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Reconnecting the Hand and Arm to the Brain: Efficacy of Neural Interfaces for Sensorimotor Restoration after Tetraplegia

BACKGROUND: Paralysis after spinal cord injury involves damage to pathways that connect neurons in the brain to peripheral nerves in the limbs. Re-establishing this communication using neural interfaces has the potential to bridge the gap and restore upper extremity function to people with high tetr...

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Autores principales: Herring, Eric Z., Graczyk, Emily L., Memberg, William D., Adams, Robert D., Baca-Vaca, Guadalupe Fernandez, Hutchison, Brianna C., Krall, John T., Alexander, Benjamin J., Conlan, Emily C., Alfaro, Kenya E., Bhat, Preethi R., Ketting-Olivier, Aaron B., Haddix, Chase A., Taylor, Dawn M., Tyler, Dustin J., Kirsch, Robert F., Ajiboye, A. Bolu, Miller, Jonathan P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10168522/
https://www.ncbi.nlm.nih.gov/pubmed/37162904
http://dx.doi.org/10.1101/2023.04.24.23288977
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author Herring, Eric Z.
Graczyk, Emily L.
Memberg, William D.
Adams, Robert D.
Baca-Vaca, Guadalupe Fernandez
Hutchison, Brianna C.
Krall, John T.
Alexander, Benjamin J.
Conlan, Emily C.
Alfaro, Kenya E.
Bhat, Preethi R.
Ketting-Olivier, Aaron B.
Haddix, Chase A.
Taylor, Dawn M.
Tyler, Dustin J.
Kirsch, Robert F.
Ajiboye, A. Bolu
Miller, Jonathan P.
author_facet Herring, Eric Z.
Graczyk, Emily L.
Memberg, William D.
Adams, Robert D.
Baca-Vaca, Guadalupe Fernandez
Hutchison, Brianna C.
Krall, John T.
Alexander, Benjamin J.
Conlan, Emily C.
Alfaro, Kenya E.
Bhat, Preethi R.
Ketting-Olivier, Aaron B.
Haddix, Chase A.
Taylor, Dawn M.
Tyler, Dustin J.
Kirsch, Robert F.
Ajiboye, A. Bolu
Miller, Jonathan P.
author_sort Herring, Eric Z.
collection PubMed
description BACKGROUND: Paralysis after spinal cord injury involves damage to pathways that connect neurons in the brain to peripheral nerves in the limbs. Re-establishing this communication using neural interfaces has the potential to bridge the gap and restore upper extremity function to people with high tetraplegia. OBJECTIVE: We report a novel approach for restoring upper extremity function using selective peripheral nerve stimulation controlled by intracortical microelectrode recordings from sensorimotor networks, along with restoration of tactile sensation of the hand using intracortical microstimulation. METHODS: A right-handed man with motor-complete C3-C4 tetraplegia was enrolled into the clinical trial. Six 64-channel intracortical microelectrode arrays were implanted into left hemisphere regions involved in upper extremity function, including primary motor and sensory cortices, inferior frontal gyrus, and anterior intraparietal area. Nine 16-channel extraneural peripheral nerve electrodes were implanted to allow targeted stimulation of right median, ulnar (2), radial, axillary, musculocutaneous, suprascapular, lateral pectoral, and long thoracic nerves, to produce selective muscle contractions on demand. Proof-of-concept studies were performed to demonstrate feasibility of a bidirectional brain-machine interface to restore function of the participant’s own arm and hand. RESULTS: Multi-unit neural activity that correlated with intended motor action was successfully recorded from intracortical arrays. Microstimulation of electrodes in somatosensory cortex produced repeatable sensory percepts of individual fingers for restoration of touch sensation. Selective electrical activation of peripheral nerves produced antigravity muscle contractions. The system was well tolerated with no operative complications. CONCLUSION: The combination of implanted cortical electrodes and nerve cuff electrodes has the potential to allow restoration of motor and sensory functions of the arm and hand after neurological injury.
