Evoking highly focal percepts in the fingertips through targeted stimulation of sulcal regions of the brain for sensory restoration
Authors: Chandrasekaran Santosh , Bickel Stephan , Herrero Jose L , Kim Joo-won , Markowitz Noah , Espinal Elizabeth , Bhagat Nikunj A , Ramdeo Richard , Xu Junqian , Glasser Matthew F , Bouton Chad E , Mehta Ashesh D 
Published: November 2020

Paralysis and neuropathy, affecting millions of people worldwide, can be accompanied by a significant loss of somatosensation. With tactile sensation being central to achieving dexterous movement, brain-computer interface (BCI) researchers have explored the use of intracortical electrical stimulation to restore sensation to the hand. However, current approaches have been restricted to stimulating the gyral areas of the brain while functional imaging suggests that the representation of fingertips lie predominantly in the sulcal regions. Here we show, for the first time, highly focal percepts can be evoked in the fingertips of the hand through electrical stimulation of the sulcal areas of the brain. To this end, we mapped and compared sensations elicited in the hand by stimulating both gyral and sulcal areas of the human primary somatosensory cortex (S1). Two participants with intractable epilepsy were implanted with stereoelectroencephalography (SEEG) and high-density electrocorticography (HD-ECoG) electrodes in S1 guided by high-resolution functional imaging. Using myelin content and cortical thickness maps developed by the Human Connectome Project, we elucidated the specific sub-regions of S1 where focal percepts were evoked. Within-participant comparisons showed that sulcal stimulation using SEEG electrodes evoked percepts that are significantly more focal, with 80% less area of spread (p=0.02) and localized to the fingertips more often than in gyral stimulation via HD-ECoG electrodes. Finally, sulcal locations exhibiting repeated modulation patterns of high-frequency neural activity during mechanical tactile stimulation of the hand showed the same somatotopic correspondence as sulcal stimulation. These findings show that minimally-invasive sulcal stimulation could lead to a clinically viable approach to restoring sensation in those living with sensory impairment.

Significance

Intracortical or cortical surface stimulation of the primary somatosensory cortex (S1) offers the promise of restoring somatotopically-relevant sensation in people with sensory impairment. However, evoking percepts in the fingertips has been challenging as their representation has been shown to be predominantly located within sulcal regions of S1 – inaccessible by these stimulation approaches. We evoked highly focal percepts in the fingertips of the hand by stimulating the sulcal regions of S1 in people with intractable epilepsy using stereoelectroencephalography (SEEG) depth electrodes. Sensory percepts in the fingertips were more focal and more frequently evoked by SEEG electrodes than by high-density electrocorticography (HD-ECoG) grids evidenced by within-participant comparisons. Our results suggest that fingertip representations are more readily targeted within the sulcal regions. SEEG electrodes potentially offer a clinically viable approach to access the sulcal regions for sensory neuroprostheses that can aid dexterous motor control.