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

Abstract

Intracortical microstimulation (ICMS) of somatosensory cortex (S1) can be used to restore tactile feedback to people with spinal cord injury via brain controlled bionic hands. Anatomical and neurophysiological evidence from various animal species points to a communication pathway between motor and somatosensory cortex, but this pathway’s normal function, and its relevance to neuroprosthetics, remains to be elucidated. To fill this gap, we delivered – in three human participants whose hands were paralyzed as a result of a spinal cord injury – ICMS to the somatosensory cortex (S1) while recording the responses evoked in the hand and arm representations of primary motor cortex (M1). We found that ICMS activated some M1 neurons at short, fixed latencies, locked to each pulse in a manner consistent with monosynaptic activation. However, most of the changes in M1 firing rates were much more variable in time, suggesting a more indirect effect of the stimulation. The spatial pattern of M1 activation varied systematically depending on the stimulating electrode: S1 electrodes that elicited percepts at a given hand location tended to activate M1 neurons with movement fields at the same location. However, the indirect effects of S1 ICMS on M1 were strongly 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 was used to convey tactile feedback about object interactions. While ICMS-evoked activation of M1 disrupted decoder performance, this disruption could be minimized with biomimetic stimulation, which emphasizes contact transients at the onset and offset of grasp, reduces sustained stimulation, and has been shown to convey useful contact-related information.