Experimental Brain Research

, Volume 170, Issue 2, pp 206–215 | Cite as

Evolution of postural stability after subthalamic nucleus stimulation in Parkinson’s disease: a combined clinical and posturometric study

  • D. GuehlEmail author
  • P. Dehail
  • M.P. de Sèze
  • E. Cuny
  • P. Faux
  • F. Tison
  • M. Barat
  • B. Bioulac
  • P. Burbaud
Research Article


Objectives: The occurrence of postural and balance disorders is a frequent feature in advanced forms of Parkinson’s disease (PD). However, the pathological substrate of these disturbances is poorly understood. Methods: In the present work, we investigated the evolution of posturometric parameters [center of pressure (CoP) displacement and CoP area] and axial scores between the pre-operative period and 3 months post-operative in seven PD patients who underwent bilateral deep brain stimulation (DBS) of the subthalamic nucleus (STN). Results: After surgery, the patients leaned backwards much more regardless of the STN stimulation, suggesting that surgery could have a deleterious effect on postural adaptation. During the post-operative period, the improvement in axial and postural scores was similar under levodopatherapy and DBS. On the other hand, DBS of the STN significantly reduced the CoP displacement and the CoP area, whereas levodopatherapy tended only to reduce the CoP displacement and to increase the CoP area significantly. Conclusions: These data suggest that DBS of the STN and levodopa do not act on the same neurological systems involved in posture regulation. DBS of the STN could improve posture via a direct effect on the pedunculopontine nucleus, which is known to be involved in posture regulation.


