Stephen T. Foldes

Intracortical microstimulation of human somatosensory cortex

Tactile percepts were consistently elicited in the hand of a person with cervical spinal cord injury using intracortical microstimulation of the somatosensory cortex. A sense of touch Touch is essential for hand use. Yet, brain-controlled prosthetic limbs have not been endowed with this critical sense. In a new study by Flesher et al., microelectrode arrays were implanted into the primary somatosensory cortex of a person with spinal cord injury and, by delivering current through the electrodes, generated sensations of touch that were perceived as coming from his own paralyzed hand. These sensations often felt like pressure, could be graded in intensity, and were stable for months. The authors suggest that this approach could be used to convey information about contact location and pressure necessary for prosthetic hands to interact with objects. Intracortical microstimulation of the somatosensory cortex offers the potential for creating a sensory neuroprosthesis to restore tactile sensation. Whereas animal studies have suggested that both cutaneous and proprioceptive percepts can be evoked using this approach, the perceptual quality of the stimuli cannot be measured in these experiments. We show that microstimulation within the hand area of the somatosensory cortex of a person with long-term spinal cord injury evokes tactile sensations perceived as originating from locations on the hand and that cortical stimulation sites are organized according to expected somatotopic principles. Many of these percepts exhibit naturalistic characteristics (including feelings of pressure), can be evoked at low stimulation amplitudes, and remain stable for months. Further, modulating the stimulus amplitude grades the perceptual intensity of the stimuli, suggesting that intracortical microstimulation could be used to convey information about the contact location and pressure necessary to perform dexterous hand movements associated with object manipulation.

Neuroprosthetic technology for individuals with spinal cord injury

Abstract Context Spinal cord injury (SCI) results in a loss of function and sensation below the level of the lesion. Neuroprosthetic technology has been developed to help restore motor and autonomic functions as well as to provide sensory feedback. Findings This paper provides an overview of neuroprosthetic technology that aims to address the priorities for functional restoration as defined by individuals with SCI. We describe neuroprostheses that are in various stages of preclinical development, clinical testing, and commercialization including functional electrical stimulators, epidural and intraspinal microstimulation, bladder neuroprosthesis, and cortical stimulation for restoring sensation. We also discuss neural recording technologies that may provide command or feedback signals for neuroprosthetic devices. Conclusion/clinical relevance Neuroprostheses have begun to address the priorities of individuals with SCI, although there remains room for improvement. In addition to continued technological improvements, closing the loop between the technology and the user may help provide intuitive device control with high levels of performance.

Collaborative approach in the development of high-performance brain-computer interfaces for a neuroprosthetic arm: Translation from animal models to human control

Our research group recently demonstrated that a person with tetraplegia could use a brain–computer interface (BCI) to control a sophisticated anthropomorphic robotic arm with skill and speed approaching that of an able‐bodied person. This multiyear study exemplifies important principles in translating research from foundational theory and animal experiments into a clinical study. We present a roadmap that may serve as an example for other areas of clinical device research as well as an update on study results. Prior to conducting a multiyear clinical trial, years of animal research preceded BCI testing in an epilepsy monitoring unit, and then in a short‐term (28 days) clinical investigation. Scientists and engineers developed the necessary robotic and surgical hardware, software environment, data analysis techniques, and training paradigms. Coordination among researchers, funding institutes, and regulatory bodies ensured that the study would provide valuable scientific information in a safe environment for the study participant. Finally, clinicians from neurosurgery, anesthesiology, physiatry, psychology, and occupational therapy all worked in a multidisciplinary team along with the other researchers to conduct a multiyear BCI clinical study. This teamwork and coordination can be used as a model for others attempting to translate basic science into real‐world clinical situations.

Brain computer interface learning for systems based on electrocorticography and intracortical microelectrode arrays

A brain-computer interface (BCI) system transforms neural activity into control signals for external devices in real time. A BCI user needs to learn to generate specific cortical activity patterns to control external devices effectively. We call this process BCI learning, and it often requires significant effort and time. Therefore, it is important to study this process and develop novel and efficient approaches to accelerate BCI learning. This article reviews major approaches that have been used for BCI learning, including computer-assisted learning, co-adaptive learning, operant conditioning, and sensory feedback. We focus on BCIs based on electrocorticography and intracortical microelectrode arrays for restoring motor function. This article also explores the possibility of brain modulation techniques in promoting BCI learning, such as electrical cortical stimulation, transcranial magnetic stimulation, and optogenetics. Furthermore, as proposed by recent BCI studies, we suggest that BCI learning is in many ways analogous to motor and cognitive skill learning, and therefore skill learning should be a useful metaphor to model BCI learning.

Stability of MEG for real-time neurofeedback

Movement-related field potentials can be extracted and processed in real-time with magnetoencephalography (MEG) and used for brain machine interfacing (BMI). However, due to its immense sensitivity to magnetic fields, MEG is prone to a low signal to noise ratio. It is therefore important to collect enough initial data to appropriately characterize motor-related activity and to ensure that decoders can be built to adequately translate brain activity into BMI-device commands. This is of particular importance for therapeutic BMI applications where less time spent collecting initial open-loop data means more time for performing neurofeedback training which could potentially promote cortical plasticity and rehabilitation. This study evaluated the amount of hand-grasp movement and rest data needed to characterize sensorimotor modulation depth and build classifier functions to decode brain states in real-time. It was determined that with only five minutes of initial open-loop MEG data, decoders can be built to classify brain activity as grasp or rest in real-time with an accuracy of 84±6%.

