Skip to main content
SpringerLink
Log in

1 Hz rTMS preconditioned by tDCS over the primary motor cortex in Parkinson’s disease: effects on bradykinesia of arm and hand

  • Movement Disorders - Original Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Abstract

To investigate whether a period of 1 Hz repetitive transcranial magnetic stimulation (rTMS) over M1 preconditioned by tDCS improves bradykinesia of the upper limb in Parkinson’s disease (PD). Fifteen patients with PD performed index finger, hand tapping and horizontal pointing movements as well as reach-to-grasp movements with either hand before (baseline conditions) and after a period of 1 Hz rTMS preconditioned by (1) sham, (2) anodal or (3) cathodal tDCS over the primary motor cortex contralateral to the more affected body side. Movement kinematics was analysed using an ultrasound-based motion analyser at baseline, immediately after and 30 min after each stimulation session. Dopaminergic medication was continued. Compared to baseline, 1 Hz rTMS significantly increased the frequency of index finger and hand tapping as well as horizontal pointing movements performed with the contralateral hand. Movement frequency increased up to 40% over 30 min after cessation of the stimulation. Preconditioning with cathodal tDCS, but not with anodal tDCS, reduced the effectiveness of 1 Hz rTMS to improve tapping and pointing movements. There was no significant increase of movement frequencies of the ipsilateral hand induced by 1 Hz rTMS preconditioned by either tDCS session. Movement kinematics of reach-to-grasp movements were not significantly influenced by either stimulation session. In PD the beneficial effects of 1 Hz rTMS over the primary motor cortex on bradykinesia of simple finger, hand and pointing movements is reduced by preconditioning with cathodal tDCS, but not with anodal tDCS. Preconditioning with tDCS is a powerful tool to modulate the behavioural effect of 1 Hz rTMS over the primary motor cortex in 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

Similar content being viewed by others

References

  • Bäumer T, Pramstaller PP, Siebner HR, Schippling S, Hagenah J, Peller M, Gerloff C, Klein C, Münchau A (2007) Sensorimotor integration is abnormal in asymptomatic Parkin mutation carriers: a TMS study. Neurology 69:1976–1981

    Article  PubMed  Google Scholar 

  • Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32–48

    CAS  PubMed  Google Scholar 

  • Brooks DJ, Samuel M (2000) The effects of surgical treatment of Parkinson’s disease on brain function: PET findings. Neurology 55:S52–S59

    CAS  PubMed  Google Scholar 

  • Buhmann C, Gorsler A, Baumer T, Hidding U, Demiralay C, Hinkelmann K, Weiler C, Siebner HR, Münchau A (2004) Abnormal excitability of premotor-motor connections in de novo Parkinson’s disease. Brain 127:2246–2732

    Article  Google Scholar 

  • Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403

    CAS  PubMed  Google Scholar 

  • Crovitz HF, Zener K (1965) A group for assessing hand and eye dominance. Am J Psychol 75:271–276

    Article  Google Scholar 

  • De Frias CM, Dixon RA, Fisher N, Camicioli R (2007) Intraindividual variability in neurocognitive speed: a comparison of Parkinson’s disease and normal older adults. Neuropsychologia 45:2499–2507

    Article  PubMed  Google Scholar 

  • Devanne H, Cohen LG, Kouchtir-Devanne N, Capaday C (2002) Integrated motor cortical control of task-related muscles during pointing in humans. J Neurophysiol 87:3006–3017

    PubMed  Google Scholar 

  • Elahi B, Elahi B, Chen R (2009) Effect of transcranial magnetic stimulation on Parkinson motor function-systematic review of controlled clinical trials. Mov Disord 24:357–363

    Article  PubMed  Google Scholar 

  • Fahn S, Elton RL, Members of the UPDRS Development Committee (1987) The Unified Parkinson’s disease Rating Scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M (eds) Recent developments in Parkinson’s disease, vol. 2. McMillan Healthcare Information, Florham Park, pp 153–163, 293–304

