Advertisement

Common and specific altered amplitude of low-frequency fluctuations in Parkinson’s disease patients with and without freezing of gait in different frequency bands

  • Huiqing Hu
  • Jingwu Chen
  • Huiyuan Huang
  • Caihong Zhou
  • Shufei Zhang
  • Xian Liu
  • Lijuan Wang
  • Ping Chen
  • Kun Nie
  • Lixiang Chen
  • Shuai Wang
  • Biao HuangEmail author
  • Ruiwang HuangEmail author
ORIGINAL RESEARCH
  • 68 Downloads

Abstract

Freezing of gait (FOG), a disabling symptom of Parkinson’s disease (PD), severely affects PD patients’ life quality. Previous studies found neuropathologies in functional connectivity related to FOG, but few studies detected abnormal regional activities related to FOG in PD patients. In the present study, we analyzed the amplitude of low-frequency fluctuations (ALFF) to detect brain regions showing abnormal activity in PD patients with FOG (PD-with-FOG) and without FOG (PD-without-FOG). As different frequencies of neural oscillations in brain may reflect distinct brain functional and physiological properties, we conducted this study in three frequency bands, slow-5 (0.01–0.027 Hz), slow-4 (0.027–0.073 Hz), and classical frequency band (0.01–0.08 Hz). We acquired rs-fMRI data from 18 PD-with-FOG patients, 18 PD-without-FOG patients, and 17 healthy controls, then calculated voxel-wise ALFF across the whole brain and compared ALFF among the three groups in each frequency band. We found: (1) in slow-5, both PD-with-FOG and PD-without-FOG patients showed lower ALFF in the bilateral putamen compared to healthy controls, (2) in slow-4, PD-with-FOG patients showed higher ALFF in left inferior temporal gyrus (ITG) and lower ALFF in right middle frontal gyrus (MFG) compared to either PD-without-FOG patients or healthy controls, (3) in classical frequency band, PD-with-FOG patients also showed higher ALFF in ITG compared to either PD-without-FOG patients or healthy controls. Furthermore, we found that ALFF in MFG and ITG in slow-4 provided the highest classification accuracy (96.7%) in distinguishing PD-with-FOG from PD-without-FOG patients by using a stepwise multivariate pattern analysis. Our findings indicated frequency-specific regional spontaneous neural activity related to FOG, which may help to elucidate the pathogenesis of FOG.

Keywords

Freezing of gait (FOG) Amplitude of low-frequency fluctuations (ALFF) Frequency band Multivariate pattern analysis (MVPA) Functional MRI 

Notes

Acknowledgments

The study was supported by grants from the National Natural Science Foundation of China [Grant numbers: 81871338, 81471654, 81428013, 81671275, and 81371535]; Planned Science and Technology Project of Guangdong Province, China [Grant numbers: 2014B020212022, 1563000653, 20160402007]; Innovation Project of Graduate School of South China Normal University. The funding organizations played no further role in study design, data collection, analysis and interpretation, and paper writing. The authors appreciate the editing assistance of Drs.Rhoda E. and Edmund F. Perozzi.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all participants for being included in the study.

