RESUMEN
Millions of people worldwide suffer from diseases that lead to paralysis through disruption of signal pathways between the brain and the muscles. Neuroprosthetic devices are designed to restore lost function and could be used to form an electronic 'neural bypass' to circumvent disconnected pathways in the nervous system. It has previously been shown that intracortically recorded signals can be decoded to extract information related to motion, allowing non-human primates and paralysed humans to control computers and robotic arms through imagined movements. In non-human primates, these types of signal have also been used to drive activation of chemically paralysed arm muscles. Here we show that intracortically recorded signals can be linked in real-time to muscle activation to restore movement in a paralysed human. We used a chronically implanted intracortical microelectrode array to record multiunit activity from the motor cortex in a study participant with quadriplegia from cervical spinal cord injury. We applied machine-learning algorithms to decode the neuronal activity and control activation of the participant's forearm muscles through a custom-built high-resolution neuromuscular electrical stimulation system. The system provided isolated finger movements and the participant achieved continuous cortical control of six different wrist and hand motions. Furthermore, he was able to use the system to complete functional tasks relevant to daily living. Clinical assessment showed that, when using the system, his motor impairment improved from the fifth to the sixth cervical (C5-C6) to the seventh cervical to first thoracic (C7-T1) level unilaterally, conferring on him the critical abilities to grasp, manipulate, and release objects. This is the first demonstration to our knowledge of successful control of muscle activation using intracortically recorded signals in a paralysed human. These results have significant implications in advancing neuroprosthetic technology for people worldwide living with the effects of paralysis.
Asunto(s)
Corteza Motora/fisiología , Movimiento/fisiología , Cuadriplejía/fisiopatología , Actividades Cotidianas , Algoritmos , Médula Cervical/lesiones , Médula Cervical/fisiología , Médula Cervical/fisiopatología , Estimulación Eléctrica , Electrodos Implantados , Antebrazo/fisiología , Mano/fisiología , Fuerza de la Mano/fisiología , Humanos , Imaginación , Aprendizaje Automático , Imagen por Resonancia Magnética , Masculino , Microelectrodos , Músculo Esquelético/fisiología , Cuadriplejía/etiología , Traumatismos de la Médula Espinal/complicaciones , Traumatismos de la Médula Espinal/fisiopatología , Adulto JovenRESUMEN
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.
Asunto(s)
Mano/fisiopatología , Músculo Esquelético/fisiopatología , Rehabilitación Neurológica/instrumentación , Cuadriplejía , Reclutamiento Neurofisiológico/fisiología , Traumatismos de la Médula Espinal , Dispositivos Electrónicos Vestibles , Adulto , Electromiografía , Estudios de Factibilidad , Humanos , Aprendizaje Automático , Masculino , Rehabilitación Neurológica/métodos , Cuadriplejía/etiología , Cuadriplejía/fisiopatología , Cuadriplejía/rehabilitación , Traumatismos de la Médula Espinal/complicaciones , Traumatismos de la Médula Espinal/fisiopatología , Traumatismos de la Médula Espinal/rehabilitaciónRESUMEN
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.
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Interfaces Cerebro-Computador , Animales , Humanos , Microelectrodos , Primates , Estudios RetrospectivosRESUMEN
OBJECTIVE: Paralysis resulting from spinal cord injury (SCI) can have a devastating effect on multiple arm and hand motor functions. Rotary hand movements, such as supination and pronation, are commonly impaired by upper extremity paralysis, and are essential for many activities of daily living. In this proof-of-concept study, we utilize a neural bypass system (NBS) to decode motor intention from motor cortex to control combinatorial rotary hand movements elicited through stimulation of the arm muscles, effectively bypassing the SCI of the study participant. We describe the NBS system architecture and design that enabled this functionality. METHODS: The NBS consists of three main functional components: 1) implanted intracortical microelectrode array, 2) neural data processing using a computer, and, 3) a noninvasive neuromuscular electrical stimulation (NMES) system. RESULTS: We address previous limitations of the NBS, and confirm the enhanced capability of the NBS to enable, in real-time, combinatorial hand rotary motor functions during a functionally relevant object manipulation task. CONCLUSION: This enhanced capability was enabled by accurate decoding of multiple movement intentions from the participant's motor cortex, interleaving NMES patterns to combine hand movements, and dynamically switching between NMES patterns to adjust for hand position changes during movement. SIGNIFICANCE: These results have implications for enabling complex rotary hand functions in sequence with other functionally relevant movements for patients suffering from SCI, stroke, and other sensorimotor dysfunctions.
