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MRI research progress on the neuromodulation mechanism of non-invasive neuromodulation for Parkinson's disease
OUYANG Yinfei  PENG Bei  HUANG Jinli  HUANG Jiazhu  DENG Demao 

Cite this article as: OUYANG Y F, PENG B, HUANG J L, et al. MRI research progress on the neuromodulation mechanism of non-invasive neuromodulation for Parkinson's disease[J]. Chin J Magn Reson Imaging, 2023, 14(10): 125-131. DOI:10.12015/issn.1674-8034.2023.10.022.


[Abstract] Parkinson's disease (PD) is a common, progressive degenerative neurological disease for which there is no cure. The non-invasive neuromodulation (NINM) possesses the advantage of significant efficacy, less adverse effects, convenience and readily accepted by patients, they have great potential in treating different motor and non-motor symptoms of Parkinson's disease. MRI can reveal the information of brain structure and function, and has been widely used in the efficacy evaluation of various neuromodulation therapies and the exploration of neuromodulation mechanisms. This paper reviews the recent MRI studies of four types of NINM in the treatment of the neuromodulation mechanism of PD, including transcranial magnetic stimulation (TMS), transcranial electrical stimulation (TES), transcranial ultrasound stimulation (TUS) and noninvasive vagal nerve stimulation (nVNS).
[Keywords] Parkinson's disease；non-invasive neuromodulation；magnetic resonance imaging；transcranial magnetic stimulation；transcranial electrical stimulation；transcranial ultrasound stimulation；noninvasive vagal nerve stimulation

OUYANG Yinfei1   PENG Bei2   HUANG Jinli2   HUANG Jiazhu2   DENG Demao2*  

1 Graduate School of Guangxi University of Chinese Medicine, Nanning 530200, China

2 Department of Radiology, the People's Hospital of Guangxi Zhuang Autonomous Region, Nanning 530021, China

Corresponding author: DENG D M, E-mail: demaodeng@163.com

Conflicts of interest   None.

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 82060315); Guangxi Key Research and Development Plan Project (No. Gui Ke AB22080053).
Received  2023-04-20
Accepted  2023-09-08
DOI: 10.12015/issn.1674-8034.2023.10.022
Cite this article as: OUYANG Y F, PENG B, HUANG J L, et al. MRI research progress on the neuromodulation mechanism of non-invasive neuromodulation for Parkinson's disease[J]. Chin J Magn Reson Imaging, 2023, 14(10): 125-131. DOI:10.12015/issn.1674-8034.2023.10.022.

[1]
GBD 2016 Parkinson's Disease Collaborators. Global, regional, and national burden of Parkinson's disease, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016[J]. Lancet Neurol, 2018, 17(11): 939-953. DOI: 10.1016/S1474-4422(18)30295-3.
[2]
BOCK M A, BROWN E G, ZHANG L, et al. Association of Motor and Nonmotor Symptoms With Health-Related Quality of Life in a Large Online Cohort of People With Parkinson Disease[J/OL]. Neurology, 2022, 98(22): e2194-e2203 [2023-04-19]. https://doi.org/10.1212/WNL.0000000000200113. DOI: 10.1212/WNL.0000000000200113.
[3]
COLE R C, OKINE D N, YEAGER B E, et al. Neuromodulation of cognition in Parkinson's disease[J]. Prog Brain Res, 2022, 269(1): 435-455. DOI: 10.1016/bs.pbr.2022.01.016.
[4]
BRITTAIN J S, CAGNAN H. Recent Trends in the Use of Electrical Neuromodulation in Parkinson's Disease[J]. Curr Behav Neurosci Rep, 2018, 5(2): 170-178. DOI: 10.1007/s40473-018-0154-9.
[5]
MITCHELL T, LEHÉRICY S, CHIU S Y, et al. Emerging Neuroimaging Biomarkers Across Disease Stage in Parkinson Disease[J]. JAMA Neurology, 2021, 78(10): 1262-1272.
