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      Analysis of the alpha activity envelope in electroencephalography in relation to the ratio of excitatory to inhibitory neural activity

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          Abstract

          Alpha waves, one of the major components of resting and awake cortical activity in human electroencephalography (EEG), are known to show waxing and waning, but this phenomenon has rarely been analyzed. In the present study, we analyzed this phenomenon from the viewpoint of excitation and inhibition. The alpha wave envelope was subjected to secondary differentiation. This gave the positive (acceleration positive, Ap) and negative (acceleration negative, An) values of acceleration and their ratio (Ap-An ratio) at each sampling point of the envelope signals for 60 seconds. This analysis was performed on 36 participants with Alzheimer’s disease (AD), 23 with frontotemporal dementia (FTD) and 29 age-matched healthy participants (NC) whose data were provided as open datasets. The mean values of the Ap-An ratio for 60 seconds at each EEG electrode were compared between the NC and AD/FTD groups. The AD (1.41 ±0.01 (SD)) and FTD (1.40 ±0.02) groups showed a larger Ap-An ratio than the NC group (1.38 ±0.02, p<0.05). A significant correlation between the envelope amplitude of alpha activity and the Ap-An ratio was observed at most electrodes in the NC group (Pearson’s correlation coefficient, r = -0.92 ±0.15, mean for all electrodes), whereas the correlation was disrupted in AD (-0.09 ±0.21, p<0.05) and disrupted in the frontal region in the FTD group. The present method analyzed the envelope of alpha waves from a new perspective, that of excitation and inhibition, and it could detect properties of the EEG, Ap-An ratio, that have not been revealed by existing methods. The present study proposed a new method to analyze the alpha activity envelope in electroencephalography, which could be related to excitatory and inhibitory neural activity.

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          "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician.

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            EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis.

            Evidence is presented that EEG oscillations in the alpha and theta band reflect cognitive and memory performance in particular. Good performance is related to two types of EEG phenomena (i) a tonic increase in alpha but a decrease in theta power, and (ii) a large phasic (event-related) decrease in alpha but increase in theta, depending on the type of memory demands. Because alpha frequency shows large interindividual differences which are related to age and memory performance, this double dissociation between alpha vs. theta and tonic vs. phasic changes can be observed only if fixed frequency bands are abandoned. It is suggested to adjust the frequency windows of alpha and theta for each subject by using individual alpha frequency as an anchor point. Based on this procedure, a consistent interpretation of a variety of findings is made possible. As an example, in a similar way as brain volume does, upper alpha power increases (but theta power decreases) from early childhood to adulthood, whereas the opposite holds true for the late part of the lifespan. Alpha power is lowered and theta power enhanced in subjects with a variety of different neurological disorders. Furthermore, after sustained wakefulness and during the transition from waking to sleeping when the ability to respond to external stimuli ceases, upper alpha power decreases, whereas theta increases. Event-related changes indicate that the extent of upper alpha desynchronization is positively correlated with (semantic) long-term memory performance, whereas theta synchronization is positively correlated with the ability to encode new information. The reviewed findings are interpreted on the basis of brain oscillations. It is suggested that the encoding of new information is reflected by theta oscillations in hippocampo-cortical feedback loops, whereas search and retrieval processes in (semantic) long-term memory are reflected by upper alpha oscillations in thalamo-cortical feedback loops. Copyright 1999 Elsevier Science B.V.
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              Mechanisms of gamma oscillations.

              Gamma rhythms are commonly observed in many brain regions during both waking and sleep states, yet their functions and mechanisms remain a matter of debate. Here we review the cellular and synaptic mechanisms underlying gamma oscillations and outline empirical questions and controversial conceptual issues. Our main points are as follows: First, gamma-band rhythmogenesis is inextricably tied to perisomatic inhibition. Second, gamma oscillations are short-lived and typically emerge from the coordinated interaction of excitation and inhibition, which can be detected as local field potentials. Third, gamma rhythm typically concurs with irregular firing of single neurons, and the network frequency of gamma oscillations varies extensively depending on the underlying mechanism. To document gamma oscillations, efforts should be made to distinguish them from mere increases of gamma-band power and/or increased spiking activity. Fourth, the magnitude of gamma oscillation is modulated by slower rhythms. Such cross-frequency coupling may serve to couple active patches of cortical circuits. Because of their ubiquitous nature and strong correlation with the "operational modes" of local circuits, gamma oscillations continue to provide important clues about neuronal population dynamics in health and disease.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Writing – original draft
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                PLOS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                13 June 2024
                2024
                : 19
                : 6
                : e0305082
                Affiliations
                [1 ] Department of Preventive Rehabilitation Sciences, School of Health Sciences, Nagoya University, Nagoya, Japan
                [2 ] Music Division, Nagoya University of the Arts, Kitanagoya, Japan
                [3 ] Department of Hand Surgery, Graduate School of Medicine, Nagoya University, Nagoya, Japan
                Tokai University, JAPAN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Article
                PONE-D-23-35942
                10.1371/journal.pone.0305082
                11175473
                38870189
                d0887c2a-3436-4e0f-a08e-4c572d5775f9
                © 2024 Sano et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 1 November 2023
                : 23 May 2024
                Page count
                Figures: 6, Tables: 3, Pages: 18
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100009619, Japan Agency for Medical Research and Development;
                Award ID: 23gm1510005h0003
                Award Recipient :
                Funded by: JSPS Grant-in-Aid for Scientific Research
                Award ID: 20K07881
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100009619, Japan Agency for Medical Research and Development;
                Award ID: 23gm1510005h0003
                Award Recipient :
                Minoru Hoshiyama reports financial support was provided by JSPS Grant-in-Aid for Scientific Research (C) (20K07881), and Minoru Hoshiyama and Hitoshi Hirata were financially supported by Japan Agency for Medical Research and Development (AMED) (AMED-CREST: 23gm1510005h0003). The authors declare that they have no known competing financial interests or personal relationships that could have potentially to influence the work reported in this article. There was no additional external funding received for this study. The above funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Bioassays and Physiological Analysis
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                Brain Electrophysiology
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                Custom metadata
                All data used are available from the open datasets, https://openneuro.org/datasets/ds004504/versions/1.0.6, (Miltiadous A, Tzimourta KD, Afrantou T, Ioannidis P, Grigoriadis N, Tsalikakis DG, Angelidis P, Tsipouras MG, Glavas E, Giannakeas N, Tzallas AT. A Dataset of Scalp EEG Recordings of Alzheimer’s Disease, Frontotemporal Dementia and Healthy Subjects from Routine EEG. Data, 2023b;8(6):95. doi: 10.3390/data8060095).

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