Share:
Share this content in WeChat
X
Original Article
Abnormal degree centrality values in the frontotemporal lobe, cerebellum and sensorimotor regions are associated with gait freezing in Parkinson's patients
TANG Wei  XU Qian  GAO Tingting  DONG Liao  YANG Guang  DU Xiaoxia  CHEN Wei 

Cite this article as: Tang W, Xu Q, Gao TT, 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.


[Abstract] Objective The purpose of this study is to investigate the changes of degree centrality (DC) in Parkinson's disease (PD) patients with freezing of gait (FOG) by resting-state functional magnetic resonance imaging (rs-fMRI) and to explore the pathological mechanism of FOG.Materials and Methods A total of 17 patients with PD with FOG (FOG+), 36 patients with PD without FOG (FOG-), and 44 healthy controls (HC) were recruited. All subjects underwent rs-fMRI scanning. Calculate the DC values of FOG+, FOG- and HC from the resting-state data. The brain regions with statistically significant difference among the three groups were obtained by F test. Two sample t-test was used to compare the differences among FOG+, FOG- and HC. The results were assigned thresholds at P<0.001 (voxel level) and Familywise error rate (FWE) corrected to P<0.05 at the cluster level and cluster size>20. The DC values of brain regions with statistically significant differences among groups were extracted and correlated with the scores of 17-item Hamilton Rating Scale for Depression (HAMD-17) and FOG questionnaire.Results The results showed that the main effects among the three groups were in the right anterior central gyrus, the right posterior central gyrus, the right insula, the right medial frontal gyrus, the right superior parietal lobule, and the right frontal lobe sub-gyral. Further two-sample analysis showed that compared with the HC group, DC value in the FOG+ group significantly decreased in the right medial frontal gyrus, left precentral gyrus, and right superior temporal gyrus; However, in the left superior frontal gyrus and the right superior frontal gyrus, there was a significant increase. Compared with the HC group, DC value in the FOG group increased significantly in the left superior frontal gyrus, right cerebellar Ⅸ lobule area, and decreased significantly in the right central posterior gyrus, left central posterior gyrus, right superior frontal gyrus, left central anterior gyrus and left external nucleus. In addition, the correlation analysis showed that the FOG questionnaire score of the FOG+ group was positively correlated with the DC values of the left precentral gyrus and the right superior temporal gyrus (r=0.574, P=0.020; r=0.506, P=0.046); HAMD-17 score was positively correlated with right medial frontal gyrus (r=0.547, P=0.028).Conclusions The abnormal DC values of the frontal lobe, anterior central gyrus, posterior central gyrus, temporal lobe, and cerebellum in PD patients may be closely related to the brain dysfunction of FOG+.
[Keywords] parkinson's disease;freezing of gait;degree centrality;magnetic resonance imaging

TANG Wei1   XU Qian2   GAO Tingting1   DONG Liao1   YANG Guang1   DU Xiaoxia3*   CHEN Wei2*  

1 Shanghai Key Laboratory of Magnetic Resonance, Department of Physics, East China Normal University, Shanghai 200062, China

2 Department of Neurology, Shanghai Ninth People's Hospital Shanghai Jiao Tong University School of Medicine, Shanghai 200011, China

3 School of Psychology, Shanghai University of Sport, Shanghai 200438, China

Du XX, E-mail: duxiaoxia@sus.edu.cn Chen W, E-mail: david_chen8106@hotmail.com

Conflicts of interest   None.

Received  2022-03-09
Accepted  2022-07-01
DOI: 10.12015/issn.1674-8034.2022.07.015
Cite this article as: Tang W, Xu Q, Gao TT, 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