Accessing and Processing MEG Signals in Real-Time: Emerging Applications and Enabling Technologies

Stephen Foldes1,2, Wei Wang1,2,3, Jennifer Collinger1,4, Xin Li5, Jinyin Zhang2,5, Gustavo Sudre2, Anto Bagic2,6 and Douglas J. Weber1,2,3 1Department of Physical Medicine and Rehabilitation, University of Pittsburgh 2Center for the Neural Basis of Cognition, Carnegie Mellon University 3Department of Bioengineering, University of Pittsburgh 4Human Engineering Research Laboratories, VA Pittsburgh Healthcare System 5Department of Electrical and Computer Engineering, Carnegie Mellon University 6Department of Neurology, University of Pittsburgh USA

Human perception of electrical stimulation on the surface of somatosensory cortex

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.

Remapping cortical modulation for electrocorticographic brain-computer interfaces: a somatotopy-based approach in individuals with upper-limb paralysis

OBJECTIVE Brain-computer interface (BCI) technology aims to provide individuals with paralysis a means to restore function. Electrocorticography (ECoG) uses disc electrodes placed on either the surface of the dura or the cortex to record field potential activity. ECoG has been proposed as a viable neural recording modality for BCI systems, potentially providing stable, long-term recordings of cortical activity with high spatial and temporal resolution. Previously we have demonstrated that a subject with spinal cord injury (SCI) could control an ECoG-based BCI system with up to three degrees of freedom (Wang et al 2013 PLoS One). Here, we expand upon these findings by including brain-control results from two additional subjects with upper-limb paralysis due to amyotrophic lateral sclerosis and brachial plexus injury, and investigate the potential of motor and somatosensory cortical areas to enable BCI control. APPROACH Individuals were implanted with high-density ECoG electrode grids over sensorimotor cortical areas for less than 30 d. Subjects were trained to control a BCI by employing a somatotopic control strategy where high-gamma activity from attempted arm and hand movements drove the velocity of a cursor. MAIN RESULTS Participants were capable of generating robust cortical modulation that was differentiable across attempted arm and hand movements of their paralyzed limb. Furthermore, all subjects were capable of voluntarily modulating this activity to control movement of a computer cursor with up to three degrees of freedom using the somatotopic control strategy. Additionally, for those subjects with electrode coverage of somatosensory cortex, we found that somatosensory cortex was capable of supporting ECoG-based BCI control. SIGNIFICANCE These results demonstrate the feasibility of ECoG-based BCI systems for individuals with paralysis as well as highlight some of the key challenges that must be overcome before such systems are translated to the clinical realm. ClinicalTrials.gov Identifier: NCT01393444.

Intracortical Microstimulation as a Feedback Source for Brain-Computer Interface Users

Dexterous object manipulation requires cutaneous sensory feedback, and in its absence, even simple grasping tasks appear clumsy and slow. In prosthetic limbs controlled through intracortical brain-computer interfaces (iBCIs), restoring this somatosensory feedback could be an important step to improving function as vision provides only impoverished cues during object interactions. Intracortical microstimulation (ICMS) of primary somatosensory cortex (S1) is a potential method to restore this sensory feedback, particularly in people who cannot benefit from stimulation of the peripheral nervous system. Here, we demonstrate the ability of ICMS delivered to S1 to produce somatotopically relevant, cutaneous percepts on individual fingers with graded intensity. This demonstrates the capabilities of ICMS for providing cutaneous feedback to iBCI users.

Altered modulation of sensorimotor rhythms with chronic paralysis

After paralysis, the disconnection between the cortex and its peripheral targets leads to neuroplasticity throughout the nervous system. However, it is unclear how chronic paralysis specifically impacts cortical oscillations associated with attempted movement of impaired limbs. We hypothesized that μ- (8-13 Hz) and β- (15-30 Hz) event-related desynchronization (ERD) would be less modulated for individuals with hand paralysis due to cervical spinal cord injury (SCI). To test this, we compared the modulation of ERD from magnetoencephalography (MEG) during attempted and imagined grasping performed by participants with cervical SCI (n = 12) and able-bodied controls (n = 13). Seven participants with tetraplegia were able to generate some electromyography (EMG) activity during attempted grasping, whereas the other five were not. The peak and area of ERD were significantly decreased for individuals without volitional muscle activity when they attempted to grasp compared with able-bodied subjects and participants with SCI,with some residual EMG activity. However, no significant differences were found between subject groups during mentally simulated tasks (i.e., motor imagery) where no muscle activity or somatosensory consequences were expected. These findings suggest that individuals who are unable to produce muscle activity are capable of generating ERD when attempting to move, but the characteristics of this ERD are altered. However, for people who maintain volitional muscle activity after SCI, there are no significant differences in ERD characteristics compared with able-bodied controls. These results provide evidence that ERD is dependent on the level of intact muscle activity after SCI.NEW & NOTEWORTHY Source space MEG was used to investigate sensorimotor cortical oscillations in individuals with SCI. This study provides evidence that individuals with cervical SCI exhibit decreased ERD when they attempt to grasp if they are incapable of generating muscle activity. However, there were no significant differences in ERD between paralyzed and able-bodied participants during motor imagery. These results have important implications for the design and evaluation of new therapies, such as motor imagery and neurofeedback interventions.