References

  1. Aarsland, D., Creese, B., Politis, M., Chaudhuri, K. R., Ffytche, D. H., Weintraub, D., & Ballard, C. (2017). Cognitive decline in Parkinson disease. Nature Reviews. Neurology, 13(4), 217–231.  https://doi.org/10.1038/nrneurol.2017.27.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anand, A., Li, Y., Wang, Y., Wu, J., Gao, S., Bukhari, L., Mathews, V. P., Kalnin, A., & Lowe, M. J. (2005). Activity and connectivity of brain mood regulating circuit in depression: A functional magnetic resonance study. Biological Psychiatry, 57(10), 1079–1088.  https://doi.org/10.1016/j.biopsych.2005.02.021.CrossRefPubMedGoogle Scholar
  3. Birn, R. M., Murphy, K., & Bandettini, P. A. (2008). The effect of respiration variations on independent component analysis results of resting state functional connectivity. Human Brain Mapping, 29(7), 740–750.  https://doi.org/10.1002/hbm.20577.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Biswal, B., Yetkin, F. Z., Haughton, V. M., & Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine, 34(4), 537–541.  https://doi.org/10.1002/mrm.1910340409.CrossRefPubMedGoogle Scholar
  5. Brodersen, K. H., Schofield, T. M., Leff, A. P., Ong, C. S., Lomakina, E. I., Buhmann, J. M., & Stephan, K. E. (2011). Generative embedding for model-based classification of fMRI data. PLoS Computational Biology, 7(6), e1002079.  https://doi.org/10.1371/journal.pcbi.1002079.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Buzsaki, G., & Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science, 304(5679), 1926–1929.  https://doi.org/10.1126/science.1099745.CrossRefPubMedGoogle Scholar
  7. Cai, S., Tao, C., Peng, Y., Shen, W., Li, J., Deneen, K. M. V., & Huang, L. (2016). Altered functional brain networks in amnestic mild cognitive impairment: A resting-state fMRI study. Brain Imaging and Behavior, 11(3), 619–631.  https://doi.org/10.1007/s11682-016-9539-0.CrossRefGoogle Scholar
  8. Caminiti, S. P., Presotto, L., Baroncini, D., Garibotto, V., Moresco, R. M., Gianolli, L., Volonté, M. A., Antonini, A., & Perani, D. (2017). Axonal damage and loss of connectivity in nigrostriatal and mesolimbic dopamine pathways in early Parkinson's disease. Neuroimage Clin, 14(C), 734–740.  https://doi.org/10.1016/j.nicl.2017.03.011.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Canu, E., Agosta, F., Sarasso, E., Volonte, M. A., Basaia, S., Stojkovic, T., Stefanova, E., Comi, G., Falini, A., Kostic, V. S., Gatti, R., & Filippi, M. (2015). Brain structural and functional connectivity in Parkinson's disease with freezing of gait. Human Brain Mapping, 36(12), 5064–5078.  https://doi.org/10.1002/hbm.22994.CrossRefPubMedGoogle Scholar
  10. Cerasa, A., Pugliese, P., Messina, D., Morelli, M., Gioia, M. C., Salsone, M., Novellino, F., Nicoletti, G., Arabia, G., & Quattrone, A. (2012). Prefrontal alterations in Parkinson's disease with levodopa-induced dyskinesia during fMRI motor task. Movement Disorders, 27(3), 364–371.  https://doi.org/10.1002/mds.24017.CrossRefPubMedGoogle Scholar
  11. Chen, H. M., Wang, Z. J., Fang, J. P., Gao, L. Y., Ma, L. Y., Wu, T., Hou, Y. N., Zhang, J. R., & Feng, T. (2015). Different patterns of spontaneous brain activity between tremor-dominant and postural instability/gait difficulty subtypes of Parkinson's disease: A resting-state fMRI study. CNS Neuroscience & Therapeutics, 21(10), 855–866.  https://doi.org/10.1111/cns.12464.CrossRefGoogle Scholar
  12. Choe, I. H., Yeo, S., Chung, K. C., Kim, S. H., & Lim, S. (2013). Decreased and increased cerebral regional homogeneity in early Parkinson's disease. Brain Research, 1527, 230–237.  https://doi.org/10.1016/j.brainres.2013.06.027.CrossRefPubMedGoogle Scholar
