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Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder

BACKGROUND: Previous autism research has hypothesized that abnormalities of functional connectivity in autism spectrum disorder (ASD) may vary with the spatial distance between two brain regions. Although several resting-state functional magnetic resonance imaging (rsfMRI) studies have extensively e...

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Autores principales: Itahashi, Takashi, Yamada, Takashi, Watanabe, Hiromi, Nakamura, Motoaki, Ohta, Haruhisa, Kanai, Chieko, Iwanami, Akira, Kato, Nobumasa, Hashimoto, Ryu-ichiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4446946/
https://www.ncbi.nlm.nih.gov/pubmed/26023326
http://dx.doi.org/10.1186/s13229-015-0026-z
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author Itahashi, Takashi
Yamada, Takashi
Watanabe, Hiromi
Nakamura, Motoaki
Ohta, Haruhisa
Kanai, Chieko
Iwanami, Akira
Kato, Nobumasa
Hashimoto, Ryu-ichiro
author_facet Itahashi, Takashi
Yamada, Takashi
Watanabe, Hiromi
Nakamura, Motoaki
Ohta, Haruhisa
Kanai, Chieko
Iwanami, Akira
Kato, Nobumasa
Hashimoto, Ryu-ichiro
author_sort Itahashi, Takashi
collection PubMed
description BACKGROUND: Previous autism research has hypothesized that abnormalities of functional connectivity in autism spectrum disorder (ASD) may vary with the spatial distance between two brain regions. Although several resting-state functional magnetic resonance imaging (rsfMRI) studies have extensively examined long-range (or distant) connectivity in the adult ASD brain, short-range (or local) connectivity has been investigated in less depth. Furthermore, the possible relationship between functional connectivity and brain activity level during the resting state remains unclear. METHODS: We acquired rsfMRI data from 50 adults with high-functioning ASD and 50 matched controls to examine the properties of spontaneous brain activity using measures of local and distant connectivity together with a measure of the amplitude of brain activity, known as fractional amplitude of low-frequency fluctuation (fALFF). The two connectivity measures were calculated using a common graph-theoretic framework. We also examined the spatial overlaps between these measures and possible relationships of these disrupted functional measures with autistic traits assessed by the Autism-Spectrum Quotient (AQ). RESULTS: Compared to the controls, participants with ASD exhibited local over-connectivity in the right superior frontal gyrus and middle frontal gyrus, accompanied by local under-connectivity in the bilateral fusiform gyri (FG) and right middle temporal gyrus (MTG). On the other hand, we did not find any significant alterations in distant connectivity. Participants with ASD also exhibited reduced fALFF in the right middle occipital gyrus, lingual gyrus, and FG. Further conjunction and spatial overlap analyses confirmed that the spatial pattern of reduced fALFF substantially overlapped with that of local under-connectivity, demonstrating the co-occurrence of disrupted connectivity and spontaneous activity level in the right inferior occipital gyrus, posterior MTG (pMTG), and FG. Finally, within the ASD group, disrupted local connectivity in the right pMTG significantly correlated with the “social interaction” subscale score of the AQ. CONCLUSIONS: These findings revealed local functional disruptions in the occipital and temporal regions, especially the right FG and pMTG, in the form of co-occurrence of spontaneous brain activity level and local connectivity, which may underline social and communicative dysfunctions in adult ASD. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13229-015-0026-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-44469462015-05-29 Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder Itahashi, Takashi Yamada, Takashi Watanabe, Hiromi Nakamura, Motoaki Ohta, Haruhisa Kanai, Chieko Iwanami, Akira Kato, Nobumasa Hashimoto, Ryu-ichiro Mol Autism Research BACKGROUND: Previous autism research has hypothesized that abnormalities of functional connectivity in autism spectrum disorder (ASD) may vary with the spatial distance between two brain regions. Although several resting-state functional magnetic resonance imaging (rsfMRI) studies have extensively examined long-range (or distant) connectivity in the adult ASD brain, short-range (or local) connectivity has been investigated in less depth. Furthermore, the possible relationship between functional connectivity and brain activity level during the resting state remains unclear. METHODS: We acquired rsfMRI data from 50 adults with high-functioning ASD and 50 matched controls to examine the properties of spontaneous brain activity using measures of local and distant connectivity together with a measure of the amplitude of brain activity, known as fractional amplitude of low-frequency fluctuation (fALFF). The two connectivity measures were calculated using a common graph-theoretic framework. We also examined the spatial overlaps between these measures and possible relationships of these disrupted functional measures with autistic traits assessed by the Autism-Spectrum Quotient (AQ). RESULTS: Compared to the controls, participants with ASD exhibited local over-connectivity in the right superior frontal gyrus and middle frontal gyrus, accompanied by local under-connectivity in the bilateral fusiform gyri (FG) and right middle temporal gyrus (MTG). On the other hand, we did not find any significant alterations in distant connectivity. Participants with ASD also exhibited reduced fALFF in the right middle occipital gyrus, lingual gyrus, and FG. Further conjunction and spatial overlap analyses confirmed that the spatial pattern of reduced fALFF substantially overlapped with that of local under-connectivity, demonstrating the co-occurrence of disrupted connectivity and spontaneous activity level in the right inferior occipital gyrus, posterior MTG (pMTG), and FG. Finally, within the ASD group, disrupted local connectivity in the right pMTG significantly correlated with the “social interaction” subscale score of the AQ. CONCLUSIONS: These findings revealed local functional disruptions in the occipital and temporal regions, especially the right FG and pMTG, in the form of co-occurrence of spontaneous brain activity level and local connectivity, which may underline social and communicative dysfunctions in adult ASD. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13229-015-0026-z) contains supplementary material, which is available to authorized users. BioMed Central 2015-05-24 /pmc/articles/PMC4446946/ /pubmed/26023326 http://dx.doi.org/10.1186/s13229-015-0026-z Text en © Itahashi et al.; licensee BioMed Central. 2015 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 work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Itahashi, Takashi
Yamada, Takashi
Watanabe, Hiromi
Nakamura, Motoaki
Ohta, Haruhisa
Kanai, Chieko
Iwanami, Akira
Kato, Nobumasa
Hashimoto, Ryu-ichiro
Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder
title Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder
title_full Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder
title_fullStr Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder
title_full_unstemmed Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder
title_short Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder
title_sort alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4446946/
https://www.ncbi.nlm.nih.gov/pubmed/26023326
http://dx.doi.org/10.1186/s13229-015-0026-z
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