David T. Bundy

Microscale recording from human motor cortex: implications for minimally invasive electrocorticographic brain-computer interfaces

OBJECT There is a growing interest in the use of recording from the surface of the brain, known as electrocorticography (ECoG), as a practical signal platform for brain-computer interface application. The signal has a combination of high signal quality and long-term stability that may be the ideal intermediate modality for future application. The research paradigm for studying ECoG signals uses patients requiring invasive monitoring for seizure localization. The implanted arrays span cortex areas on the order of centimeters. Currently, it is unknown what level of motor information can be discerned from small regions of human cortex with microscale ECoG recording. METHODS In this study, a patient requiring invasive monitoring for seizure localization underwent concurrent implantation with a 16-microwire array (1-mm electrode spacing) placed over primary motor cortex. Microscale activity was recorded while the patient performed simple contra- and ipsilateral wrist movements that were monitored in parallel with electromyography. Using various statistical methods, linear and nonlinear relationships between these microcortical changes and recorded electromyography activity were defined. RESULTS Small regions of primary motor cortex (< 5 mm) carry sufficient information to separate multiple aspects of motor movements (that is, wrist flexion/extension and ipsilateral/contralateral movements). CONCLUSIONS These findings support the conclusion that small regions of cortex investigated by ECoG recording may provide sufficient information about motor intentions to support brain-computer interface operations in the future. Given the small scale of the cortical region required, the requisite implanted array would be minimally invasive in terms of surgical placement of the electrode array.

Nonuniform High-Gamma (60–500 Hz) Power Changes Dissociate Cognitive Task and Anatomy in Human Cortex

High-gamma-band (>60 Hz) power changes in cortical electrophysiology are a reliable indicator of focal, event-related cortical activity. Despite discoveries of oscillatory subthreshold and synchronous suprathreshold activity at the cellular level, there is an increasingly popular view that high-gamma-band amplitude changes recorded from cellular ensembles are the result of asynchronous firing activity that yields wideband and uniform power increases. Others have demonstrated independence of power changes in the low- and high-gamma bands, but to date, no studies have shown evidence of any such independence above 60 Hz. Based on nonuniformities in time-frequency analyses of electrocorticographic (ECoG) signals, we hypothesized that induced high-gamma-band (60–500 Hz) power changes are more heterogeneous than currently understood. Using single-word repetition tasks in six human subjects, we showed that functional responsiveness of different ECoG high-gamma sub-bands can discriminate cognitive task (e.g., hearing, reading, speaking) and cortical locations. Power changes in these sub-bands of the high-gamma range are consistently present within single trials and have statistically different time courses within the trial structure. Moreover, when consolidated across all subjects within three task-relevant anatomic regions (sensorimotor, Brocas area, and superior temporal gyrus), these behavior- and location-dependent power changes evidenced nonuniform trends across the population. Together, the independence and nonuniformity of power changes across a broad range of frequencies suggest that a new approach to evaluating high-gamma-band cortical activity is necessary. These findings show that in addition to time and location, frequency is another fundamental dimension of high-gamma dynamics.

A Novel Data-Driven Approach to Preoperative Mapping of Functional Cortex Using Resting-State Functional Magnetic Resonance Imaging

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An EEG-based brain computer interface for rehabilitation and restoration of hand control following stroke using ipsilateral cortical physiology

The loss of motor control severely impedes activities of daily life. Brain computer interfaces (BCIs) offer new possibilities to treat nervous system injuries, but conventional BCIs use signals from primary motor cortex, the same sites most likely damaged in a stroke causing paralysis. Recent studies found distinct cortical physiology associated with contralesional limb movements in regions distinct from primary motor cortex. To capitalize on these findings, we designed and implemented a BCI that localizes and acquires these brain signals to drive a powered, hand orthotic which opens and closes a patients hand.

