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

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 and Sliman J. Bensmaia
Additional contact information
Natalya D. Shelchkova: University of Chicago
John E. Downey: University of Chicago
Charles M. Greenspon: University of Chicago
Elizaveta V. Okorokova: University of Chicago
Anton R. Sobinov: University of Chicago
Ceci Verbaarschot: University of Pittsburgh
Qinpu He: University of Chicago
Caleb Sponheim: University of Chicago
Ariana F. Tortolani: University of Chicago
Dalton D. Moore: University of Chicago
Matthew T. Kaufman: University of Chicago
Ray C. Lee: Schwab Rehabilitation Hospital
David Satzer: University of Chicago
Jorge Gonzalez-Martinez: University of Pittsburgh
Peter C. Warnke: University of Chicago
Lee E. Miller: Northwestern University
Michael L. Boninger: University of Pittsburgh
Robert A. Gaunt: University of Pittsburgh
Jennifer L. Collinger: University of Pittsburgh
Nicholas G. Hatsopoulos: University of Chicago
Sliman J. Bensmaia: University of Chicago

Nature Communications, 2023, vol. 14, issue 1, 1-11

Abstract: 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.

Date: 2023
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Citations: View citations in EconPapers (2)

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DOI: 10.1038/s41467-023-43140-2

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