Autism Is Associated With Interindividual Variations of Gray and White Matter Morphology.
Autism
Canonical correlation analysis
Gray matter
Multimodal analysis
Multivariate analysis
White matter
Journal
Biological psychiatry. Cognitive neuroscience and neuroimaging
ISSN: 2451-9030
Titre abrégé: Biol Psychiatry Cogn Neurosci Neuroimaging
Pays: United States
ID NLM: 101671285
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
received:
15
02
2022
revised:
06
08
2022
accepted:
24
08
2022
medline:
10
11
2023
pubmed:
9
9
2022
entrez:
8
9
2022
Statut:
ppublish
Résumé
Although many studies have explored atypicalities in gray matter (GM) and white matter (WM) morphology of autism, most of them relied on unimodal analyses that did not benefit from the likelihood that different imaging modalities may reflect common neurobiology. We aimed to establish brain patterns of modalities that differentiate between individuals with and without autism and explore associations between these brain patterns and clinical measures in the autism group. We studied 183 individuals with autism and 157 nonautistic individuals (age range, 6-30 years) in a large, deeply phenotyped autism dataset (EU-AIMS LEAP [European Autism Interventions-A Multicentre Study for Developing New Medications Longitudinal European Autism Project]). Linked independent component analysis was used to link all participants' GM volume and WM diffusion tensor images, and group comparisons of modality shared variances were examined. Subsequently, we performed univariate and multivariate brain-behavior correlation analyses to separately explore the relationships between brain patterns and clinical profiles. One multimodal pattern was significantly related to autism. This pattern was primarily associated with GM volume in bilateral insula and frontal, precentral and postcentral, cingulate, and caudate areas and co-occurred with altered WM features in the superior longitudinal fasciculus. The brain-behavior correlation analyses showed a significant multivariate association primarily between brain patterns that involved variation of WM and symptoms of restricted and repetitive behavior in the autism group. Our findings demonstrate the assets of integrated analyses of GM and WM alterations to study the brain mechanisms that underpin autism and show that the complex clinical autism phenotype can be interpreted by brain covariation patterns that are spread across the brain involving both cortical and subcortical areas.
Sections du résumé
BACKGROUND
Although many studies have explored atypicalities in gray matter (GM) and white matter (WM) morphology of autism, most of them relied on unimodal analyses that did not benefit from the likelihood that different imaging modalities may reflect common neurobiology. We aimed to establish brain patterns of modalities that differentiate between individuals with and without autism and explore associations between these brain patterns and clinical measures in the autism group.
METHODS
We studied 183 individuals with autism and 157 nonautistic individuals (age range, 6-30 years) in a large, deeply phenotyped autism dataset (EU-AIMS LEAP [European Autism Interventions-A Multicentre Study for Developing New Medications Longitudinal European Autism Project]). Linked independent component analysis was used to link all participants' GM volume and WM diffusion tensor images, and group comparisons of modality shared variances were examined. Subsequently, we performed univariate and multivariate brain-behavior correlation analyses to separately explore the relationships between brain patterns and clinical profiles.
RESULTS
One multimodal pattern was significantly related to autism. This pattern was primarily associated with GM volume in bilateral insula and frontal, precentral and postcentral, cingulate, and caudate areas and co-occurred with altered WM features in the superior longitudinal fasciculus. The brain-behavior correlation analyses showed a significant multivariate association primarily between brain patterns that involved variation of WM and symptoms of restricted and repetitive behavior in the autism group.
CONCLUSIONS
Our findings demonstrate the assets of integrated analyses of GM and WM alterations to study the brain mechanisms that underpin autism and show that the complex clinical autism phenotype can be interpreted by brain covariation patterns that are spread across the brain involving both cortical and subcortical areas.
Identifiants
pubmed: 36075529
pii: S2451-9022(22)00212-9
doi: 10.1016/j.bpsc.2022.08.011
pii:
doi:
Types de publication
Multicenter Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1084-1093Subventions
Organisme : Wellcome Trust
ID : 215573/Z/19/Z
Pays : United Kingdom
Investigateurs
Jan K Buitelaar
(JK)
Jumana Ahmad
(J)
Sara Ambrosino
(S)
Bonnie Auyeung
(B)
Tobias Banaschewski
(T)
Simon Baron-Cohen
(S)
Sarah Baumeister
(S)
Christian F Beckmann
(CF)
Sven Bölte
(S)
Thomas Bourgeron
(T)
Carsten Bours
(C)
Michael Brammer
(M)
Daniel Brandeis
(D)
Claudia Brogna
(C)
Yvette de Bruijn
(Y)
Bhismadev Chakrabarti
(B)
Tony Charman
(T)
Ineke Cornelissen
(I)
Daisy Crawley
(D)
Flavio Dell'Acqua
(F)
Guillaume Dumas
(G)
Sarah Durston
(S)
Christine Ecker
(C)
Jessica Faulkner
(J)
Vincent Frouin
(V)
Pilar Garcés
(P)
David Goyard
(D)
Lindsay Ham
(L)
Hannah Hayward
(H)
Joerg Hipp
(J)
Rosemary Holt
(R)
Mark H Johnson
(MH)
Emily J H Jones
(EJH)
Prantik Kundu
(P)
Meng-Chuan Lai
(MC)
Xavier Liogier d'Ardhuy
(X)
Michael V Lombardo
(MV)
Eva Loth
(E)
David J Lythgoe
(DJ)
René Mandl
(R)
Andre Marquand
(A)
Luke Mason
(L)
Maarten Mennes
(M)
Andreas Meyer-Lindenberg
(A)
Carolin Moessnang
(C)
Nico Mueller
(N)
Declan G M Murphy
(DGM)
Bethany Oakley
(B)
Laurence O'Dwyer
(L)
Marianne Oldehinkel
(M)
Bob Oranje
(B)
Gahan Pandina
(G)
Antonio M Persico
(AM)
Annika Rausch
(A)
Barbara Ruggeri
(B)
Amber Ruigrok
(A)
Jessica Sabet
(J)
Roberto Sacco
(R)
Antonia San José Cáceres
(A)
Emily Simonoff
(E)
Will Spooren
(W)
Julian Tillmann
(J)
Roberto Toro
(R)
Heike Tost
(H)
Jack Waldman
(J)
Steve C R Williams
(SCR)
Caroline Wooldridge
(C)
Iva Ilioska
(I)
Ting Mei
(T)
Marcel P Zwiers
(MP)
Informations de copyright
Copyright © 2022 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.