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Review
Research progress on freezing of gait in Parkinson's disease based on multimodal MRI
HOU Junbao  SHI Qiye  WANG Yang  PENG Xiaohan  CAO Danna 

Cite this article as: HOU J B, SHI Q Y, WANG Y, et al. Research progress on freezing of gait in Parkinson's disease based on multimodal MRI[J]. Chin J Magn Reson Imaging, 2024, 15(2): 178-182. DOI:10.12015/issn.1674-8034.2024.02.028.


[Abstract] Freezing of gait (FOG) is a paroxysmal gait disturbance observed in patients with advanced-stage Parkinson's disease, significantly impacting their quality of life. However, there is still no clear elucidation of the pathogenesis and changes in brain structure and function during the course of the disease. In recent years, multimodal MRI imaging techniques, primarily utilizing diffusion tensor imaging (DTI), three-dimensional T1-weighted imaging (3D T1WI) and functional MRI (fMRI) have been widely employed in the exploration of the pathogenesis of neurological disorders. These techniques have provided new insights into the underlying mechanisms of FOG. Recent research indicates a close association between changes in visual, motor, and cognitive networks and the occurrence of FOG. The author aims to conduct a review by analyzing recent domestic and international literature, summarize multimodal MRI exploration of structural and functional changes in the brains of Parkinson's disease patients with freezing of gait. The review discusses the current controversial aspects of FOG research and proposes new perspectives for future comprehensive elucidation of its pathogenesis using multimodal MRI.
[Keywords] Parkinson's disease;freezing of gait;diffusion tensor imaging;magnetic resonance imaging;functional connectivity;brain network

HOU Junbao1   SHI Qiye1   WANG Yang2   PENG Xiaohan1   CAO Danna2*  

1 Graduate School of Heilongjiang University of Traditional Chinese Medicine, Harbin 150040, China

2 Department of CT & MR, the First Affiliated Hospital of Heilongjiang University of Traditional Chinese Medicine, Harbin 150040, China

Corresponding author: CAO D N, E-mail: hljanna@126.com

Conflicts of interest   None.

Received  2023-10-16
Accepted  2024-01-31
DOI: 10.12015/issn.1674-8034.2024.02.028
Cite this article as: HOU J B, SHI Q Y, WANG Y, et al. Research progress on freezing of gait in Parkinson's disease based on multimodal MRI[J]. Chin J Magn Reson Imaging, 2024, 15(2): 178-182. DOI:10.12015/issn.1674-8034.2024.02.028.

