Longitudinal increases in structural connectome segregation and functional connectome integration are associated with better recovery after mild TBI

• Published in: Human brain mapping Vol. 40; no. 15; pp. 4441 - 4456
• Main Authors: Kuceyeski, Amy F., Jamison, Keith W., Owen, Julia P., Raj, Ashish, Mukherjee, Pratik
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 15.10.2019
• Subjects: Adult; Attention; Brain; Brain damage; Brain Injuries, Traumatic - physiopathology; Brain Injuries, Traumatic - psychology; Case-Control Studies; Cognition; Cognition & reasoning; Cognition Disorders - etiology; Cognition Disorders - physiopathology; Cognitive ability; Connectome; Convalescence; Degeneration; diffusion MRI; Diffusion Tensor Imaging; Disruption; Electrochemistry; Female; Follow-Up Studies; Functional magnetic resonance imaging; Functional plasticity; Head injuries; Humans; imaging methodology; Integration; Learning Disabilities - etiology; Learning Disabilities - physiopathology; Longitude; Magnetic Resonance Imaging; Male; Males; Memory Disorders - etiology; Memory Disorders - physiopathology; Models, Neurological; Nerve Net - physiopathology; Neurodegeneration; Neuroplasticity; Neuropsychological Tests; Predictive control; Propagation; Recovery; Regression models; resting state connectivity; Structure-function relationships; Substantia alba; tractography; Traumatic brain injury; Wounds, Nonpenetrating - physiopathology; Wounds, Nonpenetrating - psychology; Young Adult; diffusion MRI; traumatic brain injury; connectome; tractography; imaging methodology; resting state connectivity
• ISSN: 1065-9471; 1097-0193; 1097-0193
• DOI: 10.1002/hbm.24713

Traumatic brain injury damages white matter pathways that connect brain regions, disrupting transmission of electrochemical signals and causing cognitive and emotional dysfunction. Connectome‐level mechanisms for how the brain compensates for injury have not been fully characterized. Here, we collected serial MRI‐based structural and functional connectome metrics and neuropsychological scores in 26 mild traumatic brain injury subjects (29.4 ± 8.0 years, 20 males) at 1 and 6 months postinjury. We quantified the relationship between functional and structural connectomes using network diffusion (ND) model propagation time, a measure that can be interpreted as how much of the structural connectome is being utilized for the spread of functional activation, as captured via the functional connectome. Overall cognition showed significant improvement from 1 to 6 months (t25 = −2.15, p = .04). None of the structural or functional global connectome metrics was significantly different between 1 and 6 months, or when compared to 34 age‐ and gender‐matched controls (28.6 ± 8.8 years, 25 males). We predicted longitudinal changes in overall cognition from changes in global connectome measures using a partial least squares regression model (cross‐validated R2 = .27). We observe that increased ND model propagation time, increased structural connectome segregation, and increased functional connectome integration were related to better cognitive recovery. We interpret these findings as suggesting two connectome‐based postinjury recovery mechanisms: one of neuroplasticity that increases functional connectome integration and one of remote white matter degeneration that increases structural connectome segregation. We hypothesize that our inherently multimodal measure of ND model propagation time captures the interplay between these two mechanisms.