Myelination and excitation-inhibition balance synergistically shape structure-function coupling across the human cortex

Panagiotis Fotiadis (), Matthew Cieslak, Xiaosong He, Lorenzo Caciagli, Mathieu Ouellet, Theodore D. Satterthwaite, Russell T. Shinohara and Dani S. Bassett ()
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Panagiotis Fotiadis: University of Pennsylvania
Matthew Cieslak: University of Pennsylvania
Xiaosong He: University of Science and Technology of China
Lorenzo Caciagli: University of Pennsylvania
Mathieu Ouellet: University of Pennsylvania
Theodore D. Satterthwaite: University of Pennsylvania
Russell T. Shinohara: University of Pennsylvania
Dani S. Bassett: University of Pennsylvania

Nature Communications, 2023, vol. 14, issue 1, 1-21

Abstract: Abstract Recent work has demonstrated that the relationship between structural and functional connectivity varies regionally across the human brain, with reduced coupling emerging along the sensory-association cortical hierarchy. The biological underpinnings driving this expression, however, remain largely unknown. Here, we postulate that intracortical myelination and excitation-inhibition (EI) balance mediate the heterogeneous expression of structure-function coupling (SFC) and its temporal variance across the cortical hierarchy. We employ atlas- and voxel-based connectivity approaches to analyze neuroimaging data acquired from two groups of healthy participants. Our findings are consistent across six complementary processing pipelines: 1) SFC and its temporal variance respectively decrease and increase across the unimodal-transmodal and granular-agranular gradients; 2) increased myelination and lower EI-ratio are associated with more rigid SFC and restricted moment-to-moment SFC fluctuations; 3) a gradual shift from EI-ratio to myelination as the principal predictor of SFC occurs when traversing from granular to agranular cortical regions. Collectively, our work delivers a framework to conceptualize structure-function relationships in the human brain, paving the way for an improved understanding of how demyelination and/or EI-imbalances induce reorganization in brain disorders.

Date: 2023
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DOI: 10.1038/s41467-023-41686-9

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