Skip to main content
SpringerLink
Log in

Altered Granger causality connectivity within motor-related regions of patients with Parkinson’s disease: a resting-state fMRI study

  • Functional Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

Although numerous clinical neuroimaging studies have demonstrated that there are functional abnormalities of motor-related regions in patients with Parkinson’s disease (PD) by resting-state functional magnetic resonance imaging (fMRI), little studies have explored the causal interactions within these motor-related regions. The present study aimed to examine Granger causality connectivity patterns within motor-related regions in PD patients.

Methods

Resting-state fMRI was conducted to investigate the causal connectivity differences within motor-related regions between 17 PD patients and 17 matched healthy controls. Subsequently, the relationship between the Unified Parkinson’s Disease Rating Scale scores and causal connectivity values within motor-related regions was examined in PD patients.

Results

An increased causal connectivity from the left premotor cortex (PMC) to right primary motor cortex (M1) was found in PD patients compared with that of healthy controls. Also, increased causal flow from the PMC to M1 was negatively correlated with motor scores.

Conclusion

PD patients have abnormal causal connectivity in specific motor-related regions, which may reflect a compensatory role of motor deficits in PD patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Alexander GE, Crutcher MD, DeLong MR (1990) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 85:119–146

    CAS  PubMed  Google Scholar 

  2. Baudrexel S, Witte T, Seifried C, von Wegner F, Beissner F, Klein JC, Steinmetz H, Deichmann R, Roeper J, Hilker R (2011) Resting state fMRI reveals increased subthalamic nucleus–motor cortex connectivity in Parkinson’s disease. Neuroimage 55:1728–1738

    PubMed  Google Scholar 

  3. Blinowska KJ, Kus R, Kaminski M (2004) Granger causality and information flow in multivariate processes. Phys Rev E Stat Nonlin Soft Matter Phys 70:050902

    PubMed  Google Scholar 

  4. Cai S, Chong T, Peng Y, Shen W, Li J, von Deneen KM, Huang L (2017) Altered functional brain networks in amnestic mild cognitive impairment: a resting-state fMRI study. Brain Imaging Behav 11:619–631

    PubMed  Google Scholar 

  5. Chen H, Yang Q, Liao W, Gong Q, Shen S (2009) Evaluation of the effective connectivity of supplementary motor areas during motor imagery using Granger causality mapping. Neuroimage 47:1844–1853

    PubMed  Google Scholar 

  6. Cincotta M, Borgheresi A, Balestrieri F, Giovannelli F, Rossi S, Ragazzoni A, Zaccara G, Ziemann U (2004) Involvement of the human dorsal premotor cortex in unimanual motor control: an interference approach using transcranial magnetic stimulation. Neurosci Lett 367:189–193

    CAS  PubMed  Google Scholar 

  7. Deshpande G, Hu X (2012) Investigating effective brain connectivity from fMRI data: past findings and current issues with reference to granger causality analysis. Brain Connect 2:235–245

    PubMed  PubMed Central  Google Scholar 

  8. Diez-Cirarda M, Strafella AP, Kim J, Pena J, Ojeda N, Cabrera-Zubizarreta A, Ibarretxe-Bilbao N (2018) Dynamic functional connectivity in Parkinson’s disease patients with mild cognitive impairment and normal cognition. Neuroimage: Clin 17:847–855

    Google Scholar 

  9. Florin E, Pfeifer J, Visser-Vandewalle V, Schnitzler A, Timmermann L (2016) Parkinson subtype-specific granger-causal coupling and coherence frequency in the subthalamic area. Neuroscience 332:170–180

    CAS  PubMed  Google Scholar 

  10. Giovannelli F, Borgheresi A, Balestrieri F, Ragazzoni A, Zaccara G, Cincotta M, Ziemann U (2006) Role of the right dorsal premotor cortex in “physiological” mirror EMG activity. Exp Brain Res 175:633–640

    CAS  PubMed  Google Scholar 

  11. Grafton ST (2004) Contributions of functional imaging to understanding parkinsonian symptoms. Curr Opin Neurobiol 14:715–719

    CAS  PubMed  Google Scholar 

  12. Granger CWJ (1969) Investigating causal relations by econometric models and cross-spectral methods. Economa 37:424–438

    Google Scholar 

  13. Hammond C, Bergman H, Brown P (2007) Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci 30:357–364

    CAS  PubMed  Google Scholar 

  14. Haslinger B, Erhard P, Kämpfe N, Boecker H, Rummeny E, Schwaiger M, Conrad B, Ceballos-Baumann AO (2001) Event-related functional magnetic resonance imaging in Parkinson’s disease before and after levodopa. Brain 124:558–570

