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Patterns of striatal and cerebellar functional connectivity in early-stage drug-naïve patients with Parkinson’s disease subtypes

  • Functional Neuroradiology
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Abstract

Purpose

Both the striatal-thalamo-cortical (STC) circuit and cerebello-thalamo-cortical (CTC) circuit play a critical role in Parkinson’s disease (PD).

Methods

Resting-state functional MRI was used to assess functional connectivity (FC) focusing on the basal ganglia (BG) and cerebellum among early-stage drug-naïve PD patients with tremor-dominant (TD) PD patients with postural instability and gait dysfunction (PIGD) and healthy controls (HCs).

Results

Compared to HCs, both PD subgroups had higher FC between the cerebellum and paracentral lobule, sensorimotor areas; lower FC between the BG and superior frontal gyrus, and within the BG circuit; PD-TD patients showed higher FC between the BG and fusiform, paracentral lobule, cerebellum Lobule VI, and between the cerebellum and supplementary motor areas (SMA), insula; lower FC between the BG and rectus, sensorimotor areas, and within the cerebellum circuit; PD-PIGD patients showed higher FC between the cerebellum and middle frontal gyrus, precuneus; lower FC between the BG and cerebellum Crus II. Besides, compared to PD-PIGD patients and HCs, PD-TD patients had higher FC between the BG and calcarine region. In all PD patients, FC in paracentral lobule, SMA, and cerebellum Lobule VI positively correlated with tremor scores, and FC in calcarine area positively correlated with tremor scores, but negatively correlated with PIGD scores.

Conclusion

Our findings mainly suggested that the BG and cerebellum had hyper-connectivity with the cortical motor cortex, and the BG had prominent hyper-connectivity with the visual cortex in early-stage PD-TD patients. These findings may be helpful for facilitating the further understanding of potential mechanisms in the early-stage PD-TD. However, our results are preliminary, and further investigations are needed.

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References

  1. Schiess MC, Suescun J (2015) Clinical determinants of progression of Parkinson disease: predicting prognosis by subtype. JAMA Neurol 72(8):859–860. https://doi.org/10.1001/jamaneurol.2015.1067

    Article  PubMed  Google Scholar 

  2. Berardelli A, Rothwell JC, Thompson PD, Hallett M (2001) Pathophysiology of bradykinesia in Parkinson's disease. Brain 124(Pt 11):2131–2146

    Article  CAS  Google Scholar 

  3. Suchowersky O, Reich S, Perlmutter J, Zesiewicz T, Gronseth G, Weiner WJ, Quality Standards Subcommittee of the American Academy of N (2006) Practice parameter: diagnosis and prognosis of new onset Parkinson disease (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 66(7):968–975. https://doi.org/10.1212/01.wnl.0000215437.80053.d0

    Article  CAS  PubMed  Google Scholar 

  4. Piccinin CC, Campos LS, Guimaraes RP, Piovesana LG, MCA DS, Azevedo PC, Campos BM, de Rezende TJR, Amato-Filho A, Cendes F, D'Abreu A (2017) Differential pattern of cerebellar atrophy in tremor-predominant and akinetic/rigidity-predominant Parkinson's disease. Cerebellum (London, England) 16(3):623–628. https://doi.org/10.1007/s12311-016-0834-5

    Article  Google Scholar 

  5. Lewis MM, Du G, Sen S, Kawaguchi A, Truong Y, Lee S, Mailman RB, Huang X (2011) Differential involvement of striato- and cerebello-thalamo-cortical pathways in tremor- and akinetic/rigid-predominant Parkinson’s disease. Neuroscience 177:230–239. https://doi.org/10.1016/j.neuroscience.2010.12.060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Guan X, Xuan M, Gu Q, Xu X, Huang P, Wang N, Shen Z, Xu J, Luo W, Zhang M (2017) Influence of regional iron on the motor impairments of Parkinson’s disease: a quantitative susceptibility mapping study. J Magn Reson Imaging : JMRI 45(5):1335–1342. https://doi.org/10.1002/jmri.25434

    Article  CAS  PubMed  Google Scholar 

  7. Selikhova M, Williams DR, Kempster PA, Holton JL, Revesz T, Lees AJ (2009) A clinico-pathological study of subtypes in Parkinson’s disease. Brain 132(Pt 11):2947–2957. https://doi.org/10.1093/brain/awp234

