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Resting state functional connectivity alterations in motor networks of Parkinson's disease in different frequency bands
ZHANG Pengfei  CHENG Xiu  MA Laiyang  WANG Rui  LI Min  YANG Tingli  GUO Ruiqing  TAO Jiahuan  LIU Guangyao  ZHANG Jing 

Cite this article as: ZHANG P F, CHENG X, MA L Y, et al. Resting state functional connectivity alterations in motor networks of Parkinson's disease in different frequency bands[J]. Chin J Magn Reson Imaging, 2023, 14(1): 13-19. DOI:10.12015/issn.1674-8034.2023.01.003.


[Abstract] Objective Based on resting state functional magnetic resonance imaging (rs-fMRI), to investigate the functional connectivity (FC) of motor networks in Parkinson's disease (PD) patients and to explore frequency-specific FC patterns.Materials and Methods Twenty-eight PD patients and 34 healthy controls (HCs) matched for gender, age, and education were enrolled. A total of 36 regions of interest (ROI) containing the bilateral cerebellum (Ⅳ-Ⅴ, Ⅵ, Ⅷ lobules), substantia nigra (SN), basal ganglia (BG) (caudate nucleus, putamen, pallidum), thalamus, and motor cortex (precentral and postcentral gyrus, paracentral lobule) were selected from atlases to form a PD-specific motor network, using FC in conventional band (0.01-0.1 Hz), slow-3 (0.073-0.198 Hz), slow-4 (0.027-0.073 Hz) and slow-5 (0.01-0.027 Hz) as edges. After network-based statistical analysis, the frequency-specific FC change patterns were explored. Correlations between abnormal FC and clinical motor and cognitive scores were calculated using Spearman's partial correlation analysis.Results PD patients demonstrated extensive FC reduction at conventional band. In the threshold of Pedge=0.01 and Pcomponent=0.05, the component containing 22 ROIs and 29 edges were observed (P=0.017), where inter-network connections were dominated between thalamo-cerebello-BG circuits, as well as connections between SN-putamen and postcentral gyrus-cerebellum. Compared with typical band at the threshold of Pedge=0.05, slow-4 showed more thalamo-BG FC changes, while slow-5 specific FC was mainly the "cerebello-SN-BG-thalamo" related circuits. No statistically aberrant FC was detected in slow-3. The FC between thalamus-pallidum, also between inter-putamina, were negatively correlated with the Unified Parkinson's Disease Rating Scale Ⅲ (UPDRS-Ⅲ) (Pcorrected=0.04 and Pcorrected＜0.01).Conclusions PD patients showed a complex and extensive FC impairment of the integrative motor network, with frequency-specific changes. Alterations in brain functional networks containing "cerebello-SN-BG-thalamo-motor cortical" circuits may be one of the neuropathological mechanisms of PD movement dysfunction. The striatum, thalamus and other subcortical regions may be served as potential biomarkers for disease diagnosis and monitoring.
[Keywords] Parkinson's disease；magnetic resonance imaging；resting-state functional magnetic resonance imaging；functional connectivity；motor network；frequency specificity

ZHANG Pengfei1, 2   CHENG Xiu3   MA Laiyang1, 2   WANG Rui1   LI Min1   YANG Tingli1   GUO Ruiqing1   TAO Jiahuan1   LIU Guangyao1   ZHANG Jing1, 2, 4*  

1 Department of Magnetic Resonance, Lanzhou University Second Hospital, Lanzhou 730030, China

2 Second Clinical School, Lanzhou University, Lanzhou 730030, China

3 Department of Radiology, Shenzhen Bao'an People's Hospital, Shenzhen 518101, China

4 Gansu Province Clinical Research Center for Functional and Molecular Imaging, Lanzhou 730030, China

Corresponding author: Zhang J, E-mail: ery_zhangjing@lzu.edu.cn

Conflicts of interest   None.

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 81960309); Science and Technology Project of Gansu Province (No. 21JR7RA438).
Received  2022-09-20
Accepted  2023-01-04
DOI: 10.12015/issn.1674-8034.2023.01.003
Cite this article as: ZHANG P F, CHENG X, MA L Y, et al. Resting state functional connectivity alterations in motor networks of Parkinson's disease in different frequency bands[J]. Chin J Magn Reson Imaging, 2023, 14(1): 13-19. DOI:10.12015/issn.1674-8034.2023.01.003.

