Skip to main content
Log in

Gait Impairments and Postural Instability in Parkinson’s Disease on the Background of Chronic Stimulation of Subcortical Structures

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

The surgical treatment of patients with Parkinson’s disease (PD) has in recent years firmly fixed its place in the overall algorithm of managing patients with this pathology. The most advanced and promising method is deep brain electrical stimulation, which decreases the severity of the main clinical manifestations of the disease, including some of the axial symptoms. The time characteristics of parkinsonian gait remains resistant to treatment by stimulation of the subthalamic nucleus. Levodopa-sensitive freezing during walking can decrease on stimulation of the subthalamic nucleus. This review summarizes the effects of stimulation of subcortical structures on gait abnormalities and postural instability in PD.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. O. Sukhoverskaya, “Parkinson’s disease and parkinsonism syndrome: diagnosis and treatment,” Mizhdunarod. Nevrol. Zh., 6, 16–24 (2011).

    Google Scholar 

  2. J. Ferreira, R. Katzenschlager, B. Bloem, et al., “Summary of the recommendations of the EFNS/MDS-ES review on therapeutic management of Parkinson’s disease,” Eur. J. Neurol., 20, No. 1, 5–15 (2012), https://doi.org/https://doi.org/10.1111/j.1468-1331.2012.03866.x.

  3. R. Kumar, A. Lozano, E. Sime, and A. Lang, “Long-term follow-up of thalamic deep brain stimulation for essential and parkinsonian tremor,” Neurology, 61, No. 11, 1601–1604 (2003), https://doi.org/https://doi.org/10.1212/01.wnl.0000096012.07360.1c.

  4. A. Storch, C. Schneider, M. Wolz, et al., “Nonmotor fluctuations in Parkinson disease: Severity and correlation with motor complications,” Neurology, 80, No. 9, 800–809 (2013), https://doi.org/https://doi.org/10.1212/wnl.0b013e318285c0d.

  5. V. A. Korenyuk, E. A. Sosnovskii, A. A. Manuilova, et al., “Surgical treatment of Parkinson’s disease,” Molodoi Uchenyi, 16, 29–31 (2018).

    Google Scholar 

  6. E. V. Bril, A. A. Tomskiy, A. A. Gamaleya, and V. A. Shabalov, “A comparative study of neurosurgical treatment (electrical stimulation of the subthalamic nucleus) and medication therapy in patients at the established stage of Parkinson’s disease,” Zh. Nevrol. Psikhiatr., 6, 55–61 (2014).

    Google Scholar 

  7. A. Singleton, M. Farrer, and V. Bonifati, “The genetics of Parkinson’s disease: Progress and therapeutic implications,” Mov. Disord., 28, No. 1, 14–23 (2013), https://doi.org/https://doi.org/10.1002/mds.25249.

  8. G. Ebersbach, C. Moreau, F. Gandor, et al., “Clinical syndromes: Parkinsonian gait,” Mov. Disord., 28, No. 11, 1552–1559 (2013), https://doi.org/https://doi.org/10.1002/mds.25675.

  9. B. Schoneburg, M. Mancini, F. Horak, and J. Nutt, “Framework for understanding balance dysfunction in Parkinson’s disease,” Mov. Disord., 28, No. 11, 1474–1482 (2013), https://doi.org/https://doi.org/10.1002/mds.25613.

  10. K. J. Brusse, S. Zimdars, K. R. Zalewski, and T. M. Steffen, “Testing functional performance in people with Parkinson disease,” Phys. Ther., 85, 134–141 (2005), https://doi.org/https://doi.org/10.1093/ptj/85.2.134.

  11. J. Himann, D. Cunningham, P. Rechnitzer, and D. Paterson, “Agerelated changes in speed of walking,” Med. Sci. Sports Exerc., 20, No. 2, 161–166 (1988).

    Article  CAS  Google Scholar 

  12. D. White, T. Neogi, M. Nevitt, et al., “Trajectories of gait speed predict mortality in well-functioning older adults: The health, aging and body composition study,” J. Gerontol. A. Biol. Sci. Med. Sci., 68, No. 4, 456–464 (2012), https://doi.org/https://doi.org/10.1093/gerona/gls197.

  13. M. Morris, T. Matyas, R. Iansek, and J. Summers, “Temporal stability of gait in Parkinson’s disease,” Phys. Ther., 76, No. 7, 763–777 (1996), https://doi.org/https://doi.org/10.1093/ptj/76.7.763.

  14. S. Studenski, S. Perera, J. M. Wallace D Chandler, et al., “Physical performance measures in the clinical setting,” J. Am. Geriatr. Soc., 51, No. 3, 314–322 (2003), https://doi.org/https://doi.org/10.1046/j.1532-5415.2003.51104.x.

