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Effects of unilateral pedunculopontine stimulation on electromyographic activation patterns during gait in individual patients with Parkinson’s disease

  • Movement Disorders - Original Article
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Abstract

In Parkinson’s disease (PD), the effects of deep brain stimulation of the pedunculopontine nucleus (PPTg-DBS) on gait has been object of international debate. Some evidence demonstrated that, in the late swing-early stance phase of gait cycle, a reduced surface electromyographic activation (sEMG) of tibialis anterior (TA) is linked to the striatal dopamine deficiency in PD patients. In the present study we report preliminary results on the effect of PPTg-DBS on electromyographic patterns during gait in individual PD patients. To evaluate the sEMG amplitude of TA, the root mean square (RMS) of the TA burst in late swing-early stance phase (RMS-A) was normalized as a percent of the RMS of the TA burst in late stance-early swing (RMS-B). We studied three male patients in the following conditions: on PPTg-DBS/on l-dopa, on PPTg-DBS/off l-dopa, off PPTg-DBS/on l-dopa, off PPTg-DBS/off l-dopa. For each assessment the UPDRS III was filled in. We observed no difference between on PPTg-DBS/off l-dopa and off PPTg-DBS/off l-dopa in UPDRS III scores. In off PPTg-DBS/off l-dopa, patient A (right implant) showed absence of the right and left RMSA, respectively, in 80% and 83% of gait cycles. Patient B (right implant) showed absence of the right RMS-A in 86% of cycles. RMS-A of the patient C (left implant) was bilaterally normal. In on PPTg- DBS/off l-dopa, no patient showed reduced RMS-A. Although the very low number of subjects we evaluated, our observations suggest that PPTg plays a role in modulating TA activation pattern during the steady state of gait.

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References

  • Alam M, Schwabe K, Krauss JK (2011) The pedunculopontine nucleus area: critical evaluation of interspecies differences relevant for its use as a target for deep brain stimulation. Brain 134:11–23

    Article  PubMed  Google Scholar 

  • Aravamuthan BR, Muthusamy KA, Stein JF, Aziz TZ, Johansen-Berg H (2007) Topography of cortical and subcortical connections of the human pedunculopontine and subthalamic nuclei. Neuroimage 37:694–705

    Article  PubMed  CAS  Google Scholar 

  • Blin O, Ferrandez AM, Pailhous J, Serratrice G (1991) Dopa-sensitive and dopa-resistant gait parameters in Parkinson’s disease. J Neurol Sci 103(1):51–54

    Article  PubMed  CAS  Google Scholar 

  • Byrne CA, O’Keeffe DT, Donnelly AE, Lyons GM (2007) Effect of walking speed changes on tibialis anterior EMG during healthy gait for FES envelope design in drop foot correction. J Electromyogr Kinesiol 17:605–616

    Article  PubMed  CAS  Google Scholar 

  • Caliandro P, Ferrarin M, Cioni M, Bentivoglio AR, Minciotti I, D’Urso PI, Tonali PA, Padua L (2011) Levodopa effect on electromyographic activation patterns of tibialis anterior muscle during walking in Parkinson’s disease. Gait Post

  • Cappellini G, Ivanenko YP, Poppele RE, Lacquaniti F (2006) Motor patterns in human walking and running. J Neurophysio 95(6):3426–3437

    Article  CAS  Google Scholar 

  • Cioni M, Richards CL, Malouin F, Bedard PJ, Lemieux R (1997) Characteristics of the electromyographic patterns of lower limb muscles during gait in patients with Parkinson’s disease when OFF and ON l-dopa treatment. Ital J Neurol Sci 18:195–208

    Article  PubMed  CAS  Google Scholar 

  • Classen J, Schnitzler A (2010) What does the pedunculopontine nucleus do? Neurology 75(11):944–945

    Article  PubMed  Google Scholar 

  • den Otter AR, Geurts ACH, Mulder T, Duysens J (2004) Speed related changes in muscle activity from normal to very slow walking speeds. Gait Posture 19:270–278

    Article  Google Scholar 

  • Ferrarin M, Carpinella I, Rabuffetti M, Rizzone M, Lopiano L, Crenna P (2007) Unilateral and bilateral subthalamic nucleus stimulation in Parkinson’s disease: effects on EMG signals of lower limb muscles during walking. IEEE Trans Neural Syst Rehabil Eng 15:182–189

