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Bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: An electroencephalographic study

Brain connectivity is often altered in autism spectrum disorder (ASD). However, there is little consensus on the nature of these alterations, with studies pointing to either increased or decreased connectivity strength across the broad autism spectrum. An important confound in the interpretation of...

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Autores principales: Ursino, Mauro, Serra, Michele, Tarasi, Luca, Ricci, Giulia, Magosso, Elisa, Romei, Vincenzo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9412751/
https://www.ncbi.nlm.nih.gov/pubmed/36032324
http://dx.doi.org/10.3389/fnsys.2022.932128
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author Ursino, Mauro
Serra, Michele
Tarasi, Luca
Ricci, Giulia
Magosso, Elisa
Romei, Vincenzo
author_facet Ursino, Mauro
Serra, Michele
Tarasi, Luca
Ricci, Giulia
Magosso, Elisa
Romei, Vincenzo
author_sort Ursino, Mauro
collection PubMed
description Brain connectivity is often altered in autism spectrum disorder (ASD). However, there is little consensus on the nature of these alterations, with studies pointing to either increased or decreased connectivity strength across the broad autism spectrum. An important confound in the interpretation of these contradictory results is the lack of information about the directionality of the tested connections. Here, we aimed at disambiguating these confounds by measuring differences in directed connectivity using EEG resting-state recordings in individuals with low and high autistic traits. Brain connectivity was estimated using temporal Granger Causality applied to cortical signals reconstructed from EEG. Between-group differences were summarized using centrality indices taken from graph theory (in degree, out degree, authority, and hubness). Results demonstrate that individuals with higher autistic traits exhibited a significant increase in authority and in degree in frontal regions involved in high-level mechanisms (emotional regulation, decision-making, and social cognition), suggesting that anterior areas mostly receive information from more posterior areas. Moreover, the same individuals exhibited a significant increase in the hubness and out degree over occipital regions (especially the left and right pericalcarine regions, where the primary visual cortex is located), suggesting that these areas mostly send information to more anterior regions. Hubness and authority appeared to be more sensitive indices than the in degree and out degree. The observed brain connectivity differences suggest that, in individual with higher autistic traits, bottom-up signaling overcomes top-down channeled flow. This imbalance may contribute to some behavioral alterations observed in ASD.
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spelling pubmed-94127512022-08-27 Bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: An electroencephalographic study Ursino, Mauro Serra, Michele Tarasi, Luca Ricci, Giulia Magosso, Elisa Romei, Vincenzo Front Syst Neurosci Systems Neuroscience Brain connectivity is often altered in autism spectrum disorder (ASD). However, there is little consensus on the nature of these alterations, with studies pointing to either increased or decreased connectivity strength across the broad autism spectrum. An important confound in the interpretation of these contradictory results is the lack of information about the directionality of the tested connections. Here, we aimed at disambiguating these confounds by measuring differences in directed connectivity using EEG resting-state recordings in individuals with low and high autistic traits. Brain connectivity was estimated using temporal Granger Causality applied to cortical signals reconstructed from EEG. Between-group differences were summarized using centrality indices taken from graph theory (in degree, out degree, authority, and hubness). Results demonstrate that individuals with higher autistic traits exhibited a significant increase in authority and in degree in frontal regions involved in high-level mechanisms (emotional regulation, decision-making, and social cognition), suggesting that anterior areas mostly receive information from more posterior areas. Moreover, the same individuals exhibited a significant increase in the hubness and out degree over occipital regions (especially the left and right pericalcarine regions, where the primary visual cortex is located), suggesting that these areas mostly send information to more anterior regions. Hubness and authority appeared to be more sensitive indices than the in degree and out degree. The observed brain connectivity differences suggest that, in individual with higher autistic traits, bottom-up signaling overcomes top-down channeled flow. This imbalance may contribute to some behavioral alterations observed in ASD. Frontiers Media S.A. 2022-08-12 /pmc/articles/PMC9412751/ /pubmed/36032324 http://dx.doi.org/10.3389/fnsys.2022.932128 Text en Copyright © 2022 Ursino, Serra, Tarasi, Ricci, Magosso and Romei. https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Systems Neuroscience
Ursino, Mauro
Serra, Michele
Tarasi, Luca
Ricci, Giulia
Magosso, Elisa
Romei, Vincenzo
Bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: An electroencephalographic study
title Bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: An electroencephalographic study
title_full Bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: An electroencephalographic study
title_fullStr Bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: An electroencephalographic study
title_full_unstemmed Bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: An electroencephalographic study
title_short Bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: An electroencephalographic study
title_sort bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: an electroencephalographic study
topic Systems Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9412751/
https://www.ncbi.nlm.nih.gov/pubmed/36032324
http://dx.doi.org/10.3389/fnsys.2022.932128
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