Subtly altered topological asymmetry of brain structural covariance networks in autism spectrum disorder across 43 datasets from the ENIGMA consortium.


Journal

Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835

Informations de publication

Date de publication:
04 2022
Historique:
received: 03 08 2021
accepted: 14 01 2022
revised: 23 12 2021
pubmed: 10 2 2022
medline: 26 5 2022
entrez: 9 2 2022
Statut: ppublish

Résumé

Small average differences in the left-right asymmetry of cerebral cortical thickness have been reported in individuals with autism spectrum disorder (ASD) compared to typically developing controls, affecting widespread cortical regions. The possible impacts of these regional alterations in terms of structural network effects have not previously been characterized. Inter-regional morphological covariance analysis can capture network connectivity between different cortical areas at the macroscale level. Here, we used cortical thickness data from 1455 individuals with ASD and 1560 controls, across 43 independent datasets of the ENIGMA consortium's ASD Working Group, to assess hemispheric asymmetries of intra-individual structural covariance networks, using graph theory-based topological metrics. Compared with typical features of small-world architecture in controls, the ASD sample showed significantly altered average asymmetry of networks involving the fusiform, rostral middle frontal, and medial orbitofrontal cortex, involving higher randomization of the corresponding right-hemispheric networks in ASD. A network involving the superior frontal cortex showed decreased right-hemisphere randomization. Based on comparisons with meta-analyzed functional neuroimaging data, the altered connectivity asymmetry particularly affected networks that subserve executive functions, language-related and sensorimotor processes. These findings provide a network-level characterization of altered left-right brain asymmetry in ASD, based on a large combined sample. Altered asymmetrical brain development in ASD may be partly propagated among spatially distant regions through structural connectivity.

Identifiants

pubmed: 35136228
doi: 10.1038/s41380-022-01452-7
pii: 10.1038/s41380-022-01452-7
pmc: PMC9126820
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

2114-2125

Subventions

Organisme : NIBIB NIH HHS
ID : P41 EB015922
Pays : United States
Organisme : NICHD NIH HHS
ID : P50 HD105351
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG058854
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH111671
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH117601
Pays : United States
Organisme : NIBIB NIH HHS
ID : U54 EB020403
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH121246
Pays : United States
Organisme : NIMH NIH HHS
ID : K01 MH112774
Pays : United States

Informations de copyright

© 2022. The Author(s).

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Auteurs

Zhiqiang Sha (Z)

Department of Language & Genetics, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands. zhiqiang.sha@mpi.nl.

Daan van Rooij (D)

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

Evdokia Anagnostou (E)

Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital and Department of Pediatrics, University of Toronto, Toronto, ON, Canada.

Celso Arango (C)

Child and Adolescent Psychiatry Department, Institute of Psychiatry and Mental Health, Gregorio Maran General University Hospital, School of Medicine, Universidad Complutense, IiSGM, CIBERSAM, Madrid, Spain.

Guillaume Auzias (G)

Institut de Neurosciences de la Timone, UMR 7289, Aix Marseille Universit, CNRS, Marseille, France.

Marlene Behrmann (M)

Department of Psychology and Neuroscience Institute, Carnegie Mellon University, Pittsburgh, PA, USA.

Boris Bernhardt (B)

McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada.

Sven Bolte (S)

Center of Neurodevelopmental Disorders (KIND), Centre for Psychiatry Research; Department of Women's and Children's Health, Karolinska Institutet & Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden.
Child and Adolescent Psychiatry, Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden.
Curtin Autism Research Group, Curtin School of Allied Health, Curtin University, Perth, WA, Australia.

Geraldo F Busatto (GF)

Laboratory of Psychiatric Neuroimaging (LIM-21), Departamento e Instituto de Psiquiatria, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de Sao Paulo, Sao Paulo, SP, Brazil.

Sara Calderoni (S)

IRCCS Stella Maris Foundation, Pisa, Italy.
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy.

Rosa Calvo (R)

Department of Child and Adolescent Psychiatry and Psychology Hospital Clinic, Psychiatry Unit, Department of Medicine, 2017SGR881, University of Barcelona, IDIBAPS, CIBERSAM, Barcelona, Spain.

Eileen Daly (E)

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

Christine Deruelle (C)

Institut de Neurosciences de la Timone, UMR 7289, Aix Marseille Universit, CNRS, Marseille, France.

Meiyu Duan (M)

BioKnow Health Informatics Lab, College of Computer Science and Technology, and Key Laboratory of Symbolic Computation and Knowledge Engineering of Ministry of Education, Jilin University, Changchun, Jilin, 130012, China.

Fabio Luis Souza Duran (FLS)

Laboratory of Psychiatric Neuroimaging (LIM-21), Departamento e Instituto de Psiquiatria, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de Sao Paulo, Sao Paulo, SP, Brazil.

Sarah Durston (S)

Brain Center Rudolf Magnus, Department of Psychiatry, University Medical Center Utrecht, Utrecht, The Netherlands.

Christine Ecker (C)

Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital, Goethe University Frankfurt am Main, Frankfurt, Germany.
The Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Stefan Ehrlich (S)

Department of Child and Adolescent Psychiatry & Division of Psychological and Social Medicine and Developmental Neurosciences, Faculty of Medicine, TU Dresden, Dresden, Germany.

Damien Fair (D)

Institute of Child Development, Department of Pediatrics, Masonic Institute of the Developing Brain, University of Minnesota, Minneapolis, MN, USA.

Jennifer Fedor (J)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Jacqueline Fitzgerald (J)

Department of Psychiatry, School of Medicine, Trinity College, Dublin, Ireland.
The Trinity College Institute of Neuroscience, Trinity College, Dublin, Ireland.