[1]
QU Y, LI J, CHEN Y, et al. Freezing of gait is a risk factor for cognitive decline in Parkinson's disease[J]. J Neurol, 2023, 270(1): 466-476. DOI: 10.1007/s00415-022-11371-w.
[2]
KWOK J Y Y, SMITH R, CHAN L M L, et al. Managing freezing of gait in Parkinson's disease: a systematic review and network meta-analysis[J]. J Neurol, 2022, 269(6): 3310-3324. DOI: 10.1007/s00415-022-11031-z.
[3]
YOGEV-SELIGMANN G, HAUSDORFF J M, GILADI N. The role of executive function and attention in gait[J]. Mov Disord, 2008, 23(3): 329-342. DOI: 10.1002/mds.21720.
[4]
RAHIMPOUR S, GAZTANAGA W, YADAV A P, et al. Freezing of gait in Parkinson's disease: Invasive and noninvasive neuromodulation[J]. Neuromodulation, 2021, 24(5): 829-842. DOI: 10.1111/ner.13347.
[5]
BARDAKAN M M, FINK G R, ZAPPAROLI L, et al. Imaging the neural underpinnings of freezing of gait in Parkinson's disease[J/OL]. Neuroimage Clin, 2022, 35: 103123 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/35917720. DOI: 10.1016/j.nicl.2022.103123.
[6]
EHGOETZ MARTENS K A, HALL J M, GEORGIADES M J, et al. The functional network signature of heterogeneity in freezing of gait[J]. Brain, 2018, 141(4): 1145-1160. DOI: 10.1093/brain/awy019.
[7]
KOU W, WANG X, ZHENG Y, et al. Freezing of gait in Parkinson's disease is associated with the microstructural and functional changes of globus pallidus internus[J/OL]. Front Aging Neurosci, 2022, 14: 975068 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/36062153. DOI: 10.3389/fnagi.2022.975068.
[8]
ONDER H, OGUZ K K, HAS A C, et al. Comparative analysis of freezing of gait in distinct Parkinsonism types by diffusion tensor imaging method and cognitive profiles[J]. J Neural Transm (Vienna), 2023, 130(4): 521-535. DOI: 10.1007/s00702-023-02608-7.
[9]
YOUN J, CHO J W, LEE W Y, et al. Diffusion tensor imaging of freezing of gait in patients with white matter changes[J]. Mov Disord, 2012, 27(6): 760-764. DOI: 10.1002/mds.24034.
[10]
YOUN J, LEE J M, KWON H, et al. Alterations of mean diffusivity of pedunculopontine nucleus pathway in Parkinson's disease patients with freezing of gait[J]. Parkinsonism Relat Disord, 2015, 21(1): 12-17. DOI: 10.1016/j.parkreldis.2014.10.003.
[11]
BHARTI K, SUPPA A, TOMMASIN S, et al. Neuroimaging advances in Parkinson's disease with freezing of gait: A systematic review[J/OL]. Neuroimage Clin, 2019, 24: 102059 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/31795038. DOI: 10.1016/j.nicl.2019.102059.
[12]
TESSITORE A, AMBONI M, CIRILLO G, et al. Regional gray matter atrophy in patients with Parkinson disease and freezing of gait[J]. AJNR Am J Neuroradiol, 2012, 33(9): 1804-1809. DOI: 10.3174/ajnr.A3066.
[13]
CHEN J W, MAI F Z, YANG Y Z, et al. Voxel-based analysis of brain microstructural diffusion indices changes in Parkinson disease with freezing of gait[J]. Chin Med J (Engl), 2020, 134(2): 249-251. DOI: 10.1097/CM9.0000000000001042.
[14]
ILIFF J J, WANG M, LIAO Y, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta[J/OL]. Sci Transl Med, 2012, 4(147): 147ra111 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/22896675. DOI: 10.1126/scitranslmed.3003748.
[15]
JEONG S H, PARK C J, JEONG H J, et al. Association of choroid plexus volume with motor symptoms and dopaminergic degeneration in Parkinson's disease[J/OL]. J Neurol Neurosurg Psychiatry, 2023 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/37399288. DOI: 10.1136/jnnp-2023-331170.
[16]
TAOKA T, MASUTANI Y, KAWAI H, et al. Evaluation of glymphatic system activity with the diffusion MR technique: diffusion tensor image analysis along the perivascular space (DTI-ALPS) in Alzheimer's disease cases[J]. Jpn J Radiol, 2017, 35(4): 172-178. DOI: 10.1007/s11604-017-0617-z.
[17]
CHEN A M, WEN J Y, HUANG J X, et al. Evaluation of glymphatic system activity by diffusion tensor image analysis along the perivascular space index in Parkinson's disease[J]. Radiol Pract, 2022, 37(8): 954-959. DOI: 10.13609/j.cnki.1000-0313.2022.08.006.
[18]
QIN Y, HE R, CHEN J, et al. Neuroimaging uncovers distinct relationships of glymphatic dysfunction and motor symptoms in Parkinson's disease[J]. J Neurol, 2023, 270(5): 2649-2658. DOI: 10.1007/s00415-023-11594-5.
