Ali H. Alamri

Intracortical microstimulation (ICMS) of somatosensory cortex can restore a sense of touch to people with spinal cord injury. In this early feasibility clinical trial (NCT01894802), we evaluated the safety, efficacy, and longevity of ICMS because there is a paucity of such long-term studies in humans. This information is crucial to the development of clinical neuromodulation devices, particularly for restoring touch, hearing, and vision. ICMS was delivered to five participants with spinal cord injury who were each implanted with two Blackrock NeuroPort microelectrode arrays in the hand representation of Brodmann's area 1. Across implant durations spanning 2 to 10 years, we measured single-electrode detection thresholds, projected fields, quality reports, and electrode health characteristics. ICMS-related adverse events were documented throughout. More than 168 million ICMS pulses were delivered across a combined implant duration of 27 years without any serious adverse events or direct negative effects on electrode health. ICMS consistently evoked sensations localized to the hand. Rarely, sensations persisted for brief periods after stimulation offset (3 to 25 events across participants). ICMS detection thresholds increased slowly over time (about 3.5 microamperes per year), but 64 ± 13% of the electrodes still reliably evoked tactile sensations (about 21% decrease in functional electrodes), including 60% of the electrodes after 10 years in one participant. The quality and projected field coverage of ICMS-evoked sensations were both consistent. Delivering ICMS to the somatosensory cortex was safe and effective, consistently evoking informative somatosensory percepts as long as 10 years, demonstrating the clinical promise of ICMS for sensory restoration.

The sense of touch is fundamental for dexterous manipulation, object interaction, and body awareness. It is primarily processed in the somatosensory cortex (SC), yet our understanding of how tactile information is encoded at the level of neural populations and single neurons in humans remains limited. It is unclear how natural tactile signals are represented in SC and how they may be influenced by visual inputs, as well as how closely sensory and motor cortices interact during passive touch. Here, we investigated the neural basis of touch in the human SC using chronically implanted microelectrode arrays in three participants. By delivering controlled mechanical stimuli, we characterized neural responses to natural touch and mapped detailed somatotopic receptive fields (the patch of skin that elicits neural responses when stimulated) in humans, including multi-digit representations. Surprisingly, we also found strong, clearly somatotopic activation in the motor cortex (MC) during passive touch, even in the absence of movement, highlighting a tight and functionally relevant sensorimotor coupling. We further examined how vision shapes tactile processing by comparing neural activity during actual touch with and without vision, and during observation of touch on another person's hand. While touch to the participants' hands elicited robust, event-locked, and somatotopically organized responses in the SC, observation of tactile actions alone did not produce significant activation, suggesting limited vicarious encoding at this level. These findings provide a detailed characterization of human touch processing at the level of neuronal populations and give insights for the design of microstimulation strategies of the SC for the restoration of touch.

Somatosensory feedback and attention are critical for the execution of dexterous behaviors. Indeed, tactile and proprioceptive signals are sent to motor cortex such that they can be integrated into the motor plan while the expectation of feedback can shape motor responses. One downside to many of the studies that have found these interactions is that motor cortex has always been studied within the framework of a motor task, potentially squashing many of the smaller signals present and making others hard to disentangle. In this study we specifically investigate the presence of sensory expectations in human motor cortex in the absence of a motor task using two participants implanted with electrode arrays in both sensory and motor cortices, allowing us to identify signals corresponding to sensory expectation with fewer confounds. We found that the deployment of attention to individual fingers results in digit-specific activation of motor cortex while sensory cortex remains unperturbed. Moreover, we observed that, compared to an imagined movement task, the expectation signal in motor cortex existed in a distinct subspace that does not represent pure motor intent. Finally, we found that the expectation signals existed along a somatotopic axis that matched the somatotopic axis revealed by movement intent. This work highlights the fact that many signals are multiplexed in motor cortex.

Background: Intracortical microstimulation (ICMS) of somatosensory cortex can restore a sense of touch to people with spinal cord injury (SCI). In this early-feasibility clinical trial, we evaluate the safety, efficacy, and longevity of ICMS as there is a paucity of such long-term studies in humans. This information is crucial to the development of clinical neuromodulation devices, particularly for restoring touch, hearing, and vision. Methods: ICMS was delivered to five participants with SCI who were each implanted with two Blackrock NeuroPort microelectrode arrays in the hand representation of Brodmann’s Area 1. Across implant durations spanning two to ten years, we measured single-electrode detection thresholds, projected fields, quality reports, and electrode health characteristics. ICMS-related adverse events were documented throughout. Results: Over 168 million ICMS pulses were delivered across a combined implant duration of 24 years without any serious adverse events or direct negative effects on electrode health. ICMS consistently evoked sensations localized to the hand. Rarely, sensations persisted for brief periods after stimulation offset (3–25 events across participants). ICMS detection thresholds increased slowly over time (∼3.5 μA/year), but 62±15% of the electrodes still reliably evoke tactile sensations (∼25% decrease in functional electrodes), including 55% of the electrodes after 10 years in one participant. The quality and projected field coverage of ICMS-evoked sensations were both consistent. Conclusions: Delivering ICMS to somatosensory cortex was safe and reliable, consistently evoking informative somatosensory percepts as long as 10 years, demonstrating the clinical promise of ICMS for sensory restoration. (Funded by NIH; ClinicalTrials.gov: NCT01894802 ).

Intracortical microstimulation (ICMS) of somatosensory cortex evokes tactile sensations whose properties can be systematically manipulated by varying stimulation parameters. However, ICMS currently provides an imperfect sense of touch, limiting manual dexterity and tactile experience. Leveraging our understanding of how tactile features are encoded in the primary somatosensory cortex (S1), we sought to inform individuals with paralysis about local geometry and apparent motion of objects on their skin. We simultaneously delivered ICMS through electrodes with spatially patterned projected fields (PFs), evoking sensations of edges. We then created complex PFs that encode arbitrary tactile shapes and skin indentation patterns. By delivering spatiotemporally patterned ICMS, we evoked sensation of motion across the skin, the speed and direction of which could be controlled. Thus, we improved individuals’ tactile experience and use of brain-controlled bionic hands.