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      Interictal Epileptiform Discharges and the Quality of Human Intracranial Neurophysiology Data

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          Abstract

          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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          Most cited references23

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          Hippocampal interictal epileptiform activity disrupts cognition in humans.

          We investigated whether interictal epileptiform discharges (IED) in the human hippocampus are related to impairment of specific memory processes, and which characteristics of hippocampal IED are most associated with memory dysfunction. Ten patients had depth electrodes implanted into their hippocampi for preoperative seizure localization. EEG was recorded during 2,070 total trials of a short-term memory task, with memory processing categorized into encoding, maintenance, and retrieval. The influence of hippocampal IED on these processes was analyzed and adjusted to account for individual differences between patients. Hippocampal IED occurring in the memory retrieval period decreased the likelihood of a correct response when they were contralateral to the seizure focus (p < 0.05) or bilateral (p < 0.001). Bilateral IED during the memory maintenance period had a similar effect (p < 0.01), particularly with spike-wave complexes of longer duration (p < 0.01). IED during encoding had no effect, and reaction time was also unaffected by IED. Hippocampal IED in humans may disrupt memory maintenance and retrieval, but not encoding. The particular effects of bilateral IED and those contralateral to the seizure focus may relate to neural compensation in the more functional hemisphere. This study provides biological validity to animal models in the study of IED-related transient cognitive impairment. Moreover, it strengthens the argument that IED may contribute to cognitive impairment in epilepsy depending upon when and where they occur.
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            Atlas of the normal intracranial electroencephalogram: neurophysiological awake activity in different cortical areas

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              Sharp edge artifacts and spurious coupling in EEG frequency comodulation measures.

              Recent electroencephalogram (EEG), electrocorticogram (ECoG), and local field potential (LFP) observations suggest that distinct frequency bands interact. Numerous measures have been proposed to analyze such interactions, including the amplitude envelope modulation of high frequency activity by the phase or signal of low frequency activity. In this short communication, we describe how abrupt increases or decreases in voltage data may produce spurious coupling in these measures and suggest techniques to detect these effects.
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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
                03 March 2020
                2020
                : 14
                : 44
                Affiliations
                [1] 1Department of Neurological Surgery, University of California, San Francisco , San Francisco, CA, United States
                [2] 2Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco , San Francisco, CA, United States
                Author notes

                Edited by: Douglas Owen Cheyne, Hospital for Sick Children, Canada

                Reviewed by: Stefan Rampp, University Hospital Erlangen, Germany; Jean Gotman, McGill University, Canada

                *Correspondence: Edward F. Chang edward.chang@ 123456ucsf.edu

                These authors have contributed equally to this work

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

                Article
                10.3389/fnhum.2020.00044
                7062638
                6cc3b732-d1ca-4257-96cb-9d53ab42100d
                Copyright © 2020 Ammanuel, Kleen, Leonard and Chang.

                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
                : 05 December 2019
                : 31 January 2020
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 29, Pages: 7, Words: 4805
                Funding
                Funded by: National Institute of Neurological Disorders and Stroke 10.13039/100000065
                Award ID: K23NS110920
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: R01-DC012379, R25NS070680, F32-DC013486, R00-NS065120, DP2-OD00862
                Funded by: Kavli Institute for Brain and Mind, University of California, San Diego 10.13039/100012378
                Funded by: Esther A. and Joseph Klingenstein Fund 10.13039/100001207
                Categories
                Human Neuroscience
                Perspective

                Neurosciences
                epilepsy,interictal discharges,intracranial recordings,data quality,signal processing

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