Dorothea L Floris (DL)

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

Barbara Franke (B)

Department of Human Genetics, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, The Netherlands.
Department of Psychiatry, Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Nijmegen, The Netherlands.

Christine M Freitag (CM)

Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital, Goethe University Frankfurt am Main, Frankfurt, Germany.

Louise Gallagher (L)

Department of Psychiatry, School of Medicine, Trinity College, Dublin, Ireland.
The Trinity College Institute of Neuroscience, Trinity College, Dublin, Ireland.

David C Glahn (DC)

Department of Psychiatry, Boston Children's Hospital and Harvard Medical School, Boston, MA, 02115-5724, USA.
Olin Neuropsychiatric Research Center, Hartford, CT, USA.

Shlomi Haar (S)

Department of Brain Sciences, Imperial College London, London, UK.

Liesbeth Hoekstra (L)

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

Neda Jahanshad (N)

Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Marina del Rey, CA, USA.

Maria Jalbrzikowski (M)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Joost Janssen (J)

Child and Adolescent Psychiatry Department, Institute of Psychiatry and Mental Health, Gregorio Maran General University Hospital, School of Medicine, Universidad Complutense, IiSGM, CIBERSAM, Madrid, Spain.

Joseph A King (JA)

Department of Child and Adolescent Psychiatry & Division of Psychological and Social Medicine and Developmental Neurosciences, Faculty of Medicine, TU Dresden, Dresden, Germany.

Luisa Lazaro (L)

Department of Child and Adolescent Psychiatry and Psychology Hospital Clinic, Psychiatry Unit, Department of Medicine, 2017SGR881, University of Barcelona, IDIBAPS, CIBERSAM, Barcelona, Spain.

Beatriz Luna (B)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

Jane McGrath (J)

Department of Psychiatry, School of Medicine, Trinity College, Dublin, Ireland.
The Trinity College Institute of Neuroscience, Trinity College, Dublin, Ireland.

Sarah E Medland (SE)

Psychiatric Genetics, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia.

Filippo Muratori (F)

IRCCS Stella Maris Foundation, Pisa, Italy.
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy.

Declan G M Murphy (DGM)

The Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
Behavioural Genetics Clinic, Adult Autism Service, Behavioural and Developmental Psychiatry Clinical Academic Group, South London and Maudsley Foundation NHS Trust, London, UK.

Janina Neufeld (J)

Center of Neurodevelopmental Disorders (KIND), Centre for Psychiatry Research; Department of Women's and Children's Health, Karolinska Institutet & Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden.

Kirsten O'Hearn (K)

Department of Physiology and Pharmacology, Wake Forest Baptist Medical Center, Winston-Salem, NC, USA.

Bob Oranje (B)

Brain Center Rudolf Magnus, Department of Psychiatry, University Medical Center Utrecht, Utrecht, The Netherlands.

Mara Parellada (M)

Child and Adolescent Psychiatry Department, Institute of Psychiatry and Mental Health, Gregorio Maran General University Hospital, School of Medicine, Universidad Complutense, IiSGM, CIBERSAM, Madrid, Spain.

Jose C Pariente (JC)

Magnetic Resonance Image Core Facility, IDIBAPS (Institut d'Investigacions Biomdiques August Pi i Sunyer), Barcelona, Spain.

Merel C Postema (MC)

Department of Language & Genetics, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands.

Karl Lundin Remnelius (KL)

Center of Neurodevelopmental Disorders (KIND), Centre for Psychiatry Research; Department of Women's and Children's Health, Karolinska Institutet & Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden.

Alessandra Retico (A)

National Institute for Nuclear Physics, Pisa Division, Largo B. Pontecorvo 3, Pisa, Italy.

Pedro Gomes Penteado Rosa (PGP)

Laboratory of Psychiatric Neuroimaging (LIM-21), Departamento e Instituto de Psiquiatria, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de Sao Paulo, Sao Paulo, SP, Brazil.

Katya Rubia (K)

Institute of Psychiatry, King's College London, London, UK.

Devon Shook (D)

Brain Center Rudolf Magnus, Department of Psychiatry, University Medical Center Utrecht, Utrecht, The Netherlands.

Kristiina Tammimies (K)

Astrid Lindgren Children's Hospital, Karolinska University Hospital, Region, Stockholm, Sweden.
Center of Neurodevelopmental Disorders (KIND), Centre for Psychiatry Research; Department of Womens and Childrens Health, Karolinska Institutet and Child and Adolescent Psychiatry, Stockholm Health Care Services, Stockholm County Council, Stockholm, Sweden.

Margot J Taylor (MJ)

Diagnostic Imaging, The Hospital for Sick Children, and Department of Medical Imaging, University of Toronto, Toronto, ON, Canada.

Michela Tosetti (M)

IRCCS Stella Maris Foundation, Pisa, Italy.

Gregory L Wallace (GL)

Department of Speech, Language, and Hearing Sciences, The George Washington University, Washington, DC, USA.

Fengfeng Zhou (F)

BioKnow Health Informatics Lab, College of Computer Science and Technology, and Key Laboratory of Symbolic Computation and Knowledge Engineering of Ministry of Education, Jilin University, Changchun, Jilin, 130012, China.

Paul M Thompson (PM)

Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Marina del Rey, CA, USA.

Simon E Fisher (SE)

Department of Language & Genetics, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands.
Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands.

Jan K Buitelaar (JK)

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

Clyde Francks (C)

Department of Language & Genetics, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands. clyde.francks@mpi.nl.
Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands. clyde.francks@mpi.nl.

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