    Article  CAS  PubMed  Google Scholar 

  8. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24(2):197–211

    Article  Google Scholar 

  9. Helmich RC, Hallett M, Deuschl G, Toni I, Bloem BR (2012) Cerebral causes and consequences of parkinsonian resting tremor: a tale of two circuits? Brain 135(Pt 11):3206–3226. https://doi.org/10.1093/brain/aws023

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hou Y, Yang J, Luo C, Ou R, Song W, Liu W, Gong Q, Shang H (2016) Patterns of striatal functional connectivity differ in early and late onset Parkinson’s disease. J Neurol 263:1993–2003. https://doi.org/10.1007/s00415-016-8211-3

    Article  CAS  PubMed  Google Scholar 

  11. Buhmann C, Glauche V, Sturenburg HJ, Oechsner M, Weiller C, Buchel C (2003) Pharmacologically modulated fMRI--cortical responsiveness to levodopa in drug-naive hemiparkinsonian patients. Brain 126(Pt 2):451–461

    Article  CAS  Google Scholar 

  12. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55(3):181–184

    Article  CAS  Google Scholar 

  13. Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I, Stern M, Tanner C, Weiner W, Parkinson Study Group (1990) Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group. Neurology 40(10):1529–1534

    Article  CAS  Google Scholar 

  14. Katzman R, Zhang MY, Ouang Ya Q, Wang ZY, Liu WT, Yu E, Wong SC, Salmon DP, Grant I (1988) A Chinese version of the mini-mental state examination; impact of illiteracy in a Shanghai dementia survey. J Clin Epidemiol 41(10):971–978

    Article  CAS  Google Scholar 

  15. Helmich RC, Derikx LC, Bakker M, Scheeringa R, Bloem BR, Toni I (2010) Spatial remapping of cortico-striatal connectivity in Parkinson’s disease. Cereb Cortex 20(5):1175–1186

    Article  Google Scholar 

  16. Luo C, Song W, Chen Q, Zheng Z, Chen K, Cao B, Yang J, Li J, Huang X, Gong Q, Shang HF (2014) Reduced functional connectivity in early-stage drug-naive Parkinson’s disease: a resting-state fMRI study. Neurobiol Aging 35(2):431–441. https://doi.org/10.1016/j.neurobiolaging.2013.08.018

    Article  PubMed  Google Scholar 

  17. O'Callaghan C, Hornberger M, Balsters JH, Halliday GM, Lewis SJ, Shine JM (2016) Cerebellar atrophy in Parkinson’s disease and its implication for network connectivity. Brain 139(Pt 3):845–855. https://doi.org/10.1093/brain/awv399

    Article  PubMed  Google Scholar 

  18. 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  Google Scholar 

  19. Balsters JH, Laird AR, Fox PT, Eickhoff SB (2014) Bridging the gap between functional and anatomical features of cortico-cerebellar circuits using meta-analytic connectivity modeling. Hum Brain Mapp 35(7):3152–3169. https://doi.org/10.1002/hbm.22392

    Article  PubMed  Google Scholar 

  20. Wu T, Long X, Wang L, Hallett M, Zang Y, Li K, Chan P (2011) Functional connectivity of cortical motor areas in the resting state in Parkinson’s disease. Hum Brain Mapp 32(9):1443–1457. https://doi.org/10.1002/hbm.21118

    Article  PubMed  Google Scholar 

  21. Weil RS, Schrag AE, Warren JD, Crutch SJ, Lees AJ, Morris HR (2016) Visual dysfunction in Parkinson’s disease. Brain 139(11):2827–2843. https://doi.org/10.1093/brain/aww175

    Article  PubMed  PubMed Central  Google Scholar 

  22. Uc EY, Rizzo M, Anderson SW, Qian S, Rodnitzky RL, Dawson JD (2005) Visual dysfunction in Parkinson disease without dementia. Neurology 65(12):1907–1913. https://doi.org/10.1212/01.wnl.0000191565.11065.11

    Article  CAS  PubMed  Google Scholar 

  23. Davidsdottir S, Cronin-Golomb A, Lee A (2005) Visual and spatial symptoms in Parkinson’s disease. Vis Res 45(10):1285–1296. https://doi.org/10.1016/j.visres.2004.11.006

    Article  PubMed  Google Scholar 

  24. Owen AM (2004) Cognitive dysfunction in Parkinson’s disease: the role of frontostriatal circuitry. The Neuroscientist 10(6):525–537. https://doi.org/10.1177/1073858404266776

    Article  PubMed  Google Scholar 

  25. Jokinen P, Karrasch M, Bruck A, Johansson J, Bergman J, Rinne JO (2013) Cognitive slowing in Parkinson’s disease is related to frontostriatal dopaminergic dysfunction. J Neurol Sci 329(1–2):23–28. https://doi.org/10.1016/j.jns.2013.03.006

    Article  CAS  PubMed  Google Scholar 

  26. Ma LY, Chen XD, He Y, Ma HZ, Feng T (2017) Disrupted brain network hubs in subtype-specific Parkinson’s disease. Eur Neurol 78(3–4):200–209. https://doi.org/10.1159/000477902

    Article  PubMed  Google Scholar 

  27. Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V, Greicius MD (2009) Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci 29(26):8586–8594. https://doi.org/10.1523/JNEUROSCI.1868-09.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT (2011) The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol 106(5):2322–2345. https://doi.org/10.1152/jn.00339.2011

    Article  PubMed  PubMed Central  Google Scholar 

  29. Eisinger RS, Hess CW, Martinez-Ramirez D, Almeida L, Foote KD, Okun MS, Gunduz A (2017) Motor subtype changes in early Parkinson’s disease. Parkinsonism Relat Disord 43:67–72. https://doi.org/10.1016/j.parkreldis.2017.07.018

    Article  PubMed  PubMed Central  Google Scholar 

  30. Fereshtehnejad SM, Zeighami Y, Dagher A, Postuma RB (2017) Clinical criteria for subtyping Parkinson’s disease: biomarkers and longitudinal progression. Brain 140(7):1959–1976. https://doi.org/10.1093/brain/awx118

    Article  PubMed  Google Scholar 

  31. Rosenberg-Katz K, Herman T, Jacob Y, Giladi N, Hendler T, Hausdorff JM (2013) Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology 80(16):1476–1484. https://doi.org/10.1212/WNL.0b013e31828cfaa4

    Article  PubMed  PubMed Central  Google Scholar 

  32. Chen HM, Wang ZJ, Fang JP, Gao LY, Ma LY, Wu T, Hou YN, Zhang JR, 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 Neurosci Ther 21(10):855–866. https://doi.org/10.1111/cns.12464

    Article  CAS  PubMed  Google Scholar 

  33. Deng X, Xiao B, Li HH, Lo YL, Chew LM, Prakash KM, Tan EK (2015) Sexual dysfunction is associated with postural instability gait difficulty subtype of Parkinson’s disease. J Neurol 262(11):2433–2439. https://doi.org/10.1007/s00415-015-7855-8

    Article  PubMed  Google Scholar 

  34. Mohl B, Berman BD, Shelton E, Tanabe J (2017) Levodopa response differs in Parkinson’s motor subtypes: a task-based effective connectivity study. J Comp Neurol 525(9):2192–2201. https://doi.org/10.1002/cne.24197

    Article  CAS  PubMed  Google Scholar 

  35. Katz M, Luciano MS, Carlson K, Luo P, Marks WJ Jr, Larson PS, Starr PA, Follett KA, Weaver FM, Stern MB, Reda DJ, Ostrem JL, group CSPs (2015) Differential effects of deep brain stimulation target on motor subtypes in Parkinson’s disease. Ann Neurol 77(4):710–719. https://doi.org/10.1002/ana.24374

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Neurology, West China Hospital, Sichuan University, Chengdu, 610041, Sichuan, China

    Yanbing Hou, Ruwei Ou, Jing Yang, Wei Song & Huifang Shang

  2. Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital, Sichuan University, Chengdu, Sichuan, China

    Qiyong Gong

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  1. Yanbing Hou
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Correspondence to Huifang Shang.

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Funding

This study was funded by the National Nature Science Foundation of China (No. 81571247) and the Fundamental Research Funds for the Central Universities (No. 2012017yjsy195).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Hou, Y., Ou, R., Yang, J. et al. Patterns of striatal and cerebellar functional connectivity in early-stage drug-naïve patients with Parkinson’s disease subtypes. Neuroradiology 60, 1323–1333 (2018). https://doi.org/10.1007/s00234-018-2101-6

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  • DOI: https://doi.org/10.1007/s00234-018-2101-6

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