Biomimetic stimulation patterns drive natural artificial touch percepts using intracortical microstimulation in humans

Abstract

Objective. Intracortical microstimulation (ICMS) of human somatosensory cortex evokes tactile percepts that people describe as originating from their own body, but are not always described as feeling natural. It remains unclear whether stimulation parameters such as amplitude, frequency, and spatiotemporal patterns across electrodes can be chosen to increase the naturalness of these artificial tactile percepts. Approach. In this study, we investigated whether biomimetic stimulation patterns — ICMS patterns that reproduce essential features of natural neural activity — increased the perceived naturalness of ICMS-evoked sensations compared to a non-biomimetic pattern in three people with cervical spinal cord injuries. All participants had electrode arrays implanted in their somatosensory cortices. Rather than qualitatively asking which pattern felt more natural, participants directly compared natural residual percepts, delivered by mechanical indentation on a sensate region of their hand, to artificial percepts evoked by ICMS and were asked whether linear non-biomimetic or biomimetic stimulation felt most like the mechanical indentation. Main Results. We show that simple biomimetic ICMS, which modulated the stimulation amplitude on a single electrode, was perceived as being more like a mechanical indentation reference on 32% of the electrodes. We also tested an advanced biomimetic stimulation scheme that captured more of the spatiotemporal dynamics of cortical activity using co-modulated stimulation amplitudes and frequencies across four electrodes. Here, ICMS felt more like the mechanical reference for 75% of the electrode groups. Finally, biomimetic stimulation required less stimulus charge than their non-biomimetic counterparts. Significance. We conclude that ICMS encoding schemes that mimic naturally occurring neural spatiotemporal activation patterns in somatosensory cortex feel more like an actual touch than non-biomimetic encoding schemes. This also suggests that using key elements of neuronal activity can be a useful conceptual guide to constrain the large stimulus parameter space when designing future stimulation strategies.