A convergent structure–function substrate of cognitive imbalances in autism

Author:

Hong Seok-Jun12345ORCID,Mottron Laurent6ORCID,Park Bo-yong1237ORCID,Benkarim Oualid12ORCID,Valk Sofie L128910ORCID,Paquola Casey129,Larivière Sara12ORCID,Vos de Wael Reinder12ORCID,Degré-Pelletier Janie1211ORCID,Soulieres Isabelle11ORCID,Ramphal Bruce12ORCID,Margolis Amy12ORCID,Milham Michael513ORCID,Di Martino Adriana14ORCID,Bernhardt Boris C12ORCID

Affiliation:

1. Multimodal Imaging and Connectome Analysis Laboratory , , 3801 University Street, Montreal, Quebec H3A2B4, Canada

2. McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery and Montreal Neurological Institute and Hospital, McGill University , , 3801 University Street, Montreal, Quebec H3A2B4, Canada

3. Center for Neuroscience Imaging Research, Institute for Basic Science, Sungkyunkwan University , Seobu-ro 2066, Jangan-gu, Suwon 16419, South Korea

4. Department of Biomedical Engineering, Sungkyunkwan University , Seobu-ro 2066, Jangan-gu, Suwon 16419, South Korea

5. Center for the Developing Brain, Child Mind Institute , 101 East 56th Street, New York, NY 10022, United States

6. Centre de Recherche du CIUSSSNIM and Department of Psychiatry and Addictology, Université de Montréal , 7070 boulevard Perras, Montréal, Quebec H1E 1A4, Canada

7. Department of Data Science , Inha Univerisity, Incheon 22212, South Korea

8. Otto Hahn group Cognitive neurogenetics, Max Planck Institute for Human Cognitive and Brain Sciences , Stephanstraβe 1A. Leipzig D-04103, Germany

9. Institute of Neuroscience and Medicine , Research Centre Wilhelm-Johnen-Strasse, Jülich 52425, Germany

10. Institute of Systems Neuroscience , Heinrich Heine University, Moorenstr. 5, Düsseldorf 40225, Germany

11. Department of Psychology , Université du Québec à Montréal, 100 rue Sherbrooke Ouest, Montréal, Québec H2X 3P2, Canada

12. Department of Psychiatry , The New York State Psychiatric Institute and the College of Physicians Surgeons, Columbia University, 1051 Riverside Drive, New York, NY 10032, United States

13. Center for Biomedical Imaging and Neuromodulation , Nathan Kline Institute, 140 Old Orangeburg Road, Orangeburg, NY 10962, United States

14. Autism Center , Child Mind Institute, 101 East 56th Street, New York, NY 10022, United States

Abstract

Abstract Background Autism spectrum disorder (ASD) is a common neurodevelopmental diagnosis showing substantial phenotypic heterogeneity. A leading example can be found in verbal and nonverbal cognitive skills, which vary from elevated to impaired compared with neurotypical individuals. Moreover, deficits in verbal profiles often coexist with normal or superior performance in the nonverbal domain. Methods To study brain substrates underlying cognitive imbalance in ASD, we capitalized categorical and dimensional IQ profiling as well as multimodal neuroimaging. Results IQ analyses revealed a marked verbal to nonverbal IQ imbalance in ASD across 2 datasets (Dataset-1: 155 ASD, 151 controls; Dataset-2: 270 ASD, 490 controls). Neuroimaging analysis in Dataset-1 revealed a structure–function substrate of cognitive imbalance, characterized by atypical cortical thickening and altered functional integration of language networks alongside sensory and higher cognitive areas. Conclusion Although verbal and nonverbal intelligence have been considered as specifiers unrelated to autism diagnosis, our results indicate that intelligence disparities are accentuated in ASD and reflected by a consistent structure–function substrate affecting multiple brain networks. Our findings motivate the incorporation of cognitive imbalances in future autism research, which may help to parse the phenotypic heterogeneity and inform intervention-oriented subtyping in ASD.

Funder

Brain and Behavior Research Foundation

Institute for Basic Science

Canadian Institutes of Health Research

National Research Foundation of Korea

Institute for Information and Communications Technology Planning and Evaluation

Artificial Intelligence Convergence Research Center, Inha University

National Institute of Mental Health

National Institute of Environmental Health Sciences

National Institutes of Health

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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