Jonathan D. Breshears

Using the Electrocorticographic Speech Network to Control a Brain-Computer Interface in Humans

Electrocorticography (ECoG) has emerged as a new signal platform for brain-computer interface (BCI) systems. Classically, the cortical physiology that has been commonly investigated and utilized for device control in humans has been brain signals from the sensorimotor cortex. Hence, it was unknown whether other neurophysiological substrates, such as the speech network, could be used to further improve on or complement existing motor-based control paradigms. We demonstrate here for the first time that ECoG signals associated with different overt and imagined phoneme articulation can enable invasively monitored human patients to control a one-dimensional computer cursor rapidly and accurately. This phonetic content was distinguishable within higher gamma frequency oscillations and enabled users to achieve final target accuracies between 68% and 91% within 15 min. Additionally, one of the patients achieved robust control using recordings from a microarray consisting of 1 mm spaced microwires. These findings suggest that the cortical network associated with speech could provide an additional cognitive and physiologic substrate for BCI operation and that these signals can be acquired from a cortical array that is small and minimally invasive.

Stable and dynamic cortical electrophysiology of induction and emergence with propofol anesthesia

The mechanism(s) by which anesthetics reversibly suppress consciousness are incompletely understood. Previous functional imaging studies demonstrated dynamic changes in thalamic and cortical metabolic activity, as well as the maintained presence of metabolically defined functional networks despite the loss of consciousness. However, the invasive electrophysiology associated with these observations has yet to be studied. By recording electrical activity directly from the cortical surface, electrocorticography (ECoG) provides a powerful method to integrate spatial, temporal, and spectral features of cortical electrophysiology not possible with noninvasive approaches. In this study, we report a unique comprehensive recording of invasive human cortical physiology during both induction and emergence from propofol anesthesia. Propofol-induced transitions in and out of consciousness (defined here as responsiveness) were characterized by maintained large-scale functional networks defined by correlated fluctuations of the slow cortical potential (<0.5 Hz) over the somatomotor cortex, present even in the deeply anesthetized state of burst suppression. Similarly, phase-power coupling between θ- and γ-range frequencies persisted throughout the induction and emergence from anesthesia. Superimposed on this preserved functional architecture were alterations in frequency band power, variance, covariance, and phase–power interactions that were distinct to different frequency ranges and occurred in separable phases. These data support that dynamic alterations in cortical and thalamocortical circuit activity occur in the context of a larger stable architecture that is maintained despite anesthetic-induced alterations in consciousness.

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

Supplemental Digital Content is Available in the Text.

Electrocorticographic frequency alteration mapping for extraoperative localization of speech cortex.

OBJECTIVEElectrocortical stimulation (ECS) has long been established for delineating eloquent cortex in extraoperative mapping. However, ECS is still coarse and inefficient in delineating regions of functional cortex and can be hampered by afterdischarges. Given these constraints, an adjunct approach to defining motor cortex is the use of electrocorticographic (ECoG) signal changes associated with active regions of cortex. The broad range of frequency oscillations are categorized into 2 main groups with respect to sensorimotor cortex: low-frequency bands (LFBs) and high-frequency bands (HFBs). The LFBs tend to show a power reduction, whereas the HFBs show power increases with cortical activation. These power changes associated with activated cortex could potentially provide a powerful tool in delineating areas of speech cortex. We explore ECoG signal alterations as they occur with activated region of speech cortex and its potential in clinical brain mapping applications. METHODSWe evaluated 7 patients who underwent invasive monitoring for seizure localization. Each had extraoperative ECS mapping to identify speech cortex. Additionally, all subjects performed overt speech tasks with an auditory or a visual cue to identify associated frequency power changes in regard to location and degree of concordance with ECS results. RESULTSElectrocorticographic frequency alteration mapping (EFAM) had an 83.9% sensitivity and a 40.4% specificity in identifying any language site when considering both frequency bands and both stimulus cues. Electrocorticographic frequency alteration mapping was more sensitive in identifying the Wernicke area (100%) than the Broca area (72.2%). The HFB is uniquely suited to identifying the Wernicke area, whereas a combination of the HFB and LFB is important for Broca localization. CONCLUSIONThe concordance between stimulation and spectral power changes demonstrates the possible utility of EFAM as an adjunct method to improve the efficiency and resolution of identifying speech cortex.

Temporal evolution of gamma activity in human cortex during an overt and covert word repetition task

Several scientists have proposed different models for cortical processing of speech. Classically, the regions participating in language were thought to be modular with a linear sequence of activations. More recently, modern theoretical models have posited a more hierarchical and distributed interaction of anatomic areas for the various stages of speech processing. Traditional imaging techniques can only define the location or time of cortical activation, which impedes the further evaluation and refinement of these models. In this study, we take advantage of recordings from the surface of the brain [electrocorticography (ECoG)], which can accurately detect the location and timing of cortical activations, to study the time course of ECoG high gamma (HG) modulations during an overt and covert word repetition task for different cortical areas. For overt word production, our results show substantial perisylvian cortical activations early in the perceptual phase of the task that were maintained through word articulation. However, this broad activation is attenuated during the expressive phase of covert word repetition. Across the different repetition tasks, the utilization of the different cortical sites within the perisylvian region varied in the degree of activation dependent on which stimulus was provided (auditory or visual cue) and whether the word was to be spoken or imagined. Taken together, the data support current models of speech that have been previously described with functional imaging. Moreover, this study demonstrates that the broad perisylvian speech network activates early and maintains suprathreshold activation throughout the word repetition task that appears to be modulated by the demands of different conditions.

