Global efficiency of the motor network is decreased in Parkinson's disease in comparison with essential tremor and healthy controls

Novaes, Natalia P.; Balardin, Joana Bisol; Hirata, Fabiana Campos; Melo, Luciano Magalhães; Amaro, Edson; Barbosa, Egberto Reis; Sato, João Ricardo; Cardoso, Ellison Fernando

doi:10.1002/brb3.2178

Cited by 6 publications

(6 citation statements)

References 57 publications

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“…The global efficiency represents the information efficiency of networks at the global level. The reduced global efficiency of functional network has been reported in PD patients 90,91 were consistent with the findings reported by previous studies showing that nodal topology of caudate in functional network were significantly altered in PD [92][93][94][95] . The reduction of local information efficiency in caudate of T-carriers indicated that BIN3 rs2280104 T allele is harmful in PD, which was consistent with previous study showing that BIN3 rs2280104 T allele was associated with increased risk of PD.…”

Section: The Effects Of Bin3 Rs2280104 T Allele On Functional Networksupporting

confidence: 92%

BIN3rs2280104 T allele is associated with excessive daytime sleepiness and altered network topology in Parkinson’s disease

Chen

et al. 2023

Preprint

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Background Excessive daytime sleepiness (EDS) is one of the most common non-motor symptoms in Parkinson's disease (PD). Previous studies showed that PD patients with EDS exhibited more severe motor and non-motor symptoms. Our recent studies revealed that BIN3 rs2280104 was negatively associated with scores of Epworth Sleepiness Scale (ESS) in PD patients. The objective of this study is to examine whether BIN3 rs2280104 shapes brain networks of PD patients and whether network metrics associated with BIN3 rs2280104 mediate the effects of BIN3 rs2280104 on EDS. Methods PD patients (n = 144) receiving functional magnetic resonance imaging in Parkinson's Progression Markers Initiative (PPMI) database were investigated. The clinical manifestations and graphical metrics of structural and functional network were compared among different genotype groups of BIN3 rs2280104. The mediation analysis was used to explore the causal associations between network metrics modified by BIN3 rs2280104 and EDS of PD patients. Results ESS scores were associated with more severe motor and non-motor symptoms. BIN3 rs2280104 T allele was negatively associated with ESS scores in PD patients. Additionally, BIN3 rs2280104 significantly shaped structural and functional network metrics of PD patients. The nodal Cp of left superior temporal pole in functional network and the degree centrality of left calcarine in structural network were negatively associated with ESS scores, however, only the degree centrality of left calcarine in structural network mediated the effects of BIN3 rs2280104 on EDS of PD patients. Conclusions To summarize, BIN3 rs2280104 is significantly associated with EDS and network topology of PD patients. Additionally, the degree centrality of left calcarine in structural network mediated the effects of BIN3 rs2280104 on EDS. Future studies were required to identify the molecular mechanisms underlying the effects of BIN3 rs2280104 on EDS and brain network metrics of PD patients.

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Section: The Effects Of Bin3 Rs2280104 T Allele On Functional Networksupporting

confidence: 92%

BIN3rs2280104 T allele is associated with excessive daytime sleepiness and altered network topology in Parkinson’s disease

Chen

et al. 2023

Preprint

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“…To fill the current research gap, we used probabilistic tractography in this study, which is capable of resolving the problem of crossing fibers in white matter voxels, 19 to characterize the brain organization of the motor network in SCA3/MJD. Motor networks have been studied in other neurodegenerative diseases comprising the precentral cortex, basal ganglia, thalamus, ventral diencephalon, and cerebellum 17,20–23 . We used network‐based statistics (NBS), 24 a statistical approach that identifies connections in a graph that may be relevant to diagnostic status, 25 to find different subnetworks in preclinical and ataxic SCA3/MJD patients.…”

Section: Introductionmentioning

confidence: 99%

“…Motor networks have been studied in other neurodegenerative diseases comprising the precentral cortex, basal ganglia, thalamus, ventral diencephalon, and cerebellum. 17 , 20 , 21 , 22 , 23 We used network‐based statistics (NBS), 24 a statistical approach that identifies connections in a graph that may be relevant to diagnostic status, 25 to find different subnetworks in preclinical and ataxic SCA3/MJD patients. Given that previous imaging studies have shown that morphological changes already occur in the cerebellum at the preataxic stage, we hypothesized that motor network abnormalities are already detectible before the onset of ataxia, and motor network alterations are associated with disease severity in SCA3/MJD.…”