[6]
SOMAA F A, DE GRAAF T A, SACK A T. Transcranial Magnetic Stimulation in the Treatment of Neurological Diseases[J/OL]. Front Neurol, 2022, 13: 793253 [2023-04-19]. https://doi.org/10.3389/fneur.2022.793253. DOI: 10.3389/fneur.2022.793253.
[7]
KALIA L V, LANG A E. Parkinson's disease[J]. Lancet, 2015, 386(9996): 896-912. DOI: 10.1016/S0140-6736(14)61393-3.
[8]
CONG S, XIANG C, ZHANG S, et al. Prevalence and clinical aspects of depression in Parkinson's disease: A systematic review and meta-analysis of 129 studies[J/OL]. Neurosci Biobehav Rev, 2022, 141: 104749 [2023-04-19]. https://doi.org/10.1016/j.neubiorev.2022.104749. DOI: 10.1016/j.neubiorev.2022.104749.
[9]
ZHENG H B, LIU B, SHEN J, et al. Non-invasive brain stimulation for treating psychiatric symptoms in Parkinson's disease: A systematic review and meta-analysis[J]. J Clin Neurosci, 2022, 106: 83-90. DOI: 10.1016/j.jocn.2022.10.013.
[10]
CARDOSO E F, FREGNI F, MARTINS MAIA F, et al. rTMS treatment for depression in Parkinson's disease increases BOLD responses in the left prefrontal cortex[J]. Int J Neuropsychopharmacol, 2008, 11(2): 173-183. DOI: 10.1017/S1461145707007961.
[11]
KANG J I, LEE H, JHUNG K, et al. Frontostriatal Connectivity Changes in Major Depressive Disorder After Repetitive Transcranial Magnetic Stimulation: A Randomized Sham-Controlled Study[J]. J Clin Psychiatry, 2016, 77(9): e1137-e1143. DOI: 10.4088/JCP.15m10110.
[12]
TANG J F, ZHENG W K, AO J, et al. Clinical efficacy of Jin's three-needle therapy combined with low frequency rTMS on de-pression in Parkinson's disease based on magnetic resonance spectroscopy[J]. Journal of Epileptology and Electroneurophysiology, 2023, 32(1): 31-36. DOI: 10.19984/j.cnki.1674-8972.2023.01.06.
[13]
TANG J F, ZHENG W K, ZHANG J, et al. Clinical efficacy of repetitive transcranial magnetic stimulation in treatment of depres-sion in Parkinson's disease and the study of magnetic resonance spectroscopy analysis[J]. Journal of Epileptology and Electroneurophysiology, 2020, 29(6): 333-337.
[14]
MAGGI G, VITALE C, CERCIELLO F, et al. Sleep and wakefulness disturbances in Parkinson's disease: A meta-analysis on prevalence and clinical aspects of REM sleep behavior disorder, excessive daytime sleepiness and insomnia[J/OL]. Sleep Med Rev, 2023, 68: 101759 [2023-04-19]. https://doi.org/10.1016/j.smrv.2023.101759. DOI: 10.1016/j.smrv.2023.101759.
[15]
BAIANO C, BARONE P, TROJANO L, et al. Prevalence and clinical aspects of mild cognitive impairment in Parkinson's disease: A meta-analysis[J]. Mov Disord, 2020, 35(1): 45-54. DOI: 10.1002/mds.27902.
[16]
SHAN J, WANG Y Z, LAI C Q. Clinical efficacy of high frequency rTMS combined with selegilan hydrochloride in the treatment of PD with excessive daytime sleepiness sleep disorder and its correlation with DTI[J]. Chinese Journal of Rehabilitation, 2022, 37(10): 592-597. DOI: 10.3870/zgkf.2022.10.004.
