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Neural correlates of shared sensory symptoms in autism and attention-deficit/hyperactivity disorder

Symptoms of autism spectrum disorder and attention-deficit/hyperactivity disorder often co-occur. Among these, sensory impairment, which is a core diagnostic feature of autism spectrum disorder, is often observed in children with attention-deficit/hyperactivity disorder. However, the underlying mech...

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Autores principales: Itahashi, Takashi, Fujino, Junya, Sato, Taku, Ohta, Haruhisa, Nakamura, Motoaki, Kato, Nobumasa, Hashimoto, Ryu-Ichiro, Di Martino, Adriana, Aoki, Yuta Y
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7753051/
https://www.ncbi.nlm.nih.gov/pubmed/33381756
http://dx.doi.org/10.1093/braincomms/fcaa186
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author Itahashi, Takashi
Fujino, Junya
Sato, Taku
Ohta, Haruhisa
Nakamura, Motoaki
Kato, Nobumasa
Hashimoto, Ryu-Ichiro
Di Martino, Adriana
Aoki, Yuta Y
author_facet Itahashi, Takashi
Fujino, Junya
Sato, Taku
Ohta, Haruhisa
Nakamura, Motoaki
Kato, Nobumasa
Hashimoto, Ryu-Ichiro
Di Martino, Adriana
Aoki, Yuta Y
author_sort Itahashi, Takashi
collection PubMed
description Symptoms of autism spectrum disorder and attention-deficit/hyperactivity disorder often co-occur. Among these, sensory impairment, which is a core diagnostic feature of autism spectrum disorder, is often observed in children with attention-deficit/hyperactivity disorder. However, the underlying mechanisms of symptoms that are shared across disorders remain unknown. To examine the neural correlates of sensory symptoms that are associated with autism spectrum disorder and attention-deficit/hyperactivity disorder, we analysed resting-state functional MRI data obtained from 113 people with either autism spectrum disorder or attention-deficit/hyperactivity disorder (n = 78 autism spectrum disorder, mean age = 29.5; n = 35 attention-deficit/hyperactivity disorder, mean age = 31.2) and 96 neurotypical controls (mean age = 30.6, range: 20–55 years) using a cross-sectional study design. First, we used a multi-dimensional approach to examine intrinsic brain functional connectivity related to sensory symptoms in four domains (i.e. low registration, sensation seeking, sensory sensitivity and sensation avoidance), after controlling for age, handedness and head motion. Then, we used a partial least squares correlation to examine the link between sensory symptoms related to intrinsic brain functional connectivity and neurodevelopmental symptoms measured using the Autism Spectrum Quotient and Conners’ Adult Attention-Deficit/Hyperactivity Disorder Rating Scale, regardless of diagnosis. To test whether observed associations were specific to sensory symptoms related to intrinsic brain functional connectivity, we conducted a control analysis using a bootstrap framework. The results indicated that transdiagnostic yet distinct intrinsic brain functional connectivity neural bases varied according to the domain of the examined sensory symptom. Partial least squares correlation analysis revealed two latent components (latent component 1: q < 0.001 and latent component 2: q < 0.001). For latent component 1, a set of intrinsic brain functional connectivity was predominantly associated with neurodevelopmental symptom-related composite score (r = 0.64, P < 0.001), which was significantly correlated with Conners’ Adult Attention-Deficit/Hyperactivity Disorder Rating Scale total T scores (r = −0.99, q < 0.001). For latent component 2, another set of intrinsic brain functional connectivity was positively associated with neurodevelopmental symptom-related composite score (r = 0.58, P < 0.001), which was eventually positively associated with Autism Spectrum Quotient total scores (r = 0.92, q < 0.001). The bootstrap analysis showed that the relationship between intrinsic brain functional connectivity and neurodevelopmental symptoms was relative to sensory symptom-related intrinsic brain functional connectivity (latent component 1: P = 0.003 and latent component 2: P < 0.001). The current results suggest that sensory symptoms in individuals with autism spectrum disorder and those with attention-deficit/hyperactivity disorder have shared neural correlates. The neural correlates of the sensory symptoms were associated with the severity of both autism spectrum disorder and attention-deficit/hyperactivity disorder symptoms, regardless of diagnosis.