Section: Introductionmentioning

confidence: 99%

Altered brain white matter structural motor network in spinocerebellar ataxia type 3

Chen

Huang

Lin

et al. 2022

Ann Clin Transl Neurol

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Objectives Spinocerebellar ataxia type 3 is a disorder within the brain network. However, the relationship between the brain network and disease severity is still unclear. This study aims to investigate changes in the white matter (WM) structural motor network, both in preclinical and ataxic stages, and its relationship with disease severity. Methods For this study, 20 ataxic, 20 preclinical SCA3 patients, and 20 healthy controls were recruited and received MRI scans. Disease severity was quantified using the SARA and ICARS scores. The WM motor structural network was created using probabilistic fiber tracking and was analyzed using graph theory and network‐based statistics at global, nodal, and edge levels. In addition, the correlations between network topological measures and disease duration or clinical scores were analyzed. Results Preclinical patients showed increasing assortativity of the motor network, altered subnetwork including 12 edges of 11 nodes, and 5 brain regions presenting reduced nodal strength. In ataxic patients assortativity of the motor network also increased, but global efficiency, global strength, and transitivity decreased. Ataxic patients showed a wider altered subnetwork and a higher number of reduced nodal strengths. A negative correlation between the transitivity of the motor network and SARA and ICARS scores was observed in ataxic patients. Interpretation Changes to the WM motor network in SCA3 start before ataxia onset, and WM motor network involvement increases with disease progression. Global network topological measures of the WM motor network appear to be a promising image biomarker for disease severity. This study provides new insights into the pathophysiology of disease in SCA3/MJD.

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“…It has also been demonstrated that brain structural and functional connections are damaged in the early stages of PD. A previous rs-fMRI study of 54 PD patients found that the global efficiency of the motor network was decreased in PD patients compared with tremor patients and HCs (Novaes et al, 2021). Another rs-fMRI study showed that the global and local efficiency of the sensorimotor network and the visual network were disrupted in PD (Fang et al, 2017).…”

Section: Discussionmentioning

confidence: 96%

Topological patterns of motor networks in Parkinson’s disease with different sides of onset: A resting-state-informed structural connectome study

Zhang

Li²,

Xia³

et al. 2022

Front. Aging Neurosci.

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Parkinson’s disease (PD) has a characteristically unilateral pattern of symptoms at onset and in the early stages; this lateralization is considered a diagnostically important diagnosis feature. We aimed to compare the graph-theoretical properties of whole-brain networks generated by using resting-state functional MRI (rs-fMRI), diffusion tensor imaging (DTI), and the resting-state-informed structural connectome (rsSC) in patients with left-onset PD (LPD), right-onset PD (RPD), and healthy controls (HCs). We recruited 26 patients with PD (13 with LPD and 13 with RPD) as well as 13 age- and sex-matched HCs. Rs-fMRI and DTI were performed in all subjects. Graph-theoretical analysis was used to calculate the local and global efficiency of a whole-brain network generated by rs-fMRI, DTI, and rsSC. Two-sample t-tests and Pearson correlation analysis were conducted. Significantly decreased global and local efficiency were revealed specifically in LPD patients compared with HCs when the rsSC network was used; no significant intergroup difference was found by using rs-fMRI or DTI alone. For rsSC network analysis, multiple network metrics were found to be abnormal in LPD. The degree centrality of the left precuneus was significantly correlated with the Unified Parkinson’s Disease Rating Scale (UPDRS) score and disease duration (p = 0.030, r = 0.599; p = 0.037, r = 0.582). The topological properties of motor-related brain networks can differentiate LPD and RPD. Nodal metrics may serve as important structural features for PD diagnosis and monitoring of disease progression. Collectively, these findings may provide neurobiological insights into the lateralization of PD onset.

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Global efficiency of the motor network is decreased in Parkinson's disease in comparison with essential tremor and healthy controls

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 6 publications

References 57 publications

BIN3rs2280104 T allele is associated with excessive daytime sleepiness and altered network topology in Parkinson’s disease

BIN3rs2280104 T allele is associated with excessive daytime sleepiness and altered network topology in Parkinson’s disease

Altered brain white matter structural motor network in spinocerebellar ataxia type 3

Topological patterns of motor networks in Parkinson’s disease with different sides of onset: A resting-state-informed structural connectome study

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