Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex
Abstract 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...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-11-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-43140-2 |
| _version_ | 1797630088609529856 |
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| author | Natalya D. Shelchkova John E. Downey Charles M. Greenspon Elizaveta V. Okorokova Anton R. Sobinov Ceci Verbaarschot Qinpu He Caleb Sponheim Ariana F. Tortolani Dalton D. Moore Matthew T. Kaufman Ray C. Lee David Satzer Jorge Gonzalez-Martinez Peter C. Warnke Lee E. Miller Michael L. Boninger Robert A. Gaunt Jennifer L. Collinger Nicholas G. Hatsopoulos Sliman J. Bensmaia |
| author_facet | Natalya D. Shelchkova John E. Downey Charles M. Greenspon Elizaveta V. Okorokova Anton R. Sobinov Ceci Verbaarschot Qinpu He Caleb Sponheim Ariana F. Tortolani Dalton D. Moore Matthew T. Kaufman Ray C. Lee David Satzer Jorge Gonzalez-Martinez Peter C. Warnke Lee E. Miller Michael L. Boninger Robert A. Gaunt Jennifer L. Collinger Nicholas G. Hatsopoulos Sliman J. Bensmaia |
| author_sort | Natalya D. Shelchkova |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-03-11T11:03:02Z |
| format | Article |
| id | doaj.art-315382d1179645d4af2cb80aef00d14b |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-11T11:03:02Z |
| publishDate | 2023-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-315382d1179645d4af2cb80aef00d14b2023-11-12T12:22:43ZengNature PortfolioNature Communications2041-17232023-11-0114111110.1038/s41467-023-43140-2Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortexNatalya D. Shelchkova0John E. Downey1Charles M. Greenspon2Elizaveta V. Okorokova3Anton R. Sobinov4Ceci Verbaarschot5Qinpu He6Caleb Sponheim7Ariana F. Tortolani8Dalton D. Moore9Matthew T. Kaufman10Ray C. Lee11David Satzer12Jorge Gonzalez-Martinez13Peter C. Warnke14Lee E. Miller15Michael L. Boninger16Robert A. Gaunt17Jennifer L. Collinger18Nicholas G. Hatsopoulos19Sliman J. Bensmaia20Committee on Computational Neuroscience, University of ChicagoDepartment of Organismal Biology and Anatomy, University of ChicagoDepartment of Organismal Biology and Anatomy, University of ChicagoCommittee on Computational Neuroscience, University of ChicagoDepartment of Organismal Biology and Anatomy, University of ChicagoRehab Neural Engineering Labs, University of PittsburghCommittee on Computational Neuroscience, University of ChicagoCommittee on Computational Neuroscience, University of ChicagoCommittee on Computational Neuroscience, University of ChicagoCommittee on Computational Neuroscience, University of ChicagoCommittee on Computational Neuroscience, University of ChicagoSchwab Rehabilitation HospitalDepartment of Neurological Surgery, University of ChicagoDepartment of Neurosurgery, University of PittsburghNeuroscience Institute, University of ChicagoDepartment of Physiology, Northwestern UniversityRehab Neural Engineering Labs, University of PittsburghRehab Neural Engineering Labs, University of PittsburghRehab Neural Engineering Labs, University of PittsburghCommittee on Computational Neuroscience, University of ChicagoCommittee on Computational Neuroscience, University of ChicagoAbstract 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.https://doi.org/10.1038/s41467-023-43140-2 |
| spellingShingle | Natalya D. Shelchkova John E. Downey Charles M. Greenspon Elizaveta V. Okorokova Anton R. Sobinov Ceci Verbaarschot Qinpu He Caleb Sponheim Ariana F. Tortolani Dalton D. Moore Matthew T. Kaufman Ray C. Lee David Satzer Jorge Gonzalez-Martinez Peter C. Warnke Lee E. Miller Michael L. Boninger Robert A. Gaunt Jennifer L. Collinger Nicholas G. Hatsopoulos Sliman J. Bensmaia Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex Nature Communications |
| 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 |
| url | https://doi.org/10.1038/s41467-023-43140-2 |
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