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spelling pubmed-77530512020-12-29 Neural correlates of shared sensory symptoms in autism and attention-deficit/hyperactivity disorder Itahashi, Takashi Fujino, Junya Sato, Taku Ohta, Haruhisa Nakamura, Motoaki Kato, Nobumasa Hashimoto, Ryu-Ichiro Di Martino, Adriana Aoki, Yuta Y Brain Commun Original Article Symptoms of autism spectrum disorder and attention-deficit/hyperactivity disorder often co-occur. Among these, sensory impairment, which is a core diagnostic feature of autism spectrum disorder, is often observed in children with attention-deficit/hyperactivity disorder. However, the underlying mechanisms of symptoms that are shared across disorders remain unknown. To examine the neural correlates of sensory symptoms that are associated with autism spectrum disorder and attention-deficit/hyperactivity disorder, we analysed resting-state functional MRI data obtained from 113 people with either autism spectrum disorder or attention-deficit/hyperactivity disorder (n = 78 autism spectrum disorder, mean age = 29.5; n = 35 attention-deficit/hyperactivity disorder, mean age = 31.2) and 96 neurotypical controls (mean age = 30.6, range: 20–55 years) using a cross-sectional study design. First, we used a multi-dimensional approach to examine intrinsic brain functional connectivity related to sensory symptoms in four domains (i.e. low registration, sensation seeking, sensory sensitivity and sensation avoidance), after controlling for age, handedness and head motion. Then, we used a partial least squares correlation to examine the link between sensory symptoms related to intrinsic brain functional connectivity and neurodevelopmental symptoms measured using the Autism Spectrum Quotient and Conners’ Adult Attention-Deficit/Hyperactivity Disorder Rating Scale, regardless of diagnosis. To test whether observed associations were specific to sensory symptoms related to intrinsic brain functional connectivity, we conducted a control analysis using a bootstrap framework. The results indicated that transdiagnostic yet distinct intrinsic brain functional connectivity neural bases varied according to the domain of the examined sensory symptom. Partial least squares correlation analysis revealed two latent components (latent component 1: q < 0.001 and latent component 2: q < 0.001). For latent component 1, a set of intrinsic brain functional connectivity was predominantly associated with neurodevelopmental symptom-related composite score (r = 0.64, P < 0.001), which was significantly correlated with Conners’ Adult Attention-Deficit/Hyperactivity Disorder Rating Scale total T scores (r = −0.99, q < 0.001). For latent component 2, another set of intrinsic brain functional connectivity was positively associated with neurodevelopmental symptom-related composite score (r = 0.58, P < 0.001), which was eventually positively associated with Autism Spectrum Quotient total scores (r = 0.92, q < 0.001). The bootstrap analysis showed that the relationship between intrinsic brain functional connectivity and neurodevelopmental symptoms was relative to sensory symptom-related intrinsic brain functional connectivity (latent component 1: P = 0.003 and latent component 2: P < 0.001). The current results suggest that sensory symptoms in individuals with autism spectrum disorder and those with attention-deficit/hyperactivity disorder have shared neural correlates. The neural correlates of the sensory symptoms were associated with the severity of both autism spectrum disorder and attention-deficit/hyperactivity disorder symptoms, regardless of diagnosis. Oxford University Press 2020-11-02 /pmc/articles/PMC7753051/ /pubmed/33381756 http://dx.doi.org/10.1093/braincomms/fcaa186 Text en © The Author(s) (2020). Published by Oxford University Press on behalf of the Guarantors of Brain. 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Itahashi, Takashi
Fujino, Junya
Sato, Taku
Ohta, Haruhisa
Nakamura, Motoaki
Kato, Nobumasa
Hashimoto, Ryu-Ichiro
Di Martino, Adriana
Aoki, Yuta Y
Neural correlates of shared sensory symptoms in autism and attention-deficit/hyperactivity disorder
title Neural correlates of shared sensory symptoms in autism and attention-deficit/hyperactivity disorder
title_full Neural correlates of shared sensory symptoms in autism and attention-deficit/hyperactivity disorder
title_fullStr Neural correlates of shared sensory symptoms in autism and attention-deficit/hyperactivity disorder
title_full_unstemmed Neural correlates of shared sensory symptoms in autism and attention-deficit/hyperactivity disorder
title_short Neural correlates of shared sensory symptoms in autism and attention-deficit/hyperactivity disorder
title_sort neural correlates of shared sensory symptoms in autism and attention-deficit/hyperactivity disorder
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7753051/
https://www.ncbi.nlm.nih.gov/pubmed/33381756
http://dx.doi.org/10.1093/braincomms/fcaa186
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