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. HatsopoulosSliman J. Bensmaia

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

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.

Original languageEnglish (US)
Article number7270
JournalNature communications
Volume14
Issue number1
DOIs
StatePublished - Dec 2023

Funding

N.H. and R.G. serve as consultants for Blackrock Microsystems, Inc. R.G. is also on the scientific advisory boards of Braingrade GmbH and Neurowired LLC. M.B., J.C., and R.G. received research funding from Blackrock Microsystems, Inc. though that funding did not support the work presented here. The remaining authors declare no competing interests. This work was supported by NINDS grants UH3 NS107714 and R35 NS122333.

ASJC Scopus subject areas

  • General Chemistry
  • General Biochemistry, Genetics and Molecular Biology
  • General Physics and Astronomy

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