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Journal of Neurology, Neurosurgery, and Psychiatry logoLink to Journal of Neurology, Neurosurgery, and Psychiatry
. 1999 Sep;67(3):308–314. doi: 10.1136/jnnp.67.3.308

Improvement of levodopa induced dyskinesias by thalamic deep brain stimulation is related to slight variation in electrode placement: possible involvement of the centre median and parafascicularis complex

D Caparros-Lefebvre 1, S Blond 1, M Feltin 1, P Pollak 1, A L Benabid 1
PMCID: PMC1736532  PMID: 10449551

Abstract

OBJECTIVE—To define the reason why two teams using the same procedure and the same target for deep brain stimulation (DBS) obtained different results on levodopa induced dyskinesias, whereas in both, parkinsonian tremor was improved or totally suppressed.
METHODS—Deep brain stimulation can replace lesions in the surgical treatment of abnormal movements. After 10 years of experience with DBS in Parkinson's disease, a comparison of results between the teams of Lille (A) and Grenoble (B) was carried out, for as long as they used intraoperative ventriculography. Both teams aimed at the same target, the ventralis intermedius nucleus of the thalamus (VIM), but team A found a clear improvement of choreic peak dose dyskinesias, whereas team B did not consistently. Therefore all teleradioanatomical data of both teams were re-examined and compared with the therapeutic effects. Location of 99 monopolar electrodes of thalamic stimulation applied to treat parkinsonian tremor has been retrospectively measured (team A included 21 patients, 22electrodes; team B included 52 patients, 74 electrodes). Peak dose levodopa dyskinesias were suppressed by DBS in all nine patients of team A, four of which were severely disabling. Only eight out of 32 patients from team B experienced a moderate (four) or clear (four) improvement of dyskinesias, whereas in the remaining 24patients, dyskinesias were unchanged with stimulation.
RESULTS—The mean centre of team A's electrodes was on average 2.9 mm deeper, more posterior and medial than team B's (t=8.05; p<0.0001). This does not correspond to the coordinates of the VIM, but seems to be closer to those of the centre median and parafascicularis complex (CM-Pf), according to stereotaxic atlases. Considering only the dyskinetic patients, significant differences were found in the electrode position according to the therapeutic effects on levodopa dyskinesias, but they were not related to the team membership. Improvement in levodopa dyskinesias was significantly associated with deeper and more medial placement of electrodes.
CONCLUSION—The retrospective analysis of patients treated with DBS using comparable methodologies provides important information concerning electrode position and therapeutic outcome. The position of the electrode is related to the therapeutic effects of DBS. The results support the hypothesis that patients experiencing an improvement of dyskinesias under DBS are actually stimulated in a structure which is more posterior, more internal, and deeper than the VIM, very close to the CM-Pf. These results are consistent with neuroanatomical and neurophysiological data showing that the CM-Pf is included in the motor circuits of the basal ganglia system and receives an important input from the internal pallidum. This suggests that the CM-Pf could be involved specifically in the pathophysiology of levodopa peak dose dyskinesias.



