Altered Intra- and Inter-regional Functional Connectivity of the Anterior Cingulate Gyrus in Patients With Tremor-Dominant Parkinson's Disease Complicated With Sleep Disorder.

Xinjie Chen,Sifan Zhou,Xiaodong Luo,Xiaoyan Hou,Xian Liu,Bo Liu,Jun Chen

doi:10.3389/fnagi.2019.00319

Abstract

Objective: To investigate changes in brain function at the regional and whole-brain levels in patients with tremor-dominant Parkinson’s disease (TDPD) complicated by sleep disorder (SD) by regional homogeneity (ReHo) and functional connectivity (FC) analysis of whole-brain resting-state functional magnetic resonance images.Materials and Methods: ReHo and seed-based FC analyses were conducted among 32 patients with TDPD and SD (TDPD-SD), 24 with TDPD and no SD (TDPD-NSD), and 23 healthy controls (HCs) to assess spontaneous brain activity and network-level brain function. Correlation analyses were used to examine the associations between brain activity and the clinical data.Results: Anterior cingulate gyrus (ACC) ReHo values differed significantly among the groups. ACC ReHo values were increased in TDPD-SD vs. HC and TDPD-SD vs. TDPD-NSD. ACC ReHo values were reduced in TDPD-NSD vs. HC. TDPD-SD ReHo values were positively correlated with Pittsburgh Sleep Quality Index (PSQI) scores (r = 0.41, p = 0.020) but negatively correlated with Parkinson’s Disease Sleep Scale (PDSS) scores (r = −0.38, p = 0.030). FC analysis using ACC as a mask showed that FC of the left olfactory cortex (L-OC), right straight gyrus (R-SG), right superior parietal gyrus (R-SPG), and right precuneus differed significantly among the groups. FC values between R-SG and ACC were significantly lower in TDPD-SD than in TDPD-NSD, while the FC of L-OC and R-OC with ACC was significantly lower in TDPD-SD than in HC. FC between ACC and L-OC, R-SPG, and the right precuneus was lower in TDPD-NSD than in HC. There was no correlation between the FC values and other clinical data in any of the groups.Conclusion: Localized abnormal activity in TDPD-SD was chiefly triggered by ACC. The change in the ReHo of ACC is closely related to the severity of TDPD-associated SD, revealing the role of this region as a regulator of the sleep mechanism in TDPD. Significant abnormal FC was found between R-SG and ACC in TDPD-SD but was not shown to correlate with clinical data.

Highlights

Parkinson’s disease (PD) is a degenerative neurological disorder characterized by extrapyramidal dyskinesia with a variety of accompanying non-motor symptoms (Jankovic, 2008)
Post hoc analysis results showed the following: (1) compared with the tremor-dominant PD (TDPD)-NSD group, TDPD-Sleep disorder (SD) exhibited significantly lower functional connectivity (FC) values in R-SG with ACC (p-voxel < 0.001, p-cluster correction < 0.05); (2) compared with the Healthy controls (HCs) group, TDPD-SD exhibited significantly lower FC values in L-OC and R-OC with ACC (p < 0.05 uncorrected); and (3) compared with the HC group, the FC of L-OC, R-SPG, and the right precuneus decreased in TDPD-NSDs with ACC (p-voxel < 0.001, p-cluster correction < 0.05; see Table 2 and Figure 2)
We found that Regional homogeneity (ReHo) values of ACC in the TDPD-SD group had a characteristic increase, which was positively correlated with Pittsburgh Sleep Quality Index (PSQI) scores but negatively correlated with Parkinson’s Disease Sleep Scale (PDSS) scores

Summary

Introduction

Parkinson’s disease (PD) is a degenerative neurological disorder characterized by extrapyramidal dyskinesia with a variety of accompanying non-motor symptoms (Jankovic, 2008). Sleep disorder (SD) is a common non-motor symptom of PD, with an incidence of approximately 60–98% in PD patients (Kumar et al, 2002). In addition to the disease itself, anti-Parkinson’s drugs and other related psychiatric symptoms can further affect sleep-related brain neural activity (Videnovic and Golombek, 2013). Previous studies have examined magnetic resonance imaging structural changes (cortical thickness, cortical and subcortical volume) in PD patients with SD (Radziunas et al, 2018). Studies have started to use functional magnetic resonance imaging (fMRI) to study rapid eye movement sleep behavior disorder (RBD), a subtype of PD-associated SD (Li et al, 2017), and found abnormal changes in neural signals in the caudate, putamen, and prefrontal cortex (PFC) in PD patients with RBD

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