[1]
Chinese Society of Parkinson's Disease and Movement Disorders, Parkinson's Disease and Movement Disorder Section of Neurologist Branch of Chinese Medical Doctor Association, Chinese Society of Neuropsychology and Behavioral Neurology. The diagnostic criteria and treatment guideline for Parkinson's disease dementia (second version)[J]. Chin J Neurol, 2021, 54(8): 762-771.
[2]
ZHANG Z X, ROMAN G C, HONG Z, et al. Parkinson's disease in China: prevalence in Beijing, Xi'an, and Shanghai[J]. Lancet, 2005, 365(9459): 595-597. DOI: 10.1016/s0140-6736(05)17909-4.
[3]
SIMON D K, TANNER C M, BRUNDIN P. Parkinson Disease Epidemiology, Pathology, Genetics, and Pathophysiology[J]. Clin Geriatr Med, 2020, 36(1): 1-12. DOI: 10.1016/j.cger.2019.08.002.
[4]
ZHONG Y, LIU H, LIU G, et al. A review on pathology, mechanism, and therapy for cerebellum and tremor in Parkinson's disease[J/OL]. NPJ Parkinsons Dis, 2022, 8(1): 82 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9232614/. DOI: 10.1038/s41531-022-00347-2.
[5]
YANG J, GOHEL S, VACHHA B. Current methods and new directions in resting state fMRI[J]. Clin Imaging, 2020, 65: 47-53. DOI: 10.1016/j.clinimag.2020.04.004.
[6]
FILIPPI M, SARASSO E, AGOSTA F. Resting-state Functional MRI in Parkinsonian Syndromes[J]. Mov Disord Clin Pract, 2019, 6(2): 104-117. DOI: 10.1002/mdc3.12730.
[7]
RUPPERT M C, GREUEL A, TAHMASIAN M, et al. Network degeneration in Parkinson's disease: multimodal imaging of nigro-striato-cortical dysfunction[J]. Brain, 2020, 143(3): 944-959. DOI: 10.1093/brain/awaa019.
[8]
POSTUMA R B, BERG D, STERN M, et al. MDS clinical diagnostic criteria for Parkinson's disease[J]. Mov Disord, 2015, 30(12): 1591-1601. DOI: 10.1002/mds.26424.
[9]
CHAO-GAN Y, YU-FENG Z. DPARSF: A MATLAB Toolbox for "Pipeline" Data Analysis of Resting-State fMRI[J/OL]. Front Syst Neurosci, 2010, 4: 13 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2889691/. DOI: 10.3389/fnsys.2010.00013.
[10]
BUZSÁKI G, DRAGUHN A. Neuronal oscillations in cortical networks[J]. Science, 2004, 304(5679): 1926-1929. DOI: 10.1126/science.1099745.
[11]
RONG S, ZHANG P, HE C, et al. Abnormal Neural Activity in Different Frequency Bands in Parkinson's Disease With Mild Cognitive Impairment[J/OL]. Front Aging Neurosci, 2021, 13: 709998 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8417797/. DOI: 10.3389/fnagi.2021.709998.
[12]
CALIGIURI M E, QUATTRONE A, BIANCO M G, et al. Structural connectivity alterations in the motor network of patients with scans without evidence of dopaminergic deficit (SWEDD)[J]. J Neurol, 2022, 269(11): 5926-5933. DOI: 10.1007/s00415-022-11259-9.
[13]
DESIKAN R S, SÉGONNE F, FISCHL B, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest[J]. Neuroimage, 2006, 31(3): 968-980. DOI: 10.1016/j.neuroimage.2006.01.021.
[14]
FAN L, LI H, ZHUO J, et al. The Human Brainnetome Atlas: A New Brain Atlas Based on Connectional Architecture[J]. Cereb Cortex, 2016, 26(8): 3508-3526. DOI: 10.1093/cercor/bhw157.
[15]
ROLLS E T, HUANG C C, LIN C P, et al. Automated anatomical labelling atlas 3[J/OL]. Neuroimage, 2020, 206: 116189 [2022-09-19]. https://linkinghub.elsevier.com/retrieve/pii/S1053-8119(19)30780-3. DOI: 10.1016/j.neuroimage.2019.116189.
[16]
MURTY V P, SHERMOHAMMED M, SMITH D V, et al. Resting state networks distinguish human ventral tegmental area from substantia nigra[J]. Neuroimage, 2014, 100: 580-589. DOI: 10.1016/j.neuroimage.2014.06.047.
[17]
ZALESKY A, FORNITO A, BULLMORE E T. Network-based statistic: identifying differences in brain networks[J]. Neuroimage, 2010, 53(4): 1197-1207. DOI: 10.1016/j.neuroimage.2010.06.041.
[18]
WANG J, WANG X, XIA M, et al. GRETNA: a graph theoretical network analysis toolbox for imaging connectomics[J/OL]. Front Hum Neurosci, 2015, 9: 386 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/26175682/. DOI: 10.3389/fnhum.2015.00386.
[19]
XIA M, WANG J, HE Y. BrainNet Viewer: a network visualization tool for human brain connectomics[J/OL]. PLoS One, 2013, 8(7): e68910 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23861951/. DOI: 10.1371/journal.pone.0068910.