  • Folstein MF, Folstein SE, McHugh PR (1975) Mini-Mental State (a practical method for grading the state of patients for the clinician). J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  • Fregni F, Boggio PS, Santos MC, Lima M, Vieira AL, Rigonatti SP, Silva MT, Barbosa ER, Nitsche MA, Pascual-Leone A (2006) Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov Disord 21:1693–1702

    Article  PubMed  Google Scholar 

  • Ginanneschi F, Dominici F, Biasella A, Gelli F, Rossi A (2006) Changes in corticomotor excitability of forearm muscles in relation to static shoulder positions. Brain Res 1073:332–338

    Article  PubMed  Google Scholar 

  • Helmich RC, Derikx LC, Bakker M, Scheeringa R, Bloem BR, Toni I (2009) Spatial remapping of cortico-striatal connectivity in Parkinson’s disease. Cereb Cortex [Epub ahead of print]

  • Hermsdörfer J, Marquardt C, Wack S, Mai N (1999) Comparative analysis of diadochokinetic movements. J Electromyogr Kinesiol 9:283–295

    Article  PubMed  Google Scholar 

  • Hoehn M, Yahr M (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442

    CAS  PubMed  Google Scholar 

  • Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. I. 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 

  • Khedr EM, Farweez HM, Islam H (2003) Therapeutic effect of repetitive transcranial magnetic stimulation on motor function in Parkinson’s disease patients. Eur J Neurol 10:567–572

    Article  CAS  PubMed  Google Scholar 

  • Krack P, Pollak P, Limousin P, Hoffmann D, Xie J, Benazzouz A (1998) Subthalamic nucleus or internal pallidal stimulation in young onset Parkinson’s disease. Brain 121:141–147

    Article  Google Scholar 

  • Lefaucheur JP (2005) Motor cortex dysfunction revealed by cortical excitability studies in Parkinson’s disease: influence of antiparkinsonian treatment and cortical stimulation. Clin Neurophysiol 116:244–253

    Article  CAS  PubMed  Google Scholar 

  • Lefaucheur JP, Drouot X, Von Raison F, Ménard-Lefaucheur I, Cesaro P, Nguyen JP (2004) Improvement of motor performance and modulation of cortical excitability by repetitive transcranial magnetic stimulation of the motor cortex in Parkinson’s disease. Clin Neurophysiol 115:2530–2541

    Article  PubMed  Google Scholar 

  • Mally J, Stone TW (1999) Improvement in Parkinsonian symptoms after repetitive transcranial magnetic stimulation. J Neurol Sci 162:179–184

    Article  CAS  PubMed  Google Scholar 

  • Mir P, Matsunaga K, Gilio F, Quinn NP, Siebner HR, Rothwell JC (2005) Dopaminergic drugs restore facilitatory premotor–motor interactions in Parkinson disease. Neurology 64:1906–1912

    Article  CAS  PubMed  Google Scholar 

  • Morgante F, Espay AJ, Gunraj C, Lang AE, Chen R (2006) Motor cortex plasticity in Parkinson’s disease and levodopa-induced dyskinesias. Brain 129:1059–1069

    Article  PubMed  Google Scholar 

  • Nowak DA (2008) The impact of stroke on the performance of grasping: usefulness of kinetic and kinematic motion analysis. Neurosci Biobehav Rev 32:1439–1450

    Article  PubMed  Google Scholar 

  • Okabe S, Ugawa Y, Kanazawa I (2003) Effectiveness of rTMS on Parkinson’s Disease Study Group. 0.2-Hz repetitive transcranial magnetic stimulation has no add-on effects as compared to a realistic sham stimulation in Parkinson’s disease. Mov Disord 18:382–388

    Article  PubMed  Google Scholar 

  • Palmer SJ, Ng B, Abugharbieh R, Eigenraam L, McKeown MJ (2009) Motor reserve and novel area recruitment: amplitude and spatial characteristics of compensation in Parkinson’s disease. Eur J Neurosci 29:2187–2196