  13. Curtis, C. E. (2006). Prefrontal and parietal contributions to spatial working memory. Neuroscience, 139(1), 173–180.  https://doi.org/10.1016/j.neuroscience.2005.04.070.CrossRefPubMedGoogle Scholar
  14. Dai, Z., Yan, C., Wang, Z., Wang, J., Xia, M., Li, K., & He, Y. (2012). Discriminative analysis of early Alzheimer's disease using multi-modal imaging and multi-level characterization with multi-classifier (M3). Neuroimage, 59(3), 2187–2195.  https://doi.org/10.1016/j.neuroimage.2011.10.003.CrossRefPubMedGoogle Scholar
  15. Di Martino, A., Ghaffari, M., Curchack, J., Reiss, P., Hyde, C., Vannucci, M., Petkova, E., Klein, D. F., & Castellanos, F. X. (2008). Decomposing intra-subject variability in children with attention-deficit/hyperactivity disorder. Biological Psychiatry, 64(7), 607–614.  https://doi.org/10.1016/j.biopsych.2008.03.008.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Diener, C., Kuehner, C., Brusniak, W., Ubl, B., Wessa, M., & Flor, H. (2012). A meta-analysis of neurofunctional imaging studies of emotion and cognition in major depression. Neuroimage, 61(3), 677–685.  https://doi.org/10.1016/j.neuroimage.2012.04.005.CrossRefPubMedGoogle Scholar
  17. Esposito, F., Tessitore, A., Giordano, A., De Micco, R., Paccone, A., Conforti, R., Pignataro, G., Annunziato, L., & Tedeschi, G. (2013). Rhythm-specific modulation of the sensorimotor network in drug-naive patients with Parkinson's disease by levodopa. Brain, 136(Pt 3), 710–725.  https://doi.org/10.1093/brain/awt007.CrossRefPubMedGoogle Scholar
  18. Ffytche, D. H., Creese, B., Politis, M., Chaudhuri, K. R., Weintraub, D., Ballard, C., & Aarsland, D. (2017). The psychosis spectrum in Parkinson disease. Nature Reviews. Neurology, 13(2), 81–95.  https://doi.org/10.1038/nrneurol.2016.200.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189–198.  https://doi.org/10.1016/0022-3956(75)90026-6.CrossRefPubMedGoogle Scholar
  20. Fransson, P. (2005). Spontaneous low-frequency BOLD signal fluctuations: An fMRI investigation of the resting-state default mode of brain function hypothesis. Human Brain Mapping, 26(1), 15–29.  https://doi.org/10.1002/hbm.20113.CrossRefPubMedGoogle Scholar
  21. Giladi, N., & Nieuwboer, A. (2008). Understanding and treating freezing of gait in parkinsonism, proposed working definition, and setting the stage. Movement Disorders, 23(Suppl 2), S423–S425.  https://doi.org/10.1002/mds.21927.CrossRefPubMedGoogle Scholar
  22. Giladi, N., Shabtai, H., Simon, E. S., Biran, S., Tal, J., & Korczyn, A. D. (2000). Construction of freezing of gait questionnaire for patients with parkinsonism. Parkinsonism & Related Disorders, 6(3), 165–170.  https://doi.org/10.1016/S1353-8020(99)00062-0.CrossRefGoogle Scholar
  23. Goetz, C. G. (2003). The unified Parkinson's disease rating scale (UPDRS): Status and recommendations. Movement Disorders, 18(7), 738–750.  https://doi.org/10.1002/mds.10473.CrossRefGoogle Scholar
  24. Goldstein, D. S., Sullivan, P., Holmes, C., Mash, D. C., Kopin, I. J., & Sharabi, Y. (2017). Determinants of denervation-independent depletion of putamen dopamine in Parkinson's disease and multiple system atrophy. Parkinsonism & Related Disorders, 35, 88–91.  https://doi.org/10.1016/j.parkreldis.2016.12.011.CrossRefGoogle Scholar
  25. Gratwicke, J., Jahanshahi, M., & Foltynie, T. (2015). Parkinson’s disease dementia: A neural networks perspective. Brain, 138(6), 1454–1476.  https://doi.org/10.1093/brain/awv104.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hoehn, M. M., & Yahr, M. D. (1998). Parkinsonism: onset, progression, and mortality. Neurology, 50(2), 11–26.  https://doi.org/10.1212/WNL.17.5.427.CrossRefGoogle Scholar
