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

Author:

Shelchkova Natalya D.ORCID,Downey John E.ORCID,Greenspon Charles M.ORCID,Okorokova Elizaveta V.ORCID,Sobinov Anton R.ORCID,Verbaarschot Ceci,He Qinpu,Sponheim CalebORCID,Tortolani Ariana F.,Moore Dalton D.,Kaufman Matthew T.ORCID,Lee Ray C.,Satzer David,Gonzalez-Martinez Jorge,Warnke Peter C.,Miller Lee E.ORCID,Boninger Michael L.,Gaunt Robert A.ORCID,Collinger Jennifer L.,Hatsopoulos Nicholas G.ORCID,Bensmaia Sliman J.ORCID

Abstract

AbstractThe 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.

Funder

U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke

Publisher

Springer Science and Business Media LLC

Subject

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

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