[17]
JIANG Y, AN H, XI Q, et al. Diffusion tensor imaging reveals deep brain structure changes in early Parkinson's disease patients with various sleep disorders[J/OL]. Brain Sci, 2022, 12(4): 463 [2023-04-19]. https://doi.org/10.3390/brainsci12040463. DOI: 10.3390/brainsci12040463.
[18]
LANG S, GAN L S, YOON E J, et al. Theta-burst stimulation for cognitive enhancement in Parkinson's disease with mild cognitive impairment: A randomized, double-blind, sham-controlled trial[J/OL]. Front Neurol, 2020, 11: 584374 [2023-04-19]. https://doi.org/10.3389/fneur.2020.584374. DOI: 10.3389/fneur.2020.584374.
[19]
MADRID J, BENNINGER D H. Non-invasive brain stimulation for Parkinson's disease: Clinical evidence, latest concepts and future goals: A systematic review[J/OL]. J Neurosci Methods, 2021, 347: 108957 [2023-04-19]. https://doi.org/10.1016/j.jneumeth.2020.108957. DOI: 10.1016/j.jneumeth.2020.108957.
[20]
BHAT P, GOYAL V, KUMARAN S S, et al. Mechanisms of 1Hz inhibitory and 5Hz excitatory repetitive transcranial magnetic stimulations in Parkinson's Disease- An fMRI study[J]. Brain Connect, 2023, 13(4): 247-263. DOI: 10.1089/brain.2022.0043.
[21]
JI G J, LIU T, LI Y, et al. Structural correlates underlying accelerated magnetic stimulation in Parkinson's disease[J]. Hum Brain Mapp, 2021, 42(6): 1670-1681. DOI: 10.1002/hbm.25319.
[22]
GONZALEZ-GARCIA N, ARMONY J L, SOTO J, et al. Effects of rTMS on Parkinson's disease: a longitudinal fMRI study[J]. J Neurol, 2011, 258(7): 1268-1280. DOI: 10.1007/s00415-011-5923-2.
[23]
WEN X, CHI S, YU Y, et al. The Cerebellum is Involved in Motor Improvements After Repetitive Transcranial Magnetic Stimulation in Parkinson's Disease Patients[J]. Neuroscience, 2022, 499: 1-11. DOI: 10.1016/j.neuroscience.2022.07.004.
[24]
CHI S, WEN X, YU Y, et al. Sensorimotor network connectivity correlates with motor improvement after repetitive transcranial magnetic stimulation in patients with Parkinson's disease[J/OL]. Parkinsonism Relat Disord, 2023, 106: 105218 [2023-04-19]. https://doi.org/10.1016/j.parkreldis.2022.11.010. DOI: 10.1016/j.parkreldis.2022.11.010.
[25]
LEODORI G, BELVISI D, DE BARTOLO M I, et al. Re-emergent Tremor in Parkinson's Disease: The Role of the Motor Cortex[J]. Mov Disord, 2020, 35(6): 1002-1011. DOI: 10.1002/mds.28022.
[26]
LEODORI G, DE BARTOLO M I, FABBRINI A, et al. The Role of the Motor Cortex in Tremor Suppression in Parkinson's Disease[J]. J Parkinsons Dis, 2022, 12(6): 1957-1963. DOI: 10.3233/JPD-223316.
[27]
ZHANG W S, GAO C, TAN Y Y, et al. Prevalence of freezing of gait in Parkinson's disease: a systematic review and meta-analysis[J]. J Neurol, 2021, 268(11): 4138-4150. DOI: 10.1007/s00415-021-10685-5.
[28]
MI T M, GARG S, BA F, et al. Repetitive transcranial magnetic stimulation improves Parkinson's freezing of gait via normalizing brain connectivity[J/OL]. NPJ Parkinsons Dis, 2020, 6: 16 [2023-04-19]. https://doi.org/10.1038/s41531-020-0118-0. DOI: 10.1038/s41531-020-0118-0.