  27. Hou, Y., Wu, X., Hallett, M., Chan, P., & Wu, T. (2014). Frequency-dependent neural activity in Parkinson's disease. Human Brain Mapping, 35(12), 5815–5833.  https://doi.org/10.1002/hbm.22587.CrossRefPubMedGoogle Scholar
  28. Hughes, A. J., Daniel, S. E., Kilford, L., & Lees, A. J. (1992). Accuracy of clinical diagnosis of idiopathic Parkinson's disease: A clinico-pathological study of 100 cases. Journal of Neurology, Neurosurgery, and Psychiatry, 55(3), 181–184.  https://doi.org/10.1136/jnnp.55.3.181.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Jackson, R. L., Bajada, C. J., Rice, G. E., Cloutman, L. L., & Lambon Ralph, M. A. (2018). An emergent functional parcellation of the temporal cortex. Neuroimage, 170, 385–399.  https://doi.org/10.1016/j.neuroimage.2017.04.024.CrossRefPubMedGoogle Scholar
  30. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage, 17(2), 825–841.  https://doi.org/10.1006/nimg.2002.1132.CrossRefPubMedGoogle Scholar
  31. Kalia, L. V., & Lang, A. E. (2015). Parkinson's disease. Lancet, 386(9996), 896–912.  https://doi.org/10.1016/s0140-6736(14)61393-3.CrossRefPubMedGoogle Scholar
  32. Kamei, S. (2013). Executive dysfunction in Parkinson’s disease: A review. Journal of Neuropsychology, 7(2), 193–224.  https://doi.org/10.1111/jnp.12028.CrossRefGoogle Scholar
  33. Kish, S. J., Boileau, I., Callaghan, R. C., & Tong, J. (2017). Brain dopamine neurone 'damage': Methamphetamine users vs. Parkinson's disease - a critical assessment of the evidence. The European Journal of Neuroscience, 45(1), 58–66.  https://doi.org/10.1111/ejn.13363.CrossRefPubMedGoogle Scholar
  34. Kiviniemi, V., Kantola, J. H., Jauhiainen, J., Hyvarinen, A., & Tervonen, O. (2003). Independent component analysis of nondeterministic fMRI signal sources. Neuroimage, 19(2 Pt 1), 253–260.  https://doi.org/10.1016/S1053-8119(03)00097-1.CrossRefPubMedGoogle Scholar
  35. Kwak, Y., Peltier, S. J., Bohnen, N. I., Muller, M. L., Dayalu, P., & Seidler, R. D. (2012). L-DOPA changes spontaneous low-frequency BOLD signal oscillations in Parkinson's disease: A resting state fMRI study. Frontiers in Systems Neuroscience, 6(6), 52.  https://doi.org/10.3389/fnsys.2012.00052.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lee, S. Y., Kim, M. S., Chang, W. H., Cho, J. W., Youn, J. Y., & Kim, Y. H. (2014). Effects of repetitive transcranial magnetic stimulation on freezing of gait in patients with parkinsonism. Restorative Neurology and Neuroscience, 32(6), 743–753.  https://doi.org/10.3233/rnn-140397.CrossRefPubMedGoogle Scholar
  37. Lefaucheur, J. P., Andre-Obadia, N., Antal, A., Ayache, S. S., Baeken, C., Benninger, D. H., Cantello, R. M., Cincotta, M., de Carvalho, M., De Ridder, D., Devanne, H., Di Lazzaro, V., Filipovic, S. R., Hummel, F. C., Jaaskelainen, S. K., Kimiskidis, V. K., Koch, G., Langguth, B., Nyffeler, T., Oliviero, A., Padberg, F., Poulet, E., Rossi, S., Rossini, P. M., Rothwell, J. C., Schonfeldt-Lecuona, C., Siebner, H. R., Slotema, C. W., Stagg, C. J., Valls-Sole, J., Ziemann, U., Paulus, W., & Garcia-Larrea, L. (2014). Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clinical Neurophysiology, 125(11), 2150–2206.  https://doi.org/10.1016/j.clinph.2014.05.021.CrossRefPubMedGoogle Scholar
