Brain-charting autism and attention deficit hyperactivity disorder reveals distinct and overlapping neurobiology.

ADHD Neuroimaging autism cortex normative modelling structural MRI

Journal

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

Informations de publication

Date de publication:
09 Aug 2024
Historique:
received: 16 11 2023
revised: 30 05 2024
accepted: 11 07 2024
medline: 12 8 2024
pubmed: 12 8 2024
entrez: 11 8 2024
Statut: aheadofprint

Résumé

Autism and attention deficit hyperactivity disorder (ADHD) are heterogeneous neurodevelopmental conditions with complex underlying neurobiology that is still poorly understood. Despite overlapping presentation and sex-biased prevalence, autism and ADHD are rarely studied together, and sex differences are often overlooked. Population modelling, often referred to as normative modelling, provides a unified framework for studying age-specific and sex-specific divergences in brain development. Here we used population modelling and a large, multi-site neuroimaging dataset (N = 4255 after quality control) to characterise cortical anatomy associated with autism and ADHD, benchmarked against models of average brain development based on a sample of over 75,000 individuals. We also examined sex and age differences, relationship with autistic traits, and explored the co-occurrence of autism and ADHD (autism+ADHD). We observed robust neuroanatomical signatures of both autism and ADHD. Overall, autistic individuals showed greater cortical thickness and volume, that was localised to the superior temporal cortex, whereas individuals with ADHD showed more global increases in cortical thickness, but lower cortical volume and surface area across much of the cortex. The autism+ADHD group displayed a unique pattern of widespread increases in cortical thickness, and certain decreases in surface area. We also found evidence that sex modulates the neuroanatomy of autism but not ADHD, and an age-by-diagnosis interaction for ADHD only. These results indicate distinct cortical differences in autism and ADHD that are differentially impacted by age, sex, and potentially unique patterns related to their co-occurrence.

Sections du résumé

BACKGROUND BACKGROUND
Autism and attention deficit hyperactivity disorder (ADHD) are heterogeneous neurodevelopmental conditions with complex underlying neurobiology that is still poorly understood. Despite overlapping presentation and sex-biased prevalence, autism and ADHD are rarely studied together, and sex differences are often overlooked. Population modelling, often referred to as normative modelling, provides a unified framework for studying age-specific and sex-specific divergences in brain development.
METHODS METHODS
Here we used population modelling and a large, multi-site neuroimaging dataset (N = 4255 after quality control) to characterise cortical anatomy associated with autism and ADHD, benchmarked against models of average brain development based on a sample of over 75,000 individuals. We also examined sex and age differences, relationship with autistic traits, and explored the co-occurrence of autism and ADHD (autism+ADHD).
RESULTS RESULTS
We observed robust neuroanatomical signatures of both autism and ADHD. Overall, autistic individuals showed greater cortical thickness and volume, that was localised to the superior temporal cortex, whereas individuals with ADHD showed more global increases in cortical thickness, but lower cortical volume and surface area across much of the cortex. The autism+ADHD group displayed a unique pattern of widespread increases in cortical thickness, and certain decreases in surface area. We also found evidence that sex modulates the neuroanatomy of autism but not ADHD, and an age-by-diagnosis interaction for ADHD only.
CONCLUSIONS CONCLUSIONS
These results indicate distinct cortical differences in autism and ADHD that are differentially impacted by age, sex, and potentially unique patterns related to their co-occurrence.

Identifiants

DOI: 10.1016/j.biopsych.2024.07.024 PMID: 39128574
pubmed: 39128574
pii: S0006-3223(24)01513-0
doi: 10.1016/j.biopsych.2024.07.024
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024. Published by Elsevier Inc.

Auteurs

Saashi A Bedford (SA)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, CB2 8AH, UK; Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, CB2 0SZ, UK. Electronic address: ajb349@cam.ac.uk.

Meng-Chuan Lai (MC)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, CB2 8AH, UK; The Margaret and Wallace McCain Centre for Child, Youth & Family Mental Health and Azrieli Adult Neurodevelopmental Centre, Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, ON M6J 1H4, Canada; Department of Psychiatry, The Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Psychiatry, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5T 1R8, Canada; Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei 100229, Taiwan.

