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Recent advancement in electrocorticography (ECoG)-based brain-computer interface technology has sparked a new interest in providing somatosensory feedback using ECoG electrodes, i.e., cortical surface electrodes. We conducted a 28-day study of cortical surface stimulation in an individual with arm paralysis due to brachial plexus injury to examine the sensation produced by electrical stimulation of the somatosensory cortex. A high-density ECoG grid was implanted over the somatosensory and motor cortices. Stimulation through cortical surface electrodes over the somatosensory cortex successfully elicited arm and hand sensations in our participant with chronic paralysis. There were three key findings. First, the intensity of perceived sensation increased monotonically with both pulse amplitude and pulse frequency. Second, changing pulse width changed the type of sensation based on qualitative description provided by the human participant. Third, the participant could distinguish between stimulation applied to two neighboring cortical surface electrodes, 4.5 mm center-to-center distance, for three out of seven electrode pairs tested. Taken together, we found that it was possible to modulate sensation intensity, sensation type, and evoke sensations across a range of locations from the fingers to the upper arm using different stimulation electrodes even in an individual with chronic impairment of somatosensory function. These three features are essential to provide effective somatosensory feedback for neuroprosthetic applications.

Restoring somatosensory feedback to people with limb amputations is crucial to improve prosthetic control. Multiple studies have demonstrated that peripheral nerve stimulation and targeted reinnervation can provide somatotopically relevant sensory feedback. While effective, the surgical procedures required for these techniques remain a major barrier to translatability. Here, we demonstrate in four people with upper-limb amputation that epidural spinal cord stimulation (SCS), a common clinical technique to treat pain, evoked somatosensory percepts that were perceived as emanating from the missing arm and hand. Over up to 29 days, stimulation evoked sensory percepts in consistent locations in the missing hand regardless of time since amputation or level of amputation. Evoked sensations were occasionally described as naturalistic (e.g. touch or pressure), but were often paresthesias. Increasing stimulus amplitude increased the perceived intensity linearly, without increasing area of the sensations. These results demonstrate the potential of SCS as a tool to restore somatosensation after amputations. Even some of the most advanced prosthetic arms lack an important feature: the ability to relay information about touch or pressure to the wearer. In fact, many people prefer to use simpler prostheses whose cables and harnesses pass on information about tension. However, recent studies suggest that electrical stimulation might give prosthesis users more sensation and better control. After an amputation, the nerves that used to deliver sensory information from the hand still exist above the injury. Stimulating these nerves can help to recreate sensations in the missing limb and improve the control of the prosthesis. Still, this stimulation requires complicated surgical interventions to implant electrodes in or around the nerves. Spinal cord stimulation – a technique where a small electrical device is inserted near the spinal cord to stimulate nerves – may be an easier alternative. This approach only requires a simple outpatient procedure, and it is routinely used to treat chronic pain conditions. Now, Chandrasekaran, Nanivadekar et al. show that spinal cord stimulation can produce the feeling of sensations in a person’s missing hand or arm. In the experiments, four people who had an arm amputation underwent spinal cord stimulation over 29 days. During the stimulation, the participants reported feeling electrical buzzing, vibration, or pressure in their missing limb. Changing the strength of the electric signals delivered to the spinal cord altered the intensity of these sensations. The experiments are a step toward developing better prosthetics that restore some sensation. Further studies are now needed to determine whether spinal cord stimulation would allow people to perform sensory tasks with a prosthetic, for example handling an object that they cannot see.

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.

The primary motor (M1) and somatosensory (S1) cortices play critical roles in motor control but the signaling between these structures is poorly understood. To fill this gap, we recorded – in three participants in an ongoing human clinical trial (NCT01894802) for people with paralyzed hands – the responses evoked in the hand and arm representations of M1 during intracortical microstimulation (ICMS) in the hand representation of S1. We found that ICMS of S1 activated some M1 neurons at short, fixed latencies consistent with monosynaptic activation. Additionally, most of the ICMS-evoked responses in M1 were more variable in time, suggesting indirect effects of stimulation. The spatial pattern of M1 activation varied systematically: S1 electrodes that elicited percepts in a finger preferentially activated M1 neurons excited during that finger’s movement. Moreover, the indirect effects of S1 ICMS on M1 were context dependent, such that the magnitude and even sign relative to baseline varied across tasks. We tested the implications of these effects for brain-control of a virtual hand, in which ICMS conveyed tactile feedback. While ICMS-evoked activation of M1 disrupted decoder performance, this disruption was minimized using biomimetic stimulation, which emphasizes contact transients at the onset and offset of grasp, and reduces sustained stimulation. Here the authors record the responses evoked in the hand and arm representations of M1 during intracortical microstimulation in the hand representation of S1, and show somatotopically organized connections with motor cortex. The resulting interference with motor decoding is task dependent but can be alleviated by using biomimetic stimulation.

