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Resting state EEG power spectrum and functional connectivity in autism: a cross-sectional analysis

BACKGROUND: Understanding the development of the neuronal circuitry underlying autism spectrum disorder (ASD) is critical to shed light into its etiology and for the development of treatment options. Resting state EEG provides a window into spontaneous local and long-range neuronal synchronization a...

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Autores principales: Garcés, Pilar, Baumeister, Sarah, Mason, Luke, Chatham, Christopher H., Holiga, Stefan, Dukart, Juergen, Jones, Emily J. H., Banaschewski, Tobias, Baron-Cohen, Simon, Bölte, Sven, Buitelaar, Jan K., Durston, Sarah, Oranje, Bob, Persico, Antonio M., Beckmann, Christian F., Bougeron, Thomas, Dell’Acqua, Flavio, Ecker, Christine, Moessnang, Carolin, Charman, Tony, Tillmann, Julian, Murphy, Declan G. M., Johnson, Mark, Loth, Eva, Brandeis, Daniel, Hipp, Joerg F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9118870/
https://www.ncbi.nlm.nih.gov/pubmed/35585637
http://dx.doi.org/10.1186/s13229-022-00500-x
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author Garcés, Pilar
Baumeister, Sarah
Mason, Luke
Chatham, Christopher H.
Holiga, Stefan
Dukart, Juergen
Jones, Emily J. H.
Banaschewski, Tobias
Baron-Cohen, Simon
Bölte, Sven
Buitelaar, Jan K.
Durston, Sarah
Oranje, Bob
Persico, Antonio M.
Beckmann, Christian F.
Bougeron, Thomas
Dell’Acqua, Flavio
Ecker, Christine
Moessnang, Carolin
Charman, Tony
Tillmann, Julian
Murphy, Declan G. M.
Johnson, Mark
Loth, Eva
Brandeis, Daniel
Hipp, Joerg F.
author_facet Garcés, Pilar
Baumeister, Sarah
Mason, Luke
Chatham, Christopher H.
Holiga, Stefan
Dukart, Juergen
Jones, Emily J. H.
Banaschewski, Tobias
Baron-Cohen, Simon
Bölte, Sven
Buitelaar, Jan K.
Durston, Sarah
Oranje, Bob
Persico, Antonio M.
Beckmann, Christian F.
Bougeron, Thomas
Dell’Acqua, Flavio
Ecker, Christine
Moessnang, Carolin
Charman, Tony
Tillmann, Julian
Murphy, Declan G. M.
Johnson, Mark
Loth, Eva
Brandeis, Daniel
Hipp, Joerg F.
author_sort Garcés, Pilar
collection PubMed
description BACKGROUND: Understanding the development of the neuronal circuitry underlying autism spectrum disorder (ASD) is critical to shed light into its etiology and for the development of treatment options. Resting state EEG provides a window into spontaneous local and long-range neuronal synchronization and has been investigated in many ASD studies, but results are inconsistent. Unbiased investigation in large and comprehensive samples focusing on replicability is needed. METHODS: We quantified resting state EEG alpha peak metrics, power spectrum (PS, 2–32 Hz) and functional connectivity (FC) in 411 children, adolescents and adults (n = 212 ASD, n = 199 neurotypicals [NT], all with IQ > 75). We performed analyses in source-space using individual head models derived from the participants’ MRIs. We tested for differences in mean and variance between the ASD and NT groups for both PS and FC using linear mixed effects models accounting for age, sex, IQ and site effects. Then, we used machine learning to assess whether a multivariate combination of EEG features could better separate ASD and NT participants. All analyses were embedded within a train-validation approach (70%–30% split). RESULTS: In the training dataset, we found an interaction between age and group for the reactivity to eye opening (p = .042 uncorrected), and a significant but weak multivariate ASD vs. NT classification performance for PS and FC (sensitivity 0.52–0.62, specificity 0.59–0.73). None of these findings replicated significantly in the validation dataset, although the effect size in the validation dataset overlapped with the prediction interval from the training dataset. LIMITATIONS: The statistical power to detect weak effects—of the magnitude of those found in the training dataset—in the validation dataset is small, and we cannot fully conclude on the reproducibility of the training dataset’s effects. CONCLUSIONS: This suggests that PS and FC values in ASD and NT have a strong overlap, and that differences between both groups (in both mean and variance) have, at best, a small effect size. Larger studies would be needed to investigate and replicate such potential effects. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-022-00500-x.