  38. Lenka, A., Naduthota, R. M., Jha, M., Panda, R., Prajapati, A., Jhunjhunwala, K., Saini, J., Yadav, R., Bharath, R. D., & Pal, P. K. (2016). Freezing of gait in Parkinson's disease is associated with altered functional brain connectivity. Parkinsonism & Related Disorders, 24, 100–106.  https://doi.org/10.1016/j.parkreldis.2015.12.016.CrossRefGoogle Scholar
  39. Lewis, S. J., & Shine, J. M. (2016). The next step: A common neural mechanism for freezing of gait. Neuroscientist, 22(1), 72–82.  https://doi.org/10.1177/1073858414559101.CrossRefPubMedGoogle Scholar
  40. Li, C., Huang, B., Zhang, R., Ma, Q., Yang, W., Wang, L., Wang, L., Xu, Q., Feng, J., Liu, L., Zhang, Y., & Huang, R. (2017a). Impaired topological architecture of brain structural networks in idiopathic Parkinson's disease: A DTI study. Brain Imaging and Behavior, 11(1), 113–128.  https://doi.org/10.1007/s11682-015-9501-6.CrossRefPubMedGoogle Scholar
  41. Li, D., Huang, P., Zang, Y., Lou, Y., Cen, Z., Gu, Q., Xuan, M., Xie, F., Ouyang, Z., Wang, B., Zhang, M., & Luo, W. (2017b). Abnormal baseline brain activity in Parkinson's disease with and without REM sleep behavior disorder: A resting-state functional MRI study. Journal of Magnetic Resonance Imaging, 46(3), 697–703.  https://doi.org/10.1002/jmri.25571.CrossRefPubMedGoogle Scholar
  42. Man, A., Tsoi, T. H., Mok, V., Cheung, C. M., Lee, C. N., Li, R., & Yeung, E. (2012). Ten year survival and outcomes in a prospective cohort of new onset Chinese Parkinson's disease patients. Journal of Neurology, Neurosurgery, and Psychiatry, 83(6), 607–611.  https://doi.org/10.1136/jnnp-2011-301590.CrossRefGoogle Scholar
  43. Mi, T. M., Mei, S. S., Liang, P. P., Gao, L. L., Li, K. C., Wu, T., & Chan, P. (2017). Altered resting-state brain activity in Parkinson's disease patients with freezing of gait. Scientific Reports, 7(1), 16711.  https://doi.org/10.1038/s41598-017-16922-0.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Michely, J., Volz, L. J., Barbe, M. T., Hoffstaedter, F., Viswanathan, S., Timmermann, L., Eickhoff, S. B., Fink, G. R., & Grefkes, C. (2015). Dopaminergic modulation of motor network dynamics in Parkinson's disease. Brain, 138(Pt 3), 664–678.  https://doi.org/10.1093/brain/awu381.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Moore, S. T., Yungher, D. A., Morris, T. R., Dilda, V., MacDougall, H. G., Shine, J. M., Naismith, S. L., & Lewis, S. J. (2013). Autonomous identification of freezing of gait in Parkinson's disease from lower-body segmental accelerometry. Journal of Neuroengineering and Rehabilitation, 10, 19.  https://doi.org/10.1186/1743-0003-10-19.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Naismith, S. L., Shine, J. M., & Lewis, S. J. (2010). The specific contributions of set-shifting to freezing of gait in Parkinson's disease. Movement Disorders, 25(8), 1000–1004.  https://doi.org/10.1002/mds.23005.CrossRefPubMedGoogle Scholar
  47. Nitschke, K., Kostering, L., Finkel, L., Weiller, C., & Kaller, C. P. (2017). A meta-analysis on the neural basis of planning: Activation likelihood estimation of functional brain imaging results in the tower of London task. Human Brain Mapping, 38(1), 396–413.  https://doi.org/10.1002/hbm.23368.CrossRefPubMedGoogle Scholar
  48. Nonnekes, J., Snijders, A. H., Nutt, J. G., Deuschl, G., Giladi, N., & Bloem, B. R. (2015). Freezing of gait: A practical approach to management. Lancet Neurology, 14(7), 768–778.  https://doi.org/10.1016/S1474-4422(15)00041-1.CrossRefPubMedGoogle Scholar
  49. Nutt, J. G., Bloem, B. R., Giladi, N., Hallett, M., Horak, F. B., & Nieuwboer, A. (2011). Freezing of gait: Moving forward on a mysterious clinical phenomenon. Lancet Neurology, 10(8), 734–744.  https://doi.org/10.1016/s1474-4422(11)70143-0.CrossRefPubMedGoogle Scholar