  15. R. Elbers, E. Wegen, J. Verhoef, and G. Kwakkel, “Is gait speed a valid measure to predict community ambulation in patients with Parkinson’s disease?” J. Rehabil. Med., 45, No. 4, 370–375 (2013), https://doi.org/https://doi.org/10.2340/16501977-1123.

  16. J. Roper, N. Kang, J. Ben, et al., “Deep brain stimulation improves gait velocity in Parkinson’s disease: a systematic review and meta-analysis,” J. Neurol., 263, No. 6, 1195–1203 (2016), https://doi.org/https://doi.org/10.1007/s00415-016-8129-9.

  17. T. Ellis, J. Cavanaugh, G. Earhart, et al., “Identifying clinical measures that most accurately reflect the progression of disability in Parkinson disease,” Parkinsonism Relat. Disord., 25, 65–71 (2016), https://doi.org/https://doi.org/10.1016/j.parkreldis.2016.02.006.

  18. T. Boonstra, H. van der Kooij, M. Munneke, and B. Bloem, “Gait disorders and balance disturbances in Parkinson’s disease: clinical update and pathophysiology,” Curr. Opin. Neurol., 24, No. 4, 461–471 (2008), https://doi.org/https://doi.org/10.1097/wco.0b013e328305bdaf.

  19. M. Hely, W. Reid, M. Adena, et al., “The Sydney multicenter study of Parkinson’s disease: The inevitability of dementia at 20 years,” Mov. Disord., 23, No. 6, 837–844 (2008), https://doi.org/https://doi.org/10.1002/mds.21956.

  20. E. Stack, A. Ashburn, and K. Jupp, “Strategies used by people with Parkinson’s disease who report difficulty turning,” Parkinsonism Relat. Disord., 12, No. 2, 87– 92 (2006), https://doi.org/https://doi.org/10.1016/j.parkreldis.2005.08.008.

  21. P. Crenna, I. Carpinella, M. Rabuffetti, et al., “The association between impaired turning and normal straight walking in Parkinson’s disease,” Gait Posture, 26, No. 2, 172–178 (2007), https://doi.org/https://doi.org/10.1016/j.gaitpost.2007.04.010.

  22. A. Willems, A. Nieuwboer, F. Chavret, et al., “Turning in Parkinson’s disease patients and controls: The effect of auditory cues,” Mov. Disord., 22, No. 13, 1871–1878 (2007), https://doi.org/https://doi.org/10.1002/mds.21445.

  23. F. Huxham, J. Gong, R. Baker, et al., “Defining spatial parameters for non-linear walking,” Gait Posture, 23, No. 2, 159–163 (2006), https://doi.org/https://doi.org/10.1016/j.gaitpost.2005.01.001.

  24. G. Yogev-Seligmann, J. Hausdorff, and N. Giladi, “The role of executive function and attention in gait,” Mov. Disord., 23, No. 3, 329–342 (2008), https://doi.org/https://doi.org/10.1002/mds.21720.

  25. B. Bloem, Y. Grimbergen, J. van Dijk, and M. Munneke, “The ‘posture second’ strategy: A review of wrong priorities in Parkinson’s disease,” J. Neurol. Sci., 248, No. 1–2, 196–204 (2006), https://doi.org/https://doi.org/10.1002/mds.21720.

  26. M. Vaugoyeau, S. Viel, C. Assaiante, et al., “Impaired vertical postural control and proprioceptive integration deficits in Parkinson’s disease,” Neuroscience, 146, No. 2, 852–863 (2007), https://doi.org/https://doi.org/10.1016/j.neuroscience.2007.01.052.

  27. M. Selikhova, P. Kempster, T. Revesz, et al., “Neuropathological findings in benign tremulous Parkinsonism,” Mov. Disord., 28, No. 2, 145–152 (2012), https://doi.org/https://doi.org/10.1002/mds.25220.

  28. N. Giladi, D. McMahon, S. Przedborski, et al., “Motor blocks in Parkinson’s disease,” Neurology, 42, No. 2, 333–333 (1992), https://doi.org/https://doi.org/10.1212/wnl.42.2.333.

  29. P. Lamberti, S. Armenise, M. Castaldo V de Mari, et al., “Freezing gait in Parkinson’s disease,” Eur. Neurol., 38, No. 4, 297–301 (1997), https://doi.org/https://doi.org/10.1159/000113398.

  30. N. Giladi, M. McDermott, S. Fahn, et al., the Parkinson Study Group, “Freezing of gait in PD: Prospective assessment in the DATATOP cohort,” Neurology, 56, No. 12, 1712–1721 (2001), https://doi.org/https://doi.org/10.1212/wnl.56.12.1712.

