Static and dynamic topological organization of brain functional connectome in acute mild traumatic brain injury

Abstract

Background Prior studies have detected topological changes of brain functional networks in patients with acute mild traumatic brain injury (mTBI). However, the alterations of dynamic topological characteristics in mTBI have been scarcely elucidated. Purpose To evaluate static and dynamic functional connectivity topological networks in patients with acute mTBI using resting-state functional magnetic resonance imaging (fMRI). Material and Methods A total of 55 patients with acute mTBI and 55 age-, sex-, and education-matched healthy controls (HCs) were enrolled in this study. All participants underwent resting-state fMRI scans, and data were analyzed using graph-theory methods and a sliding window approach. Post-traumatic cognitive performance and resting-state fMRI data were collected within one week after injury. Static and dynamic functional connectivity patterns were determined by independent component analysis. Spearman’s correlation analysis was further performed between fMRI changes and Montreal cognitive assessment (MoCA) scores. Results Global efficiency was lower ( P = 0.02), and local efficiency ( P < 0.001) and mean Cp ( P < 0.001) were higher in patients with acute mTBI than in HCs. Local efficiency was correlated with visuospatial/executive performance ( r = −0.421; P = 0.002) in patients with acute mTBI. Significant differences in nodal efficiency and node degree centrality ( P < 0.01) were found between the mTBI and HC groups. For dynamic properties, patients with mTBI showed higher variance ( P = 0.016) in global efficiency than HCs. Conclusions The present study shows that patients with mTBI have abnormal brain functional connectome topology, especially the dynamic graph theory characteristics, which provide new insights into the role of topological network properties in patients with acute mTBI.

Disrupted topological organization of functional brain networks in traumatic axonal injury

“…TAI is characterized by widespread axonal damage caused by shearing forces of rotational acceleration and deceleration occurring at the time of injury. The recent development of new neuroimaging techniques has substantially improved our understanding of the underlying pathophysiology of persistent cognitive impairment after TBI by allowing the visualization of local changes in brain structure and function networks (Li et al, 2023;Pan et al, 2023;Sharp et al, 2014). Unlike focal injuries that affect specific brain regions, axonal injury fundamentally impairs the substrate through which brain networks communicate with each other.…”

“…This finding indicates a disrupted balance between local specialization and global integration in functional connectivity networks. Similarly, functional connectivity alterations associated with TBI have recently been studied using the mathematical concepts of graph theory (Boroda et al, 2021;Fagerholm et al, 2015;Kim et al, 2022;Li et al, 2023;Pandit et al, 2013;Raizman et al, 2020). However, the findings in these studies were contradictory and inconsistent due to the heterogeneity of patients with TBI, with large differences in severity, etiology, type of injury and mechanism, as well as recovery rate and burden of chronic symptoms (Maas, 2016;O'Brien et al, 2020;Caeyenberghs et al, 2017).…”