Atypical functional connectome hierarchy in autism

• Published in: Nature communications Vol. 10; no. 1; p. 1022
• Main Authors: Hong, Seok-Jun, Vos de Wael, Reinder, Bethlehem, Richard A. I., Lariviere, Sara, Paquola, Casey, Valk, Sofie L., Milham, Michael P., Di Martino, Adriana, Margulies, Daniel S., Smallwood, Jonathan, Bernhardt, Boris C.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 04.03.2019; Nature Publishing Group; Nature Portfolio
• Subjects: 59/36; 59/57; 631/378/116/1925; 631/378/1689/1373; 631/378/2649; 631/378/3920; Adolescent; Adult; Autism; Autistic Disorder - diagnostic imaging; Autistic Disorder - pathology; Autistic Disorder - physiopathology; Cerebral Cortex - pathology; Cerebral Cortex - physiopathology; Cognition; Cognitive ability; Cognitive Sciences; Connectivity analysis; Connectome; Disruption; Female; Functional magnetic resonance imaging; Humanities and Social Sciences; Humans; Information processing; Life Sciences; Magnetic resonance imaging; Magnetic Resonance Imaging - methods; Male; Motion; multidisciplinary; Nerve Net - pathology; Nerve Net - physiopathology; Neurons and Cognition; Science; Science (multidisciplinary); Sensory integration; Signs and symptoms; Social Behavior Disorders - pathology; Social Behavior Disorders - physiopathology; Social interactions; Young Adult
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-019-08944-1

One paradox of autism is the co-occurrence of deficits in sensory and higher-order socio-cognitive processing. Here, we examined whether these phenotypical patterns may relate to an overarching system-level imbalance—specifically a disruption in macroscale hierarchy affecting integration and segregation of unimodal and transmodal networks. Combining connectome gradient and stepwise connectivity analysis based on task-free functional magnetic resonance imaging (fMRI), we demonstrated atypical connectivity transitions between sensory and higher-order default mode regions in a large cohort of individuals with autism relative to typically-developing controls. Further analyses indicated that reduced differentiation related to perturbed stepwise connectivity from sensory towards transmodal areas, as well as atypical long-range rich-club connectivity. Supervised pattern learning revealed that hierarchical features predicted deficits in social cognition and low-level behavioral symptoms, but not communication-related symptoms. Our findings provide new evidence for imbalances in network hierarchy in autism, which offers a parsimonious reference frame to consolidate its diverse features. Autism spectrum disorder (ASD) is associated with symptoms ranging from sensory hypersensitivity to social difficulties. Here, the authors provide evidence of atypical connectivity transitions between sensory and higher-order cortical areas in people with ASD, which could underlie the diverse symptoms.