  31. N. Giladi, T. Treves, E. Simon, et al., “Freezing of gait in patients with advanced Parkinson’s disease,” J. Neural. Transm. (Vienna), 108, No. 1, 53–61 (2001), https://doi.org/https://doi.org/10.1007/s007020170096.

  32. I. Shoulson, D. Oakes, S. Fahn, et al., the Parkinson Study Group, “Impact of sustained deprenyl (selegiline) in levodopa-treated Parkinson’s disease: A randomized placebo-controlled extension of the deprenyl and tocopherol antioxidative therapy of parkinsonism trial,” Ann. Neurol., 51, No. 5, 604–612 (2002), https://doi.org/https://doi.org/10.1002/ana.10191.

  33. Y. Okuma, “Freezing of gait in Parkinson’s disease,” J. Neurol., 253, No. 7, 27–32 (2006), https://doi.org/https://doi.org/10.1007/s00415-006-7007-2.

  34. L. Sudarsky, “Gait disorders among elderly patients,” Arch. Neurol., 40, No. 12, 740 (1983), https://doi.org/https://doi.org/10.1001/archneur.1983.04050110058009.

  35. N. Giladi, H. Shabtai, E. Simon, et al., “Construction of freezing of gait questionnaire for patients with Parkinsonism,” Parkins. Relat. Disord., 6, No. 3, 165–170 (2000), https://doi.org/https://doi.org/10.1016/s1353-8020(99)00062-0.

  36. N. Giladi, J. Tal, O. Azulay, et al., “Validation of the freezing of gait questionnaire in patients with Parkinson’s disease,” Mov. Disord., 24, No. 5, 655–661 (2009), https://doi.org/https://doi.org/10.1002/mds.21745.

  37. L. Yardley, N. Beyer, K. Hauer, et al., “Development and initial validation of the Falls Efficacy Scale-International (FES I),” Age Ageing, 34, No. 6, 614–619 (2005), https://doi.org/https://doi.org/10.1093/ageing/afi.196.

  38. J. Guralnik, L. Ferrucci, E. Simonsick, et al., “Lower-extremity function in persons over the age of 70 years as a predictor of subsequent disability,” N. Engl. J. Med., 332, No. 9, 556–562 (1995), https://doi.org/https://doi.org/10.1056/nejm199503023320902.

  39. K. Berg, “Measuring balance in the elderly: preliminary development of an instrument,” Physiother. Can., 41, No. 6, 304–311 (1989), https://doi.org/https://doi.org/10.3138/ptc.41.6.304.

  40. F. Horak, D. Wrisley, and J. Frank, “The Balance Evaluation Systems Test (BESTest) to differentiate balance deficits,” Phys. Ther., 89, No. 5, 484–498 (2009), https://doi.org/https://doi.org/10.2522/ptj.20080071.

  41. M. Thomas, J. Jankovic, M. Suteerawattananon, et al., “Clinical Gait And Balance Scale (GABS): validation and utilization,” J. Neurol. Sci., 217, No. 1, 89–99 (2004), https://doi.org/https://doi.org/10.1016/j.jns.2003.09.005.

  42. P. Martínez-Martín, D. Urra, T. Quijano, et al., “A new clinical tool for gait evaluation in Parkinson’s disease,” Clin. Neuropharmacol., 20, No. 3, 183–194 (1997), https://doi.org/https://doi.org/10.1097/00002826-199706000-00001.

  43. G. Ebersbach, C. Moreau, F. Gandor, et al., “Clinical syndromes: Parkinsonian gait,” Mov. Disord., 28, No. 11, 1552–1559 (2013), https://doi.org/https://doi.org/10.1002/mds.25675.

  44. A. A. Gamaleya, A. A. Tomskiy, E. V. Bril, and V. A. Shabalov, “Electrical stimulation of deep brain structures in extrapyramidal diseases. Principles of programming,” Nervnye Bolezni, 4, 55–61 (2012).

    Google Scholar 

  45. R. Munhoz, A. Cerasa, and M. Okun, “Surgical treatment of dyskinesia in Parkinson’s disease,” Front. Neurol., 5, 65 (2014), https://doi.org/https://doi.org/10.3389/fneur.2014.00065.

  46. C. Sidiropoulos, R. Walsh, S. Meoni, and E. Moro, “Surgical treatment of Parkinson’s disease,” Curr. Treat. Options Neurol., 14, No. 3, 211–212 (2012), https://doi.org/https://doi.org/10.1007/s11940-012-0174-9.

