Publications by authors named "Edward F Chang"

234 Publications

Thin-film microfabrication and intraoperative testing of µECoG and iEEG depth arrays for sense and stimulation.

J Neural Eng 2021 Jul 30. Epub 2021 Jul 30.

Neurological Surgery, University of California San Francisco, 513 Parnassus Ave. HSE 821, San Francisco, California, 94143, UNITED STATES.

Intracranial neural recordings and electrical stimulation are tools used in an increasing range of applications, including intraoperative clinical mapping and monitoring, therapeutic neuromodulation, and brain computer interface control and feedback. However, many of these applications suffer from a lack of spatial specificity and localization, both in terms of sensed neural signal and applied stimulation. This stems from limited manufacturing processes of commercial-off-the-shelf (COTS) arrays unable to accommodate increased channel density, higher channel count, and smaller contact size. Here, we describe a manufacturing and assembly approach using thin-film microfabrication for 32-channel high density subdural micro-electrocorticography (µECoG) surface arrays (contacts 1.2mm diameter, 2mm pitch) and intracranial electroencephalography (iEEG) depth arrays (contacts 0.5mm x 1.5mm, pitch 0.8mm/2.5mm). Crucially, we tackle the translational hurdle and test these arrays during intraoperative studies conducted in four humans under regulatory approval. We demonstrate that the higher-density contacts provide additional unique information across the recording span compared to the density of COTS arrays which typically have electrode pitch of 8mm or greater; 4mm in case of specially ordered arrays. Our intracranial stimulation study results reveal that refined spatial targeting of stimulation elicits evoked potentials with differing spatial spread. Thin-film, μECoG and iEEG depth arrays offer a promising substrate for advancing a number of clinical and research applications reliant on high-resolution neural sensing and intracranial stimulation.
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http://dx.doi.org/10.1088/1741-2552/ac1984DOI Listing
July 2021

Correlation of natural language assessment results with health-related quality of life in adult glioma patients.

J Neurosurg 2021 Jul 30:1-7. Epub 2021 Jul 30.

1Department of Neurological Surgery and.

Objective: Impairments of speech are common in patients with glioma and negatively impact health-related quality of life (HRQoL). The benchmark for clinical assessments is task-based measures, which are not always feasible to administer and may miss essential components of HRQoL. In this study, the authors tested the hypothesis that variations in natural language (NL) correlate with HRQoL in a pattern distinct from task-based measures of language performance.

Methods: NL use was assessed using audio samples collected unobtrusively from 18 patients with newly diagnosed low- and high-grade glioma. NL measures were calculated using manual segmentation and correlated with Quality of Life in Neurological Disorders (Neuro-QoL) outcomes. Spearman's rank-order correlation was used to determine relationships between Neuro-QoL scores and NL measures.

Results: The distribution of NL measures across the entire patient cohort included a mean ± SD total time speaking of 11.5 ± 2.20 seconds, total number of words of 27.2 ± 4.44, number of function words of 10.9 ± 1.68, number of content words of 16.3 ± 2.91, and speech rate of 2.61 ± 0.20 words/second. Speech rate was negatively correlated with functional domains (rho = -0.62 and p = 0.007 for satisfaction with social roles; rho = -0.74 and p < 0.001 for participation in social roles) but positively correlated with impairment domains (rho = 0.58 and p = 0.009 for fatigue) of Neuro-QoL.

Conclusions: Assessment of NL at the time of diagnosis may be a useful measure in the context of treatment planning and monitoring outcomes for adult patients with glioma.
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http://dx.doi.org/10.3171/2021.1.JNS203387DOI Listing
July 2021

Analysis-rcs-data: Open-Source Toolbox for the Ingestion, Time-Alignment, and Visualization of Sense and Stimulation Data From the Medtronic Summit RC+S System.

Front Hum Neurosci 2021 12;15:714256. Epub 2021 Jul 12.

Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, United States.

Closed-loop neurostimulation is a promising therapy being tested and clinically implemented in a growing number of neurological and psychiatric indications. This therapy is enabled by chronically implanted, bidirectional devices including the Medtronic Summit RC+S system. In order to successfully optimize therapy for patients implanted with these devices, analyses must be conducted offline on the recorded neural data, in order to inform optimal sense and stimulation parameters. The file format, volume, and complexity of raw data from these devices necessitate conversion, parsing, and time reconstruction ahead of time-frequency analyses and modeling common to standard neuroscientific analyses. Here, we provide an open-source toolbox written in Matlab which takes raw files from the Summit RC+S and transforms these data into a standardized format amenable to conventional analyses. Furthermore, we provide a plotting tool which can aid in the visualization of multiple data streams and sense, stimulation, and therapy settings. Finally, we describe an analysis module which replicates RC+S on-board power computations, a functionality which can accelerate biomarker discovery. This toolbox aims to accelerate the research and clinical advances made possible by longitudinal neural recordings and adaptive neurostimulation in people with neurological and psychiatric illnesses.
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http://dx.doi.org/10.3389/fnhum.2021.714256DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8312257PMC
July 2021

Patient specific prediction of temporal lobe epilepsy surgical outcomes.

Epilepsia 2021 Jul 18. Epub 2021 Jul 18.

Department of Neurology, University of California San Francisco Medical Center, San Francisco, CA, USA.

Objective: Drug-resistant temporal lobe epilepsy (TLE) is the most common type of epilepsy for which patients undergo surgery. Despite the best clinical judgment and currently available prediction algorithms, surgical outcomes remain variable. We aimed to build and to evaluate the performance of multidimensional Bayesian network classifiers (MBCs), a type of probabilistic graphical model, at predicting probability of seizure freedom after TLE surgery.

Methods: Clinical, neurophysiological, and imaging variables were collected from 231 TLE patients who underwent surgery at the University of California, San Francisco (UCSF) or the Montreal Neurological Institute (MNI) over a 15-year period. Postsurgical Engel outcomes at year 1 (Y1), Y2, and Y5 were analyzed as primary end points. We trained an MBC model on combined data sets from both institutions. Bootstrap bias corrected cross-validation (BBC-CV) was used to evaluate the performance of the models.

