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Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies

BACKGROUND: Although it is well recognized that autism is associated with altered patterns of over- and under-connectivity, specifics are still a matter of debate. Little has been done so far to synthesize available literature using whole-brain electroencephalography (EEG) and magnetoencephalography...

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Autores principales: O’Reilly, Christian, Lewis, John D., Elsabbagh, Mayada
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5414938/
https://www.ncbi.nlm.nih.gov/pubmed/28467487
http://dx.doi.org/10.1371/journal.pone.0175870
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author O’Reilly, Christian
Lewis, John D.
Elsabbagh, Mayada
author_facet O’Reilly, Christian
Lewis, John D.
Elsabbagh, Mayada
author_sort O’Reilly, Christian
collection PubMed
description BACKGROUND: Although it is well recognized that autism is associated with altered patterns of over- and under-connectivity, specifics are still a matter of debate. Little has been done so far to synthesize available literature using whole-brain electroencephalography (EEG) and magnetoencephalography (MEG) recordings. OBJECTIVES: 1) To systematically review the literature on EEG/MEG functional and effective connectivity in autism spectrum disorder (ASD), 2) to synthesize and critically appraise findings related with the hypothesis that ASD is characterized by long-range underconnectivity and local overconnectivity, and 3) to provide, based on the literature, an analysis of tentative factors that are likely to mediate association between ASD and atypical connectivity (e.g., development, topography, lateralization). METHODS: Literature reviews were done using PubMed and PsychInfo databases. Abstracts were screened, and only relevant articles were analyzed based on the objectives of this paper. Special attention was paid to the methodological characteristics that could have created variability in outcomes reported between studies. RESULTS: Our synthesis provides relatively strong support for long-range underconnectivity in ASD, whereas the status of local connectivity remains unclear. This observation was also mirrored by a similar relationship with lower frequencies being often associated with underconnectivity and higher frequencies being associated with both under- and over-connectivity. Putting together these observations, we propose that ASD is characterized by a general trend toward an under-expression of lower-band wide-spread integrative processes compensated by more focal, higher-frequency, locally specialized, and segregated processes. Further investigation is, however, needed to corroborate the conclusion and its generalizability across different tasks. Of note, abnormal lateralization in ASD, specifically an elevated left-over-right EEG and MEG functional connectivity ratio, has been also reported consistently across studies. CONCLUSIONS: The large variability in study samples and methodology makes a systematic quantitative analysis (i.e. meta-analysis) of this body of research impossible. Nevertheless, a general trend supporting the hypothesis of long-range functional underconnectivity can be observed. Further research is necessary to more confidently determine the status of the hypothesis of short-range overconnectivity. Frequency-band specific patterns and their relationships with known symptoms of autism also need to be further clarified.
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spelling pubmed-54149382017-05-14 Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies O’Reilly, Christian Lewis, John D. Elsabbagh, Mayada PLoS One Research Article BACKGROUND: Although it is well recognized that autism is associated with altered patterns of over- and under-connectivity, specifics are still a matter of debate. Little has been done so far to synthesize available literature using whole-brain electroencephalography (EEG) and magnetoencephalography (MEG) recordings. OBJECTIVES: 1) To systematically review the literature on EEG/MEG functional and effective connectivity in autism spectrum disorder (ASD), 2) to synthesize and critically appraise findings related with the hypothesis that ASD is characterized by long-range underconnectivity and local overconnectivity, and 3) to provide, based on the literature, an analysis of tentative factors that are likely to mediate association between ASD and atypical connectivity (e.g., development, topography, lateralization). METHODS: Literature reviews were done using PubMed and PsychInfo databases. Abstracts were screened, and only relevant articles were analyzed based on the objectives of this paper. Special attention was paid to the methodological characteristics that could have created variability in outcomes reported between studies. RESULTS: Our synthesis provides relatively strong support for long-range underconnectivity in ASD, whereas the status of local connectivity remains unclear. This observation was also mirrored by a similar relationship with lower frequencies being often associated with underconnectivity and higher frequencies being associated with both under- and over-connectivity. Putting together these observations, we propose that ASD is characterized by a general trend toward an under-expression of lower-band wide-spread integrative processes compensated by more focal, higher-frequency, locally specialized, and segregated processes. Further investigation is, however, needed to corroborate the conclusion and its generalizability across different tasks. Of note, abnormal lateralization in ASD, specifically an elevated left-over-right EEG and MEG functional connectivity ratio, has been also reported consistently across studies. CONCLUSIONS: The large variability in study samples and methodology makes a systematic quantitative analysis (i.e. meta-analysis) of this body of research impossible. Nevertheless, a general trend supporting the hypothesis of long-range functional underconnectivity can be observed. Further research is necessary to more confidently determine the status of the hypothesis of short-range overconnectivity. Frequency-band specific patterns and their relationships with known symptoms of autism also need to be further clarified. Public Library of Science 2017-05-03 /pmc/articles/PMC5414938/ /pubmed/28467487 http://dx.doi.org/10.1371/journal.pone.0175870 Text en © 2017 O’Reilly et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
O’Reilly, Christian
Lewis, John D.
Elsabbagh, Mayada
Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies
title Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies
title_full Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies
title_fullStr Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies
title_full_unstemmed Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies
title_short Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies
title_sort is functional brain connectivity atypical in autism? a systematic review of eeg and meg studies
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5414938/
https://www.ncbi.nlm.nih.gov/pubmed/28467487
http://dx.doi.org/10.1371/journal.pone.0175870
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