[20]
MCGREGOR M M, NELSON A B. Circuit Mechanisms of Parkinson's Disease[J]. Neuron, 2019, 101(6): 1042-1056. DOI: 10.1016/j.neuron.2019.03.004.
[21]
TINAZ S. Functional Connectome in Parkinson's Disease and Parkinsonism[J/OL]. Curr Neurol Neurosci Rep, 2021, 21(6): 24 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/33817766/. DOI: 10.1007/s11910-021-01111-4.
[22]
TREMBLAY C, RAHAYEL S, VO A, et al. Brain atrophy progression in Parkinson's disease is shaped by connectivity and local vulnerability[J/OL]. Brain Commun, 2021, 3(4): fcab269 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/34859216/. DOI: 10.1093/braincomms/fcab269.
[23]
CHEN R, BERARDELLI A, BHATTACHARYA A, et al. Clinical neurophysiology of Parkinson's disease and parkinsonism[J]. Clin Neurophysiol Pract, 2022, 7: 201-227. DOI: 10.1016/j.cnp.2022.06.002.
[24]
FLACE P, LIVREA P, BASILE G A, et al. The Cerebellar Dopaminergic System[J/OL]. Front Syst Neurosci, 2021, 15: 650614 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/34421548/. DOI: 10.3389/fnsys.2021.650614.
[25]
WU T, LONG X, ZANG Y, et al. Regional homogeneity changes in patients with Parkinson's disease[J]. Hum Brain Mapp, 2009, 30(5): 1502-1510. DOI: 10.1002/hbm.20622.
[26]
HORIN A P, MYERS P S, PICKETT K A, et al. Resting-state functional connectivity associated with gait characteristics in people with Parkinson's disease[J/OL]. Behav Brain Res, 2021, 411: 113398 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/34087255/. DOI: 10.1016/j.bbr.2021.113398.
[27]
HELMICH R C, HALLETT M, DEUSCHL G, et al. Cerebral causes and consequences of parkinsonian resting tremor: a tale of two circuits?[J]. Brain, 2012, 135(Pt 11): 3206-3226. DOI: 10.1093/brain/aws023.
[28]
XU H, ZHANG M, WANG Z, et al. Abnormal brain activities in multiple frequency bands in Parkinson's disease with apathy[J/OL]. Front Neurosci, 2022, 16: 975189 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/36300172/. DOI: 10.3389/fnins.2022.975189.
[29]
LIAO H, YI J, CAI S, et al. Changes in Degree Centrality of Network Nodes in Different Frequency Bands in Parkinson's Disease With Depression and Without Depression[J/OL]. Front Neurosci, 2021, 15: 638554 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/33828449/. DOI: 10.3389/fnins.2021.638554.
[30]
BOSCH T J, GROTH C, SINGH A. Resting-State Low-Frequency Cerebellar Oscillations Can Be Abnormal in Parkinson's Disease[J]. Cerebellum, 2022, 21(6): 1139-1143. DOI: 10.1007/s12311-021-01343-7.
[31]
OSWAL A, CAO C, YEH C H, et al. Neural signatures of hyperdirect pathway activity in Parkinson's disease[J/OL]. Nat Commun, 2021, 12(1): 5185 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/34465771/. DOI: 10.1038/s41467-021-25366-0.
[32]
JOHNSON L A, AMAN J E, YU Y, et al. High-Frequency Oscillations in the Pallidum: A Pathophysiological Biomarker in Parkinson's Disease?[J]. Mov Disord, 2021, 36(6): 1332-1341. DOI: 10.1002/mds.28566.
[33]
GUAN X, GUO T, ZENG Q, et al. Oscillation-specific nodal alterations in early to middle stages Parkinson's disease[J/OL]. Transl Neurodegener, 2019, 8: 36 [2022-09-19]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/31807287/. DOI: 10.1186/s40035-019-0177-5.
[34]
SHEN B, PAN Y, JIANG X, et al. Altered putamen and cerebellum connectivity among different subtypes of Parkinson's disease[J]. CNS Neurosci Ther, 2020, 26(2): 207-214. DOI: 10.1111/cns.13259.
[35]
NEUMANN W J, SCHROLL H, DE ALMEIDA MARCELINO A L, et al. Functional segregation of basal ganglia pathways in Parkinson's disease[J]. Brain, 2018, 141(9): 2655-2669. DOI: 10.1093/brain/awy206.
[36]
FAN D, LIU T, JIANG J, et al. Cognitive decline is associated with frequency-specific resting state functional changes in normal aging[J]. Brain Imaging Behav, 2022, 16(5): 2120-2132. DOI: 10.1007/s11682-022-00682-1.
[37]
SU Q, YU M, LIU F, et al. Frequency-specific alterations of the frontal-cerebellar circuit in first-episode, drug-naive somatization disorder[J]. J Affect Disord, 2021, 280(Pt A): 319-325. DOI: 10.1016/j.jad.2020.11.090.

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