    Article  PubMed  Google Scholar 

  • Ferraye MU, Debû B, Fraix V, Goetz L, Ardouin C, Yelnik J et al (2010) Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson’s disease. Brain 133:205–214

    Article  PubMed  CAS  Google Scholar 

  • Giladi N (2001) Gait disturbances in advanced stages of Parkinson’s disease. Adv Neurol 86:273–278

    PubMed  CAS  Google Scholar 

  • Giladi N, Treves TA, Simon ES, Shabtai H, Orlov Y, Kandinov B, Paleacu D, Korczyn AD (2001) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm 108:53–61

    Article  PubMed  CAS  Google Scholar 

  • Jenkinson N, Nandi D, Oram R, Stein JF, Aziz TZ (2006) Pedunculopontine nucleus electric stimulation alleviates akinesia independently of dopaminergic mechanisms. Neuroreport 17:639–641

    Article  PubMed  Google Scholar 

  • Karachi C, Grabli D, Bernard FA, Tandé D, Wattiez N, Belaid H, Bardinet E, Prigent A, Nothacker HP, Hunot S, Hartmann A, Lehéricy S, Hirsch EC, François C (2010) Cholinergic mesencephalic neurons are involved in gait and postural disorders in Parkinson disease. J Clin Invest 120(8):2745–2754

    Article  PubMed  CAS  Google Scholar 

  • Lavoie B, Parent A (1994) Pedunculopontine nucleus in the squirrel monkey: cholinergic and glutamatergic projections to the substantia nigra. J Comp Neurol 344(2):232–241

    Article  PubMed  CAS  Google Scholar 

  • Malcolm P, Segers V, Van Caekenberghe I, De Clercq D (2009) Experimental study of the influence of the M. tibialis anterior on the walk-to-run transition by means of a powered ankle-foot exoskeleton. Gait Posture 29:6–10

    Article  PubMed  CAS  Google Scholar 

  • Mazzone P, Insola A, Lozano A et al (2007) Peripeduncular and pedunculopontine nuclei: a dispute on a clinically relevant target. Neuroreport 18(13):1407–1408

    Article  PubMed  Google Scholar 

  • Mazzone P, Sposato S, Insola A, Di Lazzaro V, Scarnati E (2008) Stereotactic surgery of nucleus tegmenti pedunculopontine. Br J Neurosurg 22S1:S33–S40

    Google Scholar 

  • Mazzone P, Insola A, Sposato S, Scarnati E (2009) The deep brain stimulation of the pedunculopontine tegmental nucleus. Neuromodulation 12:191–204

    Article  Google Scholar 

  • Mazzone P, Sposato S, Insola A, Scarnati E (2011) The deep brain stimulation of the pedunculopontine tegmental nucleus: towards a new stereotactic neurosurgery. J Neural Transm 2011. doi:10.1007/s00702-011-0593-x

  • Mitoma H, Hayashi R, Yanagisawa N, Tsukagoshi H (2000) Characteristics of parkinsonian and ataxic gaits: a study using surface electromyograms, angular displacements and floor reaction forces. J Neurol Sci 174:22–39

    Article  PubMed  CAS  Google Scholar 

  • Moro E, Hamani C, Poon YY, Al-Khairallah T, Dostrovsky JO, Hutchison WD et al (2010) Unilateral pedunculopontine stimulation improves falls in Parkinson’s disease. Brain 133:215–224

    Article  PubMed  Google Scholar 

  • Morris M, Iansek R, Matyas T, Summers J (1998) Abnormalities in the stride length-cadence relation in parkinsonian gait. Mov Disord 13:61–69

    Article  PubMed  CAS  Google Scholar 

  • Movement Disorder Society Task Force on Rating Scales for Parkinson’s Disease (2003) The Unified Parkinson’s Disease Rating Scale (UPDRS): status and recommendations. Mov Disord 18:738–750

    Google Scholar 

  • Nieuwboer A, Dom R, De Weerdt W, Desloovere K, Janssens L, Stijn V (2004) Electromyographic profiles of gait prior to onset of freezing episodes in patients with Parkinson’s disease. Brain 127:1650–1660

    Article  PubMed  Google Scholar 

  • Peppe A, Pierantozzi M, Chiavalon C, Marchetti F, Caltagirone C, Musicco M, Stanzione P, Stefani A (2010) Deep brain stimulation of the pedunculopontine tegmentum and subthalamic nucleus: effects on gait in Parkinson’s disease. Gait Posture 32(4):512–518