  50. Ogawa, S., & Lee, T. M. (1990). Magnetic resonance imaging of blood vessels at high fields: In vivo and in vitro measurements and image simulation. Magnetic Resonance in Medicine, 16(1), 9–18.  https://doi.org/10.1002/mrm.1910160103.CrossRefPubMedGoogle Scholar
  51. Pan, P., Zhang, Y., Liu, Y., Zhang, H., Guan, D., & Xu, Y. (2017). Abnormalities of regional brain function in Parkinson's disease: A meta-analysis of resting state functional magnetic resonance imaging studies. Scientific Reports, 7, 40469.  https://doi.org/10.1038/srep40469.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Pereira, F., Mitchell, T., & Botvinick, M. (2009). Machine learning classifiers and fMRI: A tutorial overview. Neuroimage, 45(1), S199–S209.  https://doi.org/10.1016/j.neuroimage.2008.11.007.CrossRefPubMedGoogle Scholar
  53. Prodoehl, J., Spraker, M., Corcos, D., Comella, C., & Vaillancourt, D. (2010). Blood oxygenation level dependent activation in basal ganglia nuclei relates to specific symptoms in De novo Parkinson's disease. Movement Disorders, 25(13), 2035–2043.  https://doi.org/10.1002/mds.23360.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ricciardi, L., Bloem, B. R., Snijders, A. H., Daniele, A., Quaranta, D., Bentivoglio, A. R., & Fasano, A. (2014). Freezing of gait in Parkinson's disease: The paradoxical interplay between gait and cognition. Parkinsonism & Related Disorders, 20(8), 824–829.  https://doi.org/10.1016/j.parkreldis.2014.04.009.CrossRefGoogle Scholar
  55. Rodriguez-Oroz, M. C., Jahanshahi, M., Krack, P., Litvan, I., Macias, R., Bezard, E., & Obeso, J. A. (2009). Initial clinical manifestations of Parkinson's disease: Features and pathophysiological mechanisms. Lancet Neurology, 8(12), 1128–1139.  https://doi.org/10.1016/s1474-4422(09)70293-5.CrossRefPubMedGoogle Scholar
  56. Salvador, R., Martinez, A., Pomarol-Clotet, E., Gomar, J., Vila, F., Sarro, S., Capdevila, A., & Bullmore, E. (2008). A simple view of the brain through a frequency-specific functional connectivity measure. Neuroimage, 39(1), 279–289.  https://doi.org/10.1016/j.neuroimage.2007.08.018.CrossRefPubMedGoogle Scholar
  57. Shine, J. M., Matar, E., Ward, P. B., Frank, M. J., Moustafa, A. A., Pearson, M., Naismith, S. L., & Lewis, S. J. (2013). Freezing of gait in Parkinson's disease is associated with functional decoupling between the cognitive control network and the basal ganglia. Brain, 136(Pt 12), 3671–3681.  https://doi.org/10.1093/brain/awt272.CrossRefPubMedGoogle Scholar
  58. Skidmore, F. M., Yang, M., Baxter, L., von Deneen, K. M., Collingwood, J., He, G., White, K., Korenkevych, D., Savenkov, A., Heilman, K. M., Gold, M., & Liu, Y. (2013). Reliability analysis of the resting state can sensitively and specifically identify the presence of Parkinson disease. Neuroimage, 75, 249–261.  https://doi.org/10.1016/j.neuroimage.2011.06.056.CrossRefPubMedGoogle Scholar
  59. Snijders, A. H., Takakusaki, K., Debu, B., Lozano, A. M., Krishna, V., Fasano, A., Aziz, T. Z., Papa, S. M., Factor, S. A., & Hallett, M. (2016). Physiology of freezing of gait. Annals of Neurology, 80(5), 644–659.  https://doi.org/10.1002/ana.24778.CrossRefPubMedGoogle Scholar
  60. Tahmasian, M., Eickhoff, S.B., Giehl, K., Schwartz, F., Herz, D.M., Drzezga, A., van Eimeren, T., Laird, A.R., Fox, P.T., Khazaie, H., Zarei, M., Eggers, C., Eickhoff, C.R. Resting-state functional reorganization in Parkinson's disease: An activation likelihood estimation meta-analysis. Cortex 2017; 92: 119–138.  https://doi.org/10.1016/j.cortex.2017.03.016.