Results: The MBC was compared with logistic regression and Cox proportional hazards according to the area under the receiver-operating characteristic curve (AUC). The MBC achieved an AUC of 0.67 at Y1, 0.72 at Y2, and 0.67 at Y5, which indicates modest performance yet superior to what has been reported in the state-of-the-art studies to date.

Significance: The MBC can more precisely encode probabilistic relationships between predictors and class variables (Engel outcomes), achieving promising experimental results compared to other well-known statistical methods. Multisite application of the MBC could further optimize its classification accuracy with prospective data sets. Online access to the MBC is provided, paving the way for its use as an adjunct clinical tool in aiding pre-operative TLE surgical counseling.
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http://dx.doi.org/10.1111/epi.17002DOI Listing
July 2021

Neuroprosthesis for Decoding Speech in a Paralyzed Person with Anarthria.

N Engl J Med 2021 07;385(3):217-227

From the Department of Neurological Surgery (D.A.M., S.L.M., J.R.L., G.K.A., J.G.M., P.F.S., J.C., M.E.D., E.F.C.), the Weill Institute for Neuroscience (D.A.M., S.L.M., J.R.L., G.K.A., J.G.M., P.F.S., J.C., K.G., E.F.C.), and the Departments of Rehabilitation Services (P.M.L.) and Neurology (G.M.A., A.T.-C., K.G.), University of California, San Francisco (UCSF), San Francisco, and the Graduate Program in Bioengineering, University of California, Berkeley-UCSF, Berkeley (S.L.M., J.R.L., E.F.C.).

Background: Technology to restore the ability to communicate in paralyzed persons who cannot speak has the potential to improve autonomy and quality of life. An approach that decodes words and sentences directly from the cerebral cortical activity of such patients may represent an advancement over existing methods for assisted communication.

Methods: We implanted a subdural, high-density, multielectrode array over the area of the sensorimotor cortex that controls speech in a person with anarthria (the loss of the ability to articulate speech) and spastic quadriparesis caused by a brain-stem stroke. Over the course of 48 sessions, we recorded 22 hours of cortical activity while the participant attempted to say individual words from a vocabulary set of 50 words. We used deep-learning algorithms to create computational models for the detection and classification of words from patterns in the recorded cortical activity. We applied these computational models, as well as a natural-language model that yielded next-word probabilities given the preceding words in a sequence, to decode full sentences as the participant attempted to say them.

Results: We decoded sentences from the participant's cortical activity in real time at a median rate of 15.2 words per minute, with a median word error rate of 25.6%. In post hoc analyses, we detected 98% of the attempts by the participant to produce individual words, and we classified words with 47.1% accuracy using cortical signals that were stable throughout the 81-week study period.

Conclusions: In a person with anarthria and spastic quadriparesis caused by a brain-stem stroke, words and sentences were decoded directly from cortical activity during attempted speech with the use of deep-learning models and a natural-language model. (Funded by Facebook and others; ClinicalTrials.gov number, NCT03698149.).
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http://dx.doi.org/10.1056/NEJMoa2027540DOI Listing
July 2021

Musical Hallucinations in Chronic Pain: The Anterior Cingulate Cortex Regulates Internally Generated Percepts.

Front Neurol 2021 4;12:669172. Epub 2021 May 4.

Division of Pain Medicine, Department of Anesthesiology and Perioperative Care, University of California, San Francisco, San Francisco, CA, United States.

The anterior cingulate cortex (ACC) has been extensively implicated in the functional brain network underlying chronic pain. Electrical stimulation of the ACC has been proposed as a therapy for refractory chronic pain, although, mechanisms of therapeutic action are still unclear. As stimulation of the ACC has been reported to produce many different behavioral and perceptual responses, this region likely plays a varied role in sensory and emotional integration as well as modulating internally generated perceptual states. In this case series, we report the emergence of subjective musical hallucinations (MH) after electrical stimulation of the ACC in two patients with refractory chronic pain. In an N-of-1 analysis from one patient, we identified neural activity (local field potentials) that distinguish MH from both the non-MH condition and during a task involving music listening. Music hallucinations were associated with reduced alpha band activity and increased gamma band activity in the ACC. Listening to similar music was associated with different changes in ACC alpha and gamma power, extending prior results that internally generated perceptual phenomena are supported by circuits in the ACC. We discuss these findings in the context of phantom perceptual phenomena and posit a framework whereby chronic pain may be interpreted as a persistent internally generated percept.
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http://dx.doi.org/10.3389/fneur.2021.669172DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8129573PMC
May 2021

Bidirectional propagation of low frequency oscillations over the human hippocampal surface.

Nat Commun 2021 05 12;12(1):2764. Epub 2021 May 12.

Department of Neurological Surgery, Weill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, USA.

The hippocampus is diversely interconnected with other brain systems along its axis. Cycles of theta-frequency activity are believed to propagate from the septal to temporal pole, yet it is unclear how this one-way route supports the flexible cognitive capacities of this structure. We leveraged novel thin-film microgrid arrays conformed to the human hippocampal surface to track neural activity two-dimensionally in vivo. All oscillation frequencies identified between 1-15 Hz propagated across the tissue. Moreover, they dynamically shifted between two roughly opposite directions oblique to the long axis. This predominant propagation axis was mirrored across participants, hemispheres, and consciousness states. Directionality was modulated in a participant who performed a behavioral task, and it could be predicted by wave amplitude topography over the hippocampal surface. Our results show that propagation directions may thus represent distinct meso-scale network computations, operating along versatile spatiotemporal processing routes across the hippocampal body.
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http://dx.doi.org/10.1038/s41467-021-22850-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8115072PMC
May 2021

Are preoperative chlorhexidine gluconate showers associated with a reduction in surgical site infection following craniotomy? A retrospective cohort analysis of 3126 surgical procedures.

J Neurosurg 2021 Apr 30:1-9. Epub 2021 Apr 30.

Departments of1Neurological Surgery.

