Altered Global Synchronizations in Patients With Parkinson's Disease: A Resting-State fMRI Study

Abstract

Background: Abnormalities of cognitive and movement functions are widely reported in Parkinson's disease (PD). The mechanisms therein are complicated and assumed to a coordination of various brain regions. This study explored the alterations of global synchronizations of brain activities and investigated the neural correlations of cognitive and movement function in PD patients. Methods: Thirty-five age-matched patients with PD and 35 normal controls (NC) were enrolled in resting-state functional magnetic resonance imaging (rs-fMRI) scanning. Degree centrality (DC) was calculated to measure the global synchronizations of brain activity for two groups. Neural correlations between DC and cognitive function Frontal Assessment Battery (FAB), as well as movement function Unified Parkinson's Disease Rating Scale (UPDRS-III), were examined across the whole brain within Anatomical Automatic Labeling (AAL) templates. Results: In the PD group, increased DC was observed in left fusiform gyrus extending to inferior temporal gyrus, left middle temporal gyrus (MTG) and angular gyrus, while it was decreased in right inferior opercular-frontal gyrus extending to superior temporal gyrus (STG). The DC in a significant region of the fusiform gyrus was positively correlated with UPDRS-III scores in PD (r = 0.41, p = 0.0145). Higher FAB scores were shown in NC than PD (p < 0.0001). Correlative analysis of PD between DC and FAB showed negative results (p < 0.05) in frontal cortex, whereas positive in insula and cerebellum. As for the correlations between DC and UPDRS-III, negative correlation (p < 0.05) was observed in bilateral inferior parietal lobule (IPL) and right cerebellum, whereas positive correlation (p < 0.05) in bilateral hippocampus and para-hippocampus gyrus (p < 0.01). Conclusion: The altered global synchronizations revealed altered cognitive and movement functions in PD. The findings suggested that the global functional connectivity in fusiform gyrus, cerebellum and hippocampus gyrus are critical regions in the identification of cognitive and movement functions in PD. This study provides new insights on the interactions among global coordination of brain activity, cognitive and movement functions in PD.

Keywords: Parkinson’s disease; cognitive function; global synchronizations; movement function; resting-state fMRI.

Figure 1

Between-group degree centrality (DC) differences. (A) T-maps of DC differences between normal controls (NC) and patients with Parkinson’s disease (PD). Multiple comparison corrections were implemented by Gaussian Random Field (GRF) with voxel p < 0.005 and cluster p < 0.05 within gray matter mask (T > 2.91, cluster size > 1,350 mm³). The color bar indicated the statistical t-value. Warm/Cool overlays indicated increased/decreased DC in PD. L/R = left/right hemisphere. (B) Positive correlation between DC and motor part of Unified Parkinson’s Disease Rating Scale (UPDRS-III) in left fusiform gyrus.

Figure 2

Significant correlations between cognitive function and the global signal synchronizations within the whole brain [Automated Anatomical Labeling (AAL) templates] in patients with PD. (A) The Frontal Assessment Battery (FAB) scores of NC and PD. Significant correlations between FAB and DC in bilateral superior frontal gyrus (SFG; B,C), right medial-SFG (D), bilateral insula (E,F), bilateral cerebellum-curs1 (G,H) and right cerebellum-6 (I). Significance notations: *p < 0.05, **p < 0.01, ***p < 0.005. The dots and lines were demonstrated in red/blue color for positive/negative correlations.

Figure 3

Correlative analysis between cognitive function and the global signal synchronizations in bilateral hippocampus in both NC and patients with PD. Significance notations: *p < 0.05, ***p < 0.005, n.s = no significance. The dots and lines were demonstrated in blue/green color for negative/no correlations.

Figure 4

Significant correlations between movement measurements and the global signal synchronizations within the whole brain (AAL templates) in patients with PD. Correlations between Part three of UPDRS-III and DC in bilateral inferior parietal lobule (IPL; A,D), right angular gyrus (G), right cerebellum-6 (H), bilateral hippocampus (B,E) and bilateral para-hippocampus gyrus (C,F). The dots and lines were demonstrated in red/blue color for positive/negative correlations.