Dorsal striatal functional connectivity and repetitive behaviour dimensions in children and youth with neurodevelopmental disorders.

ADHD Dorsal striatal functional connectivity NDD OCD autism repetitive behaviour

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:
22 Nov 2023
Historique:
received: 01 02 2022
revised: 20 10 2023
accepted: 30 10 2023
medline: 25 11 2023
pubmed: 25 11 2023
entrez: 24 11 2023
Statut: aheadofprint

Résumé

Impairing repetitive behaviours are one of the core diagnostic symptoms in autism spectrum disorder (ASD) and obsessive-compulsive disorder (OCD), but also manifest in attention-deficit/hyperactivity disorder (ADHD). Although the dorsal striatal circuit has been implicated in repetitive behaviours, extensive heterogeneity and cross-diagnostic manifestations in these behaviours have suggested phenotypic and likely neurobiological heterogeneity across neurodevelopmental disorders (NDDs). Intrinsic dorsal striatal functional connectivity in three NDDs (ASD, OCD, and ADHD) and typically developing controls (TD) were examined in a large single-cohort sample (N=412). To learn how diagnostic labels and overlapping behaviours manifest in dorsal striatal functional connectivity measured with fMRI, the main and interaction effects of diagnosis and behaviour were examined in 8 models (2 seed functional connectivity [caudate and putamen] x 4 sub-behavioural domains [sameness/ritualistic, self-injury, stereotypy, compulsions]). The OCD group demonstrated distinctive patterns in visual and visuo-motor coordination regions compared to other diagnostic groups. Lower-order repetitive behaviours (self-injury and stereotypy) manifesting across all participants were implicated in regions involved in motor and cognitive control, although the findings did not survive multiple comparisons, suggesting heterogeneity in these behavioural domains. An interaction between self-injurious behaviour and ADHD diagnosis were observed on the caudate-cerebellum functional connectivity. These findings confirmed high heterogeneity and overlapping behavioural manifestations in NDDs and their complex underlying neural mechanisms. A call for diagnosis-free symptom measures that can capture not only observable symptoms and severity across NDDs but also the underlying functions and motivations of such behaviours across diagnoses is needed.

Sections du résumé

BACKGROUND BACKGROUND
Impairing repetitive behaviours are one of the core diagnostic symptoms in autism spectrum disorder (ASD) and obsessive-compulsive disorder (OCD), but also manifest in attention-deficit/hyperactivity disorder (ADHD). Although the dorsal striatal circuit has been implicated in repetitive behaviours, extensive heterogeneity and cross-diagnostic manifestations in these behaviours have suggested phenotypic and likely neurobiological heterogeneity across neurodevelopmental disorders (NDDs).
METHODS METHODS
Intrinsic dorsal striatal functional connectivity in three NDDs (ASD, OCD, and ADHD) and typically developing controls (TD) were examined in a large single-cohort sample (N=412). To learn how diagnostic labels and overlapping behaviours manifest in dorsal striatal functional connectivity measured with fMRI, the main and interaction effects of diagnosis and behaviour were examined in 8 models (2 seed functional connectivity [caudate and putamen] x 4 sub-behavioural domains [sameness/ritualistic, self-injury, stereotypy, compulsions]).
RESULTS RESULTS
The OCD group demonstrated distinctive patterns in visual and visuo-motor coordination regions compared to other diagnostic groups. Lower-order repetitive behaviours (self-injury and stereotypy) manifesting across all participants were implicated in regions involved in motor and cognitive control, although the findings did not survive multiple comparisons, suggesting heterogeneity in these behavioural domains. An interaction between self-injurious behaviour and ADHD diagnosis were observed on the caudate-cerebellum functional connectivity.
CONCLUSIONS CONCLUSIONS
These findings confirmed high heterogeneity and overlapping behavioural manifestations in NDDs and their complex underlying neural mechanisms. A call for diagnosis-free symptom measures that can capture not only observable symptoms and severity across NDDs but also the underlying functions and motivations of such behaviours across diagnoses is needed.

Identifiants

DOI: 10.1016/j.bpsc.2023.10.014 PMID: 38000717
pubmed: 38000717
pii: S2451-9022(23)00313-0
doi: 10.1016/j.bpsc.2023.10.014
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2023. Published by Elsevier Inc.

Auteurs

Eun Jung Choi (EJ)

Autism Research Centre, Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, ON, Canada; Neurosciences & Mental Health, Research Institute, The Hospital for Sick Children, Toronto, Canada; Department of Psychology, Western University, London, ON, Canada. Electronic address: echoi@hollandbloorview.ca.

Marlee M Vandewouw (MM)

Autism Research Centre, Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, ON, Canada; Neurosciences & Mental Health, Research Institute, The Hospital for Sick Children, Toronto, Canada; Diagnostic Imaging, The Hospital for Sick Children, Toronto, ON, Canada; Institute of Biomedical Engineering, University of Toronto, Toronto, ON, Canada.

Margot J Taylor (MJ)

Neurosciences & Mental Health, Research Institute, The Hospital for Sick Children, Toronto, Canada; Diagnostic Imaging, The Hospital for Sick Children, Toronto, ON, Canada; Departments of Psychology and Medical Imaging, University of Toronto, Toronto, ON, Canada.

Ryan A Stevenson (RA)

Department of Psychology, Western University, London, ON, Canada; Brain and Mind Institute, Western University, London, ON, Canada.

Paul D Arnold (PD)

Mathison Centre for Mental Health Research & Education, Hotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada.

Jessica Brian (J)

Autism Research Centre, Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, ON, Canada; Department of Paediatrics, University of Toronto, Toronto, ON, Canada.

Jennifer Crosbie (J)

Neurosciences & Mental Health, Research Institute, The Hospital for Sick Children, Toronto, Canada; Department of Psychiatry, University of Toronto, Toronto, ON, Canada.

Elizabeth Kelley (E)

Department of Psychology and Centre for Neuroscience Studies, Queens' University, Kingston, ON, Canada; Department of Psychiatry, Queen's University, Kingston, ON, Canada.

Xudong Liu (X)

Department of Psychiatry, Queen's University, Kingston, ON, Canada.

Jessica Jones (J)

Department of Psychiatry, Queen's University, Kingston, ON, Canada.

Meng-Chuan Lai (MC)

Neurosciences & Mental Health, Research Institute, The Hospital for Sick Children, Toronto, Canada; Department of Psychiatry, University of Toronto, Toronto, ON, Canada; 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, ON, Canada; Autism Research Centre, Department of Psychiatry, University of Cambridge, Cambridge, UK; Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan.

Russell J Schachar (RJ)

Neurosciences & Mental Health, Research Institute, The Hospital for Sick Children, Toronto, Canada; Department of Psychiatry, University of Toronto, Toronto, ON, Canada.

Jason P Lerch (JP)

Mouse Imaging Centre, The Hospital for Sick Children, Toronto, ON, Canada; Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UK; Department of Medical Biophysics, University of Toronto, Toronto, ON, Canada.

Evdokia Anagnostou (E)

Autism Research Centre, Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, ON, Canada; Neurosciences & Mental Health, Research Institute, The Hospital for Sick Children, Toronto, Canada; Department of Paediatrics, University of Toronto, Toronto, ON, Canada.

Classifications MeSH