Objective: Surgical site infection (SSI) is a complication linked to increased costs and length of hospital stay. Prevention of SSI is important to reduce its burden on individual patients and the healthcare system. The authors aimed to assess the efficacy of preoperative chlorhexidine gluconate (CHG) showers on SSI rates following cranial surgery.

Methods: In November 2013, a preoperative CHG shower protocol was implemented at the authors' institution. A total of 3126 surgical procedures were analyzed, encompassing a time frame from April 2012 to April 2016. Cohorts before and after implementation of the CHG shower protocol were evaluated for differences in SSI rates.

Results: The overall SSI rate was 0.6%. No significant differences (p = 0.11) were observed between the rate of SSI of the 892 patients in the preimplementation cohort (0.2%) and that of the 2234 patients in the postimplementation cohort (0.8%). Following multivariable analysis, implementation of preoperative CHG showers was not associated with decreased SSI (adjusted OR 2.96, 95% CI 0.67-13.1; p = 0.15).

Conclusions: This is the largest study, according to sample size, to examine the association between CHG showers and SSI following craniotomy. CHG showers did not significantly alter the risk of SSI after a cranial procedure.
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http://dx.doi.org/10.3171/2020.10.JNS201255DOI Listing
April 2021

Functional maps of direct electrical stimulation-induced speech arrest and anomia: a multicentre retrospective study.

Brain 2021 Apr 1. Epub 2021 Apr 1.

Department of Neurological Surgery, University of California, San Francisco, CA, USA.

Direct electrical stimulation, the transient "lesional" method probing brain function, has been utilized in identifying the language cortex and preserving language function during epilepsy and neuro-oncological surgeries for about a century. However, comparison of functional maps of the language cortex across languages/continents based on cortical stimulation remains unclear. We conducted a retrospective multi-center study including four cohorts of direct electrical stimulation mapping from four centers across three continents, where three indigenous languages (English, French, and Mandarin) are spoken. All subjects performed the two most common language tasks: Number counting and picture naming during stimulation. All language sites were recorded and normalized to the same brain template. Next, Spearman's correlation analysis was performed to explore the consistency of the distributions of the language cortex across centers, a kernel density estimation to localize the peak coordinates, and a hierarchical cluster analysis was performed to detect the crucial epicenters. A total of 598 subjects with 917 speech arrest sites (complete interruption of ongoing counting) and 423 anomia sites (inability to name or misnaming) were included. Different centers presented highly consistent distribution patterns for speech arrest (Spearman's coefficient r ranged from 0.60-0.85, all pair-wise correlations p < 0.05), and similar patterns for anomia (Spearman's coefficient r ranged from 0.37-0.80). The combinational speech arrest map was divided into four clusters: Cluster 1 mainly located in ventral precentral gyrus and pars opercularis, which contained the peak of speech arrest in ventral precentral gyrus; cluster 2 in ventral and dorsal precentral gyrus; cluster 3 in supplementary motor area; cluster 4 in the posterior superior temporal gyrus and supramarginal gyrus. The anomia map revealed two clusters: One was in the posterior part of the superior and middle temporal gyri, which peaked at the posterior superior temporal gyrus; the other within the inferior frontal gyrus, peaked at the pars triangularis. This study constitutes the largest series to date of language maps generated from direct electrical stimulation mapping. The consistency of data provides evidence for common language networks across languages, in the context of both speech and naming circuit. Our results not only clinically offer an atlas for language mapping and protection, but also scientifically provide better insight into the functional organization of language networks.
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http://dx.doi.org/10.1093/brain/awab125DOI Listing
April 2021

Accuracy of omni-planar and surface casting of epileptiform activity for intracranial seizure localization.

Epilepsia 2021 Apr 26;62(4):947-959. Epub 2021 Feb 26.

Department of Neurology and Weill Institute for Neurosciences, University of California, San Francisco, California, USA.

Objective: Intracranial electroencephalography (ICEEG) recordings are performed for seizure localization in medically refractory epilepsy. Signal quantifications such as frequency power can be projected as heatmaps on personalized three-dimensional (3D) reconstructed cortical surfaces to distill these complex recordings into intuitive cinematic visualizations. However, simultaneously reconciling deep recording locations and reliably tracking evolving ictal patterns remain significant challenges.

Methods: We fused oblique magnetic resonance imaging (MRI) slices along depth probe trajectories with cortical surface reconstructions and projected dynamic heatmaps using a simple mathematical metric of epileptiform activity (line-length). This omni-planar and surface casting of epileptiform activity approach (OPSCEA) thus illustrated seizure onset and spread among both deep and superficial locations simultaneously with minimal need for signal processing supervision. We utilized the approach on 41 patients at our center implanted with grid, strip, and/or depth electrodes for localizing medically refractory seizures. Peri-ictal data were converted into OPSCEA videos with multiple 3D brain views illustrating all electrode locations. Five people of varying expertise in epilepsy (medical student through epilepsy attending level) attempted to localize the seizure-onset zones.

Results: We retrospectively compared this approach with the original ICEEG study reports for validation. Accuracy ranged from 73.2% to 97.6% for complete or overlapping onset lobe(s), respectively, and ~56.1% to 95.1% for the specific focus (or foci). Higher answer certainty for a given case predicted better accuracy, and scorers had similar accuracy across different training levels.

Significance: In an era of increasing stereo-EEG use, cinematic visualizations fusing omni-planar and surface functional projections appear to provide a useful adjunct for interpreting complex intracranial recordings and subsequent surgery planning.
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http://dx.doi.org/10.1111/epi.16841DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8276628PMC
April 2021

Adaptive tracking of human ECoG network dynamics.

J Neural Eng 2021 02 24;18(1):016011. Epub 2021 Feb 24.

Ming Hsieh Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA, United States of America. Equal contribution.

Objective: Extracting and modeling the low-dimensional dynamics of multi-site electrocorticogram (ECoG) network activity is important in studying brain functions and dysfunctions and for developing translational neurotechnologies. Dynamic latent state models can be used to describe the ECoG network dynamics with low-dimensional latent states. But so far, non-stationarity of ECoG network dynamics has largely not been addressed in these latent state models. Such non-stationarity can happen due to a change in brain state or recording instability over time. A critical question is whether adaptive tracking of ECoG network dynamics can lead to further dimensionality reduction and more parsimonious and precise modeling. This question is largely unaddressed.