[29]
LENCH D H, DEVRIES W, KEARNEY-RAMOS T E, et al. Paired inhibitory stimulation and gait training modulates supplemental motor area connectivity in freezing of gait[J]. Parkinsonism Relat Disord, 2021, 88: 28-33. DOI: 10.1016/j.parkreldis.2021.05.028.
[30]
GONG S, GAO Y, LIU J, et al. The prevalence and associated factors of dysphagia in Parkinson's disease: A systematic review and meta-analysis[J/OL]. Front Neurol, 2022, 13: 1000527 [2023-04-19]. https://doi.org/10.3171/2021.12.JNS211729. DOI: 10.3389/fneur.2022.1000527.
[31]
KLUIN K J, MOSSNER J M, COSTELLO J T, et al. Motor speech effects in subthalamic deep brain stimulation for Parkinson's disease[J]. J Neurosurg, 2022: 1-7. DOI: 10.3171/2021.12.JNS211729.
[32]
KHEDR E M, MOHAMED K O, SOLIMAN R K, et al. The Effect of High-Frequency Repetitive Transcranial Magnetic Stimulation on Advancing Parkinson's Disease With Dysphagia: Double Blind Randomized Clinical Trial[J]. Neurorehabil Neural Repair, 2019, 33(6): 442-452. DOI: 10.1177/1545968319847968.
[33]
HUANG P L, WANG S J, SUN R F, et al. Increased activation of the caudate nucleus and parahippocampal gyrus in Parkinson's disease patients with dysphagia after repetitive transcranial magnetic stimulation: a case-control study[J]. Neural Regen Res, 2022, 17(5): 1051-1058. DOI: 10.4103/1673-5374.324863.
[34]
BRABENEC L, SIMKO P, SEJNOHA MINSTEROVA A, et al. Repetitive transcranial magnetic stimulation for hypokinetic dysarthria in Parkinson's disease enhances white matter integrity of the auditory-motor loop[J]. Eur J Neurol, 2023, 30(4): 881-886. DOI: 10.1111/ene.15665.
[35]
BRABENEC L, KLOBUSIAKOVA P, SIMKO P, et al. Non-invasive brain stimulation for speech in Parkinson's disease: A randomized controlled trial[J]. Brain Stimul, 2021, 14(3): 571-578. DOI: 10.1016/j.brs.2021.03.010.
[36]
HERZ D M, HAAGENSEN B N, NIELSEN S H, et al. Resting-state connectivity predicts levodopa-induced dyskinesias in Parkinson's disease[J]. Mov Disord, 2016, 31(4): 521-529. DOI: 10.1002/mds.26540.
[37]
CERASA A, MESSINA D, PUGLIESE P, et al. Increased prefrontal volume in PD with levodopa-induced dyskinesias: a voxel-based morphometry study[J]. Mov Disord, 2011, 26(5): 807-812. DOI: 10.1002/mds.23660.
[38]
CERASA A, PUGLIESE P, MESSINA D, et al. Prefrontal alterations in Parkinson's disease with levodopa-induced dyskinesia during fMRI motor task[J]. Mov Disord, 2012, 27(3): 364-371. DOI: 10.1002/mds.24017.
[39]
CERASA A, KOCH G, DONZUSO G, et al. A network centred on the inferior frontal cortex is critically involved in levodopa-induced dyskinesias[J]. Brain, 2015, 138(Pt 2): 414-427. DOI: 10.1093/brain/awu329.
[40]
XIA Q L, JIANG B, LIU D H, et al. The application and prospect of combined functional magnetic resonance imaging and transcranial magnetic stimulation on the modulation of brain functional network[J]. Chin J Magn Reson Imaging, 2022, 13(8): 117-120, 129. DOI: 10.12015/issn.1674-8034.2022.08.026.
