Alteration of Brain Functional Networks in Early-Stage Parkinson's Disease: A Resting-State fMRI Study

Abstract

Although alterations of topological organization have previously been reported in the brain functional network of Parkinson's disease (PD) patients, the topological properties of the brain network in early-stage PD patients who received antiparkinson treatment are largely unknown. This study sought to determine the topological characteristics of the large-scale functional network in early-stage PD patients. First, 26early-stage PD patients (Hoehn and Yahr stage:1-2) and 30 age-matched normal controls were scanned using resting-state functional MRI. Subsequently, graph theoretical analysis was employed to investigate the abnormal topological configuration of the brain network in early-stage PD patients. We found that both the PD patient and control groups showed small-world properties in their functional brain networks. However, compared with the controls, the early-stage PD patients exhibited abnormal global properties, characterized by lower global efficiency. Moreover, the modular structure and the hub distribution were markedly altered in early-stage PD patients. Furthermore, PD patients exhibited increased nodal centrality, primarily in the bilateral pallidum, the inferior parietal lobule, and the medial superior frontal gyrus, and decreased nodal centrality in the caudate nucleus, the supplementary motor areas, the precentral gyrus, and the middle frontal gyrus. There were significant negative correlations between the Unified Parkinson Disease Rating Scale motor scores and nodal centralities of superior parietal gyrus. These results suggest that the topological organization of the brain functional network was altered in early-stage PD patients who received antiparkinson treatment, and we speculated that the antiparkinson treatment may affect the efficiency of the brain network to effectively relieve clinical symptoms of PD.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Network efficiency of functional brain networks as a function of sparsity among early-stage PD patients and normal controls.

(A) Mean global efficiency and (B) mean local efficiency of the functional brain networks. (C) Normalized global efficiency and (D) normalized local efficiency of the functional brain networks. The functional brain networks showed increased local network efficiency but approximately identical global network efficiency of parallel information transmission compared with the matched random network. Error bars denote standard deviations. Red stars indicate statistically significant differences between the PD patients and the normal controls (p

Fig 2. Network modularity of functional brain networks as a function of sparsity among PD patients and normal controls.

Fig 3. Modules of the functional brain networks in each group.

(A) Modules of the brain network in normal controls. (B) Modules of the brain network in PD patients. Colors in nodes and links correspond to different modules. Only intramodular edges are shown. The results were visualized using the BrainNet Viewer (NKLCNL, Beijing Normal University).

Fig 4. Hubs of the functional brain networks in each group.

The results were visualized using the BrainNet Viewer (NKLCNL, Beijing Normal University). The maps showed the hubs of the brain network in normal controls (top panel) and in PD patients (bottom panel). Colors in nodes indicate different modules. Detailed brain region information corresponding to the anatomical labels can be found in S1 Table.

Fig 5. Brain regions showing significant alterations in nodal centrality between PD patients and normal controls (p

The results were visualized using the BrainNet Viewer (NKLCNL, Beijing Normal University).Three-dimensional maps show the differences in nodal degree (top panel),nodal efficiency (middle panel),and nodal betweenness (bottom panel)between the PD group and the control group. Red/blue spheres denote regions of increased/decreased nodal centrality in PD patients. Detailed brain region information corresponding to the anatomical labels can be found in S1 Table.

Fig 6. Correlation between abnormal network properties and UPDRS motor scores.

SPG.L: the left superior parietal gyrus.