Approach: We investigate this question by employing an adaptive linear state-space model for ECoG network activity constructed from ECoG power feature time-series over tens of hours from 10 human subjects with epilepsy. We study how adaptive modeling affects the prediction and dimensionality reduction for ECoG network dynamics compared with prior non-adaptive models, which do not track non-stationarity.

Main Results: Across the 10 subjects, adaptive modeling significantly improved the prediction of ECoG network dynamics compared with non-adaptive modeling, especially for lower latent state dimensions. Also, compared with non-adaptive modeling, adaptive modeling allowed for additional dimensionality reduction without degrading prediction performance. Finally, these results suggested that ECoG network dynamics over our recording periods exhibit non-stationarity, which can be tracked with adaptive modeling.

Significance: These results have important implications for studying low-dimensional neural representations using ECoG, and for developing future adaptive neurotechnologies for more precise decoding and modulation of brain states in neurological and neuropsychiatric disorders.
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http://dx.doi.org/10.1088/1741-2552/abae42DOI Listing
February 2021

Human cortical encoding of pitch in tonal and non-tonal languages.

Nat Commun 2021 02 19;12(1):1161. Epub 2021 Feb 19.

Department of Neurological Surgery, University of California, San Francisco, CA, USA.

Languages can use a common repertoire of vocal sounds to signify distinct meanings. In tonal languages, such as Mandarin Chinese, pitch contours of syllables distinguish one word from another, whereas in non-tonal languages, such as English, pitch is used to convey intonation. The neural computations underlying language specialization in speech perception are unknown. Here, we use a cross-linguistic approach to address this. Native Mandarin- and English- speaking participants each listened to both Mandarin and English speech, while neural activity was directly recorded from the non-primary auditory cortex. Both groups show language-general coding of speaker-invariant pitch at the single electrode level. At the electrode population level, we find language-specific distribution of cortical tuning parameters in Mandarin speakers only, with enhanced sensitivity to Mandarin tone categories. Our results show that speech perception relies upon a shared cortical auditory feature processing mechanism, which may be tuned to the statistics of a given language.
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http://dx.doi.org/10.1038/s41467-021-21430-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7896081PMC
February 2021

Evidence of state-dependence in the effectiveness of responsive neurostimulation for seizure modulation.

Brain Stimul 2021 Mar-Apr;14(2):366-375. Epub 2021 Feb 6.

Department of Neurology and Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, United States.

Background: An implanted device for brain-responsive neurostimulation (RNS® System) is approved as an effective treatment to reduce seizures in adults with medically-refractory focal epilepsy. Clinical trials of the RNS System demonstrate population-level reduction in average seizure frequency, but therapeutic response is highly variable.

Hypothesis: Recent evidence links seizures to cyclical fluctuations in underlying risk. We tested the hypothesis that effectiveness of responsive neurostimulation varies based on current state within cyclical risk fluctuations.

Methods: We analyzed retrospective data from 25 adults with medically-refractory focal epilepsy implanted with the RNS System. Chronic electrocorticography was used to record electrographic seizures, and hidden Markov models decoded seizures into fluctuations in underlying risk. State-dependent associations of RNS System stimulation parameters with changes in risk were estimated.

Results: Higher charge density was associated with improved outcomes, both for remaining in a low seizure risk state and for transitioning from a high to a low seizure risk state. The effect of stimulation frequency depended on initial seizure risk state: when starting in a low risk state, higher stimulation frequencies were associated with remaining in a low risk state, but when starting in a high risk state, lower stimulation frequencies were associated with transition to a low risk state. Findings were consistent across bipolar and monopolar stimulation configurations.

Conclusion: The impact of RNS on seizure frequency exhibits state-dependence, such that stimulation parameters which are effective in one seizure risk state may not be effective in another. These findings represent conceptual advances in understanding the therapeutic mechanism of RNS, and directly inform current practices of RNS tuning and the development of next-generation neurostimulation systems.
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http://dx.doi.org/10.1016/j.brs.2021.01.023DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8083819PMC
February 2021

State-dependent responses to intracranial brain stimulation in a patient with depression.

Nat Med 2021 02 18;27(2):229-231. Epub 2021 Jan 18.

Department of Psychiatry, University of California, San Francisco, San Francisco, CA, USA.

Deep brain stimulation is a promising treatment for severe depression, but lack of efficacy in randomized trials raises questions regarding anatomical targeting. We implanted multi-site intracranial electrodes in a severely depressed patient and systematically assessed the acute response to focal electrical neuromodulation. We found an elaborate repertoire of distinctive emotional responses that were rapid in onset, reproducible, and context and state dependent. Results provide proof of concept for personalized, circuit-specific medicine in psychiatry.
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http://dx.doi.org/10.1038/s41591-020-01175-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8284979PMC
February 2021

Data-Driven, Visual Framework for the Characterization of Aphasias Across Stroke, Post-resective, and Neurodegenerative Disorders Over Time.

Front Neurol 2020 29;11:616764. Epub 2020 Dec 29.

Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, United States.

Aphasia classifications and specialized language batteries differ across the fields of neurodegenerative disorders and lesional brain injuries, resulting in difficult comparisons of language deficits across etiologies. In this study, we present a simplified framework, in which a widely-used aphasia battery captures clinical clusters across disease etiologies and provides a quantitative and visual method to characterize and track patients over time. The framework is used to evaluate populations representing three disease etiologies: stroke, primary progressive aphasia (PPA), and post-operative aphasia. A total of 330 patients across three populations with cerebral injury leading to aphasia were investigated, including 76 patients with stroke, 107 patients meeting criteria for PPA, and 147 patients following left hemispheric resective surgery. Western Aphasia Battery (WAB) measures (Information Content, Fluency, answering Yes/No questions, Auditory Word Recognition, Sequential Commands, and Repetition) were collected across the three populations and analyzed to develop a multi-dimensional aphasia model using dimensionality reduction techniques. Two orthogonal dimensions were found to explain 87% of the variance across aphasia phenotypes and three disease etiologies. The first dimension reflects shared weighting across aphasia subscores and correlated with aphasia severity. The second dimension incorporates fluency and comprehension, thereby separating Wernicke's from Broca's aphasia, and the non-fluent/agrammatic from semantic PPA variants. Clusters representing clinical classifications, including late PPA presentations, were preserved within the two-dimensional space. Early PPA presentations were not classifiable, as specialized batteries are needed for phenotyping. Longitudinal data was further used to visualize the trajectory of aphasias during recovery or disease progression, including the rapid recovery of post-operative aphasic patients. This method has implications for the conceptualization of aphasia as a spectrum disorder across different disease etiology and may serve as a framework to track the trajectories of aphasia progression and recovery.
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http://dx.doi.org/10.3389/fneur.2020.616764DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7801263PMC
December 2020