Intracortical microstimulation (ICMS) is a powerful tool to investigate the functional role of neural circuits and may provide a means to restore sensation for patients for whom peripheral stimulation is not an option. In a series of psychophysical experiments with nonhuman primates, we investigate how stimulation parameters affect behavioral sensitivity to ICMS. Specifically, we deliver ICMS to primary somatosensory cortex through chronically implanted electrode arrays across a wide range of stimulation regimes. First, we investigate how the detectability of ICMS depends on stimulation parameters, including pulse width, frequency, amplitude, and pulse train duration. Then, we characterize the degree to which ICMS pulse trains that differ in amplitude lead to discriminable percepts across the range of perceptible and safe amplitudes. We also investigate how discriminability of pulse amplitude is modulated by other stimulation parameters—namely, frequency and duration. Perceptual judgments obtained across these various conditions will inform the design of stimulation regimes for neuroscience and neuroengineering applications.

Microstimulation of the somatosensory cortex can evoke tactile percepts in people with spinal cord injury, providing a means to restore touch. While location and intensity can be reliably conveyed, two issues that prevent creating more complex naturalistic sensations are a lack of methods to effectively scan the large stimulus parameter space and difficulties with assessing percept quality. Here, we address both challenges with an experimental paradigm that enables three male individuals with tetraplegia to control their stimulation parameters in a blinded fashion to create sensations for different virtual objects. Using this method, participants can reliably create object-specific sensations and report vivid object-appropriate characteristics. Moreover, both linear classifiers and participants can match stimulus profiles with their respective objects significantly above chance without any visual cues. Confusion between two sensations increases as the associated objects share more tactile characteristics. We conclude that while visual information contributes to the experience of the artificially evoked sensations, microstimulation in the somatosensory cortex itself can evoke intuitive percepts with a variety of tactile properties. This self-guided stimulation approach may be used to effectively characterize percepts from future stimulation paradigms. In this study, three individuals with tetraplegia designed vivid, reliable and object-appropriate sensations with a variety of tactile characteristics using self-selected stimulus parameters that stimulated their somatosensory cortex upon digital object contact

Brain-computer interfaces are being developed to restore movement for people living with paralysis due to injury or disease. Although the therapeutic potential is great, long-term stability of the interface is critical for widespread clinical implementation. While many factors can affect recording and stimulation performance including electrode material stability and host tissue reaction, these factors have not been investigated in human implants. In this clinical study, we sought to characterize the material integrity and biological tissue encapsulation via explant analysis in an effort to identify factors that influence electrophysiological performance. We examined a total of six Utah arrays explanted from two human participants involved in intracortical BCI studies. Two platinum (Pt) arrays were implanted for 980 days in one participant (P1) and two Pt and two iridium oxide (IrOx) arrays were implanted for 182 days in the second participant (P2). We observed that the recording quality followed a similar trend in all six arrays with an initial increase in peak-to-peak voltage during the first 30–40 days and gradual decline thereafter in P1. Using optical and two-photon microscopy we observed a higher degree of tissue encapsulation on both arrays implanted for longer durations in participant P1. We then used scanning electron microscopy and energy dispersive X-ray spectroscopy to assess material degradation. All measures of material degradation for the Pt arrays were found to be more prominent in the participant with a longer implantation time. Two IrOx arrays were subjected to brief survey stimulations, and one of these arrays showed loss of iridium from most of the stimulated sites. Recording performance appeared to be unaffected by this loss of iridium, suggesting that the adhesion of IrOx coating may have been compromised by the stimulation, but the metal layer did not detach until or after array removal. In summary, both tissue encapsulation and material degradation were more pronounced in the arrays that were implanted for a longer duration. Additionally, these arrays also had lower signal amplitude and impedance. New biomaterial strategies that minimize fibrotic encapsulation and enhance material stability should be developed to achieve high quality recording and stimulation for longer implantation periods.