  61. Tessitore, A., Amboni, M., Esposito, F., Russo, A., Picillo, M., Marcuccio, L., Pellecchia, M. T., Vitale, C., Cirillo, M., Tedeschi, G., & Barone, P. (2012). Resting-state brain connectivity in patients with Parkinson's disease and freezing of gait. Parkinsonism & Related Disorders, 18(6), 781–787.  https://doi.org/10.1016/j.parkreldis.2012.03.018.CrossRefGoogle Scholar
  62. van Buuren, M., Gladwin, T. E., Zandbelt, B. B., van den Heuvel, M., Ramsey, N. F., Kahn, R. S., & Vink, M. (2009). Cardiorespiratory effects on default-mode network activity as measured with fMRI. Human Brain Mapping, 30(9), 3031–3042.  https://doi.org/10.1002/hbm.20729.CrossRefPubMedGoogle Scholar
  63. Vandenbossche, J., Deroost, N., Soetens, E., Spildooren, J., Vercruysse, S., Nieuwboer, A., & Kerckhofs, E. (2011). Freezing of gait in Parkinson disease is associated with impaired conflict resolution. Neurorehabilitation and Neural Repair, 25(8), 765–773.  https://doi.org/10.1177/1545968311403493.CrossRefPubMedGoogle Scholar
  64. Vercruysse, S., Spildooren, J., Heremans, E., Wenderoth, N., Swinnen, S. P., Vandenberghe, W., & Nieuwboer, A. (2014). The neural correlates of upper limb motor blocks in Parkinson's disease and their relation to freezing of gait. Cerebral Cortex, 24(12), 3154–3166.  https://doi.org/10.1093/cercor/bht170.CrossRefPubMedGoogle Scholar
  65. Vervoort, G., Heremans, E., Bengevoord, A., Strouwen, C., Nackaerts, E., Vandenberghe, W., & Nieuwboer, A. (2016). Dual-task-related neural connectivity changes in patients with Parkinson' disease. Neuroscience, 317, 36–46.  https://doi.org/10.1016/j.neuroscience.2015.12.056.CrossRefPubMedGoogle Scholar
  66. Visser, M., Jefferies, E., Embleton, K. V., & Lambon Ralph, M. A. (2012). Both the middle temporal gyrus and the ventral anterior temporal area are crucial for multimodal semantic processing: Distortion-corrected fMRI evidence for a double gradient of information convergence in the temporal lobes. Journal of Cognitive Neuroscience, 24(8), 1766–1778.  https://doi.org/10.1162/jocn_a_00244.CrossRefPubMedGoogle Scholar
  67. Wu, T., & Hallett, M. (2013). The cerebellum in Parkinson's disease. Brain, 136(Pt 3), 696–709.  https://doi.org/10.1093/brain/aws360.CrossRefPubMedGoogle Scholar
  68. Xue, S., Wang, X., Wang, W., Liu, J., & Qiu, J. (2016). Frequency-dependent alterations in regional homogeneity in major depression. Behavioural Brain Research, 306, 13–19.  https://doi.org/10.1016/j.bbr.2016.03.012.CrossRefPubMedGoogle Scholar
  69. Yang, H., Long, X. Y., Yang, Y., Yan, H., Zhu, C. Z., Zhou, X. P., Zang, Y. F., & Gong, Q. Y. (2007). Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI. Neuroimage, 36(1), 144–152.  https://doi.org/10.1016/j.neuroimage.2007.01.054.CrossRefPubMedGoogle Scholar