Parkinson’s disease Subthalamic nucleus DBS Posturometry 


  1. Abbruzzese G, Berardelli A (2003) Sensorimotor integration in movement disorders. Mov Disord 18:231–240PubMedCrossRefGoogle Scholar
  2. Agid Y (1991) Parkinson’s disease: pathophysiology. Lancet 337:1321–1324PubMedCrossRefGoogle Scholar
  3. Allert N, Volkmann J, Dotse S, Hefter H, Sturm V, Freund HJ (2001) Effects of bilateral pallidal or subthalamic stimulation on gait in advanced Parkinson’s disease. Mov Disord 16:1076–1085PubMedCrossRefGoogle Scholar
  4. Bejjani BP, Gervais D, Arnulf I, Papadopoulos S, Demeret S, Bonnet AM, Cornu P, Damier P, Agid Y (2000) Axial parkinsonian symptoms can be improved: the role of levodopa and bilateral subthalamic stimulation. J Neurol Neurosurg Psychiatry 68:595–600PubMedCrossRefGoogle Scholar
  5. Bloem BR, Beckley DJ, Remler MP, Roos RA, van Dijk JG (1995) Postural reflexes in Parkinson’s disease during ‘resist’ and ‘yield’ tasks. J Neurol Sci 129:109–119PubMedCrossRefGoogle Scholar
  6. Bloem BR, Beckley DJ, van Dijk JG, Zwinderman AH, Remler MP, Roos RA (1996) Influence of dopaminergic medication on automatic postural responses and balance impairment in Parkinson’s disease. Mov Disord 11:509–521PubMedCrossRefGoogle Scholar
  7. Bonnet AM, Loria Y, Saint-Hilaire MH, Lhermitte F, Agid Y (1987) Does long-term aggravation of Parkinson’s disease result from nondopaminergic lesions? Neurology 37:1539–1542PubMedGoogle Scholar
  8. Bosek M, Grzegorzewski B, Kowalczyk A, Lubinski I (2005) Degradation of postural control system as a consequence of Parkinson’s disease and ageing. Neurosci Lett 376:215–220PubMedCrossRefGoogle Scholar
  9. Cuny E, Guehl D, Burbaud P, Gross C, Dousset V, Rougier A (2002) Lack of agreement between direct magnetic resonance imaging and statistical determination of a subthalamic target: the role of electrophysiological guidance. J Neurosurg 97:591–597PubMedCrossRefGoogle Scholar
  10. Defebvre L, Blatt JL, Blond S, Bourriez JL, Gieu JD, Destee A (1996) Effect of thalamic stimulation on gait in Parkinson’s disease. Arch Neurol 53:898–903PubMedGoogle Scholar
  11. Defebvre LJ, Krystkowiak P, Blatt JL, Duhamel A, Bourriez JL, Perina M, Blond S, Guieu JD, Destee A (2002) Influence of pallidal stimulation and levodopa on gait and preparatory postural adjustments in Parkinson’s disease. Mov Disord 17:76–83PubMedCrossRefGoogle Scholar
  12. Diener HC, Dichgans J (1988) On the role of vestibular, visual and somatosensory information for dynamic postural control in humans. Prog Brain Res 76:253–262PubMedGoogle Scholar
  13. Fahn Y, Elton R (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden C, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease, vol 2. Macmillan, NY, pp 153–163Google Scholar
  14. Faist M, Xie J, Kurz D, Berger W, Maurer C, Pollak P, Lucking CH (2001) Effect of bilateral subthalamic nucleus stimulation on gait in Parkinson’s disease. Brain 124:1590–1600PubMedCrossRefGoogle Scholar
  15. Fraix V, Pollak P, Van Blercom N, Xie J, Krack P, Koudsie A, Benabid AL (2000) Effect of subthalamic nucleus stimulation on levodopa-induced dyskinesia in Parkinson’s disease. Neurology 55:1921–1923PubMedGoogle Scholar
  16. Frank JS, Horak FB, Nutt J (2000) Centrally initiated postural adjustments in parkinsonian patients on and off levodopa. J Neurophysiol 84:2440–2448PubMedGoogle Scholar
  17. Gantchev N, Viallet F, Aurenty R, Massion J (2000) Forward versus backward oriented stepping movements in Parkinsonian patients. Motor Control 4:453–468PubMedGoogle Scholar
  18. Garcia L, Audin J, D’Alessandro G, Bioulac B, Hammond C (2003) Dual effect of high-frequency stimulation on subthalamic neuron activity. J Neurosci 23:8743–8751PubMedGoogle Scholar
  19. Goetz CG, Stebbins GT, Shale HM, Lang AE, Chernik DA, Chmura TA, Ahlskog JE, Dorflinger EE (1994) Utility of an objective dyskinesia rating scale for Parkinson’s disease: inter- and intrarater reliability assessment. Mov Disord 9:390–394PubMedCrossRefGoogle Scholar
  20. Gross C, Rougier A, Guehl D, Boraud T, Julien J, Bioulac B (1997) High-frequency stimulation of the globus pallidus internalis in Parkinson’s disease: a study of seven cases. J Neurosurg 87:491–498PubMedGoogle Scholar
  21. Group DBSfPsdS (2001) Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson’s disease. N Engl J Med 345:956–963CrossRefGoogle Scholar
  22. Herzog J, Volkmann J, Krack P, Kopper F, Potter M, Lorenz D, Steinbach M, Klebe S, Hamel W, Schrader B, Weinert D, Muller D, Mehdorn HM, Deuschl G (2003) Two-year follow-up of subthalamic deep brain stimulation in Parkinson’s disease. Mov Disord 18:1332–1337PubMedCrossRefGoogle Scholar