A Review of Cortical and Subcortical Stimulation Mapping for Language.

Neurosurgery 2021 Jan 14. Epub 2021 Jan 14.

Department of Neurological Surgery, University of California, San Francisco, San Francisco, California.

Since the early descriptions of language function based on observations of patients with language deficits by Broca and Wernicke, neurosurgeons have been focused on characterizing the anatomic regions necessary for language perception and production, and preserving these structures during surgery to minimize patient deficits post operatively. In this supplementary issue on awake intraoperative mapping, we review language processing across multiple domains, highlighting key advances in direct electrical stimulation of different cortical and subcortical regions involved in naming, repetition, reading, writing, and syntax. We then discuss different intraoperative tasks for assessing the function of a given area and avoiding injury to critical, eloquent regions.
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http://dx.doi.org/10.1093/neuros/nyaa436DOI Listing
January 2021

Human Responses to Visually Evoked Threat.

Curr Biol 2021 Feb 25;31(3):601-612.e3. Epub 2020 Nov 25.

Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305, USA; Department of Ophthalmology, Stanford University School of Medicine, Stanford, CA 94305, USA; BioX, Stanford University School of Medicine, Stanford, CA 94305, USA. Electronic address:

Vision is the primary sense humans use to evaluate and respond to threats. Understanding the biological underpinnings of the human threat response has been hindered by lack of realistic in-lab threat paradigms. We established an immersive virtual reality (VR) platform to simultaneously measure behavior, physiological state, and neural activity from the human brain using chronically implanted electrodes. Subjects with high anxiety showed increased visual scanning in response to threats as compared to healthy controls. In both healthy and anxious subjects, the amount of scanning behavior correlated with the magnitude of physiological arousal, suggesting that visual scanning behavior is directly linked to internal state. Intracranial electroencephalography (iEEG) recordings from three subjects suggested that high-frequency gamma activity in the insula positively correlates with physiological arousal induced by visual threats and that low-frequency theta activity in the orbitofrontal cortex (OFC) negatively correlates with physiological arousal induced by visual threats. These findings reveal a key role of eye movements and suggest that distinct insula and OFC activation dynamics may be important for detecting and adjusting human stress in response to visually perceived threats.
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http://dx.doi.org/10.1016/j.cub.2020.11.035DOI Listing
February 2021

Brain2Char: a deep architecture for decoding text from brain recordings.

J Neural Eng 2020 Nov 3. Epub 2020 Nov 3.

University of California San Francisco, San Francisco, UNITED STATES.

Objective: Decoding language representations directly from the brain can enable new Brain-Computer Interfaces (BCI) for high bandwidth human-human and human-machine communication. Clinically, such technologies can restore communication in people with neurological conditions affecting their ability to speak.

Approach: In this study, we propose a novel deep network architecture Brain2Char, for directly decoding text (specifically character sequences) from direct brain recordings (called Electrocorticography, ECoG). Brain2Char framework combines state-of-the-art deep learning modules --- 3D Inception layers for multiband spatiotemporal feature extraction from neural data and bidirectional recurrent layers, dilated convolution layers followed by language model weighted beam search to decode character sequences, optimizing a connectionist temporal classification (CTC) loss. Additionally, given the highly non-linear transformations that underlie the conversion of cortical function to character sequences, we perform regularizations on the network's latent representations motivated by insights into cortical encoding of speech production and artifactual aspects specific to ECoG data acquisition. To do this, we impose auxiliary losses on latent representations for articulatory movements, speech acoustics and session specific non-linearities.

Main Results: In 3 (out of 4) participants reported here, Brain2Char achieves 10.6%, 8.5% and 7.0%Word Error Rates (WER) respectively on vocabulary sizes ranging from 1200 to 1900 words.

Significance: These results establish a new end-to-end approach on decoding text from brain signals and demonstrate the potential of Brain2Char as a high-performance communication BCI.
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http://dx.doi.org/10.1088/1741-2552/abc742DOI Listing
November 2020

Operative Technique and Lessons Learned From Surgical Implantation of the NeuroPace Responsive Neurostimulation® System in 57 Consecutive Patients.

Oper Neurosurg (Hagerstown) 2021 01;20(2):E98-E109

Department of Neurosurgery, University of California, San Francisco, San Francisco, California.

Background: The Responsive Neurostimulation (RNS)® System (NeuroPace, Inc) is an implantable device designed to improve seizure control in patients with medically refractory focal epilepsy. Because it is relatively new, surgical pearls and operative techniques optimized from experience beyond a small case series have yet to be described.

Objective: To provide a detailed description of our operative technique and surgical pearls learned from implantation of the RNS System in 57 patients at our institution. We describe our method for frame-based placement of amygdalo-hippocampal depth leads, open implantation of cortical strip leads, and open installation of the neurostimulator.

Methods: We outline considerations for patient selection, preoperative planning, surgical positioning, incision planning, stereotactic depth lead implantation, cortical strip lead implantation, craniotomy for neurostimulator implantation, device testing, closure, and intraoperative imaging.

Results: The median reduction in clinical seizure frequency was 60% (standard deviation 63.1) with 27% of patients achieving seizure freedom at last follow up (median 23.1 mo). No infections, intracerebral hemorrhages, or lead migrations were encountered. Two patients experienced lead fractures, and four lead exchanges have been performed.

