Exploring the multidimensional nature of repetitive and restricted behaviors and interests (RRBI) in autism: neuroanatomical correlates and clinical implications.


Journal

Molecular autism
ISSN: 2040-2392
Titre abrégé: Mol Autism
Pays: England
ID NLM: 101534222

Informations de publication

Date de publication:
27 Nov 2023
Historique:
received: 10 04 2023
accepted: 06 11 2023
medline: 29 11 2023
pubmed: 28 11 2023
entrez: 28 11 2023
Statut: epublish

Résumé

Repetitive and restricted behaviors and interests (RRBI) are core symptoms of autism with a complex entity and are commonly categorized into 'motor-driven' and 'cognitively driven'. RRBI symptomatology depends on the individual's clinical environment limiting the understanding of RRBI physiology, particularly their associated neuroanatomical structures. The complex RRBI heterogeneity needs to explore the whole RRBI spectrum by integrating the clinical context [autistic individuals, their relatives and typical developing (TD) individuals]. We hypothesized that different RRBI dimensions would emerge by exploring the whole spectrum of RRBI and that these dimensions are associated with neuroanatomical signatures-involving cortical and subcortical areas. A sample of 792 individuals composed of 267 autistic subjects, their 370 first-degree relatives and 155 TD individuals was enrolled in the study. We assessed the whole patterns of RRBI in each individual by using the Repetitive Behavior Scale-Revised and the Yale-Brown Obsessive Compulsive Scale. We estimated brain volumes using MRI scanner for a subsample of the subjects (n = 152, 42 ASD, 89 relatives and 13 TD). We first investigated the dimensionality of RRBI by performing a principal component analysis on all items of these scales and included all the sampling population. We then explored the relationship between RRBI-derived factors with brain volumes using linear regression models. We identified 3 main factors (with 30.3% of the RRBI cumulative variance): Factor 1 (FA1, 12.7%) reflected mainly the 'motor-driven' RRBI symptoms; Factor 2 and 3 (respectively, 8.8% and 7.9%) gathered mainly Y-BOCS related items and represented the 'cognitively driven' RRBI symptoms. These three factors were significantly associated with the right/left putamen volumes but with opposite effects: FA1 was negatively associated with an increased volume of the right/left putamen conversely to FA2 and FA3 (all uncorrected p < 0.05). FA1 was negatively associated with the left amygdala (uncorrected p < 0.05), and FA2 was positively associated with the left parietal structure (uncorrected p = 0.001). Our results suggested 3 coherent RRBI dimensions involving the putamen commonly and other structures according to the RRBI dimension. The exploration of the putamen's integrative role in RSBI needs to be strengthened in further studies.

Sections du résumé

BACKGROUND BACKGROUND
Repetitive and restricted behaviors and interests (RRBI) are core symptoms of autism with a complex entity and are commonly categorized into 'motor-driven' and 'cognitively driven'. RRBI symptomatology depends on the individual's clinical environment limiting the understanding of RRBI physiology, particularly their associated neuroanatomical structures. The complex RRBI heterogeneity needs to explore the whole RRBI spectrum by integrating the clinical context [autistic individuals, their relatives and typical developing (TD) individuals]. We hypothesized that different RRBI dimensions would emerge by exploring the whole spectrum of RRBI and that these dimensions are associated with neuroanatomical signatures-involving cortical and subcortical areas.
METHOD METHODS
A sample of 792 individuals composed of 267 autistic subjects, their 370 first-degree relatives and 155 TD individuals was enrolled in the study. We assessed the whole patterns of RRBI in each individual by using the Repetitive Behavior Scale-Revised and the Yale-Brown Obsessive Compulsive Scale. We estimated brain volumes using MRI scanner for a subsample of the subjects (n = 152, 42 ASD, 89 relatives and 13 TD). We first investigated the dimensionality of RRBI by performing a principal component analysis on all items of these scales and included all the sampling population. We then explored the relationship between RRBI-derived factors with brain volumes using linear regression models.
RESULTS RESULTS
We identified 3 main factors (with 30.3% of the RRBI cumulative variance): Factor 1 (FA1, 12.7%) reflected mainly the 'motor-driven' RRBI symptoms; Factor 2 and 3 (respectively, 8.8% and 7.9%) gathered mainly Y-BOCS related items and represented the 'cognitively driven' RRBI symptoms. These three factors were significantly associated with the right/left putamen volumes but with opposite effects: FA1 was negatively associated with an increased volume of the right/left putamen conversely to FA2 and FA3 (all uncorrected p < 0.05). FA1 was negatively associated with the left amygdala (uncorrected p < 0.05), and FA2 was positively associated with the left parietal structure (uncorrected p = 0.001).
CONCLUSION CONCLUSIONS
Our results suggested 3 coherent RRBI dimensions involving the putamen commonly and other structures according to the RRBI dimension. The exploration of the putamen's integrative role in RSBI needs to be strengthened in further studies.

