1. Neuroscience
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Neural ensemble dynamics in dorsal motor cortex during speech in people with paralysis

  1. Sergey D Stavisky  Is a corresponding author
  2. Francis R Willett
  3. Guy H Wilson
  4. Brian A Murphy
  5. Paymon Rezaii
  6. Donald T Avansino
  7. William D Memberg
  8. Jonathan P Miller
  9. Robert F Kirsch
  10. Leigh R Hochberg
  11. A Bolu Ajiboye
  12. Shaul Druckmann
  13. Krishna V Shenoy
  14. Jaimie M Henderson
  1. Stanford University, United States
  2. Case Western Reserve University, United States
  3. University Hospitals Cleveland Medical Center, United States
  4. Brown University, United States
Research Article
  • Cited 3
  • Views 3,047
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Cite this article as: eLife 2019;8:e46015 doi: 10.7554/eLife.46015

Abstract

Speaking is a sensorimotor behavior whose neural basis is difficult to study with single neuron resolution due to the scarcity of human intracortical measurements. We used electrode arrays to record from the motor cortex 'hand knob' in two people with tetraplegia, an area not previously implicated in speech. Neurons modulated during speaking and during non-speaking movements of the tongue, lips, and jaw. This challenges whether the conventional model of a 'motor homunculus' division by major body regions extends to the single-neuron scale. Spoken words and syllables could be decoded from single trials, demonstrating the potential of intracortical recordings for brain-computer interfaces to restore speech. Two neural population dynamics features previously reported for arm movements were also present during speaking: a component that was mostly invariant across initiating different words, followed by rotatory dynamics during speaking. This suggests that common neural dynamical motifs may underlie movement of arm and speech articulators.

Article and author information

Author details

  1. Sergey D Stavisky

    Department of Neurosurgery, Stanford University, Stanford, United States
    For correspondence
    sergey.stavisky@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5238-0573
  2. Francis R Willett

    Department of Neurosurgery, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
  3. Guy H Wilson

    Neurosciences Program, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
  4. Brian A Murphy

    Department of Biomedical Engineering, Case Western Reserve University, Cleveland, United States
    Competing interests
    No competing interests declared.
  5. Paymon Rezaii

    Department of Neurosurgery, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4803-0853
  6. Donald T Avansino

    Department of Neurosurgery, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
  7. William D Memberg

    Department of Biomedical Engineering, Case Western Reserve University, Cleveland, United States
    Competing interests
    No competing interests declared.
  8. Jonathan P Miller

    Department of Neurosurgery, University Hospitals Cleveland Medical Center, Cleveland, United States
    Competing interests
    No competing interests declared.
  9. Robert F Kirsch

    Department of Biomedical Engineering, Case Western Reserve University, Cleveland, United States
    Competing interests
    No competing interests declared.
  10. Leigh R Hochberg

    School of Engineering and Carney Institute for Brain Science, Brown University, Providence, United States
    Competing interests
    Leigh R Hochberg, The MGH Translational Research Center has clinical research support agreements with Paradromics and Synchron Med, for which L.R.H provides consultative input.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0261-2273
  11. A Bolu Ajiboye

    Department of Biomedical Engineering, Case Western Reserve University, Cleveland, United States
    Competing interests
    No competing interests declared.
  12. Shaul Druckmann

    Department of Neurobiology, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
  13. Krishna V Shenoy

    Department of Electrical Engineering, Stanford University, Stanford, United States
    Competing interests
    Krishna V Shenoy, is a consultant for Neuralink Corp. and on the scientific advisory boards of CTRL-Labs Inc., MIND-X Inc., Inscopix Inc., and Heal Inc.
  14. Jaimie M Henderson

    Department of Neurosurgery, Stanford University, Stanford, United States
    Competing interests
    Jaimie M Henderson, is a consultant for Neuralink Corp.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3276-2267

Funding

ALS Association Milton Safenowitz Postdoctoral Fellowship (17-PDF-364)

  • Sergey D Stavisky

National Institute of Neurological Disorders and Stroke (5U01NS098968-02)

  • Leigh R Hochberg
  • Jaimie M Henderson

Howard Hughes Medical Institute

  • Krishna V Shenoy

National Institute on Deafness and Other Communication Disorders (R01DC009899)

  • Leigh R Hochberg

NSF GRFP (DGE - 1656518)

  • Guy H Wilson

Regina Casper Stanford Graduate Fellowship

  • Guy H Wilson

Office of Research and Development, Rehabilitation R&D Service, Department of Veterans Affairs (A2295R)

  • Leigh R Hochberg

Office of Research and Development, Rehabilitation R&D Service, Department of Veterans Affairs (B6453R)

  • Leigh R Hochberg

A. P. Giannini Foundation Postdoctoral Research Fellowship

  • Sergey D Stavisky

Wu Tsai Neurosciences Institute Interdisciplinary Scholar Award

  • Sergey D Stavisky

Larry and Pamela Garlick Foundation

  • Krishna V Shenoy
  • Jaimie M Henderson

Samuel and Betsy Reeves

  • Krishna V Shenoy
  • Jaimie M Henderson

National Institute on Deafness and Other Communication Disorders (R01DC014034)

  • Jaimie M Henderson

Office of Research and Development, Rehabilitation R&D Service, Department of Veterans Affairs (N9288C)

  • Leigh R Hochberg

Executive Committee on Research of Massachusetts General Hospital

  • Leigh R Hochberg

Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD077220)

  • Robert F Kirsch

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

Ethics

Human subjects: The two participants in this study were enrolled in the BrainGate2 Neural Interface System pilot clinical trial (ClinicalTrials.gov Identifier: NCT00912041). The overall purpose of the study is to obtain preliminary safety information and demonstrate proof of principle that an intracortical brain-computer interface can enable people with tetraplegia to communicate and control external devices. Permission for the study was granted by the U.S. Food and Drug Administration under an Investigational Device Exemption (Caution: Investigational device. Limited by federal law to investigational use). The study was also approved by the Institutional Review Boards of Stanford University Medical Center (protocol #20804), Brown University (#0809992560), University Hospitals of Cleveland Medical Center (#04-12-17), Partners HealthCare and Massachusetts General Hospital (#2011P001036), and the Providence VA Medical Center (#2011-009). Both participants gave informed consent to the study and publications resulting from the research, including consent to publish photographs and audiovisual recordings of them.

Reviewing Editor

  1. Tamar R Makin, University College London, United Kingdom

Publication history

  1. Received: February 14, 2019
  2. Accepted: November 14, 2019
  3. Accepted Manuscript published: December 10, 2019 (version 1)
  4. Version of Record published: January 10, 2020 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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