Neural ensemble dynamics in dorsal motor cortex during speech in people with paralysis
- Stanford University, United States
- Case Western Reserve University, United States
- University Hospitals Cleveland Medical Center, United States
- Brown University, United States
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.
Data availability
The sharing of the raw human neural data is restricted due to the potential sensitivity of this data. These data are available upon request to the senior authors (K.V.S. or J.M.H.). To respect the participants' expectation of privacy, a legal agreement between the researcher's institution and the BrainGate consortium would need to be set up to facilitate the sharing of these datasets. Processed data is provided as source data, and analysis code is available at https://github.com/sstavisk/speech_in_dorsal_motor_cortex_eLife_2019.
Article and author information
Author details
Jaimie M Henderson
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.
Reviewing Editor
- Tamar R Makin, University College London, United Kingdom
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.
Version history
- Received: February 14, 2019
- Accepted: November 14, 2019
- Accepted Manuscript published: December 10, 2019 (version 1)
- 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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Neural ensemble dynamics in dorsal motor cortex during speech in people with paralysis
eLife 8:e46015.
https://doi.org/10.7554/eLife.46015
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