Frequency-specific mechanism links human brain networks for spatial attention

Significance Humans have the remarkable ability to flexibly attend to stimuli in the environment and seamlessly shift behaviors, depending on sensory conditions and internal goals. Neuroimaging studies have shown that tasks involving particular cognitive domains consistently recruit specific broadly distributed functional brain networks. A fundamental question in neuroscience is how the brain flexibly manages communication within and between these brain networks, allowing task-relevant regions to interact while minimizing the influence of task-irrelevant activity. In this report we show that low-frequency neuronal oscillations, which reflect fluctuations in neuronal excitability, are modulated selectively within task-relevant, but not -irrelevant brain networks. This modulation of oscillatory activity may coordinate the selective routing of neuronal information within the brain during everyday behavior. Selective attention allows us to filter out irrelevant information in the environment and focus neural resources on information relevant to our current goals. Functional brain-imaging studies have identified networks of broadly distributed brain regions that are recruited during different attention processes; however, the dynamics by which these networks enable selection are not well understood. Here, we first used functional MRI to localize dorsal and ventral attention networks in human epileptic subjects undergoing seizure monitoring. We subsequently recorded cortical physiology using subdural electrocorticography during a spatial-attention task to study network dynamics. Attention networks become selectively phase-modulated at low frequencies (δ, θ) during the same task epochs in which they are recruited in functional MRI. This mechanism may alter the excitability of task-relevant regions or their effective connectivity. Furthermore, different attention processes (holding vs. shifting attention) are associated with synchrony at different frequencies, which may minimize unnecessary cross-talk between separate neuronal processes.

Decoding three-dimensional reaching movements using electrocorticographic signals in humans

OBJECTIVE Electrocorticography (ECoG) signals have emerged as a potential control signal for brain-computer interface (BCI) applications due to balancing signal quality and implant invasiveness. While there have been numerous demonstrations in which ECoG signals were used to decode motor movements and to develop BCI systems, the extent of information that can be decoded has been uncertain. Therefore, we sought to determine if ECoG signals could be used to decode kinematics (speed, velocity, and position) of arm movements in 3D space. APPROACH To investigate this, we designed a 3D center-out reaching task that was performed by five epileptic patients undergoing temporary placement of ECoG arrays. We used the ECoG signals within a hierarchical partial-least squares (PLS) regression model to perform offline prediction of hand speed, velocity, and position. MAIN RESULTS The hierarchical PLS regression model enabled us to predict hand speed, velocity, and position during 3D reaching movements from held-out test sets with accuracies above chance in each patient with mean correlation coefficients between 0.31 and 0.80 for speed, 0.27 and 0.54 for velocity, and 0.22 and 0.57 for position. While beta band power changes were the most significant features within the model used to classify movement and rest, the local motor potential and high gamma band power changes, were the most important features in the prediction of kinematic parameters. SIGNIFICANCE We believe that this study represents the first demonstration that truly three-dimensional movements can be predicted from ECoG recordings in human patients. Furthermore, this prediction underscores the potential to develop BCI systems with multiple degrees of freedom in human patients using ECoG.

Mapping sensorimotor cortex with slow cortical potential resting-state networks while awake and under anesthesia.

BACKGROUND The emerging insight into resting-state cortical networks has been important in our understanding of the fundamental architecture of brain organization. These networks, which were originally identified with functional magnetic resonance imaging, are also seen in the correlation topography of the infraslow rhythms of local field potentials. Because of the fundamental nature of these networks and their independence from task-related activations, we posit that, in addition to their neuroscientific relevance, these slow cortical potential networks could play an important role in clinical brain mapping. OBJECTIVE To assess whether these networks would be useful in identifying eloquent cortex such as sensorimotor cortex in patients both awake and under anesthesia. METHODS This study included 9 subjects undergoing surgical treatment for intractable epilepsy. Slow cortical potentials were recorded from the cortical surface in patients while awake and under propofol anesthesia. To test brain-mapping utility, slow cortical potential networks were identified with data-driven (seed-independent) and anatomy-driven (seed-based) approaches. With electrocortical stimulation used as the gold standard for comparison, the sensitivity and specificity of these networks for identifying sensorimotor cortex were calculated. RESULTS Networks identified with a data-driven approach in patients under anesthesia and awake were 90% and 93% sensitive and 58% and 55% specific for sensorimotor cortex, respectively. Networks identified with systematic seed selection in patients under anesthesia and awake were 78% and 83% sensitive and 67% and 60% specific, respectively. CONCLUSION Resting-state networks may be useful for tailoring stimulation mapping and could provide a means of identifying eloquent regions in patients while under anesthesia.