  70. Zach, H., Janssen, A. M., Snijders, A. H., Delval, A., Ferraye, M. U., Auff, E., Weerdesteyn, V., Bloem, B. R., & Nonnekes, J. (2015). Identifying freezing of gait in Parkinson's disease during freezing provoking tasks using waist-mounted accelerometry. Parkinsonism & Related Disorders, 21(11), 1362–1366.  https://doi.org/10.1016/j.parkreldis.2015.09.051.CrossRefGoogle Scholar
  71. Zang, Y. F., He, Y., Zhu, C. Z., Cao, Q. J., Sui, M. Q., Liang, M., Tian, L. X., Jiang, T. Z., & Wang, Y. F. (2007). Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain & Development, 29(2), 83–91.  https://doi.org/10.1016/j.braindev.2006.07.002.CrossRefGoogle Scholar
  72. Zhong, M., Yang, W., Huang, B., Jiang, W., Zhang, X., Liu, X., Wang, L., Wang, J., Zhao, L., Zhang, Y., Liu, Y., Lin, J., & Huang, R. (2018). Effects of levodopa therapy on voxel-based degree centrality in Parkinson's disease. Brain Imaging and Behavior.  https://doi.org/10.1007/s11682-018-9936-7.
  73. Zhu, W., Fu, X., Cui, F., Yang, F., Ren, Y., Zhang, X., Zhang, X., Chen, Z., Ling, L., & Huang, X. (2015). ALFF value in right Parahippocampal gyrus acts as a potential marker monitoring amyotrophic lateral sclerosis progression: A neuropsychological, voxel-based morphometry, and resting-state functional MRI study. Journal of Molecular Neuroscience, 57(1), 106–113.  https://doi.org/10.1007/s12031-015-0583-9.CrossRefPubMedGoogle Scholar
  74. Zuo, X. N., Di Martino, A., Kelly, C., Shehzad, Z. E., Gee, D. G., Klein, D. F., Castellanos, F. X., Biswal, B. B., & Milham, M. P. (2010). The oscillating brain: Complex and reliable. Neuroimage, 49(2), 1432–1445.  https://doi.org/10.1016/j.neuroimage.2009.09.037.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Huiqing Hu
    • 1
  • Jingwu Chen
    • 2
  • Huiyuan Huang
    • 1
  • Caihong Zhou
    • 2
  • Shufei Zhang
    • 1
  • Xian Liu
    • 3
  • Lijuan Wang
    • 4
  • Ping Chen
    • 1
  • Kun Nie
    • 4
  • Lixiang Chen
    • 1
  • Shuai Wang
    • 1
  • Biao Huang
    • 2
    Email author
  • Ruiwang Huang
    • 1
    Email author
  1. 1.Center for the Study of Applied Psychology, Key Laboratory of Mental Health and Cognitive Science of Guangdong Province, School of PsychologySouth China Normal UniversityGuangzhouPeople’s Republic of China
  2. 2.Department of Radiology, Guangdong Academy of Medical SciencesGuangdong General HospitalGuangzhouPeople’s Republic of China
  3. 3.Department of RadiologyGuangdong Provincial Hospital of Chinese MedicineGuangzhouPeople’s Republic of China
  4. 4.Department of Neurology, Guangdong General HospitalGuangdong Academy of Medical SciencesGuangzhouPeople’s Republic of China

Personalised recommendations