Modern myoelectric prosthetic hands have multiple independently controllable degrees of freedom, but require constant visual attention to use effectively. Somatosensory feedback provides information not available through vision alone and is essential for fine motor control of our limbs. Similarly, stimulation of the nervous system can potentially provide artificial somatosensory feedback to reduce the reliance on visual cues to efficiently operate prosthetic devices. We have shown previously that epidural stimulation of the lateral cervical spinal cord can evoke tactile sensations perceived as emanating from the missing arm and hand in people with upper-limb amputation. In this case study, two subjects with upper-limb amputation used this somatotopically-matched tactile feedback to discriminate object size and compliance while controlling a prosthetic hand. With less than 30 min of practice each day, both subjects were able to use artificial somatosensory feedback to perform a subset of the discrimination tasks at a success level well above chance. Subject 1 was consistently more adept at determining object size (74% accuracy; chance: 33%) while Subject 2 achieved a higher accuracy level in determining object compliance (60% accuracy; chance 33%). In each subject, discrimination of the other object property was only slightly above or at chance level suggesting that the task design and stimulation encoding scheme are important determinants of which object property could be reliably identified. Our observations suggest that changes in the intensity of artificial somatosensory feedback provided via spinal cord stimulation can be readily used to infer information about object properties with minimal training.

Computational models of the musculoskeletal system are scientific tools used to study human movement, quantify the effects of injury and disease, plan surgical interventions, or control realistic high-dimensional articulated prosthetic limbs. If the models are sufficiently accurate, they may embed complex relationships within the sensorimotor system. These potential benefits are limited by the challenge of implementing fast and accurate musculoskeletal computations. A typical hand muscle spans over 3 degrees of freedom (DOF), wrapping over complex geometrical constraints that change its moment arms and lead to complex posture-dependent variation in torque generation. Here, we report a method to accurately and efficiently calculate musculotendon length and moment arms across all physiological postures of the forearm muscles that actuate the hand and wrist. Then, we use this model to test the hypothesis that the functional similarities of muscle actions are embedded in muscle structure. The posture dependent muscle geometry, moment arms and lengths of modeled muscles were captured using autogenerating polynomials that expanded their optimal selection of terms using information measurements. The iterative process approximated 33 musculotendon actuators, each spanning up to 6 DOFs in an 18 DOF model of the human arm and hand, defined over the full physiological range of motion. Using these polynomials, the entire forearm anatomy could be computed in <10 μs, which is far better than what is required for real-time performance, and with low errors in moment arms (below 5%) and lengths (below 0.4%). Moreover, we demonstrate that the number of elements in these autogenerating polynomials does not increase exponentially with increasing muscle complexity; complexity increases linearly instead. Dimensionality reduction using the polynomial terms alone resulted in clusters comprised of muscles with similar functions, indicating the high accuracy of approximating models. We propose that this novel method of describing musculoskeletal biomechanics might further improve the applications of detailed and scalable models to describe human movement.

Wrist posture impacts the muscle lengths and moment arms of the extrinsic finger muscles that cross the wrist. As a result, the electromyographic (EMG) activity associated with digit movement at different wrist postures must also change. We sought to quantify the posture-dependence of extrinsic finger muscle activity using bipolar fine-wire electrodes inserted into the extrinsic finger muscles of able-bodied subjects during unrestricted wrist and finger movements across the entire range of motion. EMG activity of all the recorded finger muscles were significantly different (p < 0.05, ANOVA) when performing the same digit movement in five different wrist postures. Depending on the wrist posture, EMG activity changed by up to 70% in individual finger muscles for the same movement, with the highest levels of activity observed in finger extensors when the wrist was extended. Similarly, finger flexors were most active when the wrist was flexed. For the finger flexors, EMG variations with wrist posture were most prominent for index finger muscles, while the EMG activity of all finger extensor muscles were modulated in a similar way across all digits. In addition to comprehensively quantifying the effect of wrist posture on extrinsic finger EMG activity in able-bodied subjects, these results may contribute to designing control algorithms for myoelectric prosthetic hands in the future.