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spelling pubmed-91188702022-05-20 Resting state EEG power spectrum and functional connectivity in autism: a cross-sectional analysis Garcés, Pilar Baumeister, Sarah Mason, Luke Chatham, Christopher H. Holiga, Stefan Dukart, Juergen Jones, Emily J. H. Banaschewski, Tobias Baron-Cohen, Simon Bölte, Sven Buitelaar, Jan K. Durston, Sarah Oranje, Bob Persico, Antonio M. Beckmann, Christian F. Bougeron, Thomas Dell’Acqua, Flavio Ecker, Christine Moessnang, Carolin Charman, Tony Tillmann, Julian Murphy, Declan G. M. Johnson, Mark Loth, Eva Brandeis, Daniel Hipp, Joerg F. Mol Autism Research BACKGROUND: Understanding the development of the neuronal circuitry underlying autism spectrum disorder (ASD) is critical to shed light into its etiology and for the development of treatment options. Resting state EEG provides a window into spontaneous local and long-range neuronal synchronization and has been investigated in many ASD studies, but results are inconsistent. Unbiased investigation in large and comprehensive samples focusing on replicability is needed. METHODS: We quantified resting state EEG alpha peak metrics, power spectrum (PS, 2–32 Hz) and functional connectivity (FC) in 411 children, adolescents and adults (n = 212 ASD, n = 199 neurotypicals [NT], all with IQ > 75). We performed analyses in source-space using individual head models derived from the participants’ MRIs. We tested for differences in mean and variance between the ASD and NT groups for both PS and FC using linear mixed effects models accounting for age, sex, IQ and site effects. Then, we used machine learning to assess whether a multivariate combination of EEG features could better separate ASD and NT participants. All analyses were embedded within a train-validation approach (70%–30% split). RESULTS: In the training dataset, we found an interaction between age and group for the reactivity to eye opening (p = .042 uncorrected), and a significant but weak multivariate ASD vs. NT classification performance for PS and FC (sensitivity 0.52–0.62, specificity 0.59–0.73). None of these findings replicated significantly in the validation dataset, although the effect size in the validation dataset overlapped with the prediction interval from the training dataset. LIMITATIONS: The statistical power to detect weak effects—of the magnitude of those found in the training dataset—in the validation dataset is small, and we cannot fully conclude on the reproducibility of the training dataset’s effects. CONCLUSIONS: This suggests that PS and FC values in ASD and NT have a strong overlap, and that differences between both groups (in both mean and variance) have, at best, a small effect size. Larger studies would be needed to investigate and replicate such potential effects. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-022-00500-x. BioMed Central 2022-05-18 /pmc/articles/PMC9118870/ /pubmed/35585637 http://dx.doi.org/10.1186/s13229-022-00500-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Garcés, Pilar
Baumeister, Sarah
Mason, Luke
Chatham, Christopher H.
Holiga, Stefan
Dukart, Juergen
Jones, Emily J. H.
Banaschewski, Tobias
Baron-Cohen, Simon
Bölte, Sven
Buitelaar, Jan K.
Durston, Sarah
Oranje, Bob
Persico, Antonio M.
Beckmann, Christian F.
Bougeron, Thomas
Dell’Acqua, Flavio
Ecker, Christine
Moessnang, Carolin
Charman, Tony
Tillmann, Julian
Murphy, Declan G. M.
Johnson, Mark
Loth, Eva
Brandeis, Daniel
Hipp, Joerg F.
Resting state EEG power spectrum and functional connectivity in autism: a cross-sectional analysis
title Resting state EEG power spectrum and functional connectivity in autism: a cross-sectional analysis
title_full Resting state EEG power spectrum and functional connectivity in autism: a cross-sectional analysis
title_fullStr Resting state EEG power spectrum and functional connectivity in autism: a cross-sectional analysis
title_full_unstemmed Resting state EEG power spectrum and functional connectivity in autism: a cross-sectional analysis
title_short Resting state EEG power spectrum and functional connectivity in autism: a cross-sectional analysis
title_sort resting state eeg power spectrum and functional connectivity in autism: a cross-sectional analysis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9118870/
https://www.ncbi.nlm.nih.gov/pubmed/35585637
http://dx.doi.org/10.1186/s13229-022-00500-x
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