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Chronic ambulatory electrocorticography from human speech cortex.

ABSTRACT: Direct intracranial recording of human brain activity is an important approach for deciphering neural mechanisms of cognition. Such recordings, usually made in patients with epilepsy undergoing inpatient monitoring for seizure localization, are limited in duration and depend on patients' tolerance for the challenges associated with recovering from brain surgery. Thus, typical intracranial recordings, similar to most non-invasive approaches in humans, provide snapshots of brain activity in acute, highly constrained settings, limiting opportunities to understand long timescale and natural, real-world phenomena. A new device for treating some forms of drug-resistant epilepsy, the NeuroPace RNS® System, includes a cranially-implanted neurostimulator and intracranial electrodes that continuously monitor brain activity and respond to incipient seizures with electrical counterstimulation. The RNS System can record epileptic brain activity over years, but whether it can record meaningful, behavior-related physiological responses has not been demonstrated. Here, in a human subject with electrodes implanted over high-level speech-auditory cortex (Wernicke's area; posterior superior temporal gyrus), we report that cortical evoked responses to spoken sentences are robust, selective to phonetic features, and stable over nearly 1.5 years. In a second subject with RNS System electrodes implanted over frontal cortex (Broca's area, posterior inferior frontal gyrus), we found that word production during a naming task reliably evokes cortical responses preceding speech onset. The spatiotemporal resolution, high signal-to-noise, and wireless nature of this system's intracranial recordings make it a powerful new approach to investigate the neural correlates of human cognition over long timescales in natural ambulatory settings.

SUBMITTER: Rao VR

PROVIDER: S-EPMC5482367 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Chronic ambulatory electrocorticography from human speech cortex.

Rao Vikram R VR Leonard Matthew K MK Kleen Jonathan K JK Lucas Ben A BA Mirro Emily A EA Chang Edward F EF

NeuroImage 20170407

Direct intracranial recording of human brain activity is an important approach for deciphering neural mechanisms of cognition. Such recordings, usually made in patients with epilepsy undergoing inpatient monitoring for seizure localization, are limited in duration and depend on patients' tolerance for the challenges associated with recovering from brain surgery. Thus, typical intracranial recordings, similar to most non-invasive approaches in humans, provide snapshots of brain activity in acute, ...[more]

PMID: 28396294

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Project description:ObjectivePatients with suspected mesial temporal lobe (MTL) epilepsy typically undergo inpatient video-electroencephalography (EEG) monitoring with scalp and/or intracranial electrodes for 1 to 2 weeks to localize and lateralize the seizure focus or foci. Chronic ambulatory electrocorticography (ECoG) in patients with MTL epilepsy may provide additional information about seizure lateralization. This analysis describes data obtained from chronic ambulatory ECoG in patients with suspected bilateral MTL epilepsy in order to assess the time required to determine the seizure lateralization and whether this information could influence treatment decisions.MethodsAmbulatory ECoG was reviewed in patients with suspected bilateral MTL epilepsy who were among a larger cohort with intractable epilepsy participating in a randomized controlled trial of responsive neurostimulation. Subjects were implanted with bilateral MTL leads and a cranially implanted neurostimulator programmed to detect abnormal interictal and ictal ECoG activity. ECoG data stored by the neurostimulator were reviewed to determine the lateralization of electrographic seizures and the interval of time until independent bilateral MTL electrographic seizures were recorded.ResultsEighty-two subjects were implanted with bilateral MTL leads and followed for 4.7 years on average (median 4.9 years). Independent bilateral MTL electrographic seizures were recorded in 84%. The average time to record bilateral electrographic seizures in the ambulatory setting was 41.6 days (median 13 days, range 0-376 days). Sixteen percent had only unilateral electrographic seizures after an average of 4.6 years of recording.SignificanceAbout one third of the subjects implanted with bilateral MTL electrodes required >1 month of chronic ambulatory ECoG before the first contralateral MTL electrographic seizure was recorded. Some patients with suspected bilateral MTL seizures had only unilateral electrographic seizures. Chronic ambulatory ECoG in patients with suspected bilateral MTL seizures provides data in a naturalistic setting, may complement data from inpatient video-EEG monitoring, and can contribute to treatment decisions.

Project description:BackgroundElectrocorticography studies are typically conducted in patients undergoing video EEG monitoring, but these studies are subject to confounds such as the effects of pain, recent anesthesia, analgesics, drug changes, antibiotics, and implant effects.New methodTechniques were developed to obtain electrocorticographic (ECoG) data from freely moving subjects performing navigational tasks using the RNS® System (NeuroPace, Inc., Mountain View, CA), a brain-responsive neurostimulation medical device used to treat focal onset epilepsy, and to align data from the RNS System with cognitive task events with high precision. These subjects had not had recent surgery, and were therefore not confounded by the perioperative variables that affect video EEG studies.ResultsTask synchronization using the synchronization marker technique provides a quantitative measure of clock uncertainty, and can align data to task events with less than 4 ms of uncertainty. Hippocampal ECoG activity was found to change immediately before an incorrect response to a math problem compared to hippocampal activity before a correct response. In addition, subjects were found to have variable but significant changes in theta band power in the hippocampus during navigation compared to when subjects were not navigating. We found that there is theta-gamma phase-amplitude coupling in the right hippocampus while subjects stand still during a navigation task.Comparison with existing methodsAn alignment technique described in this study improves the upper bound on task-ECoG alignment uncertainty from approximately 30 ms to under 4 ms. The RNS System is one of the first platforms capable of providing untethered ambulatory ECoG recording in humans, allowing for the study of real world instead of virtual navigation. Compared to intracranial video EEG studies, studies using the RNS System platform are not subject to confounds caused by the drugs and recent surgery inherent to the perioperative environment. Furthermore, these subjects provide the opportunity to record from the same electrodes over the course of many years.ConclusionsThe RNS System enables us to study human navigation with unprecedented clarity. While RNS System patients have fewer electrodes implanted than video EEG patients, the lack of external artifact and confounds from recent surgery make this system a useful tool to further human electrophysiology research.

Project description:ObjectiveThis study was undertaken to measure the duration of chronic electrocorticography (ECoG) needed to attain stable estimates of the seizure laterality ratio in patients with drug-resistant bilateral temporal lobe epilepsy (BTLE).MethodsWe studied 13 patients with drug-resistant BTLE who were implanted for at least 1 year with a responsive neurostimulation device (RNS System) that provides chronic ambulatory ECoG. Bootstrap analysis and nonlinear regression were applied to model the relationship between chronic ECoG duration and the probability of capturing at least one seizure. Laterality of electrographic seizures in chronic ECoG was compared with the seizure laterality ratio from Phase 1 scalp video-electroencephalographic (vEEG) monitoring. The Kaplan-Meier estimator was used to evaluate time to seizure laterality ratio convergence.ResultsSeizure laterality ratios from Phase 1 scalp vEEG monitoring correlated poorly with those from RNS chronic ECoG (r = .31, p = .30). Across the 13 patients, average electrographic seizure frequencies ranged from 1.4 seizures/month to 5.1 seizures/day. A 50% probability of recording at least one electrographic seizure required 9.1 days of chronic ECoG, and 90% probability required 44.3 days of chronic ECoG. A median recording duration of 150.9 days (5 months), corresponding to a median of 16 seizures, was needed before confidence intervals for the seizure laterality ratio reliably contained the long-term value. The median recording duration before the point estimate of the seizure laterality ratio converged to a stationary value was 236.8 days (7.9 months).SignificanceRNS chronic ECoG overcomes temporal sampling limitations intrinsic to inpatient Phase 1 vEEG evaluations. In patients with drug-resistant BTLE, approximately 8 months of chronic RNS ECoG are needed to precisely estimate the seizure laterality ratio, with 75% of people with BTLE achieving convergence after 1 year of RNS recording. For individuals who are candidates for unilateral resection based on seizure laterality, optimized recording duration may help avert morbidity associated with delay to definitive treatment.

Dataset Information

Chronic ambulatory electrocorticography from human speech cortex.

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Chronic ambulatory electrocorticography from human speech cortex.

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