[19]
RUAN X, HUANG X, LI Y, et al. Diffusion tensor imaging analysis along the perivascular space index in primary Parkinson's disease patients with and without freezing of gait[J]. Neuroscience, 2022, 506: 51-57. DOI: 10.1016/j.neuroscience.2022.10.013.
[20]
LI Q, QIU L H. Research progress of magnetic resonance 3D-T1 weighted imaging and diffusion tensor imaging in tremor-dominant Parkinson's disease[J]. Chin J Magn Reson Imaging, 2023, 14(8): 124-128. DOI: 10.12015/issn.1674-8034.2023.08.021.
[21]
KARACHI C, CORMIER-DEQUAIRE F, GRABLI D, et al. Clinical and anatomical predictors for freezing of gait and falls after subthalamic deep brain stimulation in Parkinson's disease patients[J]. Parkinsonism Relat Disord, 2019, 62: 91-97. DOI: 10.1016/j.parkreldis.2019.01.021.
[22]
BUCKLEY M J, GAFFAN D, MURRAY E A. Functional double dissociation between two inferior temporal cortical areas: perirhinal cortex versus middle temporal gyrus[J]. J Neurophysiol, 1997, 77(2): 587-598. DOI: 10.1152/jn.1997.77.2.587.
[23]
GAN L, YAN R, SU D, et al. Alterations of structure and functional connectivity of visual brain network in patients with freezing of gait in Parkinson's disease[J/OL]. Front Aging Neurosci, 2022, 14: 978976 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/36158540. DOI: 10.3389/fnagi.2022.978976.
[24]
ALENIKOVA O A, DYMKOVSKAYA M N. Features of visual, cognitive and neuroimaging changes in Parkinson's disease patients with freezing of gait[J]. Zh Nevrol Psikhiatr Im S S Korsakova, 2023, 123(1): 59-66. DOI: 10.17116/jnevro202312301159.
[25]
MIELING M, MEIER H, BUNZECK N. Structural degeneration of the nucleus basalis of Meynert in mild cognitive impairment and Alzheimer's disease-Evidence from an MRI-based meta-analysis[J/OL]. Neurosci Biobehav Rev, 2023, 154: 105393 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/37717861. DOI: 10.1016/j.neubiorev.2023.105393.
[26]
GAN C, CAO X, WANG L, et al. Cholinergic basal forebrain atrophy in Parkinson's disease with freezing of gait[J]. Ann Clin Transl Neurol, 2023, 10(5): 814-824. DOI: 10.1002/acn3.51769.
[27]
GHIELEN I, KOENE P, TWISK J W, et al. The association between freezing of gait, fear of falling and anxiety in Parkinson's disease: a longitudinal analysis[J]. Neurodegener Dis Manag, 2020, 10(3): 159-168. DOI: 10.2217/nmt-2019-0028.
[28]
GILAT M, EHGOETZ MARTENS K A, MIRANDA-DOMINGUEZ O, et al. Dysfunctional limbic circuitry underlying freezing of gait in Parkinson's disease[J]. Neuroscience, 2018, 374: 119-132. DOI: 10.1016/j.neuroscience.2018.01.044.
[29]
LV L, ZHANG H, TAN X, et al. Associated factors and abnormal dorsal raphe nucleus connectivity patterns of freezing of gait in Parkinson's disease[J]. J Neurol, 2022, 269(12): 6452-6466. DOI: 10.1007/s00415-022-11294-6.
[30]
TOGO H, NAKAMURA T, WAKASUGI N, et al. Interactions across emotional, cognitive and subcortical motor networks underlying freezing of gait[J/OL]. Neuroimage Clin, 2023, 37: 103342 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/36739790. DOI: 10.1016/j.nicl.2023.103342.
[31]
STEIDEL K, RUPPERT M C, PALAGHIA I, et al. Dopaminergic pathways and resting-state functional connectivity in Parkinson's disease with freezing of gait[J/OL]. Neuroimage Clin, 2021, 32: 102899 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/34911202. DOI: 10.1016/j.nicl.2021.102899.
[32]
POTVIN-DESROCHERS A, ATRI A, MORENO A M, et al. Levodopa alters resting-state functional connectivity more selectively in Parkinson's disease with freezing of gait[J]. Eur J Neurosci, 2023, 57(1): 163-177. DOI: 10.1111/ejn.15849.
[33]
MATSUI T, YAMASHITA K I. Static and Dynamic Functional Connectivity Alterations in Alzheimer's Disease and Neuropsychiatric Diseases[J]. Brain Connect, 2023, 13(5): 307-314. DOI: 10.1089/brain.2022.0044.
[34]
HUTCHISON R M, WOMELSDORF T, ALLEN E A, et al. Dynamic functional connectivity: promise, issues, and interpretations[J]. Neuroimage, 2013, 80: 360-378. DOI: 10.1016/j.neuroimage.2013.05.079.
[35]
