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Functional MRI in Parkinson’s disease with freezing of gait: a systematic review of the literature

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Abstract

Background

Freezing of gait (FOG), a common and disabling symptom of Parkinson’s disease (PD), is characterized by an episodic inability to generate effective stepping. Functional MRI (fMRI) has been used to evaluate abnormal brain connectivity patterns at rest and brain activation patterns during specific tasks in patients with PD-FOG. This review has examined the existing functional neuroimaging literature in PD-FOG, including those with treatment. Summarizing these articles provides an opportunity for a better understanding of the underlying pathophysiology in PD-FOG.

Methods

According to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, we performed a literature review of studies using fMRI to investigate the underlying pathophysiological mechanisms of PD-FOG.

Results

We initially identified 201 documents. After excluding the duplicates, reviews, and other irrelevant articles, 39 articles were finally identified, including 18 task-based fMRI studies and 21 resting-state fMRI studies.

Conclusions

Studies using fMRI techniques to evaluate PD-FOG have found dysfunctional connectivity in widespread cortical and subcortical regions. Standardized imaging protocols and detailed subtypes of PD-FOG are furthered required to elucidate current findings.

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Availability of data and code

Any data and code associated with this review will be made available by reasonable request to the corresponding author (PP).

References

  1. Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10(8):734–744. https://doi.org/10.1016/s1474-4422(11)70143-0

    Article  PubMed  PubMed Central  Google Scholar 

  2. Okuma Y, Silva de Lima AL, Fukae J, Bloem BR, Snijders AH (2018) A prospective study of falls in relation to freezing of gait and response fluctuations in Parkinson’s disease. Parkinsonism Relat Disord 46:30–35. https://doi.org/10.1016/j.parkreldis.2017.10.013

    Article  PubMed  Google Scholar 

  3. Bharti K, Suppa A, Tommasin S, Zampogna A, Pietracupa S, Berardelli A, Pantano P (2019) Neuroimaging advances in Parkinson’s disease with freezing of gait: a systematic review. Neuroimage Clin 24:102059. https://doi.org/10.1016/j.nicl.2019.102059

    Article  PubMed  PubMed Central  Google Scholar 

  4. Ramsey NF, Tallent K, van Gelderen P, Frank JA, Moonen CT, Weinberger DR (1996) Reproducibility of human 3D fMRI brain maps acquired during a motor task. Hum Brain Mapp 4(2):113–121. https://doi.org/10.1002/(SICI)1097-0193(1996)4:2<113::AID-HBM3>3.0.CO;2-6

    Article  CAS  PubMed  Google Scholar 

  5. Shine JM, Matar E, Bolitho SJ, Dilda V, Morris TR, Naismith SL, Moore ST, Lewis SJ (2013) Modeling freezing of gait in Parkinson’s disease with a virtual reality paradigm. Gait Posture 38(1):104–108. https://doi.org/10.1016/j.gaitpost.2012.10.026

    Article  CAS  PubMed  Google Scholar 

  6. Shine JM, Ward PB, Naismith SL, Pearson M, Lewis SJ (2011) Utilising functional MRI (fMRI) to explore the freezing phenomenon in Parkinson’s disease. J Clin Neurosci 18(6):807–810. https://doi.org/10.1016/j.jocn.2011.02.003

    Article  PubMed  Google Scholar 

  7. Jeannerod M (1995) Mental imagery in the motor context. Neuropsychologia 33(11):1419–1432. https://doi.org/10.1016/0028-3932(95)00073-c

    Article  CAS  PubMed  Google Scholar 

  8. Biswal BB (2012) Resting state fMRI: a personal history. Neuroimage 62(2):938–944. https://doi.org/10.1016/j.neuroimage.2012.01.090

    Article  PubMed  Google Scholar 

  9. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34(4):537–541. https://doi.org/10.1002/mrm.1910340409

    Article  CAS  PubMed  Google Scholar 

  10. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700–711. https://doi.org/10.1038/nrn2201

    Article  CAS  PubMed  Google Scholar 

  11. Beckmann CF, Smith SM (2004) Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging 23(2):137–152. https://doi.org/10.1109/TMI.2003.822821

    Article  PubMed  Google Scholar 

  12. Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22(1):394–400. https://doi.org/10.1016/j.neuroimage.2003.12.030

    Article  PubMed  Google Scholar 

  13. Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10(3):186–198. https://doi.org/10.1038/nrn2575

