Imbalanced social-communicative and restricted repetitive behavior subtypes of autism spectrum disorder exhibit different neural circuitry.


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
14 05 2021
Historique:
received: 04 11 2020
accepted: 23 03 2021
entrez: 15 5 2021
pubmed: 16 5 2021
medline: 10 8 2021
Statut: epublish

Résumé

Social-communication (SC) and restricted repetitive behaviors (RRB) are autism diagnostic symptom domains. SC and RRB severity can markedly differ within and between individuals and may be underpinned by different neural circuitry and genetic mechanisms. Modeling SC-RRB balance could help identify how neural circuitry and genetic mechanisms map onto such phenotypic heterogeneity. Here, we developed a phenotypic stratification model that makes highly accurate (97-99%) out-of-sample SC = RRB, SC > RRB, and RRB > SC subtype predictions. Applying this model to resting state fMRI data from the EU-AIMS LEAP dataset (n = 509), we find that while the phenotypic subtypes share many commonalities in terms of intrinsic functional connectivity, they also show replicable differences within some networks compared to a typically-developing group (TD). Specifically, the somatomotor network is hypoconnected with perisylvian circuitry in SC > RRB and visual association circuitry in SC = RRB. The SC = RRB subtype show hyperconnectivity between medial motor and anterior salience circuitry. Genes that are highly expressed within these networks show a differential enrichment pattern with known autism-associated genes, indicating that such circuits are affected by differing autism-associated genomic mechanisms. These results suggest that SC-RRB imbalance subtypes share many commonalities, but also express subtle differences in functional neural circuitry and the genomic underpinnings behind such circuitry.

Identifiants

pubmed: 33990680
doi: 10.1038/s42003-021-02015-2
pii: 10.1038/s42003-021-02015-2
pmc: PMC8121854
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

574

Subventions

Organisme : Wellcome Trust
ID : 098369/Z/12/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/T003057/1
Pays : United Kingdom
Organisme : Department of Health
Pays : United Kingdom
Organisme : CIHR
ID : GSB 171373
Pays : Canada
Organisme : Wellcome Trust
Pays : United Kingdom

Investigateurs

Jumana Ahmad (J)
Sara Ambrosino (S)
Tobias Banaschewski (T)
Carsten Bours (C)
Michael Brammer (M)
Daniel Brandeis (D)
Claudia Brogna (C)
Yvette de Bruijn (Y)
Bhismadev Chakrabarti (B)
Chris Chatham (C)
Ineke Cornelissen (I)
Daisy Crawley (D)
Flavio Dell'Acqua (F)
Jessica Faulkner (J)
Vincent Frouin (V)
Pilar Garcés (P)
David Goyard (D)
Lindsay Ham (L)
Hannah Hayward (H)
Joerg Hipp (J)
Rosemary J Holt (RJ)
Xavier Liogier D'ardhuy (XL)
David J Lythgoe (DJ)
René Mandl (R)
Andre Marquand (A)
Maarten Mennes (M)
Nico Mueller (N)
Bethany Oakley (B)
Laurence O'Dwyer (L)
Bob Oranje (B)
Gahan Pandina (G)
Antonio M Persico (AM)
Barbara Ruggeri (B)
Amber N V Ruigrok (ANV)
Jessica Sabet (J)
Roberto Sacco (R)
Antonia San José Cáceres (ASJ)
Emily Simonoff (E)
Roberto Toro (R)
Heike Tost (H)
Jack Waldman (J)
Steve C R Williams (SCR)
Caroline Wooldridge (C)
Marcel P Zwiers (MP)

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Auteurs

Natasha Bertelsen (N)

Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy.
Center for Mind/Brain Sciences, University of Trento, Rovereto, TN, Italy.

Isotta Landi (I)

Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy.

Richard A I Bethlehem (RAI)

Department of Psychiatry, University of Cambridge, Cambridge, UK.

Jakob Seidlitz (J)

Department of Child and Adolescent Psychiatry and Behavioral Science, Children's Hospital of Philadelphia, Philadelphia, PA, USA.
Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA.

Elena Maria Busuoli (EM)

Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy.
Center for Mind/Brain Sciences, University of Trento, Rovereto, TN, Italy.

Veronica Mandelli (V)

Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy.
Center for Mind/Brain Sciences, University of Trento, Rovereto, TN, Italy.

Eleonora Satta (E)

Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy.

Stavros Trakoshis (S)

Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy.
Department of Psychology, University of Cyprus, Nicosia, Cyprus.

Bonnie Auyeung (B)

Department of Psychology, School of Philosophy, Psychology, and Language Sciences, University of Edinburgh, Edinburgh, UK.
Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.

Prantik Kundu (P)

Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, UK.

Eva Loth (E)

Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Guillaume Dumas (G)

Human Genetics and Cognitive Functions, Institut Pasteur, UMR3571 CNRS, Université de Paris, Paris, France.

Sarah Baumeister (S)

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

Christian F Beckmann (CF)

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

Sven Bölte (S)

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

Thomas Bourgeron (T)

Human Genetics and Cognitive Functions, Institut Pasteur, UMR3571 CNRS, Université de Paris, Paris, France.

Tony Charman (T)

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

Sarah Durston (S)

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

Christine Ecker (C)

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

Rosemary J Holt (RJ)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.

Mark H Johnson (MH)

Department of Psychology, University of Cambridge, Cambridge, UK.

Emily J H Jones (EJH)

Centre for Brain and Cognitive Development, Birkbeck, University of London, Henry Wellcome Building, London, UK.

Luke Mason (L)

Centre for Brain and Cognitive Development, Birkbeck, University of London, Henry Wellcome Building, London, UK.

Andreas Meyer-Lindenberg (A)

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

Carolin Moessnang (C)

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

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 Sciences, Monash University, Victoria, Australia.

Antonio M Persico (AM)

Child and Adolescent Neuropsychiatry Unit, Gaetano Martino University Hospital, University of Messina, Messina, Italy.
University Campus Bio-Medico, Rome, Italy.

Julian Tillmann (J)

Department of Psychology, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
Department of Applied Psychology: Health, Development, Enhancement, and Intervention, University of Vienna, Vienna, Austria.

Steve C R Williams (SCR)

Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Will Spooren (W)

Roche Pharma Research and Early Development, Neuroscience, Ophthalmology and Rare Diseases, Roche Innovation Center Basel, Basel, Switzerland.

Declan G M Murphy (DGM)

Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
Department of Forensic and Neurodevelopmental Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Jan K Buitelaar (JK)

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

Simon Baron-Cohen (S)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.

Meng-Chuan Lai (MC)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK.
The Margaret and Wallace McCain Centre for Child, Youth & Family Mental Health, Azrieli Adult Neurodevelopmental Centre, and Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, Canada.
Department of Psychiatry and Autism Research Unit, The Hospital for Sick Children, Toronto, Canada.
Department of Psychiatry, Faculty of Medicine, University of Toronto, Toronto, Canada.
Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan.

Michael V Lombardo (MV)

Laboratory for Autism and Neurodevelopmental Disorders, Center for Neuroscience and Cognitive Systems @UniTn, Istituto Italiano di Tecnologia, Rovereto, TN, Italy. michael.lombardo@iit.it.
Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK. michael.lombardo@iit.it.

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