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      EEG Microstates Temporal Dynamics Differentiate Individuals with Mood and Anxiety Disorders From Healthy Subjects

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          Abstract

          Electroencephalography (EEG) measures the brain’s electrophysiological spatio-temporal activities with high temporal resolution. Multichannel and broadband analysis of EEG signals is referred to as EEG microstates (EEG-ms) and can characterize such dynamic neuronal activity. EEG-ms have gained much attention due to the increasing evidence of their association with mental activities and large-scale brain networks identified by functional magnetic resonance imaging (fMRI). Spatially independent EEG-ms are quasi-stationary topographies (e.g., stable, lasting a few dozen milliseconds) typically classified into four canonical classes (microstates A through D). They can be identified by clustering EEG signals around EEG global field power (GFP) maxima points. We examined the EEG-ms properties and the dynamics of cohorts of mood and anxiety (MA) disorders subjects ( n = 61) and healthy controls (HCs; n = 52). In both groups, we found four distinct classes of EEG-ms (A through D), which did not differ among cohorts. This suggests a lack of significant structural cortical abnormalities among cohorts, which would otherwise affect the EEG-ms topographies. However, both cohorts’ brain network dynamics significantly varied, as reflected in EEG-ms properties. Compared to HC, the MA cohort features a lower transition probability between EEG-ms B and D and higher transition probability from A to D and from B to C, with a trend towards significance in the average duration of microstate C. Furthermore, we harnessed a recently introduced theoretical approach to analyze the temporal dependencies in EEG-ms. The results revealed that the transition matrices of MA group exhibit higher symmetrical and stationarity properties as compared to HC ones. In addition, we found an elevation in the temporal dependencies among microstates, especially in microstate B for the MA group. The determined alteration in EEG-ms temporal dependencies among the cohorts suggests that brain abnormalities in mood and anxiety disorders reflect aberrant neural dynamics and a temporal dwelling among ceratin brain states (i.e., mood and anxiety disorders subjects have a less dynamicity in switching between different brain states).

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          Most cited references48

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          Electrophysiological signatures of resting state networks in the human brain.

          Functional neuroimaging and electrophysiological studies have documented a dynamic baseline of intrinsic (not stimulus- or task-evoked) brain activity during resting wakefulness. This baseline is characterized by slow (<0.1 Hz) fluctuations of functional imaging signals that are topographically organized in discrete brain networks, and by much faster (1-80 Hz) electrical oscillations. To investigate the relationship between hemodynamic and electrical oscillations, we have adopted a completely data-driven approach that combines information from simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI). Using independent component analysis on the fMRI data, we identified six widely distributed resting state networks. The blood oxygenation level-dependent signal fluctuations associated with each network were correlated with the EEG power variations of delta, theta, alpha, beta, and gamma rhythms. Each functional network was characterized by a specific electrophysiological signature that involved the combination of different brain rhythms. Moreover, the joint EEG/fMRI analysis afforded a finer physiological fractionation of brain networks in the resting human brain. This result supports for the first time in humans the coalescence of several brain rhythms within large-scale brain networks as suggested by biophysical studies.
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            BOLD correlates of EEG topography reveal rapid resting-state network dynamics.

            Resting-state functional connectivity studies with fMRI showed that the brain is intrinsically organized into large-scale functional networks for which the hemodynamic signature is stable for about 10s. Spatial analyses of the topography of the spontaneous EEG also show discrete epochs of stable global brain states (so-called microstates), but they remain quasi-stationary for only about 100 ms. In order to test the relationship between the rapidly fluctuating EEG-defined microstates and the slowly oscillating fMRI-defined resting states, we recorded 64-channel EEG in the scanner while subjects were at rest with their eyes closed. Conventional EEG-microstate analysis determined the typical four EEG topographies that dominated across all subjects. The convolution of the time course of these maps with the hemodynamic response function allowed to fit a linear model to the fMRI BOLD responses and revealed four distinct distributed networks. These networks were spatially correlated with four of the resting-state networks (RSNs) that were found by the conventional fMRI group-level independent component analysis (ICA). These RSNs have previously been attributed to phonological processing, visual imagery, attention reorientation, and subjective interoceptive-autonomic processing. We found no EEG-correlate of the default mode network. Thus, the four typical microstates of the spontaneous EEG seem to represent the neurophysiological correlate of four of the RSNs and show that they are fluctuating much more rapidly than fMRI alone suggests. Copyright 2010 Elsevier Inc. All rights reserved.
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              Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic.

              Recent decades have witnessed tremendous advances in the neuroscience of emotion, learning and memory, and in animal models for understanding depression and anxiety. This review focuses on new rationally designed psychiatric treatments derived from preclinical human and animal studies. Nonpharmacological treatments that affect disrupted emotion circuits include vagal nerve stimulation, rapid transcranial magnetic stimulation and deep brain stimulation, all borrowed from neurological interventions that attempt to target known pathological foci. Other approaches include drugs that are given in relation to specific learning events to enhance or disrupt endogenous emotional learning processes. Imaging data suggest that common regions of brain activation are targeted with pharmacological and somatic treatments as well as with the emotional learning in psychotherapy. Although many of these approaches are experimental, the rapidly developing understanding of emotional circuit regulation is likely to provide exciting and powerful future treatments for debilitating mood and anxiety disorders.
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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
                26 February 2019
                2019
                : 13
                : 56
                Affiliations
                [1] 1Laureate Institute for Brain Research , Tulsa, OK, United States
                [2] 2Department of Electrical and Computer Engineering, University of Oklahoma , Tulsa, OK, United States
                [3] 3Japan Society for the Promotion Science , Tokyo, Japan
                [4] 4Research Center for Child Development, Chiba University , Chiba, Japan
                [5] 5Stephenson School of Biomedical Engineering, University of Oklahoma , Norman, OK, United States
                [6] 6Oxley College of Health Sciences, University of Tulsa , Tulsa, OK, United States
                Author notes

                Edited by: Raffaella Franciotti, Università degli Studi G. d’Annunzio Chieti e Pescara, Italy

                Reviewed by: J. Ignacio Serrano, Spanish National Research Council (CSIC), Spain; Antonio Ivano Triggiani, University of Foggia, Italy

                *Correspondence: Jerzy Bodurka jbodurka@ 123456laureateinstitute.org
                Article
                10.3389/fnhum.2019.00056
                6399140
                30863294
                d5bd88bf-eac6-4914-8bba-b4b4a33304fd
                Copyright © 2019 Al Zoubi, Mayeli, Tsuchiyagaito, Misaki, Zotev, Refai, Paulus, Bodurka and the Tulsa 1000 Investigators.

                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 October 2018
                : 31 January 2019
                Page count
                Figures: 7, Tables: 1, Equations: 0, References: 65, Pages: 10, Words: 7727
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Categories
                Neuroscience
                Original Research

                Neurosciences
                eeg microstate,brain,mood and anxiety disorders,temporal dynamic,transition probabilites

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