[1]
Teive HAG, Cunha P, Ferreira MG, et al. Freezing of gait (FOG) in Parkinson's disease patients-the contribution of Garcin and Melaragno[J]. Neurol Sci, 2021, 42(12): 5413-5417. DOI: 10.1007/s10072-021-05381-1.
[2]
Weiss D, Schoellmann A, Fox MD, et al. Freezing of gait: understanding the complexity of an enigmatic phenomenon[J]. Brain, 2020, 143(1): 14-30. DOI: 10.1093/brain/awz314.
[3]
Li KP, Zhou ZL, Zhou RZ, et al. Improvement of freezing of gait in patients with Parkinson's disease by music exercise therapy: a study protocol for a randomized controlled trial[J]. Trials, 2021, 22(1): 335. DOI: 10.1186/s13063-021-05258-w.
[4]
Rutz DG, Benninger DH. Physical therapy for freezing of gait and gait impairments in parkinson disease: a systematic review[J]. PM R, 2020, 12(11): 1140-1156. DOI: 10.1002/pmrj.12337.
[5]
Rahimpour S, Gaztanaga W, Yadav AP, 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.
[6]
Sparacia G, Parla G, Mamone G, et al. Resting-state functional magnetic resonance imaging for surgical neuro-oncology planning: towards a standardization in clinical settings[J]. Brain Sci, 2021, 11(12): 1613. DOI: 10.3390/brainsci11121613.
[7]
Bharti K, Suppa A, Pietracupa S, et al. Aberrant functional connectivity in patients with Parkinson's disease and freezing of gait: a within- and between-network analysis[J]. Brain Imaging Behav, 2020, 14(5): 1543-1554. DOI: 10.1007/s11682-019-00085-9.
[8]
Gallardo MJ, Cabello JP, Corrales MJ, et al. Freezing of gait in Parkinson's disease: functional neuroimaging studies of the frontal lobe[J]. Neurol Res, 2018, 40(10): 900-905. DOI: 10.1080/01616412.2018.1484985.
[9]
Bharti K, Suppa A, Pietracupa S, et al. Abnormal cerebellar connectivity patterns in patients with Parkinson's disease and freezing of gait[J]. Cerebellum, 2019, 18(3): 298-308. DOI: 10.1007/s12311-018-0988-4.
[10]
Myers PS, McNeely ME, Pickett KA, et al. Effects of exercise on gait and motor imagery in people with Parkinson disease and freezing of gait[J]. Parkinsonism Relat Disord, 2018, 53: 89-95. DOI: 10.1016/j.parkreldis.2018.05.006.
[11]
Mi TM, Mei SS, Liang PP, et al. Author Correction: altered resting-state brain activity in Parkinson's disease patients with freezing of gait[J]. Sci Rep, 2018, 8: 4792. DOI: 10.1038/s41598-018-23233-5.
[12]
Pietracupa S, Suppa A, Upadhyay N, et al. Freezing of gait in Parkinson's disease: gray and white matter abnormalities[J]. J Neurol, 2018, 265(1): 52-62. DOI: 10.1007/s00415-017-8654-1.
[13]
Song WJ, Raza HK, 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.
[14]
Xing CH, Chen YC, Tong ZP, et al. Aberrant brain functional hubs and causal connectivity in presbycusis[J]. Brain Imaging Behav, 2021, 15(1): 453-463. DOI: 10.1007/s11682-020-00386-4.
[15]
Zuo XN, Ehmke R, Mennes M, et al. Network centrality in the human functional connectome[J]. Cereb Cortex, 2012, 22(8): 1862-1875. DOI: 10.1093/cercor/bhr269.
[16]
Zuo XN, Xing XX. Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: a systems neuroscience perspective[J]. Neurosci Biobehav Rev, 2014, 45: 100-118. DOI: 10.1016/j.neubiorev.2014.05.009.
[17]
Guo MR, Ren Y, Yu HM, et al. Alterations in degree centrality and functional connectivity in Parkinson's disease patients with freezing of gait: a resting-state functional magnetic resonance imaging study[J]. Front Neurosci, 2020, 14: 582079. DOI: 10.3389/fnins.2020.582079.
[18]
Jin CY, Qi SL, Teng YY, et al. Altered degree centrality of brain networks in Parkinson's disease with freezing of gait: a resting-state functional MRI study[J]. Front Neurol, 2021, 12: 743135. DOI: 10.3389/fneur.2021.743135.
[19]
Giladi N, Shabtai H, Simon ES, et al. Construction of freezing of gait questionnaire for patients with Parkinsonism[J]. Parkinsonism Relat Disord, 2000, 6(3): 165-170. DOI: 10.1016/s1353-8020(99)00062-0.
[20]
Postuma RB, 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.
[21]
Murphy K, Birn RM, Handwerker DA, et al. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?[J]. NeuroImage, 2009, 44(3): 893-905. DOI: 10.1016/j.neuroimage.2008.09.036.
[22]