Conclusion: The techniques set forth here will help with the safe and efficient implantation of these new devices.
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http://dx.doi.org/10.1093/ons/opaa300DOI Listing
January 2021

A Deep Brain Stimulation Trial Period for Treating Chronic Pain.

J Clin Med 2020 Sep 29;9(10). Epub 2020 Sep 29.

Department of Neurological Surgery, University of California San Francisco, San Francisco, CA 94143, USA.

Early studies of deep brain stimulation (DBS) for various neurological disorders involved a temporary trial period where implanted electrodes were externalized, in which the electrical contacts exiting the patient's brain are connected to external stimulation equipment, so that stimulation efficacy could be determined before permanent implant. As the optimal brain target sites for various diseases (i.e., Parkinson's disease, essential tremor) became better established, such trial periods have fallen out of favor. However, deep brain stimulation trial periods are experiencing a modern resurgence for at least two reasons: (1) studies of newer indications such as depression or chronic pain aim to identify new targets and (2) a growing interest in adaptive DBS tools necessitates neurophysiological recordings, which are often done in the peri-surgical period. In this review, we consider the possible approaches, benefits, and risks of such inpatient trial periods with a specific focus on developing new DBS therapies for chronic pain.
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http://dx.doi.org/10.3390/jcm9103155DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7600449PMC
September 2020

Long-term pain outcomes in elderly patients with trigeminal neuralgia: comparison of first-time microvascular decompression and stereotactic radiosurgery.

Neurosurg Focus 2020 10;49(4):E23

1Department of Neurological Surgery, University of California, San Francisco, California; and.

Objective: Common surgical treatments for trigeminal neuralgia (TN) include microvascular decompression (MVD) and stereotactic radiosurgery (SRS). The use of MVD in elderly patients has been described but has yet to be prospectively compared to SRS, which is well-tolerated and noninvasive. The authors aimed to directly compare long-term pain control and adverse event rates for first-time surgical treatments for idiopathic TN in the elderly.

Methods: A prospectively collected database was reviewed for TN patients who had undergone treatment between 1997 and 2017 at a single institution. Standardized collection of preoperative demographics, surgical procedure, and postoperative outcomes was performed. Data analysis was limited to patients over the age of 65 years who had undergone a first-time procedure for the treatment of idiopathic TN with at least 1 year of follow-up.

Results: One hundred ninety-three patients meeting the study inclusion criteria underwent surgical procedures for TN during the study period (54 MVD, 24 MVD+Rhiz, 115 SRS). In patients in whom an artery was not compressing the trigeminal nerve during MVD, a partial sensory rhizotomy (MVD+Rhiz) was performed. Patients in the SRS cohort were older than those in the MVD and MVD+Rhiz cohorts (mean ± SD, 79.2 ± 7.8 vs 72.9 ± 5.7 and 70.9 ± 4.8 years, respectively; p < 0.0001) and had a higher mean Charlson Comorbidity Index (3.8 ± 1.1 vs 3.0 ± 0.9 and 2.9 ± 1.0, respectively; p < 0.0001). Immediate or short-term postoperative pain-free rates (Barrow Neurological Institute [BNI] pain intensity score I) were 98.1% for MVD, 95.8% for MVD+Rhiz, and 78.3% for SRS (p = 0.0008). At the last follow-up, 72.2% of MVD patients had a favorable outcome (BNI score I-IIIa) compared to 54.2% and 49.6% of MVD+Rhiz and SRS patients, respectively (p = 0.02). In total, 0 (0%) SRS, 5 (9.3%) MVD, and 1 (4.2%) MVD+Rhiz patients developed any adverse event. Multivariate Cox proportional hazards analysis demonstrated that procedure type (p = 0.001) and postprocedure sensory change (p = 0.003) were statistically significantly associated with pain control.

Conclusions: In this study cohort, patients who had undergone MVD had a statistically significantly longer duration of pain freedom than those who had undergone MVD+Rhiz or SRS as their first procedure. Fewer adverse events were seen after SRS, though the MVD-associated complication rate was comparable to published rates in younger patients. Overall, the results suggest that both MVD and SRS are effective options for the elderly, despite their advanced age. Treatment choice can be tailored to a patient's unique condition and wishes.
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http://dx.doi.org/10.3171/2020.7.FOCUS20446DOI Listing
October 2020

Early seizure spread and epilepsy surgery: A systematic review.

Epilepsia 2020 10 17;61(10):2163-2172. Epub 2020 Sep 17.

Department of Neurological Surgery, School of Medicine, University of California-San Francisco, San Francisco, California, USA.

Objective: A fundamental question in epilepsy surgery is how to delineate the margins of cortex that must be resected to result in seizure freedom. Whether and which areas showing seizure activity early in ictus must be removed to avoid postoperative recurrence of seizures is an area of ongoing research. Seizure spread dynamics in the initial seconds of ictus are often correlated with postoperative outcome; there is neither a consensus definition of early spread nor a concise summary of the existing literature linking seizure spread to postsurgical seizure outcomes. The present study is intended to summarize the literature that links seizure spread to postoperative seizure outcome and to provide a framework for quantitative assessment of early seizure spread.

Methods: A systematic review was carried out according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. A Medline search identified clinical studies reporting data on seizure spread measured by intracranial electrodes, having at least 10 subjects and reporting at least 1-year postoperative outcome in the English literature from 1990 to 2019. Studies were evaluated regarding support for a primary hypothesis: Areas of early seizure spread represent cortex with seizure-generating potential.

Results: The search yielded 4562 studies: 15 studies met inclusion criteria and 7 studies supported the primary hypothesis. The methods and metrics used to describe seizure spread were heterogenous. The timeframe of seizure spread associated with seizure outcome ranged from 1-14 seconds, with large, well-designed, retrospective studies pointing to 3-10 seconds as most likely to provide meaningful correlates of postoperative seizure freedom.

