White matter engagement in brain networks assessed by integration of functional and structural connectivity

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2024-11, Vol.302, p.120887, Article 120887
• Main Authors: Li, Muwei, Schilling, Kurt G, Xu, Lyuan, Choi, Soyoung, Gao, Yurui, Zu, Zhongliang, Anderson, Adam W, Ding, Zhaohua, Gore, John C
• Format: Article
• Language: English
• Subjects: Adult; BOLD; Brain - diagnostic imaging; Brain - physiology; Brain architecture; Brain mapping; Brain Mapping - methods; Brain research; Cognitive ability; Engagement; Female; fMRI; Functional anatomy; Functional connectivity; Functional magnetic resonance imaging; Functional morphology; Gray Matter - anatomy & histology; Gray Matter - diagnostic imaging; Gray Matter - physiology; Humans; Magnetic Resonance Imaging - methods; Male; Nerve Net - diagnostic imaging; Nerve Net - physiology; Neural networks; Neural Pathways - diagnostic imaging; Neural Pathways - physiology; Neuroimaging; Neurological diseases; Physiology; Structural connectivity; Structure-function relationships; Substantia alba; Substantia grisea; White matter; White Matter - diagnostic imaging; White Matter - physiology; Young Adult
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2024.120887

•Integrated functional and structural MRI maps white matter engagement.•White matter engagement correlates with other functional and structural properties.•Significant gender differences were found in white matter engagement.•Distribution of white matter engagement varies over time.•White matter engagement shows promise as a biomarker for neurological conditions. Current models of brain networks may potentially be improved by integrating our knowledge of structural connections, within and between circuits, with metrics of functional interactions between network nodes. The former may be obtained from diffusion MRI of white matter (WM), while the latter may be derived by measuring correlations between resting state BOLD signals from pairs of gray matter (GM) regions. From inspection of diffusion MRI data, it is clear that each WM voxel within a 3D image array may be traversed by multiple WM structural tracts, each of which connects a pair of GM nodes. We hypothesized that by appropriately weighting and then integrating the functional connectivity of each such connected pair, the overall engagement of any WM voxel in brain functions could be evaluated. This model introduces a structural constraint to earlier studies of WM engagement and addresses some limitations of previous efforts to relate structure and function. Using concepts derived from graph theory, we obtained spatial maps of WM engagement which highlight WM regions critical for efficient communications across the brain. The distributions of WM engagement are highly reproducible across subjects and depict a notable interdependence between the distribution of GM activities and the detailed organization of WM. Additionally, we provide evidence that the engagement varies over time and shows significant differences between genders. These findings suggest the potential of WM engagement as a measure of the integrity of normal brain functions and as a biomarker for neurological and cognitive disorders.