Skip to main content
SpringerLink
Log in

Hypoactivation of the primary sensorimotor cortex in de novo Parkinson’s disease

A motor fMRI study under controlled conditions

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

Abstract

Introduction

Nuclear medicine studies in Parkinson’s disease (PD) indicate that nigrostriatal damage causes a widespread cortical hypoactivity assumed to be due to reduced excitatory thalamic outflow. However, so far, functional MRI (fMRI) studies have provided controversial data about this “functional deafferentation” phenomenon. To further clarify this issue, we assessed, with fMRI, de novo drug-naive PD patients using a relatively complex motor task under strictly controlled conditions.

Methods

Nineteen de novo PD patients with right-predominant or bilateral symptoms and 13 age-matched healthy volunteers performed continuous writing of “8” figures with the right-dominant hand using a MR-compatible device that enables identification of incorrectly performed tasks and measures the size and the frequency of the “8”s. The data were analyzed with FSL software and correlated with the clinical severity rated according to the Hoehn and Yahr (HY) staging system.

Results

Fifteen (89%) of 19 PD patients and 12 (92%) of 13 controls correctly executed the task. PD patients showed significant hypoactivation of the left primary sensorimotor cortex (SM1) and cerebellum and no hyperactive areas as compared to controls. However, activation in SM1 and supplementary motor area bilaterally, in left supramarginal, parietal inferior, parietal superior and frontal superior gyri as well as in right parietal superior and angular gyri paralleled increasing disease severity as assessed with the HY stage.

Conclusions

In line with the “deafferentation hypothesis”, fMRI demonstrates hypoactivation of the SM1 in the early clinical stage of PD.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366–375

    Article  PubMed  CAS  Google Scholar 

  2. Rascol O, Sabatini U, Chollet F, Celsis P, Montastruc JL, Marc-Vergnes JP, Rascol A (1992) Supplementary and primary sensory motor area activity in Parkinson’s disease. Regional cerebral blood flow changes during finger movements and effects of apomorphine. Arch Neurol 49:144–148

    Article  PubMed  CAS  Google Scholar 

  3. Jenkins IH, Fernandez W, Playford ED, Lees AJ, Frackowiak RS, Passingham RE, Brooks DJ (1992) Impaired activation of the supplementary motor area in Parkinson’s disease is reversed when akinesia is treated with apomorphine. Ann Neurol 32:749–757

    Article  PubMed  CAS  Google Scholar 

  4. Playford ED, Jenkins IH, Passingham RE, Nutt J, Frackowiak RS, Brooks DJ (1992) Impaired mesial frontal and putamen activation in Parkinson’s disease: a positron emission tomography study. Ann Neurol 32:151–161

    Article  PubMed  CAS  Google Scholar 

  5. Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118:913–933

    Article  PubMed  Google Scholar 

  6. Samuel M, Ceballos Baumann AO, Turjanski N, Boecker H, Gorospe A, Linazasoro G, Holmes AP, DeLong MR, Vitek JL, Thomas DG, Quinn NP, Obeso JA, Brooks DJ (1997) Pallidotomy in Parkinson’s disease increases supplementary motor area and prefrontal activation during performance of volitional movements. An H2O PET study. Brain 120:1301–1313

    Article  PubMed  Google Scholar 

  7. Eckert T, Tang C, Eidelberg D (2007) Assessing the progression of Parkinson’s disease: a metabolic network approach. Lancet Neurol 6:926–932

    Article  PubMed  Google Scholar 

  8. Teune LK, Bartels AL, De Jong BM, Willemsen AT, Eshuis SA, de Vries JJ, van Oostrom JC, Leenders KL (2010) Typical cerebral metabolic patterns in neurodegenerative brain diseases. Mov Disord 25:2395–2404

    Article  PubMed  Google Scholar 

  9. Limousin P, Greens J, Pollak P, Rothwell J, Bernabid AL, Frackowiak R (1997) Changes in cerebral activity pattern due to subthalamic nuckeus or internal pallidum stimulation in Parkinson’s disease. Ann Neurol 42:283–291

    Article  PubMed  CAS  Google Scholar 

  10. Ceballos-Baumann AO, Boecker H, Bartestenstein P, von Falkenhayn I, Riescher H, Conrad B, Moringlane JR, Alesch F (1999) A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch Neurol 56:997–1003

    Article  PubMed  CAS  Google Scholar 

  11. Strafella AP, Dagher A, Sadikot AF (2003) Cerebral blood flow changes induced by subthalamic stimulation in Parkinson’s disease. Neurology 60:1039–1042