WANG S, CAI H, CAO Z, et al. More Than Just Static: Dynamic Functional Connectivity Changes of the Thalamic Nuclei to Cortex in Parkinson's Disease With Freezing of Gait[J/OL]. Front Neurol, 2021, 12: 735999 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/34721266. DOI: 10.3389/fneur.2021.735999.
[36]
GAN C, JI M, SUN H, et al. Dynamic functional connectivity reveals hyper-connected pattern and abnormal variability in freezing of gait of Parkinson's disease[J/OL]. Neurobiol Dis, 2023, 185: 106265 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/37597816. DOI: 10.1016/j.nbd.2023.106265.
[37]
GUAN B, XU Y, CHEN Y C, et al. Reorganized Brain Functional Network Topology in Presbycusis[J/OL]. Front Aging Neurosci, 2022, 14: 905487 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/35693344. DOI: 10.3389/fnagi.2022.905487.
[38]
WANG L, GAN C, SUN H, et al. Impaired structural and reserved functional topological organizations of brain networks in Parkinson's disease with freezing of gait[J]. Quant Imaging Med Surg, 2023, 13(1): 66-79. DOI: 10.21037/qims-22-351.
[39]
LI N, SUO X, ZHANG J, et al. Disrupted functional brain network topology in Parkinson's disease patients with freezing of gait[J/OL]. Neurosci Lett, 2021, 759: 135970 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/34023405. DOI: 10.1016/j.neulet.2021.135970.
[40]
Tang W, Xu Q, Gao T T, et al. Abnormal degree centrality values in the frontotemporal lobe, cerebellum and sensorimotor regions are associated with gait freezing in Parkinson's patients[J]. Chin J Magn Reson Imaging, 2022, 13(7): 84-89. DOI: 10.12015/issn.1674-8034.2022.07.015.
[41]
RUAN X, HUANG X, LI Y, et al. Dysfunction of human brain network hierarchy in Parkinson's disease patients with freezing of gait[J/OL]. Parkinsonism Relat Disord, 2023, 112: 105446 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/37245278. DOI: 10.1016/j.parkreldis.2023.105446.
[42]
DANG L C, O'NEIL J P, JAGUST W J. Dopamine supports coupling of attention-related networks[J]. J Neurosci, 2012, 32(28): 9582-9587. DOI: 10.1523/JNEUROSCI.0909-12.2012.
[43]
MAIDAN I, JACOB Y, GILADI N, et al. Altered organization of the dorsal attention network is associated with freezing of gait in Parkinson's disease[J]. Parkinsonism Relat Disord, 2019, 63: 77-82. DOI: 10.1016/j.parkreldis.2019.02.036.
[44]
SREENIVASAN K, BAYRAM E, ZHUANG X, et al. Topological reorganization of functional hubs in patients with Parkinson's disease with freezing of gait[J]. J Neuroimaging, 2023, 33(4): 547-557. DOI: 10.1111/jon.13107.
[45]
SONG W, RAZA H K, LU L, et al. Functional MRI in Parkinson's disease with freezing of gait: a systematic review of the literature[J]. Neurol Sci, 2021, 42(5): 1759-1771. DOI: 10.1007/s10072-021-05121-5.
[46]
SNIJDERS A H, LEUNISSEN I, BAKKER M, et al. Gait-related cerebral alterations in patients with Parkinson's disease with freezing of gait[J]. Brain, 2011, 134(Pt 1): 59-72. DOI: 10.1093/brain/awq324.
[47]
MOREIRA-NETO A, UGRINOWITSCH C, COELHO D B, et al. Freezing of gait, gait initiation, and gait automaticity share a similar neural substrate in Parkinson's disease[J/OL]. Hum Mov Sci, 2022, 86: 103018 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/36334382. DOI: 10.1016/j.humov.2022.103018.
[48]
HUANG H C, CHEN C M, LU M K, et al. Gait-Related Brain Activation During Motor Imagery of Complex and Simple Ambulation in Parkinson's Disease With Freezing of Gait[J/OL]. Front Aging Neurosci, 2021, 13: 731332 [2023-10-16]. https://www.ncbi.nlm.nih.gov/pubmed/34630069. DOI: 10.3389/fnagi.2021.731332.
[49]
QUEK D Y L, ECONOMOU K, MACDOUGALL H, et al. Validating a Seated Virtual Reality Threat Paradigm for Inducing Anxiety and Freezing of Gait in Parkinson's Disease[J]. J Parkinsons Dis, 2021, 11(3): 1443-1454. DOI: 10.3233/JPD-212619.
[50]
TAYLOR N L, WAINSTEIN G, QUEK D, et al. The Contribution of Noradrenergic Activity to Anxiety-Induced Freezing of Gait[J]. Mov Disord, 2022, 37(7): 1432-1443. DOI: 10.1002/mds.28999.
[51]
LEWIS S J, BARKER R A. A pathophysiological model of freezing of gait in Parkinson's disease[J]. Parkinsonism Relat Disord, 2009, 15(5): 333-338. DOI: 10.1016/j.parkreldis.2008.08.006.

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