    Article  PubMed  CAS  Google Scholar 

  • Rainoldi A, Melchiorri G, Caruso I (2004) A method for positioning electrodes during surface EMG recordings in lower limb muscles. J Neurosci Methods 134:37–43

    Article  PubMed  CAS  Google Scholar 

  • Rolland AS, Tandé D, Herrero MT, Luquin MR, Vazquez-Claverie M, Karachi C, Hirsch EC, François C (2009) Evidence for a dopaminergic innervation of the pedunculopontine nucleus in monkeys, and its drastic reduction after MPTP intoxication. J Neurochem 110(4):1321–1329

    Article  PubMed  CAS  Google Scholar 

  • Segers V, Lenoir M, Aerts P, De Clercq D (2007) Influence of M. tibialis anterior fatigue on the walk-to-run and run-to-walk transition in non-steady condition locomotion. Gait Posture 25:639–647

    Article  PubMed  CAS  Google Scholar 

  • Shiavi R (1985) Electromyographic pattern in adult locomotion: a comprehensive review. J Rehabil Res Dev 22:85–98

    Article  PubMed  CAS  Google Scholar 

  • Siderowf A, McDermott M, Kieburtz K, Blindauer K, Plumb S, Shoulson I (2002) The Parkinson Study Group: 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

    Article  PubMed  Google Scholar 

  • Tsang EW, Hamani C, Moro E et al (2010) Involvement of the human pedunculopontine nucleus region in voluntary movements. Neurology 75:950–959

    Article  PubMed  CAS  Google Scholar 

  • Warren GL, Maher RM, Higbie EJ (2004) Temporal patterns of plantar pressures and lower-leg muscle activity during walking: effect of speed. Gait Posture 19:91–100

    Article  PubMed  Google Scholar 

  • Wilcox RA, Cole MH, Wong D, Coyne T, Silburn P, Kerr G (2010) Pedunculopontine nucleus deep brain stimulation produces sustained improvement in primary progressive freezing of gait. J Neurol Neurosurg Psychiatry (Epub ahead of print)

  • Yelnik J (2007) PPN or PPD, what is the target for deep brain stimulation in Parkinson’s disease? Brain 130(Pt 9):e79

    Article  PubMed  Google Scholar 

  • Zrinzo L, Zrinzo L, Hariz M (2007) The peripeduncular nucleus: a novel target for deep brain stimulation? Neuroreport 18(15):1631–1632 (author reply 1632-1633)

    PubMed  Google Scholar 

  • Zweig RM, Jankel WR, Hedreen JC, Mayeux R, Price DL (1989) The pedunculopontine nucleus in Parkinson’s disease. Ann Neurol 26(1):41–46

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Claudia Garattini, Ileana Minciotti and Chiara Simbolotti for their technical support.

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Authors and Affiliations

  1. Department of Neuroscience, Institute of Neurology, Università Cattolica del Sacro Cuore, Largo F. Vito 1, 00168, Rome, Italy

    Pietro Caliandro & L. Padua

  2. Department of Medical Surgical Sciences of Communication and Behaviour, Section of Neurology, University of Ferrara, Ferrara, Italy

    Pietro Caliandro & E. Granieri

  3. Unità Operativa di Neurofisiopatologia, CTO, ASL RMC, Rome, Italy

    A. Insola

  4. Department of Sciences and Biomedical Technologies, University of L’Aquila, L’Aquila, Italy

    E. Scarnati

  5. Fondazione Don Carlo Gnocchi Onlus, Milan, Italy

    L. Padua & G. Russo

  6. Functional and Stereotactic Neurosurgery, CTO, ASL RMC, Rome, Italy

    P. Mazzone

Authors
  1. Pietro Caliandro
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  2. A. Insola
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  3. E. Scarnati
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  4. L. Padua
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  5. G. Russo
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  6. E. Granieri
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  7. P. Mazzone
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Correspondence to Pietro Caliandro.

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Caliandro, P., Insola, A., Scarnati, E. et al. Effects of unilateral pedunculopontine stimulation on electromyographic activation patterns during gait in individual patients with Parkinson’s disease. J Neural Transm 118, 1477–1486 (2011). https://doi.org/10.1007/s00702-011-0705-7

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  • DOI: https://doi.org/10.1007/s00702-011-0705-7

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