Identifiants

pubmed: 38012709
doi: 10.1186/s13229-023-00576-z
pii: 10.1186/s13229-023-00576-z
pmc: PMC10680239
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

45

Subventions

Organisme : Investissements d'Avenir program
ID : ANR-11-IDEX-0004-02, ANR-10-COHO-10-01, ANR-12-SAMA-0014
Organisme : Investissements d'Avenir program
ID : ANR-11-IDEX-0004-02, ANR-10-COHO-10-01, ANR-12-SAMA-0014
Organisme : Investissements d'Avenir program
ID : ANR-11-IDEX-0004-02, ANR-10-COHO-10-01, ANR-12-SAMA-0014

Informations de copyright

© 2023. The Author(s).

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Auteurs

Aline Lefebvre (A)

Fondation Vallée, GHT Paris Sud, Hospital of Child and Adolescent Psychiatry, Gentilly, France. aline.lefebvre@universite-paris-saclay.fr.
UMR 3571 CNRS, Human Genetics and Cognitive Functions, Institut Pasteur, Paris, France. aline.lefebvre@universite-paris-saclay.fr.
UNIACT Neurospin - INSERM UMR 1129, CEA, Saclay, France. aline.lefebvre@universite-paris-saclay.fr.
Department of Adult Psychiatry, Henri Mondor and Albert Chenevier Hospital, Créteil, France. aline.lefebvre@universite-paris-saclay.fr.
Faculty of Medicine, Université Paris-Saclay, Le Kremlin-Bicêtre, France. aline.lefebvre@universite-paris-saclay.fr.

Nicolas Traut (N)

Unité de Neuroanatomie Appliquée et Théorique, Institut Pasteur, Paris, France.

Amandine Pedoux (A)

Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris, France.

Anna Maruani (A)

UMR 3571 CNRS, Human Genetics and Cognitive Functions, Institut Pasteur, Paris, France.
Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris, France.

Anita Beggiato (A)

UMR 3571 CNRS, Human Genetics and Cognitive Functions, Institut Pasteur, Paris, France.
Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris, France.

Monique Elmaleh (M)

Department of Pediatric Radiology, Robert-Debré Hospital, APHP, Paris, France.

David Germanaud (D)

UNIACT Neurospin - INSERM UMR 1129, CEA, Saclay, France.
Department of Clinical Genetics, Robert Debré Hospital, APHP, Paris, France.
Center for Research and Interdisciplinarity (CRI), Université Paris Cité, Paris, France.

Anouck Amestoy (A)

Autism Expert Center, Charles Perrens Hospital, Bordeaux, France.
Fondation FondaMental, French National Science Foundation, Créteil, France.

Myriam Ly-Le Moal (M)

Institut Roche, Boulogne-Billancourt, France.

Christopher Chatham (C)

Roche Pharma Research and Early Development, Neuroscience and Rare Diseases, Roche Innovation Center Basel, F. Hoffmann-La Roche Ltd., Basel, Switzerland.

Lorraine Murtagh (L)

Roche Pharma Research and Early Development, Neuroscience and Rare Diseases, Roche Innovation Center Basel, F. Hoffmann-La Roche Ltd., Basel, Switzerland.

Manuel Bouvard (M)

Autism Expert Center, Charles Perrens Hospital, Bordeaux, France.
Fondation FondaMental, French National Science Foundation, Créteil, France.

Marianne Alisson (M)

Department of Pediatric Radiology, Robert-Debré Hospital, APHP, Paris, France.

Marion Leboyer (M)

Fondation FondaMental, French National Science Foundation, Créteil, France.
Institut National de la Santé et de la Recherche Médicale (INSERM), U955, Institut Mondor de Recherche Biomédicale, Psychiatrie Translationnelle, Créteil, France.

Thomas Bourgeron (T)

UMR 3571 CNRS, Human Genetics and Cognitive Functions, Institut Pasteur, Paris, France.
Université Paris Cité, Paris, France.

Roberto Toro (R)

Unité de Neuroanatomie Appliquée et Théorique, Institut Pasteur, Paris, France.

Guillaume Dumas (G)

Department of Psychiatry, Université de Montreal, CHU Ste Justine Hospital, Montreal, QC, Canada.

Clara Moreau (C)

UMR 3571 CNRS, Human Genetics and Cognitive Functions, Institut Pasteur, Paris, France.
Imaging Genetics Center, Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, Los Angeles, CA, USA.

Richard Delorme (R)

Fondation Vallée, GHT Paris Sud, Hospital of Child and Adolescent Psychiatry, Gentilly, France.
UMR 3571 CNRS, Human Genetics and Cognitive Functions, Institut Pasteur, Paris, France.
Fondation FondaMental, French National Science Foundation, Créteil, France.
Université Paris Cité, Paris, France.

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