Multiscale communication in cortico-cortical networks

• Published in: NeuroImage (Orlando, Fla.) Vol. 243; p. 118546
• Main Authors: Bazinet, Vincent, Vos de Wael, Reinder, Hagmann, Patric, Bernhardt, Boris C., Misic, Bratislav
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.11.2021; Elsevier Limited; Elsevier
• Subjects: Adult; Air transportation industry; Brain; Brain networks; Cerebral Cortex - diagnostic imaging; Circuits; Communication; Connectome; Female; Functional morphology; Hierarchy; Humans; Hypotheses; Magnetic Resonance Imaging; Male; Neighborhoods; Nerve Net - diagnostic imaging; Network communication; Neural networks; Neural Pathways - diagnostic imaging; Structure-function; Structure-function relationships; Substantia alba; White Matter - diagnostic imaging; Young Adult; Hierarchy; Network communication; Connectome; Brain networks; Structure-function
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2021.118546

•We study how communication between brain regions unfolds over multiple topological scales.•The relative centrality of individual brain regions in cortico-cortical connectomes varies across topological scales.•Variations in centrality are shaped by functional diversity.•Cortico-cortical connectomes are organized along a localized-distributed gradient of communication scale preferences.•Communication scale preferences manifest as region- and scale-specific structure-function coupling. Signaling in brain networks unfolds over multiple topological scales. Areas may exchange information over local circuits, encompassing direct neighbours and areas with similar functions, or over global circuits, encompassing distant neighbours with dissimilar functions. Here we study how the organization of cortico-cortical networks mediate localized and global communication by parametrically tuning the range at which signals are transmitted on the white matter connectome. We show that brain regions vary in their preferred communication scale. By investigating the propensity for brain areas to communicate with their neighbors across multiple scales, we naturally reveal their functional diversity: unimodal regions show preference for local communication and multimodal regions show preferences for global communication. We show that these preferences manifest as region- and scale-specific structure-function coupling. Namely, the functional connectivity of unimodal regions emerges from monosynaptic communication in small-scale circuits, while the functional connectivity of transmodal regions emerges from polysynaptic communication in large-scale circuits. Altogether, the present findings reveal that communication preferences are highly heterogeneous across the cortex, shaping regional differences in structure-function coupling.