Restoring the Sense of Touch Using a Sensorimotor Demultiplexing Neural Interface.

Paralyzed muscles can be reanimated following spinal cord injury (SCI) using a brain-computer interface (BCI) to enhance motor function alone. Importantly, the sense of touch is a key component of motor function. Here, we demonstrate that a human participant with a clinically complete SCI can use a BCI to simultaneously reanimate both motor function and the sense of touch, leveraging residual touch signaling from his own hand. In the primary motor cortex (M1), residual subperceptual hand touch signals are simultaneously demultiplexed from ongoing efferent motor intention, enabling intracortically controlled closed-loop sensory feedback. Using the closed-loop demultiplexing BCI almost fully restored the ability to detect object touch and significantly improved several sensorimotor functions. Afferent grip-intensity levels are also decoded from M1, enabling grip reanimation regulated by touch signaling. These results demonstrate that subperceptual neural signals can be decoded from the cortex and transformed into conscious perception, significantly augmenting function.

Sensing and decoding the neural drive to paralyzed muscles during attempted movements of a person with tetraplegia using a sleeve array.

Motor neurons convey information about motor intent that can be extracted and interpreted to control assistive devices. However, most methods for measuring the firing activity of single neurons rely on implanted microelectrodes. Although intracortical brain-computer interfaces (BCIs) have been shown to be safe and effective, the requirement for surgery poses a barrier to widespread use that can be mitigated by instead using noninvasive interfaces. The objective of this study was to evaluate the feasibility of deriving motor control signals from a wearable sensor that can detect residual motor unit activity in paralyzed muscles after chronic cervical spinal cord injury (SCI). Despite generating no observable hand movement, volitional recruitment of motor units below the level of injury was observed across attempted movements of individual fingers and overt wrist and elbow movements. Subgroups of motor units were coactive during flexion or extension phases of the task. Single digit movement intentions were classified offline from the electromyogram (EMG) power [root-mean-square (RMS)] or motor unit firing rates with median classification accuracies >75% in both cases. Simulated online control of a virtual hand was performed with a binary classifier to test feasibility of real-time extraction and decoding of motor units. The online decomposition algorithm extracted motor units in 1.2 ms, and the firing rates predicted the correct digit motion 88 ± 24% of the time. This study provides the first demonstration of a wearable interface for recording and decoding firing rates of motor units below the level of injury in a person with motor complete SCI.NEW & NOTEWORTHY A wearable electrode array and machine learning methods were used to record and decode myoelectric signals and motor unit firing in paralyzed muscles of a person with motor complete tetraplegia. The myoelectric activity and motor unit firing rates were task specific, even in the absence of visible motion, enabling accurate classification of attempted single-digit movements. This wearable system has the potential to enable people with tetraplegia to control assistive devices through movement intent.

Increasing Robustness of Brain-Computer Interfaces Through Automatic Detection and Removal of Corrupted Input Signals.

For brain-computer interfaces (BCIs) to be viable for long-term daily usage, they must be able to quickly identify and adapt to signal disruptions. Furthermore, the detection and mitigation steps need to occur automatically and without the need for user intervention while also being computationally tractable for the low-power hardware that will be used in a deployed BCI system. Here, we focus on disruptions that are likely to occur during chronic use that cause some recording channels to fail but leave the remaining channels unaffected. In these cases, the algorithm that translates recorded neural activity into actions, the neural decoder, should seamlessly identify and adjust to the altered neural signals with minimal inconvenience to the user. First, we introduce an adapted statistical process control (SPC) method that automatically identifies disrupted channels so that both decoding algorithms can be adjusted, and technicians can be alerted. Next, after identifying corrupted channels, we demonstrate the automated and rapid removal of channels from a neural network decoder using a masking approach that does not change the decoding architecture, making it amenable for transfer learning. Finally, using transfer and unsupervised learning techniques, we update the model weights to adjust for the corrupted channels without requiring the user to collect additional calibration data. We demonstrate with both real and simulated neural data that our approach can maintain high-performance while simultaneously minimizing computation time and data storage requirements. This framework is invisible to the user but can dramatically increase BCI robustness and usability.

Long-term intracortical microelectrode array performance in a human: a 5 year retrospective analysis.