    CAS  PubMed  Google Scholar 

  15. 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 55:181

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Jenkins IH, Jahanshahi M, Jueptner M, Passingham RE, Brooks DJ (2000) Self-initiated versus externally triggered movements II. The effect of movement predictability on regional cerebral blood flow. Brain 123:1216–1228

    PubMed  Google Scholar 

  17. Leocani L, Cohen LG, Wassermann EM, Ikoma K, Hallett M (2000) Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. Brain 123:1161–1173

    PubMed  Google Scholar 

  18. Manes JL, Tjaden K, Parrish T, Simuni T, Roberts A, Greenlee JD, Corcos DM, Kurani AS (2018) Altered resting-state functional connectivity of the putamen and internal globus pallidus is related to speech impairment in Parkinson’s disease. Brain Behav 8:1–20

    Google Scholar 

  19. Marconi B, Genovesio A, Giannetti S, Molinari M, Caminiti R (2003) Callosal connections of dorso-lateral premotor cortex. Eur J Neurosci 18:775–788

    CAS  PubMed  Google Scholar 

  20. Mears D, Pollard HB (2016) Network science and the human brain: using graph theory to understand the brain and one of its hubs, the amygdala, in health and disease. J Neurosci Res 94:590–605

    CAS  PubMed  Google Scholar 

  21. Rizzolatti G, Fogassi L, Gallese V (2002) Motor and cognitive functions of the ventral premotor cortex. Curr Opin Neurobiol 12:149–154

    CAS  PubMed  Google Scholar 

  22. Rouiller EM, Babalian A, Kazennikov O, Moret V, Yu XH, Wiesendanger M (1994) Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys. Exp Brain Res 102:227–243

    CAS  PubMed  Google Scholar 

  23. Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, Colonnese C, Bozzao L, Berry I, Montastruc JL, Chollet F, Rascol O (2000) Cortical motor reorganization in akinetic patients with Parkinson’s diseaseA functional MRI study. Brain 123:394–403

    PubMed  Google Scholar 

  24. Schubotz RI, von Cramon DY (2003) Functional–anatomical concepts of human premotor cortex: evidence from fMRI and PET studies. Neuroimage 20:S120–S131

    PubMed  Google Scholar 

  25. Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009) Neurodegenerative diseases target large-scale human brain networks. Neuron 62:42–52

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Serrien DJ, Strens LHA, Oliviero A, Brown P (2002) Repetitive transcranial magnetic stimulation of the supplementary motor area (SMA) degrades bimanual movement control in humans. Neurosci lett 328:89–92

    CAS  PubMed  Google Scholar 

  27. Sharman M, Valabregue R, Perlbarg V, Marrakchi-Kacem L, Vidailhet M, Benali H, Brice A, Lehéricy S (2012) Parkinson’s disease patients show reduced cortical-subcortical sensorimotor connectivity. Mov Disord 28:447–454

    PubMed  Google Scholar 

  28. Shen Y-T, Li J-Y, Yuan Y-S, Wang X-X, Wang M, Wang J-W, Zhang H, Zhu L, Zhang K-Z (2018) Disrupted amplitude of low-frequency fluctuations and causal connectivity in Parkinson’s disease with apathy. Neurosci Lett 683:75–81

    CAS  PubMed  Google Scholar 

  29. Siderowf A, McDermott M, Kieburtz K, Blindauer K, Plumb S, Shoulson I (2002) Test–retest reliability of the Unified Parkinson’s Disease Rating Scale in patients with early Parkinson’s disease: results from a multicenter clinical trial. Mov Disord 17:758–763

    PubMed  Google Scholar 

  30. Sohn YH, Wiltz K, Hallett M (2002) Effect of volitional inhibition on cortical inhibitory mechanisms. J Neurophysiol 88:333–338

    PubMed  Google Scholar 

  31. Taniwaki T, Okayama A, Yoshiura T, Nakamura Y, Goto Y, J-i K, Tobimatsu S (2003) Reappraisal of the motor role of basal canglia: a functional magnetic resonance image study. J Neurosci 23:3432

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Tuovinen N, Seppi K, de Pasquale F, Muller C, Nocker M, Schocke M, Gizewski ER, Kremser C, Wenning GK, Poewe W, Djamshidian A, Scherfler C, Seki M (2018) The reorganization of functional architecture in the early-stages of Parkinson’s disease. Parkinsonism Relat Disord 50:61–68

    PubMed  Google Scholar 

  33. Wang XX, Li JY, Yuan YS, Wang M, Ding J, Zhang JJ, Zhu L, Shen YT, Zhang H, Zhang KZ (2017) Altered putamen functional connectivity is associated with anxiety disorder in Parkinson’s disease. Oncotarget 8:81377–81386

    PubMed  PubMed Central  Google Scholar 

  34. Wei LQ, Zhang JQ, Long ZL, Wu GR, Hu XF, Zhang YL, Wang J (2018) Reduced topological efficiency in cortical-basal ganglia motor network of Parkinson’s disease: a resting state fMRI study. PloS One 9(10):e108124

    Google Scholar 

  35. Willis AW (2013) Parkinson disease in the elderly adult. Mo Med 110:406–410

    PubMed  PubMed Central  Google Scholar 

  36. Wu T, Hallett M (2005) A functional MRI study of automatic movements in patients with Parkinson’s disease. Brain 128:2250–2259

    PubMed  Google Scholar 

  37. Wu T, Liu J, Zhang H, Hallett M, Zheng Z, Chan P (2015) Attention to automatic movements in Parkinson’s disease: modified automatic mode in the striatum. Cereb Cortex 25:3330–3342

    PubMed  Google Scholar 

  38. Wu T, Wang L, Chen Y, Zhao C, Li KC, Chan P (2009) Changes of functional connectivity of the motor network in the resting state in Parkinson’s disease. Neurosci Lett 460:6–10

    CAS  PubMed  Google Scholar 

  39. Wu T, Wang L, Hallett M, Chen Y, Li K, Chan P (2011) Effective connectivity of brain networks during self-initiated movement in Parkinson’s disease. Neuroimage 55:204–215

    PubMed  Google Scholar 

  40. Yao Q, Zhu D, Li F, Xiao C, Lin X, Huang Q, Shi J (2017) Altered functional and causal connectivity of cerebello-cortical circuits between multiple system atrophy (parkinsonian type) and parkinson’s disease. Front Aging Neurosci 9:1–11

    Google Scholar 

  41. Yates D (2012) Neurodegenerative networking: neurodegenerative networking. Nat Rev Neurosci 13:288–289

    CAS  PubMed  Google Scholar 

  42. Yu H, Sternad D, Corcos DM, Vaillancourt DE (2007) Role of hyperactive cerebellum and motor cortex in Parkinson’s disease. Neuroimage 35:222–233

    PubMed  PubMed Central  Google Scholar 

  43. Yu R, Liu B, Wang L, Chen J, Liu X (2013) Enhanced functional connectivity between putamen and supplementary motor area in Parkinson’s disease patients. PLoS One 8(3):e59717

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Zang Z-X, Yan C-G, Dong Z-Y, Huang J, Zang Y-F (2012) Granger causality analysis implementation on MATLAB: a graphic user interface toolkit for fMRI data processing. J Neurosci Methods 203:418–426

    PubMed  Google Scholar 

  45. Zeng Q, Guan X, Guo T, Law JCF, Lun Y, Zhou C, Luo X, Shen Z, Huang P, Zhang M, Cheng G (2019) The ventral Intermediate nucleus differently modulates subtype-related networks in Parkinson’s disease. Front Neurosci 13:202–210

Download references

Funding

This study was funded by the Inner Mongolia Science & Technology Plan, the Inner Mongolia Medical University Science & Technology Billion Program (YKD2016KJBW002), the Inner Mongolia Autonomous Region University & College Science & Technology Program (NJZY17115), the Inner Mongolia Medical University Affiliated Hospital Primary Program (ZYFYZD014), the Inner Mongolia Autonomous Region Health & Family Planning Committee Science & Technology Program (201702081), and the Program For Young Talents of Science and Technology in Universities of Inner Mongolia Autonomous Region (NJYT-18-B19).

Author information

Authors and Affiliations

  1. Department of Imaging Center, The First Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010050, Inner Mongolia, China

    Li Hao, Zhao Sheng, Wang Ruijun, Zhang Peng & Hong Yu

  2. CT Room, People’s Hospital of Wu La Te Qian Qi, Bayan Nuo’er, 014400, Inner Mongolia, China

    He Zhi Kun

Authors
  1. Li Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhao Sheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wang Ruijun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. He Zhi Kun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhang Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hong Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hong Yu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Informed consent

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

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hao, L., Sheng, Z., Ruijun, W. et al. Altered Granger causality connectivity within motor-related regions of patients with Parkinson’s disease: a resting-state fMRI study. Neuroradiology 62, 63–69 (2020). https://doi.org/10.1007/s00234-019-02311-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-019-02311-z

Keywords

Search

Navigation