    Article  CAS  PubMed  Google Scholar 

  14. Stark DE, Margulies DS, Shehzad ZE, Reiss P, Kelly AM, Uddin LQ, Gee DG, Roy AK, Banich MT, Castellanos FX, Milham MP (2008) Regional variation in interhemispheric coordination of intrinsic hemodynamic fluctuations. J Neurosci 28(51):13754–13764. https://doi.org/10.1523/JNEUROSCI.4544-08.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7):e1000097. https://doi.org/10.1371/journal.pmed.1000097

    Article  PubMed  PubMed Central  Google Scholar 

  16. Shine JM, Matar E, Ward PB, Bolitho SJ, Pearson M, Naismith SL, Lewis SJ (2013) Differential neural activation patterns in patients with Parkinson’s disease and freezing of gait in response to concurrent cognitive and motor load. PLoS One 8(1):e52602. https://doi.org/10.1371/journal.pone.0052602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Shine JM, Matar E, Ward PB, Frank MJ, Moustafa AA, Pearson M, Naismith SL, Lewis SJG (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

    Article  PubMed  Google Scholar 

  18. Shine JM, Matar E, Ward PB, Bolitho SJ, Gilat M, Pearson M, Naismith SL, Lewis SJ (2013) Exploring the cortical and subcortical functional magnetic resonance imaging changes associated with freezing in Parkinson’s disease. Brain 136(Pt 4):1204–1215. https://doi.org/10.1093/brain/awt049

    Article  PubMed  Google Scholar 

  19. Piramide N, Agosta F, Sarasso E, Canu E, Volontè MA, Filippi M (2020) Brain activity during lower limb movements in Parkinson’s disease patients with and without freezing of gait. J Neurol 267(4):1116–1126. https://doi.org/10.1007/s00415-019-09687-1

    Article  PubMed  Google Scholar 

  20. Ehgoetz Martens KA, Hall JM, Georgiades MJ, Gilat M, Walton CC, Matar E, Lewis SJG, Shine JM (2018) The functional network signature of heterogeneity in freezing of gait. Brain 141(4):1145–1160. https://doi.org/10.1093/brain/awy019

    Article  PubMed  Google Scholar 

  21. Gilat M, Shine JM, Walton CC, O'Callaghan C, Hall JM, Lewis SJG (2015) Brain activation underlying turning in Parkinson’s disease patients with and without freezing of gait: a virtual reality fMRI study. NPJ Parkinsons Dis 1:15020. https://doi.org/10.1038/npjparkd.2015.20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. van der Hoorn A, Renken RJ, Leenders KL, de Jong BM (2014) Parkinson-related changes of activation in visuomotor brain regions during perceived forward self-motion. PLoS One 9(4):e95861. https://doi.org/10.1371/journal.pone.0095861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Matar E, Shine JM, Gilat M, Ehgoetz Martens KA, Ward PB, Frank MJ, Moustafa AA, Naismith SL, Lewis SJG (2019) Identifying the neural correlates of doorway freezing in Parkinson’s disease. Hum Brain Mapp 40(7):2055–2064. https://doi.org/10.1002/hbm.24506

    Article  PubMed  PubMed Central  Google Scholar 

  24. Vastik M, Hok P, Hlustik P, Otruba P, Tudos Z, Kanovsky P (2016) Botulinum toxin treatment of freezing of gait in Parkinson’s disease patients as reflected in functional magnetic resonance imaging of leg movement. Neuro Endocrinol Lett 37(2):147–153

    CAS  PubMed  Google Scholar 

  25. Silva-Batista C, de Lima-Pardini AC, Nucci MP, Coelho DB, Batista A, Piemonte MEP, Barbosa ER, Teixeira LA, Corcos DM, Amaro E Jr, Horak FB, Ugrinowitsch C (2020) A randomized, controlled trial of exercise for parkinsonian individuals with freezing of gait. Mov Disord 35:1607–1617. https://doi.org/10.1002/mds.28128

    Article  PubMed  PubMed Central  Google Scholar 

  26. Vieira-Yano B, Martini DN, Horak FB, de Lima-Pardini A, Almeida F, Santana VP, Lima D, Batista AX, Marquesini R, Lira J, Barbosa ER, Corcos DM, Ugrinowitsch C, Silva-Batista C (2020) The adapted resistance training with instability randomized controlled trial for gait automaticity. Mov Disord 36:152–163. https://doi.org/10.1002/mds.28298

