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      Spatial-Temporal Functional Mapping Combined With Cortico-Cortical Evoked Potentials in Predicting Cortical Stimulation Results

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          Abstract

          Functional human brain mapping is commonly performed during invasive monitoring with intracranial electroencephalographic (iEEG) electrodes prior to resective surgery for drug­ resistant epilepsy. The current gold standard, electrocortical stimulation mapping (ESM), is time ­consuming, sometimes elicits pain, and often induces after discharges or seizures. Moreover, there is a risk of overestimating eloquent areas due to propagation of the effects of stimulation to a broader network of language cortex. Passive iEEG spatial-temporal functional mapping (STFM) has recently emerged as a potential alternative to ESM. However, investigators have observed less correspondence between STFM and ESM maps of language than between their maps of motor function. We hypothesized that incongruities between ESM and STFM of language function may arise due to propagation of the effects of ESM to cortical areas having strong effective connectivity with the site of stimulation. We evaluated five patients who underwent invasive monitoring for seizure localization, whose language areas were identified using ESM. All patients performed a battery of language tasks during passive iEEG recordings. To estimate the effective connectivity of stimulation sites with a broader network of task-activated cortical sites, we measured cortico-cortical evoked potentials (CCEPs) elicited across all recording sites by single-pulse electrical stimulation at sites where ESM was performed at other times. With the combination of high gamma power as well as CCEPs results, we trained a logistic regression model to predict ESM results at individual electrode pairs. The average accuracy of the classifier using both STFM and CCEPs results combined was 87.7%, significantly higher than the one using STFM alone (71.8%), indicating that the correspondence between STFM and ESM results is greater when effective connectivity between ESM stimulation sites and task-activated sites is taken into consideration. These findings, though based on a small number of subjects to date, provide preliminary support for the hypothesis that incongruities between ESM and STFM may arise in part from propagation of stimulation effects to a broader network of cortical language sites activated by language tasks, and suggest that more studies, with larger numbers of patients, are needed to understand the utility of both mapping techniques in clinical practice.

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            BCI2000: a general-purpose brain-computer interface (BCI) system.

            Many laboratories have begun to develop brain-computer interface (BCI) systems that provide communication and control capabilities to people with severe motor disabilities. Further progress and realization of practical applications depends on systematic evaluations and comparisons of different brain signals, recording methods, processing algorithms, output formats, and operating protocols. However, the typical BCI system is designed specifically for one particular BCI method and is, therefore, not suited to the systematic studies that are essential for continued progress. In response to this problem, we have developed a documented general-purpose BCI research and development platform called BCI2000. BCI2000 can incorporate alone or in combination any brain signals, signal processing methods, output devices, and operating protocols. This report is intended to describe to investigators, biomedical engineers, and computer scientists the concepts that the BC12000 system is based upon and gives examples of successful BCI implementations using this system. To date, we have used BCI2000 to create BCI systems for a variety of brain signals, processing methods, and applications. The data show that these systems function well in online operation and that BCI2000 satisfies the stringent real-time requirements of BCI systems. By substantially reducing labor and cost, BCI2000 facilitates the implementation of different BCI systems and other psychophysiological experiments. It is available with full documentation and free of charge for research or educational purposes and is currently being used in a variety of studies by many research groups.
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              Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans.

              A fundamental question in neuroscience concerns the relation between the spiking of individual neurons and the aggregate electrical activity of neuronal ensembles as seen in local field potentials (LFPs). Because LFPs reflect both spiking activity and subthreshold events, this question is not simply one of data aggregation. Recording from 20 neurosurgical patients, we directly examined the relation between LFPs and neuronal spiking. Examining 2030 neurons in widespread brain regions, we found that firing rates were positively correlated with broadband (2-150 Hz) shifts in the LFP power spectrum. In contrast, narrowband oscillations correlated both positively and negatively with firing rates at different recording sites. Broadband power shifts were a more reliable predictor of neuronal spiking than narrowband power shifts. These findings suggest that broadband LFP power provides valuable information concerning neuronal activity beyond that contained in narrowband oscillations.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                14 April 2021
                2021
                : 15
                : 661976
                Affiliations
                [1] 1Department of Neurology, Johns Hopkins University School of Medicine , Baltimore, MD, United States
                [2] 2Department of Biomedical Engineering, Johns Hopkins University School of Medicine , Baltimore, MD, United States
                [3] 3Department of Neurology, New York University School of Medicine , New York, NY, United States
                [4] 4Comprehensive Epilepsy Center, Division of Neurology, Cincinnati Children’s Hospital Medical Center , Cincinnati, OH, United States
                [5] 5Department of Pediatrics, University of Cincinnati College of Medicine , Cincinnati, OH, United States
                Author notes

                Edited by: Shozo Tobimatsu, Kyushu University, Japan

                Reviewed by: Eishi Asano, Children’s Hospital of Michigan, United States; Rei Enatsu, Sapporo Medical University, Japan; Naoto Kunii, The University of Tokyo, Japan

                *Correspondence: Yujing Wang ywang154@ 123456jhu.edu

                Specialty section: This article was submitted to Brain Imaging and Stimulation, a section of the journal Frontiers in Human Neuroscience

                Article
                10.3389/fnhum.2021.661976
                8079642
                f2235c9e-f568-49c1-97d4-544479d0c688
                Copyright © 2021 Wang, Hays, Coogan, Kang, Flinker, Arya, Korzeniewska and Crone.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 31 January 2021
                : 23 March 2021
                Page count
                Figures: 5, Tables: 3, Equations: 5, References: 70, Pages: 13, Words: 9132
                Funding
                Funded by: National Institute of Neurological Disorders and Stroke 10.13039/100000065
                Award ID: 1R01NS115929, 1R01NS091139
                Categories
                Human Neuroscience
                Original Research

                Neurosciences
                language functional mapping,electrocortical stimulation,high gamma activation,effective connectivity,cortico-cortical evoked potentials

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