[41]
FARNAD L, GHASEMIAN-SHIRVAN E, MOSAYEBI-SAMANI M, et al. Exploring and optimizing the neuroplastic effects of anodal transcranial direct current stimulation over the primary motor cortex of older humans[J]. Brain Stimul, 2021, 14(3): 622-634. DOI: 10.1016/j.brs.2021.03.013.
[42]
ISHIKURO K, HATTORI N, IMANISHI R, et al. A Parkinson's disease patient displaying increased neuromelanin-sensitive areas in the substantia nigra after rehabilitation with tDCS: a case report[J]. Neurocase, 2021, 27(5): 407-414. DOI: 10.1080/13554794.2021.1975768.
[43]
PEREIRA J B, JUNQUE C, BARTRES-FAZ D, et al. Modulation of verbal fluency networks by transcranial direct current stimulation (tDCS) in Parkinson's disease[J]. Brain Stimul, 2013, 6(1): 16-24. DOI: 10.1016/j.brs.2012.01.006.
[44]
MULLER D, HABEL U, BRODKIN E S, et al. High-definition transcranial direct current stimulation (HD-tDCS) for the enhancement of working memory - A systematic review and meta-analysis of healthy adults[J]. Brain Stimul, 2022, 15(6): 1475-1485. DOI: 10.1016/j.brs.2022.11.001.
[45]
DARROW D P. Focused Ultrasound for Neuromodulation[J]. Neurotherapeutics, 2019, 16(1): 88-99. DOI: 10.1007/s13311-018-00691-3.
[46]
BLACKMORE J, SHRIVASTAVA S, SALLET J, et al. Ultrasound Neuromodulation: A Review of Results, Mechanisms and Safety[J]. Ultrasound Med Biol, 2019, 45(7): 1509-1536. DOI: 10.1016/j.ultrasmedbio.2018.12.015.
[47]
LEE K S, CLENNELL B, STEWARD T G J, et al. Focused ultrasound stimulation as a neuromodulatory tool for Parkinson's disease: a scoping review[J/OL]. Brain Sci, 2022, 12(2): 289 [2023-04-19]. https://doi.org/10.3390/brainsci12020289. DOI: 10.3390/brainsci12020289.
[48]
WANG Z, YAN J, WANG X, et al. Transcranial Ultrasound Stimulation Directly Influences the Cortical Excitability of the Motor Cortex in Parkinsonian Mice[J]. Mov Disord, 2020, 35(4): 693-698. DOI: 10.1002/mds.27952.
[49]
ZHOU H, NIU L, MENG L, et al. Noninvasive Ultrasound Deep Brain Stimulation for the Treatment of Parkinson's Disease Model Mouse[J/OL]. Research (Wash D C), 2019, 2019: 1748489 [2023-04-19]. https://doi.org/10.34133/2019/1748489. DOI: 10.34133/2019/1748489.
[50]
ZHOU H, NIU L, XIA X, et al. Wearable Ultrasound Improves Motor Function in an MPTP Mouse Model of Parkinson's Disease[J]. IEEE Trans Biomed Eng, 2019, 66(11): 3006-3013. DOI: 10.1109/TBME.2019.2899631.
[51]
CHEN X, WANG D, ZHANG L, et al. Neuroprotective Effect of Low-Intensity Pulsed Ultrasound on the Mouse MPTP/MPP(+) Model of Dopaminergic Neuron Injury[J]. Ultrasound Med Biol, 2021, 47(8): 2321-2330. DOI: 10.1016/j.ultrasmedbio.2021.03.034.
[52]
SONG W S, SUNG C Y, KE C H, et al. Anti-inflammatory and Neuroprotective Effects of Transcranial Ultrasound Stimulation on Parkinson's Disease[J]. Ultrasound Med Biol, 2022, 48(2): 265-274. DOI: 10.1016/j.ultrasmedbio.2021.10.001.