    PubMed  Google Scholar 

  12. 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 126:451–461

    Article  PubMed  CAS  Google Scholar 

  13. Tessa C, Lucetti C, Diciotti S, Baldacci F, Paoli L, Cecchi P, Giannelli M, Ginestroni A, Del Dotto P, Ceravolo R, Vignali C, Bonuccelli U, Mascalchi M (2010) Decreased and increased cortical activation coexist in de-novo Parkinson’s disease. Exp Neurol 224:299–306

    Google Scholar 

  14. 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 disease: a functional MRI study. Brain 123:394–403

    Article  PubMed  Google Scholar 

  15. Haslinger B, Erhard P, Kampfe 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  17. Eckert T, Peschel T, Heinze HJ, Rotte M (2006) Increased pre-SMA activation in early PD patients during simple self-initiated hand movements. J Neurol 253:199–207

    Article  PubMed  CAS  Google Scholar 

  18. Moraschi M, Giulietti G, Giove F, Guardati M, Garreffa G, Modugno N, Colonnese C, Maraviglia B (2010) fMRI study of motor cortex activity modulation in early Parkinson’s disease. Magn Reson Imaging 28:1152–1158

    Article  PubMed  Google Scholar 

  19. Peters S, Suchan B, Rusin J, Daum J, Kster O, Przuntek H, Muller T, Schmid G (2003) Apomorphine reduces BOLD signal in fMRI during voluntary movement in parkinsonian patients. Neuroreport 14:809–812

    Article  PubMed  CAS  Google Scholar 

  20. Dagher A, Nagano-Saito A (2007) Functional and anatomical magnetic resonance imaging in Parkinson’s disease. Mol Imaging Biol 9:234–242

    Article  PubMed  Google Scholar 

  21. Gibb WRG, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752

    Article  PubMed  CAS  Google Scholar 

  22. Fahn S, Elton R, the members of the Unified Parkinson's Disease Rating Scale Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D (eds) Recent developments in Parkinson’s disease. MacMillan, New York, pp 153–163

    Google Scholar 

  23. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442

    PubMed  CAS  Google Scholar 

  24. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  25. Saini S, DeStefano N, Smith S, Guidi L, Amato MP, Federico A, Matthews PM (2004) Altered cerebellar functional connectivity mediates potential adaptive plasticity in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 75:840–846

    Article  PubMed  CAS  Google Scholar 

  26. Diciotti S, Cecchi P, Ginestroni A, Mazzoni LN, Pesaresi I, Lombardo S, Boni E, Cosottini M, Soricelli A, De Stefano N, Mascalchi M (2010) MR-compatible device for monitoring hand tracing and writing tasks in fMRI with an application to healthy subjects. Conc Magn Reson Imaging – Part A 36A:139–152

  27. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17:825–841

    Article  PubMed  Google Scholar 

  28. Smith S (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155

    Article  PubMed  Google Scholar 

  29. Woolrich W, Ripley BD, Brady JM, Smith SM (2001) Temporal autocorrelation in univariate linear modelling of FMRI data. NeuroImage 14:1370–1386

    Article  PubMed  CAS  Google Scholar 

  30. Worsley KJ (2001) Statistical analysis of activation images. In: Jezzard P, Matthews PM, Smith SM (eds), Functional MRI: an introduction to methods. OUP

  31. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156

    Article  PubMed  CAS  Google Scholar 

  32. Andersson LR, Jenkinson M, Smith SM (2007) Non-linear optimisation. FMRIB technical report TR07JA1

  33. Andersson LR, Jenkinson M, Smith SM (2007) Non-linear registration, aka spatial normalization. FMRIB technical report TR07JA2

  34. Beckmann C, Jenkinson M, Smith SM (2003) General multi-level linear modelling for group analysis in FMRI. NeuroImage 20:1052–1063

    Article  PubMed  Google Scholar 

  35. Woolrich MW, Behrens TEJ, Beckmann CF, Jenkinson M, Smith SM (2004) Multi-level linear modelling for FMRI group analysis using Bayesian inference. NeuroImage 21:1732–1747

    Article  PubMed  Google Scholar 

  36. Woolrich MW (2008) Robust group analysis using outlier inference. NeuroImage 41:286–301

    Article  PubMed  Google Scholar 

  37. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15:273–289

    Article  PubMed  CAS  Google Scholar 

  38. Ginestroni A, Diciotti S, Cecchi P, Pesaresi I, Tessa C, Giannelli M, Della Nave R, Salvatore E, Salvi F, Dotti MT, Piacentini S, Soricelli A, Cosottini M, De Stefano N, Mascalchi M (2011) Neurodegeneration in Friedreich’s ataxia is associated with a mixed activation pattern of the brain. A fMRI study. Hum Brain Mapp. doi: 10.1002/hbm.21319. Accessed 14 Jun 2011

  39. Schlaug G, Sanes JN, Thangaraj V, Darby DG, Jancke L, Edelman RR, Warach S (1996) Cerebral activations covaries with movement rate. Neuroreport 7:879–883