Objective. Brain-computer interfaces (BCIs) that record neural activity using intracortical microelectrode arrays (MEAs) have shown promise for mitigating disability associated with neurological injuries and disorders. While the chronic performance and failure modes of MEAs have been well studied and systematically described in non-human primates, there is far less reported about long-term MEA performance in humans. Our group has collected one of the largest neural recording datasets from a Utah MEA in a human subject, spanning over 5 years (2014-2019). Here we present both long-term signal quality and BCI performance as well as highlight several acute signal disruption events observed during the clinical study.Approach. Long-term Utah array performance was evaluated by analyzing neural signal metric trends and decoding accuracy for tasks regularly performed across 448 clinical recording sessions. For acute signal disruptions, we identify or hypothesize the root cause of the disruption, show how the disruption manifests in the collected data, and discuss potential identification and mitigation strategies for the disruption.Main results. Neural signal quality metrics deteriorated rapidly within the first year, followed by a slower decline through the remainder of the study. Nevertheless, BCI performance remained high 5 years after implantation, which is encouraging for the translational potential of this technology as an assistive device. We also present examples of unanticipated signal disruptions during chronic MEA use, which are critical to detect as BCI technology progresses toward home usage.Significance. Our work fills a gap in knowledge around long-term MEA performance in humans, providing longevity and efficacy data points to help characterize the performance of implantable neural sensors in a human population. The trial was registered on ClinicalTrials.gov (Identifier NCT01997125) and conformed to institutional requirements for the conduct of human subjects research.

Classifying Intracortical Brain-Machine Interface Signal Disruptions Based on System Performance and Applicable Compensatory Strategies: A Review.

Brain-machine interfaces (BMIs) record and translate neural activity into a control signal for assistive or other devices. Intracortical microelectrode arrays (MEAs) enable high degree-of-freedom BMI control for complex tasks by providing fine-resolution neural recording. However, chronically implanted MEAs are subject to a dynamic in vivo environment where transient or systematic disruptions can interfere with neural recording and degrade BMI performance. Typically, neural implant failure modes have been categorized as biological, material, or mechanical. While this categorization provides insight into a disruption's causal etiology, it is less helpful for understanding degree of impact on BMI function or possible strategies for compensation. Therefore, we propose a complementary classification framework for intracortical recording disruptions that is based on duration of impact on BMI performance and requirement for and responsiveness to interventions: (1) Transient disruptions interfere with recordings on the time scale of minutes to hours and can resolve spontaneously; (2) Reversible disruptions cause persistent interference in recordings but the root cause can be remedied by an appropriate intervention; (3) Irreversible compensable disruptions cause persistent or progressive decline in signal quality, but their effects on BMI performance can be mitigated algorithmically; and (4) Irreversible non-compensable disruptions cause permanent signal loss that is not amenable to remediation or compensation. This conceptualization of intracortical BMI disruption types is useful for highlighting specific areas for potential hardware improvements and also identifying opportunities for algorithmic interventions. We review recording disruptions that have been reported for MEAs and demonstrate how biological, material, and mechanical mechanisms of disruption can be further categorized according to their impact on signal characteristics. Then we discuss potential compensatory protocols for each of the proposed disruption classes. Specifically, transient disruptions may be minimized by using robust neural decoder features, data augmentation methods, adaptive machine learning models, and specialized signal referencing techniques. Statistical Process Control methods can identify reparable disruptions for rapid intervention. In-vivo diagnostics such as impedance spectroscopy can inform neural feature selection and decoding models to compensate for irreversible disruptions. Additional compensatory strategies for irreversible disruptions include information salvage techniques, data augmentation during decoder training, and adaptive decoding methods to down-weight damaged channels.

Dexterous Control of Seven Functional Hand Movements Using Cortically-Controlled Transcutaneous Muscle Stimulation in a Person With Tetraplegia.

Individuals with tetraplegia identify restoration of hand function as a critical, unmet need to regain their independence and improve quality of life. Brain-Computer Interface (BCI)-controlled Functional Electrical Stimulation (FES) technology addresses this need by reconnecting the brain with paralyzed limbs to restore function. In this study, we quantified performance of an intuitive, cortically-controlled, transcutaneous FES system on standardized object manipulation tasks from the Grasp and Release Test (GRT). We found that a tetraplegic individual could use the system to control up to seven functional hand movements, each with >95% individual accuracy. He was able to select one movement from the possible seven movements available to him and use it to appropriately manipulate all GRT objects in real-time using naturalistic grasps. With the use of the system, the participant not only improved his GRT performance over his baseline, demonstrating an increase in number of transfers for all objects except the Block, but also significantly improved transfer times for the heaviest objects (videocassette (VHS), Can). Analysis of underlying motor cortex neural representations associated with the hand grasp states revealed an overlap or non-separability in neural activation patterns for similarly shaped objects that affected BCI-FES performance. These results suggest that motor cortex neural representations for functional grips are likely more related to hand shape and force required to hold objects, rather than to the objects themselves. These results, demonstrating multiple, naturalistic functional hand movements with the BCI-FES, constitute a further step toward translating BCI-FES technologies from research devices to clinical neuroprosthetics.