  23. Hoehn M, Yahr M (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMedGoogle Scholar
  24. Horak FB, Frank J, Nutt J (1996) Effects of dopamine on postural control in parkinsonian subjects: scaling, set, and tone. J Neurophysiol 75:2380–2396PubMedGoogle Scholar
  25. Horak FB, Nutt JG, Nashner LM (1992) Postural inflexibility in parkinsonian subjects. J Neurol Sci 111:46–58PubMedCrossRefGoogle Scholar
  26. Houeto JL, Damier P, Bejjani PB, Staedler C, Bonnet AM, Arnulf I, Pidoux B, Dormont D, Cornu P, Agid Y (2000) Subthalamic stimulation in Parkinson’s disease: a multidisciplinary approach. Arch Neurol 57:461–465PubMedCrossRefGoogle Scholar
  27. Klawans HL (1986) Individual manifestations of Parkinson’s disease after ten or more years of levodopa. Mov Disord 1:187–192PubMedCrossRefGoogle Scholar
  28. Koller WC, Glatt S, Vetere-Overfield B, Hassanein R (1989) Falls and Parkinson’s disease. Clin Neuropharmacol 12:98–105PubMedCrossRefGoogle Scholar
  29. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, Koudsie A, Limousin PD, Benazzouz A, LeBas JF, Benabid AL, Pollak P (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934PubMedCrossRefGoogle Scholar
  30. Krause M, Fogel W, Mayer P, Kloss M, Tronnier V (2004) Chronic inhibition of the subthalamic nucleus in Parkinson’s disease. J Neurol Sci 219:119–124PubMedCrossRefGoogle Scholar
  31. Krystkowiak P, Blatt JL, Bourriez JL, Duhamel A, Perina M, Blond S, Guieu JD, Destee A, Defebvre L (2003) Effects of subthalamic nucleus stimulation and levodopa treatment on gait abnormalities in Parkinson disease. Arch Neurol 60:80–84PubMedCrossRefGoogle Scholar
  32. Krystkowiak P, Blatt JL, Bourriez JL, Duhamel A, Perina M, Kemoun G, Blond S, Guieu JD, Destee A, Defebvre L (2001) Chronic bilateral pallidal stimulation and levodopa do not improve gait in the same way in Parkinson’s disease: a study using a video motion analysis system. J Neurol 248:944–949PubMedCrossRefGoogle Scholar
  33. Kumar R, Lozano AM, Montgomery E, Lang AE (1998) Pallidotomy and deep brain stimulation of the pallidum and subthalamic nucleus in advanced Parkinson’s disease. Mov Disord 13(Suppl 1):73–82PubMedGoogle Scholar
  34. Lafond D, Duarte M, Prince F (2004) Comparison of three methods to estimate the center of mass during balance assessment. J Biomech 37:1421–1426PubMedCrossRefGoogle Scholar
  35. Lakke JP (1985) Axial apraxia in Parkinson’s disease. J Neurol Sci 69:37–46PubMedCrossRefGoogle Scholar
  36. Lakke JP, van Weerden TW, Staal-Schreinemachers A (1984) Axial apraxia, a distinct phenomenon. Clin Neurol Neurosurg 86:291–294PubMedCrossRefGoogle Scholar
  37. Limousin P, Krack P, Pollak P, Benazzouz A, Ardoin C, Hoffmann D, Benabid AL (1998) Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 339:1105–1111PubMedCrossRefGoogle Scholar
  38. Lozano AM, Lang AE, Galvez-Jimenez N, Miyasaki J, Duff J, Hutchinson WD, Dostrovsky JO (1995) Effect of GPi pallidotomy on motor function in Parkinson’s disease. Lancet 346:1383–1387PubMedCrossRefGoogle Scholar
  39. Maki BE, McIlroy WE (1996) Postural control in the older adult. Clin Geriatr Med 12:635–658PubMedGoogle Scholar
  40. Maki BE, McIlroy WE, Perry SD (1996) Influence of lateral destabilization on compensatory stepping responses. J Biomech 29:343–353PubMedCrossRefGoogle Scholar
  41. Marchese R, Diverio M, Zucchi F, Lentino C, Abbruzzese G (2000) The role of sensory cues in the rehabilitation of parkinsonian patients: a comparison of two physical therapy protocols. Mov Disord 15:879–883PubMedCrossRefGoogle Scholar
  42. Maurer C, Mergner T, Xie J, Faist M, Pollak P, Lucking CH (2003) Effect of chronic bilateral subthalamic nucleus (STN) stimulation on postural control in Parkinson’s disease. Brain 126:1146–1163PubMedCrossRefGoogle Scholar
  43. Morris ME, Iansek R, Matyas TA, Summers JJ (1996) Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain 119(Pt 2):551–568PubMedCrossRefGoogle Scholar
  44. Oliveira RM, Gurd JM, Nixon P, Marshall JC, Passingham RE (1997) Micrographia in Parkinson’s disease: the effect of providing external cues. J Neurol Neurosurg Psychiatry 63:429–433PubMedGoogle Scholar
  45. Onell A (2000) The vertical ground reaction force for analysis of balance? Gait Posture 12:7–13PubMedCrossRefGoogle Scholar
  46. Ostergaard K, Sunde N, Dupont E (2002) Effects of bilateral stimulation of the subthalamic nucleus in patients with severe Parkinson’s disease and motor fluctuations. Mov Disord 17:693–700PubMedCrossRefGoogle Scholar
