Effects of stimulus pulse rate on somatosensory adaptation in the human cortex.

BACKGROUND: Intracortical microstimulation (ICMS) of the somatosensory cortex can restore sensation to people with neurological diseases. However, many aspects of ICMS are poorly understood, including the effect of stimulation on percept intensity over time. OBJECTIVE: Here, we evaluate how tactile percepts evoked by ICMS in the somatosensory cortex of a human participant adapt over time. METHODS: We delivered continuous and intermittent ICMS to the somatosensory cortex and assessed the reported intensity of tactile percepts over time in a human participant. Experiments were conducted over approximately one year and linear mixed effects models were used to assess significance. RESULTS: Continuous stimulation at high frequencies led to rapid decreases in intensity, while low frequency stimulation maintained percept intensity for longer periods. Burst-modulated stimulation extended the time before the intensity began to decrease, but all protocols ultimately resulted in complete sensation loss within 1 min. Intermittent stimulation paradigms with several seconds between stimulus trains evoked intermittent percepts and also led to decreases in intensity on many electrodes, but never resulted in extinction of the sensation after over 3 min of stimulation. Longer breaks between each pulse train resulted in some recovery in the intensity of the stimulus-evoked percepts. For several electrodes, intermittent stimulation had almost no effect on the perceived intensity. CONCLUSIONS: Intermittent ICMS paradigms were more effective at maintaining percepts. Given that transient neural activity dominates the response in somatosensory cortex during mechanical contact onsets and offsets, providing brief stimulation trains at these times may more closely represent natural cortical activity and have the additional benefit of prolonging the ability to evoke sensations over longer time periods.

Neural stimulation and recording performance in human sensorimotor cortex over 1500 days.

Objective.Intracortical microstimulation (ICMS) in somatosensory cortex can restore sensation to people with spinal cord injury. However, the recording quality from implanted microelectrodes can degrade over time and limitations in stimulation longevity have been considered a potential barrier to the clinical use of ICMS. Our objective was to evaluate recording stability of intracortical electrodes implanted in the motor and somatosensory cortex of one person. The electrodes in motor cortex had platinum tips and were not stimulated, while the electrodes in somatosensory cortex had sputtered iridium oxide film (SIROF) tips and were stimulated. Additionally, we measured how well ICMS was able to evoke sensations over time.Approach. We implanted microelectrode arrays with SIROF tips in the somatosensory cortex (SIROF-sensory) of a human participant with a cervical spinal cord injury. We regularly stimulated these electrodes to evoke tactile sensations on the hand. Here, we quantify the stability of these electrodes in comparison to non-stimulated platinum electrodes implanted in the motor cortex (platinum-motor) over 1500 days with recorded signal quality and electrode impedances. Additionally, we quantify the stability of ICMS-evoked sensations using detection thresholds.Main results. We found that recording quality, as assessed by the number of electrodes with high-amplitude waveforms (>100µV peak-to-peak), peak-to-peak voltage, noise, and signal-to-noise ratio, decreased over time on SIROF-sensory and platinum-motor electrodes. However, SIROF-sensory electrodes were more likely to continue to record high-amplitude signals than platinum-motor electrodes. Interestingly, the detection thresholds for stimulus-evoked sensations decreased over time from a median of 31.5µA at day 100-10.4µA at day 1500, with the largest changes occurring between day 100 and 500.Significance. These results demonstrate that ICMS in human somatosensory cortex can be provided over long periods of time without deleterious effects on recording or stimulation capabilities. In fact, the sensitivity to stimulation improved over time.

Perception of microstimulation frequency in human somatosensory cortex.

Microstimulation in the somatosensory cortex can evoke artificial tactile percepts and can be incorporated into bidirectional brain-computer interfaces (BCIs) to restore function after injury or disease. However, little is known about how stimulation parameters themselves affect perception. Here, we stimulated through microelectrode arrays implanted in the somatosensory cortex of two human participants with cervical spinal cord injury and varied the stimulus amplitude, frequency, and train duration. Increasing the amplitude and train duration increased the perceived intensity on all tested electrodes. Surprisingly, we found that increasing the frequency evoked more intense percepts on some electrodes but evoked less-intense percepts on other electrodes. These different frequency-intensity relationships were divided into three groups, which also evoked distinct percept qualities at different stimulus frequencies. Neighboring electrode sites were more likely to belong to the same group. These results support the idea that stimulation frequency directly controls tactile perception and that these different percepts may be related to the organization of somatosensory cortex, which will facilitate principled development of stimulation strategies for bidirectional BCIs.

A brain-computer interface that evokes tactile sensations improves robotic arm control.

Prosthetic arms controlled by a brain-computer interface can enable people with tetraplegia to perform functional movements. However, vision provides limited feedback because information about grasping objects is best relayed through tactile feedback. We supplemented vision with tactile percepts evoked using a bidirectional brain-computer interface that records neural activity from the motor cortex and generates tactile sensations through intracortical microstimulation of the somatosensory cortex. This enabled a person with tetraplegia to substantially improve performance with a robotic limb; trial times on a clinical upper-limb assessment were reduced by half, from a median time of 20.9 to 10.2 seconds. Faster times were primarily due to less time spent attempting to grasp objects, revealing that mimicking known biological control principles results in task performance that is closer to able-bodied human abilities.