Contralesional Brain–Computer Interface Control of a Powered Exoskeleton for Motor Recovery in Chronic Stroke Survivors

Background and Purpose— There are few effective therapies to achieve functional recovery from motor-related disabilities affecting the upper limb after stroke. This feasibility study tested whether a powered exoskeleton driven by a brain–computer interface (BCI), using neural activity from the unaffected cortical hemisphere, could affect motor recovery in chronic hemiparetic stroke survivors. This novel system was designed and configured for a home-based setting to test the feasibility of BCI-driven neurorehabilitation in outpatient environments. Methods— Ten chronic hemiparetic stroke survivors with moderate-to-severe upper-limb motor impairment (mean Action Research Arm Test=13.4) used a powered exoskeleton that opened and closed the affected hand using spectral power from electroencephalographic signals from the unaffected hemisphere associated with imagined hand movements of the paretic limb. Patients used the system at home for 12 weeks. Motor function was evaluated before, during, and after the treatment. Results— Across patients, our BCI-driven approach resulted in a statistically significant average increase of 6.2 points in the Action Research Arm Test. This behavioral improvement significantly correlated with improvements in BCI control. Secondary outcomes of grasp strength, Motricity Index, and the Canadian Occupational Performance Measure also significantly improved. Conclusions— The findings demonstrate the therapeutic potential of a BCI-driven neurorehabilitation approach using the unaffected hemisphere in this uncontrolled sample of chronic stroke survivors. They also demonstrate that BCI-driven neurorehabilitation can be effectively delivered in the home environment, thus increasing the probability of future clinical translation. Clinical Trial Registration— URL: http://www.clinicaltrials.gov. Unique identifier: NCT02552368.

Current Challenges Facing the Translation of Brain Computer Interfaces from Preclinical Trials to Use in Human Patients

Current research in brain computer interface (BCI) technology is advancing beyond preclinical studies, with trials beginning in human patients. To date, these trials have been carried out with several different types of recording interfaces. The success of these devices has varied widely, but different factors such as the level of invasiveness, timescale of recorded information, and ability to maintain stable functionality of the device over a long period of time all must be considered in addition to accuracy in decoding intent when assessing the most practical type of device moving forward. Here, we discuss various approaches to BCIs, distinguishing between devices focusing on control of operations extrinsic to the subject (e.g., prosthetic limbs, computer cursors) and those focusing on control of operations intrinsic to the brain (e.g., using stimulation or external feedback), including closed-loop or adaptive devices. In this discussion, we consider the current challenges facing the translation of various types of BCI technology to eventual human application.

Decoding Motor Signals From the Pediatric Cortex: Implications for Brain-Computer Interfaces in Children

OBJECTIVE: To demonstrate the decodable nature of pediatric brain signals for the purpose of neuroprosthetic control. We hypothesized that children would achieve levels of brain-derived computer control comparable to performance previously reported for adults. PATIENTS AND METHODS: Six pediatric patients with intractable epilepsy who were invasively monitored underwent screening for electrocortical control signals associated with specific motor or phoneme articulation tasks. Subsequently, patients received visual feedback as they used these associated electrocortical signals to direct one dimensional cursor movement to a target on a screen. RESULTS: All patients achieved accuracies between 70% and 99% within 9 minutes of training using the same screened motor and articulation tasks. Two subjects went on to achieve maximum accuracies of 73% and 100% using imagined actions alone. Average mean and maximum performance for the 6 pediatric patients was comparable to that of 5 adults. The mean accuracy of the pediatric group was 81% (95% confidence interval [CI]: 71.5–90.5) over a mean training time of 11.6 minutes, whereas the adult group had a mean accuracy of 72% (95% CI: 61.2–84.3) over a mean training time of 12.5 minutes. Maximum performance was also similar between the pediatric and adult groups (89.6% [95% CI: 83–96.3] and 88.5% [95% CI: 77.1–99.8], respectively). CONCLUSIONS: Similarly to adult brain signals, pediatric brain signals can be decoded and used for BCI operation. Therefore, BCI systems developed for adults likely hold similar promise for children with motor disabilities.