Stability of motor representations after paralysis

  1. Charles Guan  Is a corresponding author
  2. Tyson Aflalo  Is a corresponding author
  3. Carey Y Zhang
  4. Elena Amoruso
  5. Emily R Rosario
  6. Nader Pouratian
  7. Richard A Andersen
  1. California Institute of Technology, United States
  2. University College London, United Kingdom
  3. Casa Colina Hospital and Centers for Healthcare, United States
  4. University of California, Los Angeles, United States

Abstract

Neural plasticity allows us to learn skills and incorporate new experiences. What happens when our lived experiences fundamentally change, such as after a severe injury? To address this question, we analyzed intracortical population activity in the posterior parietal cortex (PPC) of a tetraplegic adult as she controlled a virtual hand through a brain-computer interface (BCI). By attempting to move her fingers, she could accurately drive the corresponding virtual fingers. Neural activity during finger movements exhibited robust representational structure similar to fMRI recordings of able-bodied individuals' motor cortex, which has previously been shown to reflect able-bodied usage patterns. The finger representational structure was consistent throughout multiple sessions, even though the structure contributed to BCI decoding errors. Within individual BCI movements, the representational structure was dynamic, first resembling muscle activation patterns and then resembling the anticipated sensory consequences. Our results reveal that motor representations in PPC reflect able-bodied motor usage patterns even after paralysis, and BCIs can re-engage these representations to restore lost motor functions.

Data availability

Data is available on the BRAIN Initiative DANDI Archive at https://dandiarchive.org/dandiset/000147

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Charles Guan

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    cguan@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Tyson Aflalo

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    taflalo@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0101-2455
  3. Carey Y Zhang

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Elena Amoruso

    Institute of Cognitive Neuroscience, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Emily R Rosario

    Casa Colina Hospital and Centers for Healthcare, Pomona, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Nader Pouratian

    5David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Richard A Andersen

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Eye Institute (R01EY015545)

  • Charles Guan
  • Tyson Aflalo
  • Emily R Rosario
  • Nader Pouratian
  • Richard A Andersen

National Eye Institute (UG1EY032039)

  • Charles Guan
  • Tyson Aflalo
  • Emily R Rosario
  • Nader Pouratian
  • Richard A Andersen

Tianqiao and Chrissy Chen Brain-machine Interface Center at Caltech

  • Tyson Aflalo
  • Richard A Andersen

Boswell Foundation

  • Richard A Andersen

Amazon AI4Science Fellowship

  • Charles Guan

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

Reviewing Editor

  1. Jörn Diedrichsen, Western University, Canada

Ethics

Human subjects: All procedures were approved by the California Institute of Technology, Casa Colina Hospital and Centers for Healthcare, and the University of California, Los Angeles Institutional Review Boards. NS consented to the surgical procedure as well as to the subsequent clinical studies after understanding their nature, objectives, and potential risks.

Version history

  1. Received: October 6, 2021
  2. Preprint posted: October 9, 2021 (view preprint)
  3. Accepted: August 27, 2022
  4. Accepted Manuscript published: September 20, 2022 (version 1)
  5. Version of Record published: October 12, 2022 (version 2)

Copyright

© 2022, Guan 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. Charles Guan
  2. Tyson Aflalo
  3. Carey Y Zhang
  4. Elena Amoruso
  5. Emily R Rosario
  6. Nader Pouratian
  7. Richard A Andersen
(2022)
Stability of motor representations after paralysis
eLife 11:e74478.
https://doi.org/10.7554/eLife.74478

Share this article

https://doi.org/10.7554/eLife.74478

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