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      Atypical Temporal Dynamics of Resting State Shapes Stimulus-Evoked Activity in Depression—An EEG Study on Rest–Stimulus Interaction

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          Abstract

          Major depressive disorder (MDD) is a complex psychiatric disorder characterized by changes in both resting state and stimulus-evoked activity. Whether resting state changes are carried over to stimulus-evoked activity, however, is unclear. We conducted a combined rest (3 min) and task (three-stimulus auditory oddball paradigm) EEG study in n=28 acute depressed MDD patients, comparing them with n=25 healthy participants. Our focus was on the temporal dynamics of both resting state and stimulus-evoked activity for which reason we measured peak frequency (PF), coefficient of variation (CV), Lempel-Ziv complexity (LZC), and trial-to-trial variability (TTV). Our main findings are: i) atypical temporal dynamics in resting state, specifically in the alpha and theta bands as measured by peak frequency (PF), coefficient of variation (CV) and power; ii) decreased reactivity to external deviant stimuli as measured by decreased changes in stimulus-evoked variance and complexity—TTV, LZC, and power and frequency sliding (FS and PS); iii) correlation of stimulus related measures (TTV, LZC, PS, and FS) with resting state measures. Together, our findings show that resting state dynamics alone are atypical in MDD and, even more important, strongly shapes the dynamics of subsequent stimulus-evoked activity. We thus conclude that MDD can be characterized by an atypical temporal dynamic of its rest–stimulus interaction; that, in turn, makes it difficult for depressed patients to react to relevant stimuli such as the deviant tone in our paradigm.

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          Most cited references85

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          Alpha-band oscillations, attention, and controlled access to stored information

          Alpha-band oscillations are the dominant oscillations in the human brain and recent evidence suggests that they have an inhibitory function. Nonetheless, there is little doubt that alpha-band oscillations also play an active role in information processing. In this article, I suggest that alpha-band oscillations have two roles (inhibition and timing) that are closely linked to two fundamental functions of attention (suppression and selection), which enable controlled knowledge access and semantic orientation (the ability to be consciously oriented in time, space, and context). As such, alpha-band oscillations reflect one of the most basic cognitive processes and can also be shown to play a key role in the coalescence of brain activity in different frequencies.
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            Theta oscillations in the hippocampus.

            Theta oscillations represent the "on-line" state of the hippocampus. The extracellular currents underlying theta waves are generated mainly by the entorhinal input, CA3 (Schaffer) collaterals, and voltage-dependent Ca(2+) currents in pyramidal cell dendrites. The rhythm is believed to be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights. Nevertheless, numerous critical issues regarding both the generation of theta oscillations and their functional significance remain challenges for future research.
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              The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention

              Evidence has amassed from both animal intracranial recordings and human electrophysiology that neural oscillatory mechanisms play a critical role in a number of cognitive functions such as learning, memory, feature binding and sensory gating. The wide availability of high-density electrical and magnetic recordings (64–256 channels) over the past two decades has allowed for renewed efforts in the characterization and localization of these rhythms. A variety of cognitive effects that are associated with specific brain oscillations have been reported, which range in spectral, temporal, and spatial characteristics depending on the context. Our laboratory has focused on investigating the role of alpha-band oscillatory activity (8–14 Hz) as a potential attentional suppression mechanism, and this particular oscillatory attention mechanism will be the focus of the current review. We discuss findings in the context of intersensory selective attention as well as intrasensory spatial and feature-based attention in the visual, auditory, and tactile domains. The weight of evidence suggests that alpha-band oscillations can be actively invoked within cortical regions across multiple sensory systems, particularly when these regions are involved in processing irrelevant or distracting information. That is, a central role for alpha seems to be as an attentional suppression mechanism when objects or features need to be specifically ignored or selected against.
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                Author and article information

                Contributors
                Journal
                Front Psychiatry
                Front Psychiatry
                Front. Psychiatry
                Frontiers in Psychiatry
                Frontiers Media S.A.
                1664-0640
                15 October 2019
                2019
                : 10
                : 719
                Affiliations
                [1] 1University of Ottawa Institute of Mental Health Research , Ottawa, ON, Canada
                [2] 2Department of Cellular and Molecular Medicine and Neuroscience, Faculty of Medicine, University of Ottawa , Ottawa, ON, Canada
                [3] 3Brain and Mind Research Institute, University of Ottawa , Ottawa, ON, Canada
                [4] 4Department of Psychology, Faculty of Social Sciences, University of Ottawa , Ottawa, ON, Canada
                Author notes

                Edited by: Roberto Esposito, A.O. Ospedali Riuniti Marche Nord, Italy

                Reviewed by: Timo Ruusuvirta, University of Turku, Finland; Gennady Knyazev, State Scientific-Research Institute of Physiology & Basic Medicine, Russia; Takefumi Ueno, Hizen Psychiatric, Center (NHO), Japan

                *Correspondence: Annemarie Wolff, awolf037@ 123456uottawa.ca

                This article was submitted to Neuroimaging and Stimulation, a section of the journal Frontiers in Psychiatry

                Article
                10.3389/fpsyt.2019.00719
                6803442
                a7b982b1-5770-4ad1-a361-2830e9fb7260
                Copyright © 2019 Wolff, de la Salle, Sorgini, Lynn, Blier, Knott and Northoff

                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
                : 10 June 2019
                : 09 September 2019
                Page count
                Figures: 7, Tables: 0, Equations: 4, References: 104, Pages: 16, Words: 9338
                Funding
                Funded by: Canadian Institutes of Health Research 10.13039/501100000024
                Categories
                Psychiatry
                Original Research

                Clinical Psychology & Psychiatry
                eeg,depression,resting state,peak frequency,alpha oscillations,theta oscillations

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