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Creating a neuroprosthesis for active tactile exploration of textures

Significance Sensory neuroprostheses offer the promise of restoring perceptual function to people with impaired sensation. Here, we developed a paradigm using intracortical microstimulation (ICMS) for encoding the sensation of fingertip motion against texture. Monkeys learned to interpret time-varying ICMS patterns, evoked by the interplay of their voluntary movements and specific object textures, and discriminated texture coarseness relying solely on these pulse trains. As such, variations in exploration strategy directly affected the timing of individual stimulation pulses. Crucially, this encoding enabled real-time active exploration of textures. We propose that this approach could equip upper-limb neuroprostheses with functional access to texture features acquired during active exploration of natural objects. Intracortical microstimulation (ICMS) of the primary somatosensory cortex (S1) can produce percepts that mimic somatic sensation and, thus, has potential as an approach to sensorize prosthetic limbs. However, it is not known whether ICMS could recreate active texture exploration—the ability to infer information about object texture by using one’s fingertips to scan a surface. Here, we show that ICMS of S1 can convey information about the spatial frequencies of invisible virtual gratings through a process of active tactile exploration. Two rhesus monkeys scanned pairs of visually identical screen objects with the fingertip of a hand avatar—controlled first via a joystick and later via a brain–machine interface—to find the object with denser virtual gratings. The gratings consisted of evenly spaced ridges that were signaled through individual ICMS pulses generated whenever the avatar’s fingertip crossed a ridge. The monkeys learned to interpret these ICMS patterns, evoked by the interplay of their voluntary movements and the virtual textures of each object, to perform a sensory discrimination task. Discrimination accuracy followed Weber’s law of just-noticeable differences (JND) across a range of grating densities; a finding that matches normal cutaneous sensation. Moreover, 1 monkey developed an active scanning strategy where avatar velocity was integrated with the ICMS pulses to interpret the texture information. We propose that this approach could equip upper-limb neuroprostheses with direct access to texture features acquired during active exploration of natural objects.