Intracranial-to-intracranial bypass for posterior inferior cerebellar artery aneurysms: options, technical challenges, and results in 35 patients

OBJECT Intracranial-to-intracranial (IC-IC) bypasses are alternatives to traditional extracranial-to-intracranial (EC-IC) bypasses to reanastomose parent arteries, reimplant efferent branches, revascularize branches with in situ donor arteries, and reconstruct bifurcations with interposition grafts that are entirely intracranial. These bypasses represent an evolution in bypass surgery from using scalp arteries and remote donor sites toward a more local and reconstructive approach. IC-IC bypass can be utilized preferentially when revascularization is needed in the management of complex aneurysms. Experiences using IC-IC bypass, as applied to posterior inferior cerebellar artery (PICA) aneurysms in 35 patients, were reviewed. METHODS Patients with PICA aneurysms and vertebral artery (VA) aneurysms involving the PICAs origin were identified from a prospectively maintained database of the Vascular Neurosurgery Service, and patients who underwent bypass procedures for PICA revascularization were included. RESULTS During a 17-year period in which 129 PICA aneurysms in 125 patients were treated microsurgically, 35 IC-IC bypasses were performed as part of PICA aneurysm management, including in situ p3-p3 PICA-PICA bypass in 11 patients (31%), PICA reimplantation in 9 patients (26%), reanastomosis in 14 patients (40%), and 1 V3 VA-to-PICA bypass with an interposition graft (3%). All aneurysms were completely or nearly completely obliterated, 94% of bypasses were patent, 77% of patients were improved or unchanged after treatment, and good outcomes (modified Rankin Scale ≤ 2) were observed in 76% of patients. Two patients died expectantly. Ischemic complications were limited to 2 patients in whom the bypasses occluded, and permanent lower cranial nerve morbidity was limited to 3 patients and did not compromise independent function in any of the patients. CONCLUSIONS PICA aneurysms receive the application of IC-IC bypass better than any other aneurysm, with nearly one-quarter of all PICA aneurysms treated microsurgically at our center requiring bypass without a single EC-IC bypass. The selection of PICA bypass is almost algorithmic: trapped aneurysms at the PICA origin or p1 segment are revascularized with a PICA-PICA bypass, with PICA reimplantation as an alternative; trapped p2 segment aneurysms are reanastomosed, bypassed in situ, or reimplanted; distal p3 segment aneurysms are reanastomosed or revascularized with a PICA-PICA bypass; and aneurysms of the p4 segment that are too distal for PICA-PICA bypass are reanastomosed. Interposition grafts are reserved for when these 3 primary options are unsuitable. A constructive approach that preserves the PICA with direct clipping or replaces flow with a bypass when sacrificed should remain an alternative to deconstructive PICA occlusion and endovascular coiling when complete aneurysm occlusion is unlikely.

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.

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.

Electrocorticographic Frequency Alteration Mapping of Speech Cortex during an Awake Craniotomy: Case Report

Objective: Traditional electrocortical stimulation (ECS) mapping is limited by the lengthy serial investigation (one location at a time) and the risk of afterdischarges in localizing eloquent cortex. Electrocorticographic frequency alteration mapping (EFAM) allows the parallel investigation of many cortical sites in much less time and with no risk of afterdischarges because of its passive nature. We examined its use with ECS in the context of language mapping during an awake craniotomy for a tumor resection. Clinical Presentation: The patient was a 61-year-old right-handed Caucasian male who presented with headache and mild aphasia. Imaging demonstrated a 3-cm cystic mass in the posterior temporal-parietal lobe. The patient underwent an awake craniotomy for the mapping of his speech cortex and resection of the mass. Intervention: Using a 32-contact electrode array, electrocorticographic signals were recorded from the exposed cortex as the patient participated in a 3-min screening task involving active (patient naming visually presented words) and rest (patient silent) conditions. A spectral comparison of the 2 conditions revealed specific cortical locations associated with activation during speech. The patient was then widely mapped using ECS. Three of 4 sites identified by ECS were also identified passively and in parallel by EFAM, 2 with statistical significance and the third by qualitative inspection. Conclusion: EFAM was technically achieved in an awake craniotomy patient and had good concordance with ECS mapping. Because it poses no risk of afterdischarges and offers substantial time savings, EFAM holds promise for future development as an adjunct intraoperative mapping tool. Additionally, the cortical signals obtained by this modality can be utilized for localization in the presence of a tumor adjacent to the eloquent regions.