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      Ictal High-Frequency Oscillation for Lateralizing Patients With Suspected Bitemporal Epilepsy Using Wavelet Transform and Granger Causality Analysis

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          Abstract

          Identifying lateralization of bilateral temporal lobe epilepsy (TLE) is a challenging issue; scalp electroencephalography (EEG) and routine band electrocorticography (ECoG) fail to reveal the epileptogenic focus for further temporal lobectomy treatment. High-frequency oscillations (HFOs) can be utilized as a biomarker for lateralizing the onset zone in suspected bitemporal epilepsy. Except subjective vision detect the HFOs, objective verification should be performed to raise the accuracy. In the present research, we prospectively studied 10 patients with refractory temporal seizures and who underwent ECoG with wide-band frequency amplifiers (2,048 Hz); all patients had a class I outcome after temporal resection. Pre- and ictal HFOs will be analyzed by wavelet transform (WT) and Granger causality (GC) to objectively verify lateralization of the seizure onset zone (SOZ). WT analysis showed ictal HFOs in 10 patients mainly covered from 80 to 115 Hz (average, 92.59 ± 10.23 Hz), and there was distinct bandpass boundary between pre-ictal HFOs and ictal HFOs. GC analysis showed five patients (2, 4, 5, 6, and 7), no matter the pre-ictal or ictal state, had the highest GC degree in SOZ itself. The remaining patients (1, 3, 8, 9, and 10) had the highest GC degree in SOZ with its adjacent regions in the pre-ictal and ictal stages. GC analysis further confirmed the result of the WT and suggested HFOs are initiated and propagated in the local brain region mainly, afterward, transmitting to adjacent brain regions. These results indicated that the combination of WT and GC analyses significantly contributes to accurate lateralization in patients with suspected bitemporal epilepsy.

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          Most cited references32

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          High-frequency oscillations in human brain.

          Ripples are 100-200 Hz short-duration oscillatory field potentials that have recently been recorded in rat hippocampus and entorhinal cortex. They reflect fast IPSPs on the soma of pyramidal cells, which occur during synchronous afferent excitation of principal cells and interneuron networks. We now describe two similar types of high-frequency field oscillations recorded from the entorhinal cortex and hippocampus of patients with mesial temporal lobe epilepsy. The first type appears be the human equivalent of normal ripples in the rat. The second, which we have termed fast ripples (FR), are in the frequency range of 250-500 Hz. FR are found in the epileptogenic region and may reflect pathological hypersynchronous population spikes of bursting pyramidal cells.
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            ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery.

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              High-frequency oscillations as a new biomarker in epilepsy.

              The discovery that electroencephalography (EEG) contains useful information at frequencies above the traditional 80Hz limit has had a profound impact on our understanding of brain function. In epilepsy, high-frequency oscillations (HFOs, >80Hz) have proven particularly important and useful. This literature review describes the morphology, clinical meaning, and pathophysiology of epileptic HFOs. To record HFOs, the intracranial EEG needs to be sampled at least at 2,000Hz. The oscillatory events can be visualized by applying a high-pass filter and increasing the time and amplitude scales, or EEG time-frequency maps can show the amount of high-frequency activity. HFOs appear excellent markers for the epileptogenic zone. In patients with focal epilepsy who can benefit from surgery, invasive EEG is often required to identify the epileptic cortex, but current information is sometimes inadequate. Removal of brain tissue generating HFOs has been related to better postsurgical outcome than removing the seizure onset zone, indicating that HFOs may mark cortex that needs to be removed to achieve seizure control. The pathophysiology of epileptic HFOs is challenging, probably involving populations of neurons firing asynchronously. They differ from physiological HFOs in not being paced by rhythmic inhibitory activity and in their possible origin from population spikes. Their link to the epileptogenic zone argues that their study will teach us much about the pathophysiology of epileptogenesis and ictogenesis. HFOs show promise for improving surgical outcome and accelerating intracranial EEG investigations. Their potential needs to be assessed by future research. Copyright © 2012 American Neurological Association.
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                Author and article information

                Contributors
                Journal
                Front Neuroinform
                Front Neuroinform
                Front. Neuroinform.
                Frontiers in Neuroinformatics
                Frontiers Media S.A.
                1662-5196
                28 June 2019
                2019
                : 13
                : 44
                Affiliations
                [1] 1Department of Neurology, Xuanwu Hospital, Capital Medical University , Beijing, China
                [2] 2Beijing Key Laboratory of Neuromodulation , Beijing, China
                [3] 3Center of Epilepsy, Beijing Institute for Brain Disorders, Capital Medical University , Beijing, China
                [4] 4Department of Functional Neurosurgery, Xuanwu Hospital, Capital Medical University , Beijing, China
                Author notes

                Edited by: Tianyi Yan, Beijing Institute of Technology, China

                Reviewed by: Jiaojian Wang, University of Pennsylvania, United States; Xuyuan Zheng, Tianjin Medical University, China; Bin Wang, Taiyuan University of Technology, China

                *Correspondence: Chunyan Liu lcy_e_mail@ 123456163.com Yuping Wang wangyuping01@ 123456sina.cn

                These authors have contributed equally to this work

                Article
                10.3389/fninf.2019.00044
                6611331
                20d1e651-5020-4cc5-9346-775e1e28a28a
                Copyright © 2019 Han, Xu, Du, Zhou, Yu, Liu and Wang.

                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
                : 15 January 2019
                : 27 May 2019
                Page count
                Figures: 2, Tables: 3, Equations: 10, References: 42, Pages: 9, Words: 5779
                Funding
                Funded by: Beijing Municipal Science and Technology Commission 10.13039/501100009592
                Funded by: Beijing Municipal Administration of Hospitals Clinical Medicine Development of Special Funding Support 10.13039/501100009331
                Categories
                Neuroscience
                Original Research

                Neurosciences
                bilateral temporal epilepsy,localization,lateralization,wavelet transform,granger causality

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