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Decomposing the role of alpha oscillations during brain maturation

Childhood and adolescence are critical stages of the human lifespan, in which fundamental neural reorganizational processes take place. A substantial body of literature investigated accompanying neurophysiological changes, focusing on the most dominant feature of the human EEG signal: the alpha osci...

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Autores principales: Tröndle, Marius, Popov, Tzvetan, Dziemian, Sabine, Langer, Nicolas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9410707/
https://www.ncbi.nlm.nih.gov/pubmed/36006005
http://dx.doi.org/10.7554/eLife.77571
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author Tröndle, Marius
Popov, Tzvetan
Dziemian, Sabine
Langer, Nicolas
author_facet Tröndle, Marius
Popov, Tzvetan
Dziemian, Sabine
Langer, Nicolas
author_sort Tröndle, Marius
collection PubMed
description Childhood and adolescence are critical stages of the human lifespan, in which fundamental neural reorganizational processes take place. A substantial body of literature investigated accompanying neurophysiological changes, focusing on the most dominant feature of the human EEG signal: the alpha oscillation. Recent developments in EEG signal-processing show that conventional measures of alpha power are confounded by various factors and need to be decomposed into periodic and aperiodic components, which represent distinct underlying brain mechanisms. It is therefore unclear how each part of the signal changes during brain maturation. Using multivariate Bayesian generalized linear models, we examined aperiodic and periodic parameters of alpha activity in the largest openly available pediatric dataset (N=2529, age 5-22 years) and replicated these findings in a preregistered analysis of an independent validation sample (N=369, age 6-22 years). First, the welldocumented age-related decrease in total alpha power was replicated. However, when controlling for the aperiodic signal component, our findings provided strong evidence for an age-related increase in the aperiodic-adjusted alpha power. As reported in previous studies, also relative alpha power revealed a maturational increase, yet indicating an underestimation of the underlying relationship between periodic alpha power and brain maturation. The aperiodic intercept and slope decreased with increasing age and were highly correlated with total alpha power. Consequently, earlier interpretations on age-related changes of total alpha power need to be reconsidered, as elimination of active synapses rather links to decreases in the aperiodic intercept. Instead, analyses of diffusion tensor imaging data indicate that the maturational increase in aperiodic-adjusted alpha power is related to increased thalamocortical connectivity. Functionally, our results suggest that increased thalamic control of cortical alpha power is linked to improved attentional performance during brain maturation.
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spelling pubmed-94107072022-08-26 Decomposing the role of alpha oscillations during brain maturation Tröndle, Marius Popov, Tzvetan Dziemian, Sabine Langer, Nicolas eLife Neuroscience Childhood and adolescence are critical stages of the human lifespan, in which fundamental neural reorganizational processes take place. A substantial body of literature investigated accompanying neurophysiological changes, focusing on the most dominant feature of the human EEG signal: the alpha oscillation. Recent developments in EEG signal-processing show that conventional measures of alpha power are confounded by various factors and need to be decomposed into periodic and aperiodic components, which represent distinct underlying brain mechanisms. It is therefore unclear how each part of the signal changes during brain maturation. Using multivariate Bayesian generalized linear models, we examined aperiodic and periodic parameters of alpha activity in the largest openly available pediatric dataset (N=2529, age 5-22 years) and replicated these findings in a preregistered analysis of an independent validation sample (N=369, age 6-22 years). First, the welldocumented age-related decrease in total alpha power was replicated. However, when controlling for the aperiodic signal component, our findings provided strong evidence for an age-related increase in the aperiodic-adjusted alpha power. As reported in previous studies, also relative alpha power revealed a maturational increase, yet indicating an underestimation of the underlying relationship between periodic alpha power and brain maturation. The aperiodic intercept and slope decreased with increasing age and were highly correlated with total alpha power. Consequently, earlier interpretations on age-related changes of total alpha power need to be reconsidered, as elimination of active synapses rather links to decreases in the aperiodic intercept. Instead, analyses of diffusion tensor imaging data indicate that the maturational increase in aperiodic-adjusted alpha power is related to increased thalamocortical connectivity. Functionally, our results suggest that increased thalamic control of cortical alpha power is linked to improved attentional performance during brain maturation. eLife Sciences Publications, Ltd 2022-08-25 /pmc/articles/PMC9410707/ /pubmed/36006005 http://dx.doi.org/10.7554/eLife.77571 Text en © 2022, Tröndle et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Tröndle, Marius
Popov, Tzvetan
Dziemian, Sabine
Langer, Nicolas
Decomposing the role of alpha oscillations during brain maturation
title Decomposing the role of alpha oscillations during brain maturation
title_full Decomposing the role of alpha oscillations during brain maturation
title_fullStr Decomposing the role of alpha oscillations during brain maturation
title_full_unstemmed Decomposing the role of alpha oscillations during brain maturation
title_short Decomposing the role of alpha oscillations during brain maturation
title_sort decomposing the role of alpha oscillations during brain maturation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9410707/
https://www.ncbi.nlm.nih.gov/pubmed/36006005
http://dx.doi.org/10.7554/eLife.77571
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