Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
10 11 2023
Historique:
received: 30 09 2022
accepted: 01 11 2023
medline: 13 11 2023
pubmed: 11 11 2023
entrez: 10 11 2023
Statut: epublish

Résumé

The primary motor (M1) and somatosensory (S1) cortices play critical roles in motor control but the signaling between these structures is poorly understood. To fill this gap, we recorded - in three participants in an ongoing human clinical trial (NCT01894802) for people with paralyzed hands - the responses evoked in the hand and arm representations of M1 during intracortical microstimulation (ICMS) in the hand representation of S1. We found that ICMS of S1 activated some M1 neurons at short, fixed latencies consistent with monosynaptic activation. Additionally, most of the ICMS-evoked responses in M1 were more variable in time, suggesting indirect effects of stimulation. The spatial pattern of M1 activation varied systematically: S1 electrodes that elicited percepts in a finger preferentially activated M1 neurons excited during that finger's movement. Moreover, the indirect effects of S1 ICMS on M1 were context dependent, such that the magnitude and even sign relative to baseline varied across tasks. We tested the implications of these effects for brain-control of a virtual hand, in which ICMS conveyed tactile feedback. While ICMS-evoked activation of M1 disrupted decoder performance, this disruption was minimized using biomimetic stimulation, which emphasizes contact transients at the onset and offset of grasp, and reduces sustained stimulation.

Identifiants

pubmed: 37949923
doi: 10.1038/s41467-023-43140-2
pii: 10.1038/s41467-023-43140-2
pmc: PMC10638421
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

7270

Subventions

Organisme : NINDS NIH HHS
ID : R35 NS122333
Pays : United States
Organisme : NINDS NIH HHS
ID : UH3 NS107714
Pays : United States

Informations de copyright

© 2023. The Author(s).

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Auteurs

Natalya D Shelchkova (ND)

Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.

John E Downey (JE)

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA. johndowney@uchicago.edu.

Charles M Greenspon (CM)

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.

Elizaveta V Okorokova (EV)

Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.

Anton R Sobinov (AR)

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.

Ceci Verbaarschot (C)

Rehab Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA, USA.
Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands.

Qinpu He (Q)

Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.

Caleb Sponheim (C)

Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.

Ariana F Tortolani (AF)

Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.

Dalton D Moore (DD)

Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.

Matthew T Kaufman (MT)

Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.
Neuroscience Institute, University of Chicago, Chicago, IL, USA.

Ray C Lee (RC)

Schwab Rehabilitation Hospital, Chicago, IL, USA.

David Satzer (D)

Department of Neurological Surgery, University of Chicago, Chicago, IL, USA.

Jorge Gonzalez-Martinez (J)

Department of Neurosurgery, University of Pittsburgh, Pittsburgh, PA, USA.

Peter C Warnke (PC)

Neuroscience Institute, University of Chicago, Chicago, IL, USA.
Department of Neurological Surgery, University of Chicago, Chicago, IL, USA.

Lee E Miller (LE)

Department of Physiology, Northwestern University, Chicago, IL, USA.

Michael L Boninger (ML)

Rehab Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA.

Robert A Gaunt (RA)

Rehab Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, PA, USA.

Jennifer L Collinger (JL)

Rehab Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, PA, USA.

Nicholas G Hatsopoulos (NG)

Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.
Neuroscience Institute, University of Chicago, Chicago, IL, USA.

Sliman J Bensmaia (SJ)

Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.
Neuroscience Institute, University of Chicago, Chicago, IL, USA.

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