    Article  PubMed  Google Scholar 

  • Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117:847–858

    Article  PubMed  Google Scholar 

  • Priori A (2003) Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability. Clin Neurophysiol 114:589–595

    Article  PubMed  Google Scholar 

  • 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 a kinetic patients with Parkinson’s disease: a functional MRI study. Brain 123:394–403

    Article  PubMed  Google Scholar 

  • Siebner HR, Rossmeier C, Mentschel C, Peinemann A, Conrad B (2000) Short-term motor improvement after sub-threshold 5-Hz repetitive transcranial magnetic stimulation of the primary motor hand area in Parkinson’s disease. J Neurol Sci 178:91–94

    Article  CAS  PubMed  Google Scholar 

  • Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN, Rothwell JC (2004) Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24:3379–3385

    Article  CAS  PubMed  Google Scholar 

  • Soysal A, Sobe I, Atay T, Sen A, Arpaci B (2008) Effect of therapy on motor cortical excitability in Parkinson’s disease. Can J Neurol Sci 35:166–172

    PubMed  Google Scholar 

  • Strafella AP, Paus T, Fraraccio M, Dagher A (2003) Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain 126:2609–2615

    Article  PubMed  Google Scholar 

  • Strafella AP, Ko JH, Monchi O (2006) Therapeutic application of transcranial magnetic stimulation in Parkinson’s disease: the contribution of expectation. Neuroimage 31:1666–1672

    Article  PubMed  Google Scholar 

  • Tergau F, Wassermann EM, Paulus W, Ziemann U (1999) Lack of clinical improvement in patients with Parkinson’s disease after low and high frequency repetitive transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol (Suppl) 51:281–288

    Google Scholar 

  • Ueki Y, Mima T, Kotb MA, Sawada H, Saiki H, Ikeda A, Begum T, Reza F, Nagamine T, Fukuyama H (2006) Altered plasticity of the human motor cortex in Parkinson’s disease. Ann Neurol 59:60–71

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

The study was supported by a stipend of the Deutsche Forschungsgemeinschaft (DFG NO737/4-1) to Dennis A. Nowak.

Conflict of interest statement

None of the authors has any financial disclosures regarding the present manuscript. The study was supported by a grant of the Deutsche Forschungsgemeinschaft (DFG) to Dennis A. Nowak (NO 737/4-1).

Author information

Authors and Affiliations

  1. Department of Neurology, University of Cologne, Cologne, Germany

    Ulrike Grüner, Carsten Eggers, Mitra Ameli, Anna-Sophia Sarfeld, Gereon R. Fink & Dennis Alexander Nowak

  2. Institute of Neuroscience and Medicine (INM-3), Cognitive Neurology, Research Centre Jülich, Jülich, Germany

    Gereon R. Fink & Dennis Alexander Nowak

  3. Human Sensorimotor Control Laboratory, University of Minnesota, Minneapolis, MN, USA

    Dennis Alexander Nowak

  4. Neurochirurgische und Neurologische Fachklinik, Klinik Kipfenberg, Kindinger Strasse 13, 85110, Kipfenberg, Germany

    Dennis Alexander Nowak

Authors
  1. Ulrike Grüner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carsten Eggers
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mitra Ameli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anna-Sophia Sarfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gereon R. Fink
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dennis Alexander Nowak
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dennis Alexander Nowak.

Additional information

U. Grüner and C. Eggers have contributed equally to the study.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Grüner, U., Eggers, C., Ameli, M. et al. 1 Hz rTMS preconditioned by tDCS over the primary motor cortex in Parkinson’s disease: effects on bradykinesia of arm and hand. J Neural Transm 117, 207–216 (2010). https://doi.org/10.1007/s00702-009-0356-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-009-0356-0

Keywords

Search

Navigation