Journal Article

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

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

2023

Overview

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. Here the authors record the responses evoked in the hand and arm representations of M1 during intracortical microstimulation in the hand representation of S1, and show somatotopically organized connections with motor cortex. The resulting interference with motor decoding is task dependent but can be alleviated by using biomimetic stimulation.

• Publisher: Nature Publishing Group UK,Nature Publishing Group,Nature Portfolio
• Subject: 631/378/2620/2618 / 631/378/2632/1663 / Arm / Biomimetics / Cortex (motor) / Decoding / Electric Stimulation / Electrodes / Fingers / Hand / Hand (anatomy) / Humanities and Social Sciences / Humans / Motor Cortex - physiology / Motor task performance / Movement - physiology / multidisciplinary / Neurons / Neurons - physiology / Neurosciences / Paralysis / Representations / Science / Science (multidisciplinary) / Sensory feedback / Somatosensory cortex / Somatosensory Cortex - physiology / Stimulation