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spelling pubmed-101685222023-05-10 Reconnecting the Hand and Arm to the Brain: Efficacy of Neural Interfaces for Sensorimotor Restoration after Tetraplegia Herring, Eric Z. Graczyk, Emily L. Memberg, William D. Adams, Robert D. Baca-Vaca, Guadalupe Fernandez Hutchison, Brianna C. Krall, John T. Alexander, Benjamin J. Conlan, Emily C. Alfaro, Kenya E. Bhat, Preethi R. Ketting-Olivier, Aaron B. Haddix, Chase A. Taylor, Dawn M. Tyler, Dustin J. Kirsch, Robert F. Ajiboye, A. Bolu Miller, Jonathan P. medRxiv Article BACKGROUND: Paralysis after spinal cord injury involves damage to pathways that connect neurons in the brain to peripheral nerves in the limbs. Re-establishing this communication using neural interfaces has the potential to bridge the gap and restore upper extremity function to people with high tetraplegia. OBJECTIVE: We report a novel approach for restoring upper extremity function using selective peripheral nerve stimulation controlled by intracortical microelectrode recordings from sensorimotor networks, along with restoration of tactile sensation of the hand using intracortical microstimulation. METHODS: A right-handed man with motor-complete C3-C4 tetraplegia was enrolled into the clinical trial. Six 64-channel intracortical microelectrode arrays were implanted into left hemisphere regions involved in upper extremity function, including primary motor and sensory cortices, inferior frontal gyrus, and anterior intraparietal area. Nine 16-channel extraneural peripheral nerve electrodes were implanted to allow targeted stimulation of right median, ulnar (2), radial, axillary, musculocutaneous, suprascapular, lateral pectoral, and long thoracic nerves, to produce selective muscle contractions on demand. Proof-of-concept studies were performed to demonstrate feasibility of a bidirectional brain-machine interface to restore function of the participant’s own arm and hand. RESULTS: Multi-unit neural activity that correlated with intended motor action was successfully recorded from intracortical arrays. Microstimulation of electrodes in somatosensory cortex produced repeatable sensory percepts of individual fingers for restoration of touch sensation. Selective electrical activation of peripheral nerves produced antigravity muscle contractions. The system was well tolerated with no operative complications. CONCLUSION: The combination of implanted cortical electrodes and nerve cuff electrodes has the potential to allow restoration of motor and sensory functions of the arm and hand after neurological injury. Cold Spring Harbor Laboratory 2023-04-26 /pmc/articles/PMC10168522/ /pubmed/37162904 http://dx.doi.org/10.1101/2023.04.24.23288977 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Herring, Eric Z.
Graczyk, Emily L.
Memberg, William D.
Adams, Robert D.
Baca-Vaca, Guadalupe Fernandez
Hutchison, Brianna C.
Krall, John T.
Alexander, Benjamin J.
Conlan, Emily C.
Alfaro, Kenya E.
Bhat, Preethi R.
Ketting-Olivier, Aaron B.
Haddix, Chase A.
Taylor, Dawn M.
Tyler, Dustin J.
Kirsch, Robert F.
Ajiboye, A. Bolu
Miller, Jonathan P.
Reconnecting the Hand and Arm to the Brain: Efficacy of Neural Interfaces for Sensorimotor Restoration after Tetraplegia
title Reconnecting the Hand and Arm to the Brain: Efficacy of Neural Interfaces for Sensorimotor Restoration after Tetraplegia
title_full Reconnecting the Hand and Arm to the Brain: Efficacy of Neural Interfaces for Sensorimotor Restoration after Tetraplegia
title_fullStr Reconnecting the Hand and Arm to the Brain: Efficacy of Neural Interfaces for Sensorimotor Restoration after Tetraplegia
title_full_unstemmed Reconnecting the Hand and Arm to the Brain: Efficacy of Neural Interfaces for Sensorimotor Restoration after Tetraplegia
title_short Reconnecting the Hand and Arm to the Brain: Efficacy of Neural Interfaces for Sensorimotor Restoration after Tetraplegia
title_sort reconnecting the hand and arm to the brain: efficacy of neural interfaces for sensorimotor restoration after tetraplegia
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10168522/
https://www.ncbi.nlm.nih.gov/pubmed/37162904
http://dx.doi.org/10.1101/2023.04.24.23288977
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