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      Quantification of Phase-Amplitude Coupling in Neuronal Oscillations: Comparison of Phase-Locking Value, Mean Vector Length, Modulation Index, and Generalized-Linear-Modeling-Cross-Frequency-Coupling

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          Abstract

          Phase-amplitude coupling is a promising construct to study cognitive processes in electroencephalography (EEG) and magnetencephalography (MEG). Due to the novelty of the concept, various measures are used in the literature to calculate phase-amplitude coupling. Here, performance of the three most widely used phase-amplitude coupling measures – phase-locking value (PLV), mean vector length (MVL), and modulation index (MI) – and of the generalized linear modeling cross-frequency coupling (GLM-CFC) method is thoroughly compared with the help of simulated data. We combine advantages of previous reviews and use a realistic data simulation, examine moderators and provide inferential statistics for the comparison of all four indices of phase-amplitude coupling. Our analyses show that all four indices successfully differentiate coupling strength and coupling width when monophasic coupling is present. While the MVL was most sensitive to modulations in coupling strengths and width, only the MI and GLM-CFC can detect biphasic coupling. Coupling values of all four indices were influenced by moderators including data length, signal-to-noise-ratio, and sampling rate when approaching Nyquist frequencies. The MI was most robust against confounding influences of these moderators. Based on our analyses, we recommend the MI for noisy and short data epochs with unknown forms of coupling. For high quality and long data epochs with monophasic coupling and a high signal-to-noise ratio, the use of the MVL is recommended. Ideally, both indices are reported simultaneously for one data set.

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            The θ-γ neural code.

            Theta and gamma frequency oscillations occur in the same brain regions and interact with each other, a process called cross-frequency coupling. Here, we review evidence for the following hypothesis: that the dual oscillations form a code for representing multiple items in an ordered way. This form of coding has been most clearly demonstrated in the hippocampus, where different spatial information is represented in different gamma subcycles of a theta cycle. Other experiments have tested the functional importance of oscillations and their coupling. These involve correlation of oscillatory properties with memory states, correlation with memory performance, and effects of disrupting oscillations on memory. Recent work suggests that this coding scheme coordinates communication between brain regions and is involved in sensory as well as memory processes. Copyright © 2013 Elsevier Inc. All rights reserved.
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              Measuring phase-amplitude coupling between neuronal oscillations of different frequencies.

              Neuronal oscillations of different frequencies can interact in several ways. There has been particular interest in the modulation of the amplitude of high-frequency oscillations by the phase of low-frequency oscillations, since recent evidence suggests a functional role for this type of cross-frequency coupling (CFC). Phase-amplitude coupling has been reported in continuous electrophysiological signals obtained from the brain at both local and macroscopic levels. In the present work, we present a new measure for assessing phase-amplitude CFC. This measure is defined as an adaptation of the Kullback-Leibler distance-a function that is used to infer the distance between two distributions-and calculates how much an empirical amplitude distribution-like function over phase bins deviates from the uniform distribution. We show that a CFC measure defined this way is well suited for assessing the intensity of phase-amplitude coupling. We also review seven other CFC measures; we show that, by some performance benchmarks, our measure is especially attractive for this task. We also discuss some technical aspects related to the measure, such as the length of the epochs used for these analyses and the utility of surrogate control analyses. Finally, we apply the measure and a related CFC tool to actual hippocampal recordings obtained from freely moving rats and show, for the first time, that the CA3 and CA1 regions present different CFC characteristics.
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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
                07 June 2019
                2019
                : 13
                : 573
                Affiliations
                [1] 1Division of Cognitive Biopsychology and Methods, Department of Psychology, University of Fribourg , Fribourg, Switzerland
                [2] 2Department of General Psychology and Methodology, Faculty I – Psychology, University of Trier , Trier, Germany
                Author notes

                Edited by: Amir Shmuel, McGill University, Canada

                Reviewed by: Jennifer R. Stapleton-Kotloski, Wake Forest School of Medicine, United States; Roberto C. Sotero, University of Calgary, Canada

                *Correspondence: Mareike J. Hülsemann, mareike.huelsemann@ 123456unifr.ch

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

                Article
                10.3389/fnins.2019.00573
                6592221
                31275096
                ff88c492-ad2b-47f9-b4e4-d3b237d3398d
                Copyright © 2019 Hülsemann, Naumann and Rasch.

                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
                : 28 August 2018
                : 20 May 2019
                Page count
                Figures: 5, Tables: 0, Equations: 7, References: 43, Pages: 15, Words: 0
                Funding
                Funded by: H2020 European Research Council 10.13039/100010663
                Award ID: 677875
                Categories
                Neuroscience
                Original Research

                Neurosciences
                phase-amplitude cross-frequency coupling,phase-locking value,mean vector length,modulation index,glm-cfc,simulated eeg/meg data

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