Abstract

Autism spectrum disorder (ASD) is a heterogeneous disease that is characterized by abnormalities in social communication and interaction as well as repetitive behaviors and restricted interests. Structural brain imaging has identified significant cortical folding alterations in ASD; however, relatively less known is whether the core symptoms are related to neuroanatomical differences. In this study, we aimed to explore core-symptom-anchored gyrification alterations and their developmental trajectories in ASD. We measured the cortical vertex-wise gyrification index (GI) in 321 patients with ASD (aged 7–39 years) and 350 typically developing (TD) subjects (aged 6–33 years) across 8 sites from the Autism Brain Imaging Data Exchange I (ABIDE I) repository and a longitudinal sample (14 ASD and 7 TD, aged 9–14 years in baseline and 12–18 years in follow-up) from ABIDE II. Compared with TD, the general ASD patients exhibited a mixed pattern of both hypo- and hyper- and different developmental trajectories of gyrification. By parsing the ASD patients into three subgroups based on the subscores of the Autism Diagnostic Interview—Revised (ADI-R) scale, we identified core-symptom-specific alterations in the reciprocal social interaction (RSI), communication abnormalities (CA), and restricted, repetitive, and stereotyped patterns of behavior (RRSB) subgroups. We also showed atypical gyrification patterns and developmental trajectories in the subgroups. Furthermore, we conducted a meta-analysis to locate the core-symptom-anchored brain regions (circuits). In summary, the current study shows that ASD is associated with abnormal cortical folding patterns. Core-symptom-based classification can find more subtle changes in gyrification. These results suggest that cortical folding pattern encodes changes in symptom dimensions, which promotes the understanding of neuroanatomical basis, and clinical utility in ASD.

Highlights

  • Autism spectrum disorder (ASD) is a neurodevelopmental, heterogeneous disease that is characterized by abnormalities in social communication and interaction as well as repetitive behaviors and restricted interests (1)

  • All magnetic resonance imaging (MRI) and phenotypic data are available from the Autism Brain Imaging Data Exchange (ABIDE) repository, which is hosted by the 1000 Functional Connectomes Project/International Neuroimaging Data-sharing Initiative (INDI)

  • We employed the longitudinal data from the University of California Los Angeles (UCLA) in ABIDE II to discover the developmental trajectory of gyrification in ASD

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Summary

Introduction

Autism spectrum disorder (ASD) is a neurodevelopmental, heterogeneous disease that is characterized by abnormalities in social communication and interaction as well as repetitive behaviors and restricted interests (1). Structural brain imaging has revealed prominent morphological and developmental alterations in ASD [for a review, please see (2)]. Relatively less is known whether the core symptoms are related to neuroanatomical differences. One of the most prominent morphological changes in ASD is cortical gyrification. Gyrification refers to the process of cortical convolution (3) and has been actively investigated in ASD due to its role encoding early neurodevelopment (3, 4). Previous studies have reported altered gyrification in different ASD populations (5–7). An early study reported higher gyrification in ASD individuals during childhood and adolescence (8). There is a lack of consistent gyrification alterations across the ASD studies

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