[53]
SUNG C Y, CHIANG P K, TSAI C W, et al. Low-Intensity Pulsed Ultrasound Enhances Neurotrophic Factors and Alleviates Neuroinflammation in a Rat Model of Parkinson's Disease[J]. Cereb Cortex, 2021, 32(1): 176-185. DOI: 10.1093/cercor/bhab201.
[54]
DONG Y, LIU D, ZHAO Y, et al. Assessment of neuroprotective effects of low-intensity transcranial ultrasound stimulation in a Parkinson's disease rat model by fractional anisotropy and relaxation time T2* value[J/OL]. Front Neurosci, 2021, 15: 590354 [2023-04-19]. https://doi.org/10.3389/fnins.2021.590354. DOI: 10.3389/fnins.2021.590354.
[55]
RONG P J, ZHANG Y, LI S Y, et al. Present Status and Prospect of Transcutaneous Auricular Vagus Nerve Stimulation in the Treatment of Encephalopathy and Relating Diseases[J]. World Science and Technology-Modernization of Traditional Chinese Medicine, 2019, 21(9): 1799-1804. DOI: 10.11842/wst.20190619002.
[56]
FARRAND A Q, HELKE K L, GREGORY R A, et al. Vagus nerve stimulation improves locomotion and neuronal populations in a model of Parkinson's disease[J]. Brain Stimul, 2017, 10(6): 1045-1054. DOI: 10.1016/j.brs.2017.08.008.
[57]
KIN I, SASAKI T, YASUHARA T, et al. Vagus nerve stimulation with mild stimulation intensity exerts anti-inflammatory and neuroprotective effects in Parkinson's disease model rats[J/OL]. Biomedicines, 2021, 9(7): 789 [2023-04-19]. https://doi.org/10.3390/biomedicines9070789. DOI: 10.3390/biomedicines9070789.
[58]
WANG C, SU T, XIAO L, et al. Right vagus nerve stimulation improves motor behavior by exerting neuroprotective effects in Parkinson's disease rats[J/OL]. Ann Transl Med, 2022, 10(24): 1314 [2023-04-19]. https://doi.org/10.21037/atm-22-5366. DOI: 10.21037/atm-22-5366.
[59]
KAUT O, JANOCHA L, WEISMULLER T J, et al. Transcutaneous vagal nerve stimulation improves gastroenteric complaints in Parkinson's disease patients[J]. NeuroRehabilitation, 2019, 45(4): 449-451. DOI: 10.3233/NRE-192909.
[60]
MONDAL B, CHOUDHURY S, SIMON B, et al. Noninvasive vagus nerve stimulation improves gait and reduces freezing of gait in Parkinson's disease[J]. Mov Disord, 2019, 34(6): 917-918. DOI: 10.1002/mds.27662.
[61]
MORRIS R, YARNALL A J, HUNTER H, et al. Noninvasive vagus nerve stimulation to target gait impairment in Parkinson's disease[J]. Mov Disord, 2019, 34(6): 918-919. DOI: 10.1002/mds.27664.
[62]
MARANO M, ANZINI G, MUSUMECI G, et al. Transcutaneous Auricular Vagus Stimulation Improves Gait and Reaction Time in Parkinson's Disease[J]. Mov Disord, 2022, 37(10): 2163-2164. DOI: 10.1002/mds.29166.
[63]
TORRECILLOS F, TAN H, BROWN P, et al. Non-invasive vagus nerve stimulation modulates subthalamic beta activity in Parkinson's disease[J]. Brain Stimulation, 2022, 15(6): 1513-1516. DOI: 10.1016/j.brs.2022.11.006.
[64]
ZAEHLE T, GALAZKY I, KRAUEL K. The LC-NE system as a potential target for neuromodulation to ameliorate non-motor symptoms in Parkinson's disease[J/OL]. Auton Neurosci, 2021, 236: 102901 [2023-04-19]. https://doi.org/10.1016/j.autneu.2021.102901. DOI: 10.1016/j.autneu.2021.102901.

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