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


Journal

Neurosurgery
ISSN: 1524-4040
Titre abrégé: Neurosurgery
Pays: United States
ID NLM: 7802914

Informations de publication

Date de publication:
01 Apr 2024
Historique:
received: 03 04 2023
accepted: 01 09 2023
pubmed: 20 11 2023
medline: 20 11 2023
entrez: 20 11 2023
Statut: ppublish

Résumé

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. 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. A 27-year-old right-handed man with AIS-B (motor-complete, sensory-incomplete) 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 using a brain-machine interface to read from and write to the brain for restoring motor and sensory functions of the participant's own arm and hand. Multiunit 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, resulting in functional movements that the participant was able to command under brain control to perform virtual and actual arm and hand movements. The system was well tolerated with no operative complications. The combination of implanted cortical electrodes and nerve cuff electrodes has the potential to create bidirectional restoration of motor and sensory functions of the arm and hand after neurological injury.

Sections du résumé

BACKGROUND AND OBJECTIVES OBJECTIVE
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. 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 METHODS
A 27-year-old right-handed man with AIS-B (motor-complete, sensory-incomplete) 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 using a brain-machine interface to read from and write to the brain for restoring motor and sensory functions of the participant's own arm and hand.
RESULTS RESULTS
Multiunit 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, resulting in functional movements that the participant was able to command under brain control to perform virtual and actual arm and hand movements. The system was well tolerated with no operative complications.
CONCLUSION CONCLUSIONS
The combination of implanted cortical electrodes and nerve cuff electrodes has the potential to create bidirectional restoration of motor and sensory functions of the arm and hand after neurological injury.

Identifiants

pubmed: 37982637
doi: 10.1227/neu.0000000000002769
pii: 00006123-990000000-00967
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

864-874

Subventions

Organisme : Congressionally Directed Medical Research Programs
ID : Clinical Trial Award SC180308

Commentaires et corrections

Type : UpdateOf

Informations de copyright

Copyright © Congress of Neurological Surgeons 2024. All rights reserved.

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Auteurs

Eric Z Herring (EZ)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Neurosurgery, The Neurological Institute, University Hospital Cleveland Medical Center, Cleveland , Ohio , USA.

Emily L Graczyk (EL)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.
Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland , Ohio , USA.

William D Memberg (WD)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.
Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland , Ohio , USA.

Robert Adams (R)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Neurosurgery, The Neurological Institute, University Hospital Cleveland Medical Center, Cleveland , Ohio , USA.

Gaudalupe Fernandez Baca-Vaca (G)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Neurosurgery, The Neurological Institute, University Hospital Cleveland Medical Center, Cleveland , Ohio , USA.

Brianna C Hutchison (BC)

Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.

John T Krall (JT)

Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.

Benjamin J Alexander (BJ)

Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.

Emily C Conlan (EC)

Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.

Kenya E Alfaro (KE)

Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.

Preethisiri Bhat (P)

Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.

Aaron B Ketting-Olivier (AB)

Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.

Chase A Haddix (CA)

Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Neuroscience, The Cleveland Clinic, Cleveland , Ohio , USA.

Dawn M Taylor (DM)

Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.
Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland , Ohio , USA.
Department of Neuroscience, The Cleveland Clinic, Cleveland , Ohio , USA.

Dustin J Tyler (DJ)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.
Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland , Ohio , USA.

Jennifer A Sweet (JA)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Neurosurgery, The Neurological Institute, University Hospital Cleveland Medical Center, Cleveland , Ohio , USA.

Robert F Kirsch (RF)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.
Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland , Ohio , USA.

A Bolu Ajiboye (AB)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Biomedical Engineering, Case Western Reserve University, Cleveland , Ohio , USA.
Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland , Ohio , USA.

Jonathan P Miller (JP)

School of Medicine, Case Western Reserve University, Cleveland , Ohio , USA.
Department of Neurosurgery, The Neurological Institute, University Hospital Cleveland Medical Center, Cleveland , Ohio , USA.
Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland , Ohio , USA.

Classifications MeSH