Significance: The complex correlation between electrophysiologic seizure spread and the potential for seizure generation needs further elucidation. Prospective cohort studies or trials are needed to evaluate epilepsy surgery targeting cortex involved in the first 3-10 seconds of ictus.
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http://dx.doi.org/10.1111/epi.16668DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8139824PMC
October 2020

Plug-and-play control of a brain-computer interface through neural map stabilization.

Nat Biotechnol 2021 03 7;39(3):326-335. Epub 2020 Sep 7.

Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.

Brain-computer interfaces (BCIs) enable control of assistive devices in individuals with severe motor impairments. A limitation of BCIs that has hindered real-world adoption is poor long-term reliability and lengthy daily recalibration times. To develop methods that allow stable performance without recalibration, we used a 128-channel chronic electrocorticography (ECoG) implant in a paralyzed individual, which allowed stable monitoring of signals. We show that long-term closed-loop decoder adaptation, in which decoder weights are carried across sessions over multiple days, results in consolidation of a neural map and 'plug-and-play' control. In contrast, daily reinitialization led to degradation of performance with variable relearning. Consolidation also allowed the addition of control features over days, that is, long-term stacking of dimensions. Our results offer an approach for reliable, stable BCI control by leveraging the stability of ECoG interfaces and neural plasticity.
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http://dx.doi.org/10.1038/s41587-020-0662-5DOI Listing
March 2021

Cortical Encoding of Manual Articulatory and Linguistic Features in American Sign Language.

Curr Biol 2020 11 3;30(22):4342-4351.e3. Epub 2020 Sep 3.

Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, USA; Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, CA, USA; Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA. Electronic address:

The fluent production of a signed language requires exquisite coordination of sensory, motor, and cognitive processes. Similar to speech production, language produced with the hands by fluent signers appears effortless but reflects the precise coordination of both large-scale and local cortical networks. The organization and representational structure of sensorimotor features underlying sign language phonology in these networks remains unknown. Here, we present a unique case study of high-density electrocorticography (ECoG) recordings from the cortical surface of profoundly deaf signer during awake craniotomy. While neural activity was recorded from sensorimotor cortex, the participant produced a large variety of movements in linguistic and transitional movement contexts. We found that at both single electrode and neural population levels, high-gamma activity reflected tuning for particular hand, arm, and face movements, which were organized along dimensions that are relevant for phonology in sign language. Decoding of manual articulatory features revealed a clear functional organization and population dynamics for these highly practiced movements. Furthermore, neural activity clearly differentiated linguistic and transitional movements, demonstrating encoding of language-relevant articulatory features. These results provide a novel and unique view of the fine-scale dynamics of complex and meaningful sensorimotor actions.
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http://dx.doi.org/10.1016/j.cub.2020.08.048DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7674262PMC
November 2020

Comparison of Stereotactic Radiosurgery and Radiofrequency Ablation for Trigeminal Neuralgia in Multiple Sclerosis Patients.

Stereotact Funct Neurosurg 2020 3;98(6):378-385. Epub 2020 Sep 3.

Department of Neurological Surgery, University of California, San Francisco, San Francisco, California, USA,

Background: The optimal treatment for medically refractory trigeminal neuralgia in multiple sclerosis (MS-TN) patients is unknown.

Objective: To compare treatment outcomes between stereotactic radiosurgery (SRS) and radiofrequency ablation (RFA).

Methods: We performed a retrospective study of MS-TN patients treated with SRS or RFA between 2002 and 2019. Outcomes included degree of pain relief, pain recurrence, and sensory changes, segregated based on initial treatment, final treatment following retreatment with the same modality, and crossover patients.

Results: Sixty surgical cases for 42 MS-TN patients were reviewed. Initial pain freedom outcomes and rates of retreatment were similar (SRS: 30%; RFA: 42%). RFA resulted in faster onset of pain freedom (RFA: <1 week; SRS: 15 weeks; p < 0.001). SRS patients with pain relief had longer intervals to pain recurrence at 2 years (p = 0.044). Final treatment outcomes favored RFA for pain freedom/off-medication outcomes (RFA: 44%; SRS: 11%; p = 0.031), though RFA resulted in more paresthesia (RFA: 81%; SRS: 39%; p = 0.012). Both provided at least 80% of adequate pain relief. Crossover patients did not have improved pain relief.

Conclusions: SRS and RFA are both valid surgical options for MS-TN. Discussion with providers will need to balance patient preference with their unique treatment characteristics.
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http://dx.doi.org/10.1159/000509315DOI Listing
May 2021

Transformation of a temporal speech cue to a spatial neural code in human auditory cortex.

Elife 2020 08 25;9. Epub 2020 Aug 25.

Department of Neurological Surgery, University of California, San Francisco, San Francisco, United States.

In speech, listeners extract continuously-varying spectrotemporal cues from the acoustic signal to perceive discrete phonetic categories. Spectral cues are spatially encoded in the amplitude of responses in phonetically-tuned neural populations in auditory cortex. It remains unknown whether similar neurophysiological mechanisms encode temporal cues like voice-onset time (VOT), which distinguishes sounds like // and//. We used direct brain recordings in humans to investigate the neural encoding of temporal speech cues with a VOT continuum from // to //. We found that distinct neural populations respond preferentially to VOTs from one phonetic category, and are also sensitive to sub-phonetic VOT differences within a population's preferred category. In a simple neural network model, simulated populations tuned to detect either temporal gaps or coincidences between spectral cues captured encoding patterns observed in real neural data. These results demonstrate that a spatial/amplitude neural code underlies the cortical representation of both spectral and temporal speech cues.
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http://dx.doi.org/10.7554/eLife.53051DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7556862PMC
August 2020

Real-world experience with direct brain-responsive neurostimulation for focal onset seizures.

Epilepsia 2020 08 13;61(8):1749-1757. Epub 2020 Jul 13.

Stanford University School of Medicine, Stanford, CA, USA.

Objective: The RNS System is a direct brain-responsive neurostimulation system that is US Food and Drug Administration-approved for adults with medically intractable focal onset seizures based on safety and effectiveness data from controlled clinical trials. The purpose of this study was to retrospectively evaluate the real-world safety and effectiveness of the RNS System.

