreciated cost proportional to the rate of muscle force production, for calcium transport to activate muscle. We experimentally tested that energy cost in humans (N=10) performing bimanual reaches cyclically. The empirical cost was then demonstrated to predict smooth, discrete reaches, previously attributed to accuracy alone. A mechanistic, physiologically measurable, energy cost may therefore explain both smoothness and duration in terms of economy, and help resolve motor redundancy in reaching movements.

Data availability

Data has been deposited to Dryad Digital Repository, accessible here: doi:10.5061/dryad.qfttdz0gn

The following data sets were generated

Article and author information

Author details

  1. Jeremy D Wong

    Department of Biomedical Engineering, Faculty of Kinesiology, Department of Biomedical Enginee, Calgary, Canada
    For correspondence
    jeremy.wong2@ucalgary.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5564-1794
  2. Tyler Cluff

    Faculty of Kinesiology, Department of Biomedical Enginee, University of Calgary, Calgary, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Arthur D Kuo

    Faculty of Kinesiology, Department of Biomedical Enginee, University of Calgary, Calgary, Canada
    Competing interests
    The authors declare that no competing interests exist.

Funding

Benno Nigg Chair

  • Arthur D Kuo

NSERC Discovery and Research Chairs Program

  • Arthur D Kuo

Alberta Health Trust

  • Arthur D Kuo

NSERC Discovery

  • Tyler Cluff

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

Ethics

Human subjects: Informed consent was obtained from all subjects and the Health Research Ethics Board approved of all procedures (REB18-1521).

Reviewing Editor

  1. Alaa Ahmed, University of Colorado, United States

Version history

  1. Preprint posted: December 29, 2020 (view preprint)
  2. Received: March 3, 2021
  3. Accepted: December 15, 2021
  4. Accepted Manuscript published: December 20, 2021 (version 1)
  5. Version of Record published: January 7, 2022 (version 2)
  6. Version of Record updated: January 27, 2022 (version 3)
  7. Version of Record updated: February 3, 2022 (version 4)

Copyright

© 2021, Wong 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. Jeremy D Wong
  2. Tyler Cluff
  3. Arthur D Kuo
(2021)
The energetic basis for smooth human arm movements
eLife 10:e68013.
https://doi.org/10.7554/eLife.68013

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