    Article  PubMed  Google Scholar 

  27. Vercruysse S, Spildooren J, Heremans E, Wenderoth N, Swinnen SP, Vandenberghe W, Nieuwboer A (2014) The neural correlates of upper limb motor blocks in Parkinson’s disease and their relation to freezing of gait. Cereb Cortex 24(12):3154–3166. https://doi.org/10.1093/cercor/bht170

    Article  CAS  PubMed  Google Scholar 

  28. Nackaerts E, Nieuwboer A, Broeder S, Swinnen S, Vandenberghe W, Heremans E (2018) Altered effective connectivity contributes to micrographia in patients with Parkinson’s disease and freezing of gait. J Neurol 265(2):336–347. https://doi.org/10.1007/s00415-017-8709-3

    Article  PubMed  Google Scholar 

  29. Snijders AH, Leunissen I, Bakker M, Overeem S, Helmich RC, Bloem BR, Toni I (2011) Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain 134(Pt 1):59–72. https://doi.org/10.1093/brain/awq324

    Article  PubMed  Google Scholar 

  30. Peterson DS, Pickett KA, Duncan R, Perlmutter J, Earhart GM (2014) Gait-related brain activity in people with Parkinson disease with freezing of gait. PLoS One 9(3):e90634. https://doi.org/10.1371/journal.pone.0090634

    Article  PubMed  PubMed Central  Google Scholar 

  31. Agosta F, Gatti R, Sarasso E, Volonté MA, Canu E, Meani A, Sarro L, Copetti M, Cattrysse E, Kerckhofs E, Comi G, Falini A, Filippi M (2017) Brain plasticity in Parkinson’s disease with freezing of gait induced by action observation training. J Neurol 264(1):88–101. https://doi.org/10.1007/s00415-016-8309-7

    Article  PubMed  Google Scholar 

  32. Myers PS, McNeely ME, Pickett KA, Duncan RP, Earhart GM (2018) Effects of exercise on gait and motor imagery in people with Parkinson disease and freezing of gait. Parkinsonism Relat Disord 53:89–95. https://doi.org/10.1016/j.parkreldis.2018.05.006

    Article  PubMed  PubMed Central  Google Scholar 

  33. Jiao K, Xu H, Teng C, Song X, Xiao C, Fox PT, Zhang N, Wang C, Zhong Y (2020) Connectivity patterns of cognitive control network in first episode medication-naive depression and remitted depression. Behav Brain Res 379:112381. https://doi.org/10.1016/j.bbr.2019.112381

    Article  PubMed  Google Scholar 

  34. Haynes WI, Haber SN (2013) The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for Basal Ganglia models and deep brain stimulation. J Neurosci 33(11):4804–4814. https://doi.org/10.1523/JNEUROSCI.4674-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Fling BW, Cohen RG, Mancini M, Carpenter SD, Fair DA, Nutt JG, Horak FB (2014) Functional reorganization of the locomotor network in Parkinson patients with freezing of gait. PLoS One 9(6):e100291. https://doi.org/10.1371/journal.pone.0100291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wang M, Jiang S, Yuan Y, Zhang L, Ding J, Wang J, Zhang J, Zhang K, Wang J (2016) Alterations of functional and structural connectivity of freezing of gait in Parkinson’s disease. J Neurol 263(8):1583–1592. https://doi.org/10.1007/s00415-016-8174-4

    Article  CAS  PubMed  Google Scholar 

  37. Lench DH, Embry A, Hydar A, Hanlon CA, Revuelta G (2020) Increased on-state cortico-mesencephalic functional connectivity in Parkinson disease with freezing of gait. Parkinsonism Relat Disord 72:31–36. https://doi.org/10.1016/j.parkreldis.2020.02.008

    Article  PubMed  PubMed Central  Google Scholar 

  38. Bharti K, Suppa A, Pietracupa S, Upadhyay N, Gianni C, Leodori G, Di Biasio F, Modugno N, Petsas N, Grillea G, Zampogna A, Berardelli A, Pantano P (2019) Abnormal cerebellar connectivity patterns in patients with Parkinson’s disease and freezing of gait. Cerebellum 18(3):298–308. https://doi.org/10.1007/s12311-018-0988-4