Methods: Eight comprehensive epilepsy centers conducted a chart review of patients treated with the RNS System for at least 1 year, in accordance with the indication for use. Data included device-related serious adverse events and the median percent change in disabling seizure frequency from baseline at years 1, 2, and 3 of treatment and at the most recent follow-up.

Results: One hundred fifty patients met the criteria for analysis. The median reduction in seizures was 67% (interquartile range [IQR] = 33%-93%, n = 149) at 1 year, 75% (IQR = 50%-94%, n = 93) at 2 years, 82% (IQR = 50%-96%, n = 38) at ≥3 years, and 74% (IQR = 50%-96%, n = 150) at last follow-up (mean = 2.3 years). Thirty-five percent of patients had a ≥90% seizure frequency reduction, and 18% of patients reported being clinically seizure-free at last follow-up. Seizure frequency reductions were similar regardless of patient age, age at epilepsy onset, duration of epilepsy, seizure onset in mesial temporal or neocortical foci, magnetic resonance imaging findings, prior intracranial monitoring, prior epilepsy surgery, or prior vagus nerve stimulation treatment. The infection rate per procedure was 2.9% (6/150 patients); five of the six patients had an implant site infection, and one had osteomyelitis. Lead revisions were required in 2.7% (4/150), and 2.0% (3/150) of patients had a subdural hemorrhage, none of which had long-lasting neurological consequences.

Significance: In this real-world experience, safety was similar and clinical seizure outcomes exceeded those of the prospective clinical trials, corroborating effectiveness of this therapy and suggesting that clinical experience has informed more effective programming.
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http://dx.doi.org/10.1111/epi.16593DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7496294PMC
August 2020

A Safe Transitions Pathway for post-craniotomy neurological surgery patients: high-value care that bypasses the intensive care unit.

J Neurosurg 2020 May 29;134(5):1386-1391. Epub 2020 May 29.

4University of California San Francisco Medical Center, San Francisco; and.

Objective: High-value medical care is described as care that leads to excellent patient outcomes, high patient satisfaction, and efficient costs. Neurosurgical care in particular can be expensive for the hospital, as substantial costs are accrued during the operation and throughout the postoperative stay. The authors developed a "Safe Transitions Pathway" (STP) model in which select patients went to the postanesthesia care unit (PACU) and then the neuro-transitional care unit (NTCU) rather than being directly admitted to the neurosciences intensive care unit (ICU) following a craniotomy. They sought to evaluate the clinical and financial outcomes as well as the impact on the patient experience for patients who participated in the STP and bypassed the ICU level of care.

Methods: Patients were enrolled during the 2018 fiscal year (FY18; July 1, 2017, through June 30, 2018). The electronic medical record was reviewed for clinical information and the hospital cost accounting record was reviewed for financial information. Nurses and patients were given a satisfaction survey to assess their respective impressions of the hospital stay and of the recovery pathway.

Results: No patients who proceeded to the NTCU postoperatively were upgraded to the ICU level of care postoperatively. There were no deaths in the STP group, and no patients required a return to the operating room during their hospitalization (95% CI 0%-3.9%). There was a trend toward fewer 30-day readmissions in the STP patients than in the standard pathway patients (1.2% [95% CI 0.0%-6.8%] vs 5.1% [95% CI 2.5%-9.1%], p = 0.058). The mean number of ICU days saved per case was 1.20. The average postprocedure length of stay was reduced by 0.25 days for STP patients. Actual FY18 direct cost savings from 94 patients who went through the STP was $422,128.

Conclusions: Length of stay, direct cost per case, and ICU days were significantly less after the adoption of the STP, and ICU bed utilization was freed for acute admissions and transfers. There were no substantial complications or adverse patient outcomes in the STP group.
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http://dx.doi.org/10.3171/2020.3.JNS192133DOI Listing
May 2020

Machine translation of cortical activity to text with an encoder-decoder framework.

Nat Neurosci 2020 04 30;23(4):575-582. Epub 2020 Mar 30.

Center for Integrative Neuroscience, UCSF, San Francisco, CA, USA.

A decade after speech was first decoded from human brain signals, accuracy and speed remain far below that of natural speech. Here we show how to decode the electrocorticogram with high accuracy and at natural-speech rates. Taking a cue from recent advances in machine translation, we train a recurrent neural network to encode each sentence-length sequence of neural activity into an abstract representation, and then to decode this representation, word by word, into an English sentence. For each participant, data consist of several spoken repeats of a set of 30-50 sentences, along with the contemporaneous signals from ~250 electrodes distributed over peri-Sylvian cortices. Average word error rates across a held-out repeat set are as low as 3%. Finally, we show how decoding with limited data can be improved with transfer learning, by training certain layers of the network under multiple participants' data.
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http://dx.doi.org/10.1038/s41593-020-0608-8DOI Listing
April 2020

Interictal Epileptiform Discharges and the Quality of Human Intracranial Neurophysiology Data.

Front Hum Neurosci 2020 3;14:44. Epub 2020 Mar 3.

Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, United States.

Intracranial electroencephalography (IEEG) involves recording from electrodes placed directly onto the cortical surface or deep brain locations. It is performed on patients with medically refractory epilepsy, undergoing pre-surgical seizure localization. IEEG recordings, combined with advancements in computational capacity and analysis tools, have accelerated cognitive neuroscience. This Perspective describes a potential pitfall latent in many of these recordings by virtue of the subject population-namely interictal epileptiform discharges (IEDs), which can cause spurious results due to the contamination of normal neurophysiological signals by pathological waveforms related to epilepsy. We first discuss the nature of IED hazards, and why they deserve the attention of neurophysiology researchers. We then describe four general strategies used when handling IEDs (manual identification, automated identification, manual-automated hybrids, and ignoring by leaving them in the data), and discuss their pros, cons, and contextual factors. Finally, we describe current practices of human neurophysiology researchers worldwide based on a cross-sectional literature review and a voluntary survey. We put these results in the context of the listed strategies and make suggestions on improving awareness and clarity of reporting to enrich both data quality and communication in the field.
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http://dx.doi.org/10.3389/fnhum.2020.00044DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7062638PMC
March 2020
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