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Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex
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 re...
Autores principales: | , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10638421/ https://www.ncbi.nlm.nih.gov/pubmed/37949923 http://dx.doi.org/10.1038/s41467-023-43140-2 |
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author | Shelchkova, Natalya D. Downey, John E. Greenspon, Charles M. Okorokova, Elizaveta V. Sobinov, Anton R. Verbaarschot, Ceci He, Qinpu Sponheim, Caleb Tortolani, Ariana F. Moore, Dalton D. Kaufman, Matthew T. Lee, Ray C. Satzer, David Gonzalez-Martinez, Jorge Warnke, Peter C. Miller, Lee E. Boninger, Michael L. Gaunt, Robert A. Collinger, Jennifer L. Hatsopoulos, Nicholas G. Bensmaia, Sliman J. |
author_facet | Shelchkova, Natalya D. Downey, John E. Greenspon, Charles M. Okorokova, Elizaveta V. Sobinov, Anton R. Verbaarschot, Ceci He, Qinpu Sponheim, Caleb Tortolani, Ariana F. Moore, Dalton D. Kaufman, Matthew T. Lee, Ray C. Satzer, David Gonzalez-Martinez, Jorge Warnke, Peter C. Miller, Lee E. Boninger, Michael L. Gaunt, Robert A. Collinger, Jennifer L. Hatsopoulos, Nicholas G. Bensmaia, Sliman J. |
author_sort | Shelchkova, Natalya D. |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-10638421 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-106384212023-11-11 Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex Shelchkova, Natalya D. Downey, John E. Greenspon, Charles M. Okorokova, Elizaveta V. Sobinov, Anton R. Verbaarschot, Ceci He, Qinpu Sponheim, Caleb Tortolani, Ariana F. Moore, Dalton D. Kaufman, Matthew T. Lee, Ray C. Satzer, David Gonzalez-Martinez, Jorge Warnke, Peter C. Miller, Lee E. Boninger, Michael L. Gaunt, Robert A. Collinger, Jennifer L. Hatsopoulos, Nicholas G. Bensmaia, Sliman J. Nat Commun Article 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. Nature Publishing Group UK 2023-11-10 /pmc/articles/PMC10638421/ /pubmed/37949923 http://dx.doi.org/10.1038/s41467-023-43140-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Shelchkova, Natalya D. Downey, John E. Greenspon, Charles M. Okorokova, Elizaveta V. Sobinov, Anton R. Verbaarschot, Ceci He, Qinpu Sponheim, Caleb Tortolani, Ariana F. Moore, Dalton D. Kaufman, Matthew T. Lee, Ray C. Satzer, David Gonzalez-Martinez, Jorge Warnke, Peter C. Miller, Lee E. Boninger, Michael L. Gaunt, Robert A. Collinger, Jennifer L. Hatsopoulos, Nicholas G. Bensmaia, Sliman J. Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex |
title | Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex |
title_full | Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex |
title_fullStr | Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex |
title_full_unstemmed | Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex |
title_short | Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex |
title_sort | microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10638421/ https://www.ncbi.nlm.nih.gov/pubmed/37949923 http://dx.doi.org/10.1038/s41467-023-43140-2 |
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