    Article  PubMed  CAS  Google Scholar 

  40. Rao SM, Bandettini PA, Binder JR, Bobholz JA, Hammeke TA, Stein EA, Hyde JS (1996) Relationship between finger movement rate and functional magnetic resonance signal change in human primary motor cortex. J Cereb Blood Flow Metab 16:1250–1254

    Article  PubMed  CAS  Google Scholar 

  41. Jancke L, Peters M, Schlaug G, Posse S, Steinmetz H, Muller-Gartner HM (1998) Differential magnetic resonance signal change in human sensorimotor cortex to finger movements of different rate of the dominant hand and subdominant hand. Brain Res Cogn Brain Res 6:279–284

    Article  PubMed  CAS  Google Scholar 

  42. Deiber MP, Honda M, Ibanez V, Sadato N, Hallett M (1999) Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. J Neurophysiol 81:3065–3077

    PubMed  CAS  Google Scholar 

  43. Riecker A, Wildgruber D, Mathiak K, Grodd W, Ackermann H (2003) Parametric analysis of rate-dependent hemodynamic response functions of cortical and subcortical brain structures during auditorily cued finger tapping: a fMRI study. NeuroImage 18:731–739

    Article  PubMed  Google Scholar 

  44. Lutz K, Koeneke S, Wustenberg T, Jancke L (2005) Asymmetry of cortical activation during maximum and convenient tapping speed. Neurosci Lett 373:61–66

    Article  PubMed  CAS  Google Scholar 

  45. Cerasa A, Hagberg GE, Peppe A, Bianciardi M, Gioia MC, Costa A, Castriota-Scanderbeg A, Caltagirone C, Sabatini U (2006) Functional changes in the activity of cerebellum and frontostriatal regions during externally and internally timed movement in Parkinson’s disease. Brain Res Bull 71:259–269

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  47. Spraker MB, Prodoehl J, Corcos DM, Comella CL, Vaillancourt DE (2010) Basal ganglia hypoactivity during grip force in drug-naive Parkinson’s disease. Hum Brain Mapp 31:1928–1941

    Article  PubMed  Google Scholar 

  48. Taniwaki T, Okajama A, Yoshiura T, Togao O, Nakamura Y, Yamasaki T, Ogata K, Shigeto H, Ohyagy Y, Kira J, Tobimatsu S (2006) Functional network of the basal ganglia and cerebellar motor loops in vivo: different activation patterns between self-initiated and externally triggered movements. NeuroImage 31:745–753

    Article  PubMed  Google Scholar 

  49. Lewis MM, Slagle CG, Smith AB, Truong Y, Bai P, McKeown MJ, Mailman RB, Belger A, Huang X (2007) Task specific influences of Parkinson’s disease on the striato-thalamo-cortical and cerebello-thalamo-cortical motor circuitries. Neuroscience 147:224–235

    Article  PubMed  CAS  Google Scholar 

Download references

Conflict of interest

We declare that we have no conflict of interest.

Author information

Authors and Affiliations

  1. Division of Radiology, Versilia Hospital, AUSL Versilia, Lido di Camaiore (LU), Camaiore, Italy

    Carlo Tessa & Claudio Vignali

  2. Division of Neurology, Versilia Hospital, AUSL Versilia, Lido di Camaiore (LU), Camaiore, Italy

    Claudio Lucetti & Ubaldo Bonuccelli

  3. Radiodiagnostic Section, Department of Clinical Physiopathology, University of Florence, Viale Morgagni 85, 50134, Florence, Italy

    Stefano Diciotti, Lorenzo Paoli, Andrea Ginestroni & Mario Mascalchi

  4. Department of Neuroscience, University of Pisa, Pisa, Italy

    Paolo Cecchi, Filippo Baldacci & Ubaldo Bonuccelli

  5. Unit of Medical Physics, Azienda Ospedaliero-Universitaria Pisana, Pisa, Italy

    Marco Giannelli

Authors
  1. Carlo Tessa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudio Lucetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stefano Diciotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lorenzo Paoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paolo Cecchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marco Giannelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Filippo Baldacci
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andrea Ginestroni
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Claudio Vignali
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Mario Mascalchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ubaldo Bonuccelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mario Mascalchi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Areas of activation modulated by frequency (top row) and size variable (bottom row) of “8” figure writing task in the between-group analysis (Z > 5, p = 0.05 corrected). The figure shows multiple areas of cortical activation including SM1, posterior parietal cortex and cerebellum (DOC 412 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tessa, C., Lucetti, C., Diciotti, S. et al. Hypoactivation of the primary sensorimotor cortex in de novo Parkinson’s disease. Neuroradiology 54, 261–268 (2012). https://doi.org/10.1007/s00234-011-0955-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-011-0955-y

Keywords

Search

Navigation