    Article  PubMed  Google Scholar 

  39. Jung JH, Kim BH, Chung SJ, Yoo HS, Lee YH, Baik K, Ye BS, Sohn YH, Lee JM, Lee PH (2020) Motor cerebellar connectivity and future development of freezing of gait in de novo Parkinson’s disease. Mov Disord 35:2240–2249. https://doi.org/10.1002/mds.28243

    Article  PubMed  Google Scholar 

  40. 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

    Article  CAS  PubMed  Google Scholar 

  41. Lenka A, Naduthota RM, Jha M, Panda R, Prajapati A, Jhunjhunwala K, Saini J, Yadav R, Bharath RD, Pal PK (2016) Freezing of gait in Parkinson’s disease is associated with altered functional brain connectivity. Parkinsonism Relat Disord 24:100–106. https://doi.org/10.1016/j.parkreldis.2015.12.016

    Article  PubMed  Google Scholar 

  42. Miranda-Dominguez O, Ragothaman A, Hermosillo R, Feczko E, Morris R, Carlson-Kuhta P, Nutt JG, Mancini M, Fair D, Horak FB (2020) Lateralized connectivity between globus pallidus and motor cortex is associated with freezing of gait in Parkinson’s disease. Neuroscience 443:44–58. https://doi.org/10.1016/j.neuroscience.2020.06.036

    Article  CAS  PubMed  Google Scholar 

  43. Potvin-Desrochers A, Mitchell T, Gisiger T, Paquette C (2019) Changes in resting-state functional connectivity related to freezing of gait in Parkinson’s disease. Neuroscience 418:311–317. https://doi.org/10.1016/j.neuroscience.2019.08.042

    Article  CAS  PubMed  Google Scholar 

  44. Gilat M, Ehgoetz Martens KA, Miranda-Dominguez O, Arpan I, Shine JM, Mancini M, Fair DA, Lewis SJG, Horak FB (2018) Dysfunctional limbic circuitry underlying freezing of gait in Parkinson’s disease. Neuroscience 374:119–132. https://doi.org/10.1016/j.neuroscience.2018.01.044

    Article  CAS  PubMed  Google Scholar 

  45. Pagnussat AS, Salazar AP, Pinto C, Redivo Marchese R, Rieder CRM, Alves Filho JO, Franco AR, Kleiner AFR (2020) Plantar stimulation alters brain connectivity in idiopathic Parkinson’s disease. Acta Neurol Scand 142(3):229–238. https://doi.org/10.1111/ane.13253

    Article  PubMed  Google Scholar 

  46. Mi TM, Garg S, Ba F, Liu AP, Liang PP, Gao LL, Jia Q, Xu EH, Li KC, Chan P, McKeown MJ (2020) Repetitive transcranial magnetic stimulation improves Parkinson’s freezing of gait via normalizing brain connectivity. NPJ Parkinsons Dis 6:16. https://doi.org/10.1038/s41531-020-0118-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Tessitore A, Amboni M, Esposito F, Russo A, Picillo M, Marcuccio L, Pellecchia MT, Vitale C, Cirillo M, Tedeschi G, Barone P (2012) Resting-state brain connectivity in patients with Parkinson’s disease and freezing of gait. Parkinsonism Relat Disord 18(6):781–787. https://doi.org/10.1016/j.parkreldis.2012.03.018

    Article  PubMed  Google Scholar 

  48. Canu E, Agosta F, Sarasso E, Volonte MA, Basaia S, Stojkovic T, Stefanova E, Comi G, Falini A, Kostic VS, Gatti R, Filippi M (2015) Brain structural and functional connectivity in Parkinson’s disease with freezing of gait. Hum Brain Mapp 36(12):5064–5078. https://doi.org/10.1002/hbm.22994

    Article  PubMed  PubMed Central  Google Scholar 

  49. Bharti K, Suppa A, Pietracupa S, Upadhyay N, Gianni C, Leodori G, Di Biasio F, Modugno N, Petsas N, Grillea G, Zampogna A, Berardelli A, Pantano P (2019) Aberrant functional connectivity in patients with Parkinson’s disease and freezing of gait: a within- and between-network analysis. Brain Imaging Behav 14:1543–1554. https://doi.org/10.1007/s11682-019-00085-9

    Article  Google Scholar 

  50. Zhou C, Zhong X, Yang Y, Yang W, Wang L, Zhang Y, Nie K, Xu J, Huang B (2018) Alterations of regional homogeneity in freezing of gait in Parkinson’s disease. J Neurol Sci 387:54–59. https://doi.org/10.1016/j.jns.2018.01.021