  47. A. Merola, L. Rizzi, C. A. Zibetti M Artusi, et al., “Medical therapy and subthalamic deep brain stimulation in advanced Parkinson’s disease: a different long-term outcome?” J. Neurol. Neurosurg. Psychiatry, 85, No. 5, 552–559 (2013), https://doi.org/https://doi.org/10.1136/jnnp-2013-305271.

  48. P. Limousin, P. Krack, P. Pollak, et al., “Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease,” N. Engl. J. Med., 339, No. 16, 1105–1111 (1998), https://doi.org/https://doi.org/10.1056/nejm199810153391603.

  49. M. Pötter-Nerger and J. Volkmann, “Deep brain stimulation for gait and postural symptoms in Parkinson’s disease,” Mov. Disord., 28, No. 11, 1609– 1615 (2013), https://doi.org/https://doi.org/10.1002/mds.25677.

  50. B. van Nuenen, R. Esselink, M. Munneke, et al., “Postoperative gait deterioration after bilateral subthalamic nucleus stimulation in Parkinson’s disease,” Mov. Disord., 23, No. 16, 2404–2406 (2008), https://doi.org/https://doi.org/10.1002/mds.21986.

  51. G. Tommasi, L. Lopiano, M. Zibetti, et al., “Freezing and hypokinesia of gait induced by stimulation of the subthalamic region,” J. Neurol. Sci., 258, No. 1–2, 99–103 (2007), https://doi.org/https://doi.org/10.1016/j.jns.2007.03.002.

  52. C. Moreau, L. Defebvre, A. Destee, et al., “STN-DBS frequency effects on freezing of gait in advanced Parkinson disease,” Neurology, 71, No. 2, 80–84 (2008), https://doi.org/https://doi.org/10.1212/01.wnl.0000303972.16279.46.

  53. M. Ferraye, B. Debu, and P. Pollak, “Deep brain stimulation effect on freezing of gait,” Mov. Disord., 23, No. 2, 489–494 (2008), https://doi.org/https://doi.org/10.1002/mds.21975.

  54. N. Rowland, F. Sammartino, and A. Lozano, “Advances in surgery for movement disorders,” Mov. Disord., 32, No. 1, 5–10 (2016), https://doi.org/https://doi.org/10.1002/mds.26636.

  55. A. Stefani, A. Lozano, A. Peppe, et al., “Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson’s disease,” Brain, 130, No. 6, 1596–1607 (2007), https://doi.org/https://doi.org/10.1093/brain/awl346.

  56. P. Gildenberg, “Treatment of Spasmodic torticollis by dorsal column stimulation,” Stereotact. Funct. Neurosurg., 41, No. 1–4, 113–121 (1978), https://doi.org/https://doi.org/10.1159/000102407.

  57. R. Fuentes, P. Petersson, and M. Nicolelis, “Restoration of locomotive function in Parkinson’s disease by spinal cord stimulation: mechanistic approach,” Eur. J. Neurosci., 32, No. 7, 1100–1108 (2010), https://doi.org/https://doi.org/10.1111/j.1460-9568.2010.07417.x.

  58. O. Samotus, A. Parrent, and M. Jog, “Spinal cord stimulation therapy for gait dysfunction in advanced Parkinson’s disease patients,” Mov. Disord., 33, No. 5, 783–792 (2018), https://doi.org/https://doi.org/10.1002/mds.27299.

  59. C. Pinto de Souza, C. Hamani, C. O. Souza, et al., “Spinal cord stimulation improves gait in patients with Parkinson’s disease previously treated with deep brain stimulation,” Mov. Disord., 32, No. 2, 278–282 (2017), https://doi.org/https://doi.org/10.1002/mds.26850.

  60. A. De Lima-Pardini, D. Coelho, C. O. Souza C Souza, et al., “Effects of spinal cord stimulation on postural control in Parkinson’s disease patients with freezing of gait,” eLife, 7 (2018), https://doi.org/https://doi.org/10.7554/elife.37727.

  61. J. Nonnekes and A. Nieuwboer, “Towards personalized rehabilitation for gait impairments in Parkinson’s disease,” J. Parkins. Dis., 8, No. 1, 101–106 (2018), https://doi.org/https://doi.org/10.3233/jpd-181464.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. G. Sultanova.

Additional information

Translated from Zhurnal Nevrologii i Psikhiatrii imeni S. S. Korsakova, Vol. 119, No. 9, Iss. 1, pp. 123–130, September, 2019.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sultanova, S.G., Fedorova, N.V., Bril, E.V. et al. Gait Impairments and Postural Instability in Parkinson’s Disease on the Background of Chronic Stimulation of Subcortical Structures. Neurosci Behav Physi 50, 676–682 (2020). https://doi.org/10.1007/s11055-020-00954-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-020-00954-7

Keywords

Navigation