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

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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.

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The role of the medial frontal cortex in cognitive control.

K. Ridderinkhof, Markus Ullsperger, Eveline A. Crone … (2004)

Adaptive goal-directed behavior involves monitoring of ongoing actions and performance outcomes, and subsequent adjustments of behavior and learning. We evaluate new findings in cognitive neuroscience concerning cortical interactions that subserve the recruitment and implementation of such cognitive control. A review of primate and human studies, along with a meta-analysis of the human functional neuroimaging literature, suggest that the detection of unfavorable outcomes, response errors, response conflict, and decision uncertainty elicits largely overlapping clusters of activation foci in an extensive part of the posterior medial frontal cortex (pMFC). A direct link is delineated between activity in this area and subsequent adjustments in performance. Emerging evidence points to functional interactions between the pMFC and the lateral prefrontal cortex (LPFC), so that monitoring-related pMFC activity serves as a signal that engages regulatory processes in the LPFC to implement performance adjustments.

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Olfactory dysfunction in Parkinson disease.

Richard L. Doty (2012)

Olfactory dysfunction is among the earliest nonmotor features of Parkinson disease (PD). Such dysfunction is present in approximately 90% of early-stage PD cases and can precede the onset of motor symptoms by years. The mechanisms responsible for olfactory dysfunction are currently unknown. As equivalent deficits are observed in Alzheimer disease, Down syndrome, and the Parkinson-dementia complex of Guam, a common pathological substrate may be involved. Given that olfactory loss occurs to a lesser extent or is absent in disorders such as multiple system atrophy, corticobasal degeneration, and progressive supranuclear palsy, olfactory testing can be useful in differential diagnosis. The olfactory dysfunction in PD and a number of related diseases with smell loss correlates with decreased numbers of neurons in structures such as the locus coeruleus, the raphe nuclei, and the nucleus basalis of Meynart. These neuroanatomical findings, together with evidence for involvement of the autonomic nervous system in numerous PD-related symptoms, suggest that deficits in cholinergic, noradrenergic and serotonergic function may contribute to the olfactory loss. This Review discusses the current understanding of olfactory dysfunction in PD, including factors that may be related to its cause.

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Regional homogeneity changes in patients with Parkinson's disease.

Tao Wu, Xiangyu Long, Yufeng Zang … (2008)

Resting state brain activity in Parkinson's disease (PD) can give clues to the pathophysiology of the disorder, and might be helpful in diagnosis, but it has never been explored using functional MRI (fMRI). In the current study, we used a regional homogeneity (ReHo) method to investigate PD-related modulations of neural activity in the resting state. FMRIs were acquired in 22 patients with PD at both before and after levodopa administration, as well as in 22 age- and sex-matched normal controls. In the PD group compared with the healthy controls, we found ReHo decreased in extensive brain regions, including the putamen, thalamus, and supplementary motor area; and increased in some other areas, including the cerebellum, primary sensorimotor cortex, and premotor area. The ReHo off medication was negatively correlated with the Unified Parkinson's Disease Rating Scale (UPDRS) in the putamen and some other regions, and was positively correlated with the UPDRS in the cerebellum. Administration of levodopa relatively normalized ReHo. Our findings demonstrate that neural activity in the resting state is changed in patients with PD. This change is secondary to dopamine deficiency, and related to the severity of the disease. The different neuronal activity at the baseline state should be considered in explaining fMRI findings obtained during tasks. . (c) 2008 Wiley-Liss, Inc.

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Author and article information

Contributors

Xinjie Chen: URI : https://loop.frontiersin.org/people/793148/overview

Xiaoyan Hou: URI : https://loop.frontiersin.org/people/805354/overview

Sifan Zhou: URI : https://loop.frontiersin.org/people/830822/overview

Jun Chen: URI : https://loop.frontiersin.org/people/373398/overview

Journal

Journal ID (nlm-ta): Front Aging Neurosci

Journal ID (iso-abbrev): Front Aging Neurosci

Journal ID (publisher-id): Front. Aging Neurosci.

Title: Frontiers in Aging Neuroscience

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1663-4365

Publication date (Electronic): 21 November 2019

Publication date Collection: 2019

Volume: 11

Electronic Location Identifier: 319

Affiliations

[1] ¹The Second Affiliated Hospital of Guangzhou University of Chinese Medicine , Guangzhou, China

[2] ²Department of Radiology, Guangdong Hospital of Traditional Chinese Medicine , Guangzhou, China

[3] ³Department of Radiology, ZHUHAI Branch of Guangdong Hospital of Traditional Chinese Medicine , Zhuhai, China

Author notes

Edited by: Micaela Morelli, University of Cagliari, Italy

Reviewed by: Demao Deng, Guangxi University of Chinese Medicine, China; Baoci Shan, Institute of High Energy Physics (CAS), China

*Correspondence: Jun Chen junesums@ 123456163.com

^†These authors have contributed equally to this work

Article

DOI: 10.3389/fnagi.2019.00319

PMC ID: 6881235

SO-VID: adfd1b41-fed0-4ca7-9f20-ca7e3826d552

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 21 August 2019

Date accepted : 04 November 2019

Page count

Figures: 3, Tables: 2, Equations: 0, References: 36, Pages: 9, Words: 6940

Funding

Funded by: National Natural Science Foundation of China 10.13039/501100001809

Award ID: 81603681

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

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Most cited references 29

The role of the medial frontal cortex in cognitive control.

Olfactory dysfunction in Parkinson disease.

Regional homogeneity changes in patients with Parkinson's disease.

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