Michael V Lombardo (MV)

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

Bhismadev Chakrabarti (B)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, CB2 8AH, UK; Centre for Autism, School of Psychology and Clinical Language Sciences, University of Reading, Reading RG6 6ES, UK.

Amber Ruigrok (A)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, CB2 8AH, UK; Division of Psychology and Mental Health, School of Health Sciences, Faculty of Biology, Medicine and Health, University of Manchester.

John Suckling (J)

Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, CB2 0SZ, UK.

Evdokia Anagnostou (E)

Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, Ontario, Canada; Department of Pediatrics, Temerty Faculty of Medicine, University of Toronto, Toronto, Canada.

Jason P Lerch (JP)

Program in Neurosciences and Mental Health, Research Institute, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Mouse Imaging Centre, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, UK.

Margot Taylor (M)

Program in Neurosciences and Mental Health, Research Institute, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Department of Diagnostic Imaging, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.

Rob Nicolson (R)

Department of Psychiatry, University of Western Ontario, London, Ontario, Canada.

Georgiades Stelios (G)

McMaster University, Hamilton, Ontario, Canada.

Jennifer Crosbie (J)

Department of Psychiatry, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5T 1R8, Canada; Program in Neurosciences and Mental Health, Research Institute, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Genetics & Genome Biology, The Hospital for Sick Children, Toronto, Ontario, Canada.

Russell Schachar (R)

Department of Psychiatry, Temerty Faculty of Medicine, University of Toronto, Toronto, ON M5T 1R8, Canada; Program in Neurosciences and Mental Health, Research Institute, Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Genetics & Genome Biology, The Hospital for Sick Children, Toronto, Ontario, Canada.

Elizabeth Kelley (E)

Department of Psychology, Queen's University, Kingston, ON K7L 3N6 Canada; Centre for Neuroscience Studies, Queen's University, Kingston, ON K7L 3N6 Canada; Department of Psychiatry, Queen's University, Kingston, ON K7L 3N6 Canada.

Jessica Jones (J)

Department of Psychology, Queen's University, Kingston, ON K7L 3N6 Canada; Centre for Neuroscience Studies, Queen's University, Kingston, ON K7L 3N6 Canada; Department of Psychiatry, Queen's University, Kingston, ON K7L 3N6 Canada.

Paul D Arnold (PD)

The Mathison Centre for Mental Health Research & Education, Hotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada; Departments of Psychiatry and Medical Genetics, Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada.

Eric Courchesne (E)

Department of Neurosciences, University of California San Diego, La Jolla, California, USA.

Karen Pierce (K)

Department of Neurosciences, University of California San Diego, La Jolla, California, USA.

Lisa T Eyler (LT)

Department of Psychiatry, University of California San Diego, La Jolla, California, USA.

Kathleen Campbell (K)

Department of Neurosciences, University of California San Diego, La Jolla, California, USA.

Cynthia Carter Barnes (CC)

Department of Neurosciences, University of California San Diego, La Jolla, California, USA.

Jakob Seidlitz (J)

Department of Psychiatry, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Child and Adolescent Psychiatry and Behavioral Science, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Lifespan Brain Institute, The Children's Hospital of Philadelphia and Penn Medicine, Philadelphia, PA 19104, USA.

Aaron F Alexander-Bloch (AF)

Department of Psychiatry, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Child and Adolescent Psychiatry and Behavioral Science, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Lifespan Brain Institute, The Children's Hospital of Philadelphia and Penn Medicine, Philadelphia, PA 19104, USA.

Edward T Bullmore (ET)

Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, CB2 0SZ, UK.

Simon Baron-Cohen (S)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, CB2 8AH, UK; Cambridge Lifetime Autism Spectrum Service (CLASS), Cambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UK.

Richard A I Bethlehem (RAI)

Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, CB2 8AH, UK; Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge, CB2 0SZ, UK; Department of Psychology, University of Cambridge, Cambridge, UK.

Classifications MeSH