    Article  PubMed  Google Scholar 

  51. Liu Y, Li M, Chen H, Wei X, Hu G, Yu S, Ruan X, Zhou J, Pan X, Li Z, Luo Z, Xie Y (2019) Alterations of regional homogeneity in Parkinson’s disease patients with freezing of gait: a resting-state fMRI study. Front Aging Neurosci 11:276. https://doi.org/10.3389/fnagi.2019.00276

    Article  PubMed  PubMed Central  Google Scholar 

  52. Mi TM, Mei SS, Liang PP, Gao LL, Li KC, Wu T, Chan P (2017) Altered resting-state brain activity in Parkinson’s disease patients with freezing of gait. Sci Rep 7(1):16711. https://doi.org/10.1038/s41598-017-16922-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Hu H, Chen J, Huang H, Zhou C, Zhang S, Liu X, Wang L, Chen P, Nie K, Chen L, Wang S, Huang B, Huang R (2020) Common and specific altered amplitude of low-frequency fluctuations in Parkinson’s disease patients with and without freezing of gait in different frequency bands. Brain Imaging Behav 14(3):857–868. https://doi.org/10.1007/s11682-018-0031-x

    Article  PubMed  Google Scholar 

  54. Maidan I, Jacob Y, Giladi N, Hausdorff JM, Mirelman A (2019) Altered organization of the dorsal attention network is associated with freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 63:77–82. https://doi.org/10.1016/j.parkreldis.2019.02.036

    Article  PubMed  Google Scholar 

  55. Li J, Yuan Y, Wang M, Zhang J, Zhang L, Jiang S, Wang X, Ding J, Zhang K (2018) Decreased interhemispheric homotopic connectivity in Parkinson’s disease patients with freezing of gait: a resting state fMRI study. Parkinsonism Relat Disord 52:30–36. https://doi.org/10.1016/j.parkreldis.2018.03.015

    Article  PubMed  Google Scholar 

  56. Piramide N, Agosta F, Sarasso E, Canu E, Volonte MA, Filippi M (2020) Brain activity during lower limb movements in Parkinson’s disease patients with and without freezing of gait. J Neurol 267(4):1116–1126. https://doi.org/10.1007/s00415-019-09687-1

    Article  PubMed  Google Scholar 

  57. Vandenbossche J, Deroost N, Soetens E, Coomans D, Spildooren J, Vercruysse S, Nieuwboer A, Kerckhofs E (2012) Freezing of gait in Parkinson’s disease: disturbances in automaticity and control. Front Hum Neurosci 6:356. https://doi.org/10.3389/fnhum.2012.00356

    Article  PubMed  Google Scholar 

  58. Wu T, Hallett M (2005) A functional MRI study of automatic movements in patients with Parkinson’s disease. Brain 128(Pt 10):2250–2259. https://doi.org/10.1093/brain/awh569

    Article  PubMed  Google Scholar 

  59. Wu T, Kansaku K, Hallett M (2004) How self-initiated memorized movements become automatic: a functional MRI study. J Neurophysiol 91(4):1690–1698. https://doi.org/10.1152/jn.01052.2003

    Article  PubMed  Google Scholar 

  60. Wu T, Hallett M, Chan P (2015) Motor automaticity in Parkinson’s disease. Neurobiol Dis 82:226–234. https://doi.org/10.1016/j.nbd.2015.06.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Onder H, Ozyurek O (2020) The impact of distinct cognitive dual-tasks on gait in Parkinson’s disease and the associations with the clinical features of Parkinson’s disease. Neurol Sci. https://doi.org/10.1007/s10072-020-04874-9

  62. Almeida QJ, Lebold CA (2010) Freezing of gait in Parkinson’s disease: a perceptual cause for a motor impairment? J Neurol Neurosurg Psychiatry 81(5):513–518. https://doi.org/10.1136/jnnp.2008.160580

    Article  CAS  PubMed  Google Scholar 

  63. Cowie D, Limousin P, Peters A, Hariz M, Day BL (2012) Doorway-provoked freezing of gait in Parkinson’s disease. Mov Disord 27(4):492–499. https://doi.org/10.1002/mds.23990