van der Hoorn A, Burger H, Leenders KL, et al. Handedness correlates with the dominant Parkinson side: a systematic review and meta-analysis[J]. Mov Disord, 2012, 27(2): 206-210. DOI: 10.1002/mds.24007.
[23]
Fling BW, Cohen RG, Mancini M, et al. Asymmetric pedunculopontine network connectivity in parkinsonian patients with freezing of gait[J]. Brain, 2013, 136(Pt 8): 2405-2418. DOI: 10.1093/brain/awt172.
[24]
Vastik M, Hok P, Valosek J, et al. Freezing of gait is associated with cortical thinning in mesial frontal cortex[J]. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub, 2017, 161(4): 389-396. DOI: 10.5507/bp.2017.035.
[25]
Mirelman A, Shema S, Maidan I, et al. Gait[J]. Handb Clin Neurol, 2018, 159: 119-134. DOI: 10.1016/B978-0-444-63916-5.00007-0.
[26]
Hu HQ, Chen JW, Huang HY, et al. Common and specific altered amplitude of low-frequency fluctuations in Parkinson's disease patients with and without freezing of gait in different frequency bands[J]. Brain Imaging Behav, 2020, 14(3): 857-868. DOI: 10.1007/s11682-018-0031-x.
[27]
Wang M, Jiang SM, Yuan YS, et al. Alterations of functional and structural connectivity of freezing of gait in Parkinson's disease[J]. J Neurol, 2016, 263(8): 1583-1592. DOI: 10.1007/s00415-016-8174-4.
[28]
Bostan AC, Dum RP, Strick PL. Cerebellar networks with the cerebral cortex and basal Ganglia[J]. Trends Cogn Sci, 2013, 17(5): 241-254. DOI: 10.1016/j.tics.2013.03.003.
[29]
Piramide N, Agosta F, Sarasso E, et al. Brain activity during lower limb movements in Parkinson's disease patients with and without freezing of gait[J]. J Neurol, 2020, 267(4): 1116-1126. DOI: 10.1007/s00415-019-09687-1.
[30]
Li NN, Suo XL, Zhang JH, et al. Disrupted functional brain network topology in Parkinson's disease patients with freezing of gait[J]. Neurosci Lett, 2021, 759: 135970. DOI: 10.1016/j.neulet.2021.135970.
[31]
Bommarito G, Putzolu M, Avanzino L, et al. Functional correlates of action observation of gait in patients with Parkinson's disease[J]. Neural Plast, 2020, 2020: 8869201. DOI: 10.1155/2020/8869201.
[32]
Nutt JG, Marsden CD, Thompson PD. Human walking and higher-level gait disorders, particularly in the elderly[J]. Neurology, 1993, 43(2): 268-279. DOI: 10.1212/wnl.43.2.268.
[33]
Pagnussat AS, Salazar AP, Pinto C, et al. Plantar stimulation alters brain connectivity in idiopathic Parkinson's disease[J]. Acta Neurol Scand, 2020, 142(3): 229-238. DOI: 10.1111/ane.13253.
[34]
Hamilton M. A rating scale for depression[J]. J Neurol Neurosurg Psychiatry, 1960, 23(1): 56-62. DOI: 10.1136/jnnp.23.1.56.
[35]
Sarasso E, Agosta F, Piramide N, et al. Brain activity of the emotional circuit in Parkinson's disease patients with freezing of gait[J]. Neuroimage Clin, 2021, 30: 102649. DOI: 10.1016/j.nicl.2021.102649.
[36]
Scully A, Doshi K, Henderson S, et al. A pilot randomized controlled trial examining the benefits of an adjuvant psycho-behavioural intervention in comparison to a health education program, on psychological well-being and freezing-of-gait in patients with Parkinson's disease[J]. Parkinsonism Relat Disord, 2021, 91: 152-153. DOI: 10.1016/j.parkreldis.2021.09.023.
[37]
Ehgoetz Martens KA, Ellard CG, Almeida QJ. Does anxiety cause freezing of gait in Parkinson's disease?[J]. PLoS One, 2014, 9(9): e106561. DOI: 10.1371/journal.pone.0106561.
[38]
Lichter DG, Benedict RHB, Hershey LA. Freezing of gait in Parkinson's disease: risk factors, their interactions, and associated nonmotor symptoms[J]. Park Dis, 2021, 2021: 8857204. DOI: 10.1155/2021/8857204.
[39]
Li YT, Ruan XH, Li E, et al. Aberrant advanced cognitive and attention-related brain networks in Parkinson's disease with freezing of gait[J]. Neural Plast, 2020, 2020: 8891458. DOI: 10.1155/2020/8891458.
[40]
Gilat M, Ehgoetz Martens KA, Miranda-Domínguez 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.

PREV Preliminary study on brain network of patients with somatic symptom disorder based on probabilistic fiber tracking
NEXT Brain complexity in the patients of Parkinson,s disease with depression: a resting-state functional magnetic resonance imaging study
  



Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn