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      Unsupervised Detection of High-Frequency Oscillations Using Time-Frequency Maps and Computer Vision

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          Abstract

          High-frequency oscillations >80 Hz (HFOs) have unique features distinguishing them from spikes and artifactual components that can be well-evidenced in the time-frequency representations. We introduce an unsupervised HFO detector that uses computer-vision algorithms to detect HFO landmarks on two-dimensional (2D) time-frequency maps. To validate the detector, we introduce an analytical model of the HFO based on a sinewave having a Gaussian envelope, for which analytical equations in time-frequency space can be derived, allowing us to establish a direct correspondence between common HFO detection criteria in the time domain with the ones in the frequency domain, used by the computer-vision detection algorithm. The detector identifies potential HFO events on the time-frequency representation, which are classified as true HFOs if criteria regarding the HFO's frequency, amplitude, and duration are met. The detector is validated on simulated HFOs according to the analytical model, in the presence of noise, with different signal-to-noise ratios (SNRs) ranging from −9 to 0 dB. The detector's sensitivity was 0.64 at an SNR of −9 dB, 0.98 at −6 dB, and >0.99 at −3 dB and 0 dB, while its positive prediction value was >0.95, regardless of the SNR. Using the same simulation dataset, our detector is benchmarked against four previously published HFO detectors. The F-measure, a combined metric that takes into account both sensitivity and positive prediction value, was used to compare detection algorithms. Our detector surpassed the other detectors at −6, −3, and 0 dB and had the second best F-score at −9 dB SNR after the MNI detector (0.77 vs. 0.83). The ability to detect HFOs in clinical recordings has been tested on a set of 36 intracranial electroencephalogram (EEG) channels in six patients, with 89% of the detections being validated by two independent reviewers. The results demonstrate that the unsupervised detection of HFOs based on their 2D features in time-frequency maps is feasible and has a performance comparable or better than the most used HFO detectors.

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          Most cited references52

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          High-frequency network oscillation in the hippocampus.

          Pyramidal cells in the CA1 hippocampal region displayed transient network oscillations (200 hertz) during behavioral immobility, consummatory behaviors, and slow-wave sleep. Simultaneous, multisite recordings revealed temporal and spatial coherence of neuronal activity during population oscillations. Participating pyramidal cells discharged at a rate lower than the frequency of the population oscillation, and their action potentials were phase locked to the negative phase of the simultaneously recorded oscillatory field potentials. In contrast, interneurons discharged at population frequency during the field oscillations. Thus, synchronous output of cooperating CA1 pyramidal cells may serve to induce synaptic enhancement in target structures of the hippocampus.
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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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              Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony.

              The quantification of phase synchrony between neuronal signals is of crucial importance for the study of large-scale interactions in the brain. Two methods have been used to date in neuroscience, based on two distinct approaches which permit a direct estimation of the instantaneous phase of a signal [Phys. Rev. Lett. 81 (1998) 3291; Human Brain Mapping 8 (1999) 194]. The phase is either estimated by using the analytic concept of Hilbert transform or, alternatively, by convolution with a complex wavelet. In both methods the stability of the instantaneous phase over a window of time requires quantification by means of various statistical dependence parameters (standard deviation, Shannon entropy or mutual information). The purpose of this paper is to conduct a direct comparison between these two methods on three signal sets: (1) neural models; (2) intracranial signals from epileptic patients; and (3) scalp EEG recordings. Levels of synchrony that can be considered as reliable are estimated by using the technique of surrogate data. Our results demonstrate that the differences between the methods are minor, and we conclude that they are fundamentally equivalent for the study of neuroelectrical signals. This offers a common language and framework that can be used for future research in the area of synchronization.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                23 March 2020
                2020
                : 14
                : 183
                Affiliations
                [1] 1Physics Department, Bucharest University , Bucharest, Romania
                [2] 2Department of Neurology, Bucharest University Emergency Hospital , Bucharest, Romania
                [3] 3Department of Neurology, Carol Davila University of Medicine and Pharmacy , Bucharest, Romania
                Author notes

                Edited by: Kamran Avanaki, Wayne State University, United States

                Reviewed by: Rayyan Manwar, Wayne State University, United States; Shennan Aibel Weiss, Thomas Jefferson University, United States; Eishi Asano, Children's Hospital of Michigan, United States

                *Correspondence: Andrei Barborica andrei.barborica@ 123456fizica.unibuc.ro

                This article was submitted to Brain Imaging Methods, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2020.00183
                7104802
                32265622
                119bbe4e-858a-4014-83a4-9794b22b3d59
                Copyright © 2020 Donos, Mîndruţă and Barborica.

                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
                : 01 August 2019
                : 19 February 2020
                Page count
                Figures: 8, Tables: 1, Equations: 12, References: 59, Pages: 14, Words: 8388
                Funding
                Funded by: UEFISCDI 10.13039/501100006595
                Award ID: PN-III-P2-2.1-PTE-2016-0114
                Award ID: PN-III-P4-IDPCE-2016-0588
                Award ID: PN-III-P1-1.1-TE-2016-0706
                Award ID: COFUNDFLAGERA II-SCALES
                Categories
                Neuroscience
                Original Research

                Neurosciences
                electroencephalogram (eeg),high-frequency oscillations,time-frequency maps,computer vision,signal detection

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