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Terapia por Estimulación Eléctrica , Mano/fisiología , Corteza Motora/fisiología , Prótesis Neurales , Cuadriplejía/rehabilitación , Adulto , Terapia por Estimulación Eléctrica/instrumentación , Terapia por Estimulación Eléctrica/métodos , Diseño de Equipo , Humanos , Masculino , Movimiento/fisiología , Procesamiento de Señales Asistido por Computador/instrumentaciónRESUMEN
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.
RESUMEN
BACKGROUND: Understanding the long-term behavior of intracortically-recorded signals is essential for improving the performance of Brain Computer Interfaces. However, few studies have systematically investigated chronic neural recordings from an implanted microelectrode array in the human brain. METHODS: In this study, we show the applicability of wavelet decomposition method to extract and demonstrate the utility of long-term stable features in neural signals obtained from a microelectrode array implanted in the motor cortex of a human with tetraplegia. Wavelet decomposition was applied to the raw voltage data to generate mean wavelet power (MWP) features, which were further divided into three sub-frequency bands, low-frequency MWP (lf-MWP, 0-234 Hz), mid-frequency MWP (mf-MWP, 234 Hz-3.75 kHz) and high-frequency MWP (hf-MWP, >3.75 kHz). We analyzed these features using data collected from two experiments that were repeated over the course of about 3 years and compared their signal stability and decoding performance with the more standard threshold crossings, local field potentials (LFP), multi-unit activity (MUA) features obtained from the raw voltage recordings. RESULTS: All neural features could stably track neural information for over 3 years post-implantation and were less prone to signal degradation compared to threshold crossings. Furthermore, when used as an input to support vector machine based decoding algorithms, the mf-MWP and MUA demonstrated significantly better performance, respectively, in classifying imagined motor tasks than using the lf-MWP, hf-MWP, LFP, or threshold crossings. CONCLUSIONS: Our results suggest that using MWP features in the appropriate frequency bands can provide an effective neural feature for brain computer interface intended for chronic applications. TRIAL REGISTRATION: This study was approved by the U.S. Food and Drug Administration (Investigational Device Exemption) and the Ohio State University Medical Center Institutional Review Board (Columbus, Ohio). The study conformed to institutional requirements for the conduct of human subjects and was filed on ClinicalTrials.gov (Identifier NCT01997125).
RESUMEN
Neuroprosthetics that combine a brain computer interface (BCI) with functional electrical stimulation (FES) can restore voluntary control of a patients' own paralyzed limbs. To date, human studies have demonstrated an "all-or-none" type of control for a fixed number of pre-determined states, like hand-open and hand-closed. To be practical for everyday use, a BCI-FES system should enable smooth control of limb movements through a continuum of states and generate situationally appropriate, graded muscle contractions. Crucially, this functionality will allow users of BCI-FES neuroprosthetics to manipulate objects of different sizes and weights without dropping or crushing them. In this study, we present the first evidence that using a BCI-FES system, a human with tetraplegia can regain volitional, graded control of muscle contraction in his paralyzed limb. In addition, we show the critical ability of the system to generalize beyond training states and accurately generate wrist flexion states that are intermediate to training levels. These innovations provide the groundwork for enabling enhanced and more natural fine motor control of paralyzed limbs by BCI-FES neuroprosthetics.
Asunto(s)
Brazo/fisiología , Interfaces Cerebro-Computador , Contracción Muscular , Prótesis e Implantes , Cuadriplejía/terapia , Adulto , Estimulación Eléctrica , Humanos , Masculino , Movimiento , VoliciónRESUMEN
Recent advances in Brain Computer Interfaces (BCIs) have created hope that one day paralyzed patients will be able to regain control of their paralyzed limbs. As part of an ongoing clinical study, we have implanted a 96-electrode Utah array in the motor cortex of a paralyzed human. The array generates almost 3 million data points from the brain every second. This presents several big data challenges towards developing algorithms that should not only process the data in real-time (for the BCI to be responsive) but are also robust to temporal variations and non-stationarities in the sensor data. We demonstrate an algorithmic approach to analyze such data and present a novel method to evaluate such algorithms. We present our methodology with examples of decoding human brain data in real-time to inform a BCI.