Connectome-wide Mega-analysis Reveals Robust Patterns of Atypical Functional Connectivity in Autism.


Journal

Biological psychiatry
ISSN: 1873-2402
Titre abrégé: Biol Psychiatry
Pays: United States
ID NLM: 0213264

Informations de publication

Date de publication:
01 07 2023
Historique:
received: 06 06 2022
revised: 19 11 2022
accepted: 08 12 2022
medline: 16 6 2023
pubmed: 17 3 2023
entrez: 16 3 2023
Statut: ppublish

Résumé

Neuroimaging studies of functional connectivity (FC) in autism have been hampered by small sample sizes and inconsistent findings with regard to whether connectivity is increased or decreased in individuals with autism, whether these alterations affect focal systems or reflect a brain-wide pattern, and whether these are age and/or sex dependent. The study included resting-state functional magnetic resonance imaging and clinical data from the EU-AIMS LEAP (European Autism Interventions Longitudinal European Autism Project) and the ABIDE (Autism Brain Imaging Data Exchange) 1 and 2 initiatives of 1824 (796 with autism) participants with an age range of 5-58 years. Between-group differences in FC were assessed, and associations between FC and clinical symptom ratings were investigated through canonical correlation analysis. Autism was associated with a brainwide pattern of hypo- and hyperconnectivity. Hypoconnectivity predominantly affected sensory and higher-order attentional networks and correlated with social impairments, restrictive and repetitive behavior, and sensory processing. Hyperconnectivity was observed primarily between the default mode network and the rest of the brain and between cortical and subcortical systems. This pattern was strongly associated with social impairments and sensory processing. Interactions between diagnosis and age or sex were not statistically significant. The FC alterations observed, which primarily involve hypoconnectivity of primary sensory and attention networks and hyperconnectivity of the default mode network and subcortex with the rest of the brain, do not appear to be age or sex dependent and correlate with clinical dimensions of social difficulties, restrictive and repetitive behaviors, and alterations in sensory processing. These findings suggest that the observed connectivity alterations are stable, trait-like features of autism that are related to the main symptom domains of the condition.

Sections du résumé

BACKGROUND
Neuroimaging studies of functional connectivity (FC) in autism have been hampered by small sample sizes and inconsistent findings with regard to whether connectivity is increased or decreased in individuals with autism, whether these alterations affect focal systems or reflect a brain-wide pattern, and whether these are age and/or sex dependent.
METHODS
The study included resting-state functional magnetic resonance imaging and clinical data from the EU-AIMS LEAP (European Autism Interventions Longitudinal European Autism Project) and the ABIDE (Autism Brain Imaging Data Exchange) 1 and 2 initiatives of 1824 (796 with autism) participants with an age range of 5-58 years. Between-group differences in FC were assessed, and associations between FC and clinical symptom ratings were investigated through canonical correlation analysis.
RESULTS
Autism was associated with a brainwide pattern of hypo- and hyperconnectivity. Hypoconnectivity predominantly affected sensory and higher-order attentional networks and correlated with social impairments, restrictive and repetitive behavior, and sensory processing. Hyperconnectivity was observed primarily between the default mode network and the rest of the brain and between cortical and subcortical systems. This pattern was strongly associated with social impairments and sensory processing. Interactions between diagnosis and age or sex were not statistically significant.
CONCLUSIONS
The FC alterations observed, which primarily involve hypoconnectivity of primary sensory and attention networks and hyperconnectivity of the default mode network and subcortex with the rest of the brain, do not appear to be age or sex dependent and correlate with clinical dimensions of social difficulties, restrictive and repetitive behaviors, and alterations in sensory processing. These findings suggest that the observed connectivity alterations are stable, trait-like features of autism that are related to the main symptom domains of the condition.

Identifiants

pubmed: 36925414
pii: S0006-3223(22)01852-2
doi: 10.1016/j.biopsych.2022.12.018
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

29-39

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Auteurs

Iva Ilioska (I)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands; Turner Institute for Brain and Mental Health, School of Psychological Science, and Monash Biomedical Imaging, Monash University, Melbourne, Victoria, Australia. Electronic address: i.ilioska@donders.ru.nl.

Marianne Oldehinkel (M)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands; Turner Institute for Brain and Mental Health, School of Psychological Science, and Monash Biomedical Imaging, Monash University, Melbourne, Victoria, Australia.

Alberto Llera (A)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands.

Sidhant Chopra (S)

Turner Institute for Brain and Mental Health, School of Psychological Science, and Monash Biomedical Imaging, Monash University, Melbourne, Victoria, Australia.

Tristan Looden (T)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands.

Roselyne Chauvin (R)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands; Department of Neurology, Washington University School of Medicine, St. Louis, Missouri.

Daan Van Rooij (D)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands.

Dorothea L Floris (DL)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands; Methods of Plasticity Research, Department of Psychology, University of Zurich, Zurich, Switzerland.

Julian Tillmann (J)

Department of Psychology, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom; Roche Pharma Research and Early Development, Neuroscience and Rare Diseases, Roche Innovation Center Basel, F. Hoffmann-La Roche Ltd., Basel, Switzerland.

Carolin Moessnang (C)

Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty, University of Heidelberg, Mannheim, Germany.

Tobias Banaschewski (T)

Department of Child and Adolescent Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany.

Rosemary J Holt (RJ)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom.

Eva Loth (E)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.

Tony Charman (T)

Department of Psychology, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.

Declan G M Murphy (DGM)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.

Christine Ecker (C)

Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom; Department of Child and Adolescent Psychiatry, University Hospital, Goethe University, Frankfurt am Main, Germany.

Maarten Mennes (M)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands.

Christian F Beckmann (CF)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands; Centre for Functional MRI of the Brain, University of Oxford, Oxford, United Kingdom.

Alex Fornito (A)

Turner Institute for Brain and Mental Health, School of Psychological Science, and Monash Biomedical Imaging, Monash University, Melbourne, Victoria, Australia.

Jan K Buitelaar (JK)

Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre, Nijmegen, the Netherlands; Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, the Netherlands.

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