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Shared and Distinct Patterns of Functional Connectivity to Emotional Faces in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Children

Impairments in emotional face processing are demonstrated by individuals with neurodevelopmental disorders (NDDs), including autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD), which is associated with altered emotion processing networks. Despite accumulating evidence...

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Autores principales: Safar, Kristina, Vandewouw, Marlee M., Pang, Elizabeth W., de Villa, Kathrina, Crosbie, Jennifer, Schachar, Russell, Iaboni, Alana, Georgiades, Stelios, Nicolson, Robert, Kelley, Elizabeth, Ayub, Muhammed, Lerch, Jason P., Anagnostou, Evdokia, Taylor, Margot J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8959934/
https://www.ncbi.nlm.nih.gov/pubmed/35356352
http://dx.doi.org/10.3389/fpsyg.2022.826527
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author Safar, Kristina
Vandewouw, Marlee M.
Pang, Elizabeth W.
de Villa, Kathrina
Crosbie, Jennifer
Schachar, Russell
Iaboni, Alana
Georgiades, Stelios
Nicolson, Robert
Kelley, Elizabeth
Ayub, Muhammed
Lerch, Jason P.
Anagnostou, Evdokia
Taylor, Margot J.
author_facet Safar, Kristina
Vandewouw, Marlee M.
Pang, Elizabeth W.
de Villa, Kathrina
Crosbie, Jennifer
Schachar, Russell
Iaboni, Alana
Georgiades, Stelios
Nicolson, Robert
Kelley, Elizabeth
Ayub, Muhammed
Lerch, Jason P.
Anagnostou, Evdokia
Taylor, Margot J.
author_sort Safar, Kristina
collection PubMed
description Impairments in emotional face processing are demonstrated by individuals with neurodevelopmental disorders (NDDs), including autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD), which is associated with altered emotion processing networks. Despite accumulating evidence of high rates of diagnostic overlap and shared symptoms between ASD and ADHD, functional connectivity underpinning emotion processing across these two neurodevelopmental disorders, compared to typical developing peers, has rarely been examined. The current study used magnetoencephalography to investigate whole-brain functional connectivity during the presentation of happy and angry faces in 258 children (5–19 years), including ASD, ADHD and typically developing (TD) groups to determine possible differences in emotion processing. Data-driven clustering was also applied to determine whether the patterns of connectivity differed among diagnostic groups. We found reduced functional connectivity in the beta band in ASD compared to TD, and a further reduction in the ADHD group compared to the ASD and the TD groups, across emotions. A group-by-emotion interaction in the gamma frequency band was also observed. Greater connectivity to happy compared to angry faces was found in the ADHD and TD groups, while the opposite pattern was seen in ASD. Data-driven subgrouping identified two distinct subgroups: NDD-dominant and TD-dominant; these subgroups demonstrated emotion- and frequency-specific differences in connectivity. Atypicalities in specific brain networks were strongly correlated with the severity of diagnosis-specific symptoms. Functional connectivity strength in the beta network was negatively correlated with difficulties in attention; in the gamma network, functional connectivity strength to happy faces was positively correlated with adaptive behavioural functioning, but in contrast, negatively correlated to angry faces. Our findings establish atypical frequency- and emotion-specific patterns of functional connectivity between NDD and TD children. Data-driven clustering further highlights a high degree of comorbidity and symptom overlap between the ASD and ADHD children.
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spelling pubmed-89599342022-03-29 Shared and Distinct Patterns of Functional Connectivity to Emotional Faces in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Children Safar, Kristina Vandewouw, Marlee M. Pang, Elizabeth W. de Villa, Kathrina Crosbie, Jennifer Schachar, Russell Iaboni, Alana Georgiades, Stelios Nicolson, Robert Kelley, Elizabeth Ayub, Muhammed Lerch, Jason P. Anagnostou, Evdokia Taylor, Margot J. Front Psychol Psychology Impairments in emotional face processing are demonstrated by individuals with neurodevelopmental disorders (NDDs), including autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD), which is associated with altered emotion processing networks. Despite accumulating evidence of high rates of diagnostic overlap and shared symptoms between ASD and ADHD, functional connectivity underpinning emotion processing across these two neurodevelopmental disorders, compared to typical developing peers, has rarely been examined. The current study used magnetoencephalography to investigate whole-brain functional connectivity during the presentation of happy and angry faces in 258 children (5–19 years), including ASD, ADHD and typically developing (TD) groups to determine possible differences in emotion processing. Data-driven clustering was also applied to determine whether the patterns of connectivity differed among diagnostic groups. We found reduced functional connectivity in the beta band in ASD compared to TD, and a further reduction in the ADHD group compared to the ASD and the TD groups, across emotions. A group-by-emotion interaction in the gamma frequency band was also observed. Greater connectivity to happy compared to angry faces was found in the ADHD and TD groups, while the opposite pattern was seen in ASD. Data-driven subgrouping identified two distinct subgroups: NDD-dominant and TD-dominant; these subgroups demonstrated emotion- and frequency-specific differences in connectivity. Atypicalities in specific brain networks were strongly correlated with the severity of diagnosis-specific symptoms. Functional connectivity strength in the beta network was negatively correlated with difficulties in attention; in the gamma network, functional connectivity strength to happy faces was positively correlated with adaptive behavioural functioning, but in contrast, negatively correlated to angry faces. Our findings establish atypical frequency- and emotion-specific patterns of functional connectivity between NDD and TD children. Data-driven clustering further highlights a high degree of comorbidity and symptom overlap between the ASD and ADHD children. Frontiers Media S.A. 2022-03-09 /pmc/articles/PMC8959934/ /pubmed/35356352 http://dx.doi.org/10.3389/fpsyg.2022.826527 Text en Copyright © 2022 Safar, Vandewouw, Pang, de Villa, Crosbie, Schachar, Iaboni, Georgiades, Nicolson, Kelley, Ayub, Lerch, Anagnostou and Taylor. 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 Psychology
Safar, Kristina
Vandewouw, Marlee M.
Pang, Elizabeth W.
de Villa, Kathrina
Crosbie, Jennifer
Schachar, Russell
Iaboni, Alana
Georgiades, Stelios
Nicolson, Robert
Kelley, Elizabeth
Ayub, Muhammed
Lerch, Jason P.
Anagnostou, Evdokia
Taylor, Margot J.
Shared and Distinct Patterns of Functional Connectivity to Emotional Faces in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Children
title Shared and Distinct Patterns of Functional Connectivity to Emotional Faces in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Children
title_full Shared and Distinct Patterns of Functional Connectivity to Emotional Faces in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Children
title_fullStr Shared and Distinct Patterns of Functional Connectivity to Emotional Faces in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Children
title_full_unstemmed Shared and Distinct Patterns of Functional Connectivity to Emotional Faces in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Children
title_short Shared and Distinct Patterns of Functional Connectivity to Emotional Faces in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Children
title_sort shared and distinct patterns of functional connectivity to emotional faces in autism spectrum disorder and attention-deficit/hyperactivity disorder children
topic Psychology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8959934/
https://www.ncbi.nlm.nih.gov/pubmed/35356352
http://dx.doi.org/10.3389/fpsyg.2022.826527
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