    Article  PubMed  Google Scholar 

  64. Fietzek UM, Stuhlinger L, Plate A, Ceballos-Baumann A, Botzel K (2017) Spatial constraints evoke increased number of steps during turning in Parkinson’s disease. Clin Neurophysiol 128(10):1954–1960. https://doi.org/10.1016/j.clinph.2017.07.399

    Article  PubMed  Google Scholar 

  65. Gomez-Jordana LI, Stafford J, Peper CLE, Craig CM (2018) Crossing virtual doors: a new method to study gait impairments and freezing of gait in Parkinson’s disease. Parkinsons Dis 2018:2957427–2957428. https://doi.org/10.1155/2018/2957427

    Article  PubMed  PubMed Central  Google Scholar 

  66. Snijders AH, Takakusaki K, Debu B, Lozano AM, Krishna V, Fasano A, Aziz TZ, Papa SM, Factor SA, Hallett M (2016) Physiology of freezing of gait. Ann Neurol 80(5):644–659. https://doi.org/10.1002/ana.24778

    Article  PubMed  Google Scholar 

  67. Thevathasan W, Debu B, Aziz T, Bloem BR, Blahak C, Butson C, Czernecki V, Foltynie T, Fraix V, Grabli D, Joint C, Lozano AM, Okun MS, Ostrem J, Pavese N, Schrader C, Tai CH, Krauss JK, Moro E, Movement Disorders Society PPNDBSWGcwtWSfS, Functional N (2018) Pedunculopontine nucleus deep brain stimulation in Parkinson’s disease: a clinical review. Mov Disord 33(1):10–20. https://doi.org/10.1002/mds.27098

    Article  PubMed  Google Scholar 

  68. Bostan AC, Strick PL (2018) The basal ganglia and the cerebellum: nodes in an integrated network. Nat Rev Neurosci 19(6):338–350. https://doi.org/10.1038/s41583-018-0002-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Wu T, Hallett M (2013) The cerebellum in Parkinson’s disease. Brain 136(Pt 3):696–709. https://doi.org/10.1093/brain/aws360

    Article  PubMed  PubMed Central  Google Scholar 

  70. Blesa J, Trigo-Damas I, Dileone M, Del Rey NL, Hernandez LF, Obeso JA (2017) Compensatory mechanisms in Parkinson’s disease: circuits adaptations and role in disease modification. Exp Neurol 298(Pt B):148–161. https://doi.org/10.1016/j.expneurol.2017.10.002

    Article  CAS  PubMed  Google Scholar 

  71. Maillet A, Pollak P, Debu B (2012) Imaging gait disorders in parkinsonism: a review. J Neurol Neurosurg Psychiatry 83(10):986–993. https://doi.org/10.1136/jnnp-2012-302461

    Article  PubMed  Google Scholar 

  72. Plotnik M, Giladi N, Balash Y, Peretz C, Hausdorff JM (2005) Is freezing of gait in Parkinson’s disease related to asymmetric motor function? Ann Neurol 57(5):656–663. https://doi.org/10.1002/ana.20452

    Article  PubMed  Google Scholar 

  73. Lewis SJ, Shine JM (2016) The next step: a common neural mechanism for freezing of gait. Neuroscientist 22(1):72–82. https://doi.org/10.1177/1073858414559101

    Article  PubMed  Google Scholar 

  74. Lewis SJ, Barker RA (2009) A pathophysiological model of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 15(5):333–338. https://doi.org/10.1016/j.parkreldis.2008.08.006

    Article  PubMed  Google Scholar 

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Funding

The present study was supported in part by The Natural Science Foundation of the Jiangsu Province (BK20180991)

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Contributions

Guiyun Cui had the idea for the article; Jie Zu, Wei Zhang, and Liguo Dong performed the literature search; Chuanying Xu, Xiangyao Gong, and Bingchen Lv analyzed the data; Wenjing Song, Hafiz Khuram Raza, and Li Lu drafted the manuscript; Guiyun Cui and Zuohui Zhang critically revised the work.

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Correspondence to Guiyun Cui.

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Highlights

• Functional MRI provides relevant insights into the possible pathophysiology of FOG in PD.

• Current functional neuroimaging data support widespread dysfunctional connectivity between cortical and subcortical regions in PD-FOG.

• Further research is needed to characterize various FOG subtypes and perform multimodal neuroimaging.

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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. Neurol Sci 42, 1759–1771 (2021). https://doi.org/10.1007/s10072-021-05121-5

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