Association of aberrant brain network connectivity with visual dysfunction in patients with nonarteritic anterior ischemic optic neuropathy: a pilot study.

Abstract

Background: Nonarteritic anterior ischemic optic neuropathy (NAION) is often accompanied by degeneration of optic nerve axons and ganglion cell apoptosis, but the mechanism of its effects on the cerebral cortex and visual centers is not clear. Graph theory analysis, as a quantitative tool for complex networks, has made it possible to characterize the topological alterations of brain networks in patients with NAION. The objective of this pilot study was to investigate the topological characteristics of functional brain networks in patients with NAION and to analyze their potential correlation with visual dysfunction.

Methods: This prospective, cross-sectional study recruited 25 patients with NAION and 24 matched healthy controls (HCs) from Dongfang Hospital, Beijing University of Chinese Medicine. Following resting-state functional magnetic resonance imaging (rs-fMRI) scans, large-scale functional connectivity matrices of 90 regions were constructed. Graph theory was then used to compare global and local network parameters. Subsequently, network-based statistics (NBS) analysis was employed to detect differences in functional connectivity across the brain. Finally, correlations were assessed between the network topological properties and clinical variables.

Results: Individuals with NAION, as compared to controls, exhibited significant decreases in normalized clustering coefficient (gamma; P=0.021), small-worldness (sigma; P=0.043), and local efficiency (Eloc; P=0.030), as well as a significant increase in the size of the largest connected component (LCC; P=0.039) of the network. Additionally, the LCC showed a negative association with gamma, sigma and global efficiency (Eg) but a positive correlation with the normalized characteristic path length (lambda) of the two groups (all P values <0.05). Regionally, patients exhibited changes in nodal centralities, particularly affecting the attention, visual, and salience networks. NBS analysis identified an interconnected subnetwork consisting of 49 nodes and 77 edges (P<0.001, NBS-corrected) that showed significantly higher connectivity in patients with NAION. The mean connectivity of this subnetwork was negatively correlated with the global topological parameters gamma, sigma, and Eg in the NAION group and gamma and sigma in the HCs but positively correlated with the LCC in both groups (all P values <0.05). Moreover, the nodal betweenness centrality of the left dorsolateral superior frontal gyrus exhibited a significant positive correlation with the visual field (VF) mean deviation (MD) in the NAION group (P<0.001).

Conclusions: This study initially identified aberrant topological and connectivity changes in the functional brain networks associated with visual impairment in patients with NAION, thus expanding our existing understanding of the neurobiological mechanisms of NAION.