  47. Pahapill PA, Lozano AM (2000) The pedunculopontine nucleus and Parkinson’s disease. Brain 123 (Pt 9):1767–1783CrossRefGoogle Scholar
  48. Pinter MM, Murg M, Alesch F, Freundl B, Helscher RJ, Binder H (1999) Does deep brain stimulation of the nucleus ventralis intermedius affect postural control and locomotion in Parkinson’s disease? Mov Disord 14:958–963PubMedCrossRefGoogle Scholar
  49. Pollak P, Benabid AL, Limousin P, Benazzouz A, Hoffmann D, Le Bas JF, Perret J (1996) Subthalamic nucleus stimulation alleviates akinesia and rigidity in parkinsonian patients. Adv Neurol 69:591–594PubMedGoogle Scholar
  50. Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM (1996) Measures of postural steadiness: differences between healthy young and elderly adults. IEEE Trans Biomed Eng 43:956–966PubMedCrossRefGoogle Scholar
  51. Robertson LT, Horak FB, Anderson VC, Burchiel KJ, Hammerstad JP (2001) Assessments of axial motor control during deep brain stimulation in parkinsonian patients; Discussion 551–542. Neurosurgery 48:544–551PubMedCrossRefGoogle Scholar
  52. Rocchi L, Chiari L, Cappello A, Gross A, Horak FB (2004) Comparison between subthalamic nucleus and globus pallidus internus stimulation for postural performance in Parkinson’s disease. Gait Posture 19:172–183PubMedCrossRefGoogle Scholar
  53. Rocchi L, Chiari L, Horak FB (2002) Effects of deep brain stimulation and levodopa on postural sway in Parkinson’s disease. J Neurol Neurosurg Psychiatry 73:267–274PubMedCrossRefGoogle Scholar
  54. Schieppati M, Nardone A (1991) Free and supported stance in Parkinson’s disease. The effect of posture and ‘postural set’ on leg muscle responses to perturbation, and its relation to the severity of the disease. Brain 114(Pt 3):1227–1244PubMedCrossRefGoogle Scholar
  55. Siegfried J, Lippitz B (1994) Bilateral chronic electrostimulation of ventroposterolateral pallidum: a new therapeutic approach for alleviating all parkinsonian symptoms; Discussion 1129–1130. Neurosurgery 35:1126–1129PubMedCrossRefGoogle Scholar
  56. Smith Y, Hazrati LN, Parent A (1990) Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method. J Comp Neurol 294:306–323PubMedCrossRefGoogle Scholar
  57. Stolze H, Klebe S, Poepping M, Lorenz D, Herzog J, Hamel W, Schrader B, Raethjen J, Wenzelburger R, Mehdorn HM, Deuschl G, Krack P (2001) Effects of bilateral subthalamic nucleus stimulation on parkinsonian gait. Neurology 57:144–146PubMedGoogle Scholar
  58. Takakusaki K, Habaguchi T, Saitoh K, Kohyama J (2004) Changes in the excitability of hindlimb motoneurons during muscular atonia induced by stimulating the pedunculopontine tegmental nucleus in cats. Neuroscience 124:467–480PubMedCrossRefGoogle Scholar
  59. Takakusaki K, Shimoda N, Matsuyama K, Mori S (1994) Discharge properties of medullary reticulospinal neurons during postural changes induced by intrapontine injections of carbachol, atropine and serotonin, and their functional linkages to hindlimb motoneurons in cats. Exp Brain Res 99:361–374PubMedCrossRefGoogle Scholar
  60. van Wegen EE, van Emmerik RE, Wagenaar RC, Ellis T (2001) Stability boundaries and lateral postural control in parkinson’s disease. Motor Control 5:254–269PubMedGoogle Scholar
  61. Welter ML, Houeto JL, Tezenas du Montcel S, Mesnage V, Bonnet AM, Pillon B, Arnulf I, Pidoux B, Dormont D, Cornu P, Agid Y (2002) Clinical predictive factors of subthalamic stimulation in Parkinson’s disease. Brain 125:575–583PubMedCrossRefGoogle Scholar
  62. Xie J, Krack P, Benabid AL, Pollak P (2001) Effect of bilateral subthalamic nucleus stimulation on parkinsonian gait. J Neurol 248:1068–1072PubMedCrossRefGoogle Scholar
  63. Zetusky WJ, Jankovic J, Pirozzolo FJ (1985) The heterogeneity of Parkinson’s disease: clinical and prognostic implications. Neurology 35:522–526PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • D. Guehl
    • 1
    Email author
  • P. Dehail
    • 2
  • M.P. de Sèze
    • 2
  • E. Cuny
    • 3
  • P. Faux
    • 2
  • F. Tison
    • 4
  • M. Barat
    • 2
  • B. Bioulac
    • 1
  • P. Burbaud
    • 1
  1. 1.Service de Neurophysiologie Clinique, Hôpital Pellegrin, Place Amélie-Raba-LéonCNRS UMR 5543, Université de BordeauxBordeauxFrance
  2. 2.Service de Médecine physique et réadaptation, Hôpital Pellegrin, Place Amélie-Raba-LéonCNRS UMR 5543, Université de BordeauxBordeauxFrance
  3. 3.Service de Neurochirurgie, Hôpital Pellegrin, Hôpital Pellegrin, Place Amélie-Raba-LéonCNRS UMR 5543, Université de BordeauxBordeauxFrance
  4. 4.Service de Neurologie, Hôpital Hauī Lēvĉque, PessacCNRS UMR 5543, Université de BordeauxBordeauxFrance

Personalised recommendations