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Selected References

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  1. Alexander G. E., Crutcher M. D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990 Jul;13(7):266–271. doi: 10.1016/0166-2236(90)90107-l. [DOI] [PubMed] [Google Scholar]
  2. Andy O. J. Parafascicular-center median nuclei stimulation for intractable pain and dyskinesia (painful-dyskinesia). Appl Neurophysiol. 1980;43(3-5):133–144. doi: 10.1159/000102247. [DOI] [PubMed] [Google Scholar]
  3. Andy O. J. Thalamic stimulation for control of movement disorders. Appl Neurophysiol. 1983;46(1-4):107–111. doi: 10.1159/000101248. [DOI] [PubMed] [Google Scholar]
  4. Arecchi-Bouchhioua P., Yelnik J., François C., Percheron G., Tandé D. Three-dimensional morphology and distribution of pallidal axons projecting to both the lateral region of the thalamus and the central complex in primates. Brain Res. 1997 Apr 18;754(1-2):311–314. doi: 10.1016/s0006-8993(97)00181-9. [DOI] [PubMed] [Google Scholar]
  5. Barbeau A. Letter: Diphasic dyskinesia during levodopa therapy. Lancet. 1975 Mar 29;1(7909):756–756. doi: 10.1016/s0140-6736(75)91676-1. [DOI] [PubMed] [Google Scholar]
  6. Benabid A. L., Pollak P., Gao D., Hoffmann D., Limousin P., Gay E., Payen I., Benazzouz A. Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J Neurosurg. 1996 Feb;84(2):203–214. doi: 10.3171/jns.1996.84.2.0203. [DOI] [PubMed] [Google Scholar]
  7. Benabid A. L., Pollak P., Gervason C., Hoffmann D., Gao D. M., Hommel M., Perret J. E., de Rougemont J. Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet. 1991 Feb 16;337(8738):403–406. doi: 10.1016/0140-6736(91)91175-t. [DOI] [PubMed] [Google Scholar]
  8. Benabid A. L., Pollak P., Louveau A., Henry S., de Rougemont J. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol. 1987;50(1-6):344–346. doi: 10.1159/000100803. [DOI] [PubMed] [Google Scholar]
  9. Blond S., Caparros-Lefebvre D., Parker F., Assaker R., Petit H., Guieu J. D., Christiaens J. L. Control of tremor and involuntary movement disorders by chronic stereotactic stimulation of the ventral intermediate thalamic nucleus. J Neurosurg. 1992 Jul;77(1):62–68. doi: 10.3171/jns.1992.77.1.0062. [DOI] [PubMed] [Google Scholar]
  10. Caparros-Lefebvre D., Blond S., Vermersch P., Pécheux N., Guieu J. D., Petit H. Chronic thalamic stimulation improves tremor and levodopa induced dyskinesias in Parkinson's disease. J Neurol Neurosurg Psychiatry. 1993 Mar;56(3):268–273. doi: 10.1136/jnnp.56.3.268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Caparros-Lefebvre D., Ruchoux M. M., Blond S., Petit H., Percheron G. Long-term thalamic stimulation in Parkinson's disease: postmortem anatomoclinical study. Neurology. 1994 Oct;44(10):1856–1860. doi: 10.1212/wnl.44.10.1856. [DOI] [PubMed] [Google Scholar]
  12. Crossman A. R. Primate models of dyskinesia: the experimental approach to the study of basal ganglia-related involuntary movement disorders. Neuroscience. 1987 Apr;21(1):1–40. doi: 10.1016/0306-4522(87)90322-8. [DOI] [PubMed] [Google Scholar]
  13. Deiber M. P., Pollak P., Passingham R., Landais P., Gervason C., Cinotti L., Friston K., Frackowiak R., Mauguière F., Benabid A. L. Thalamic stimulation and suppression of parkinsonian tremor. Evidence of a cerebellar deactivation using positron emission tomography. Brain. 1993 Feb;116(Pt 1):267–279. doi: 10.1093/brain/116.1.267. [DOI] [PubMed] [Google Scholar]
  14. Duffau H., Tzourio N., Caparros-Lefebvre D., Parker F., Mazoyer B. Tremor and voluntary repetitive movement in Parkinson's disease: comparison before and after L-dopa with positron emission tomography. Exp Brain Res. 1996;107(3):453–462. doi: 10.1007/BF00230425. [DOI] [PubMed] [Google Scholar]
  15. Hughes A. J., Daniel S. E., Kilford L., Lees A. J. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. 1992 Mar;55(3):181–184. doi: 10.1136/jnnp.55.3.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kim R., Nakano K., Jayaraman A., Carpenter M. B. Projections of the globus pallidus and adjacent structures: an autoradiographic study in the monkey. J Comp Neurol. 1976 Oct 1;169(3):263–290. doi: 10.1002/cne.901690302. [DOI] [PubMed] [Google Scholar]
  17. Künzle H. Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res. 1975 May 2;88(2):195–209. doi: 10.1016/0006-8993(75)90384-4. [DOI] [PubMed] [Google Scholar]
  18. Laitinen L. V. Brain targets in surgery for Parkinson's disease. Results of a survey of neurosurgeons. J Neurosurg. 1985 Mar;62(3):349–351. doi: 10.3171/jns.1985.62.3.0349. [DOI] [PubMed] [Google Scholar]
  19. Lamarre Y., Filion M., Cordeau J. P. Neuronal discharges of the ventrolateral nucleus of the thalamus during sleep and wakefulness in the cat. I. Spontaneous activity. Exp Brain Res. 1971 Jun 29;12(5):480–498. doi: 10.1007/BF00234244. [DOI] [PubMed] [Google Scholar]
  20. Lenz F. A., Normand S. L., Kwan H. C., Andrews D., Rowland L. H., Jones M. W., Seike M., Lin Y. C., Tasker R. R., Dostrovsky J. O. Statistical prediction of the optimal site for thalamotomy in parkinsonian tremor. Mov Disord. 1995 May;10(3):318–328. doi: 10.1002/mds.870100315. [DOI] [PubMed] [Google Scholar]
  21. Limousin P., Pollak P., Benazzouz A., Hoffmann D., Le Bas J. F., Broussolle E., Perret J. E., Benabid A. L. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet. 1995 Jan 14;345(8942):91–95. doi: 10.1016/s0140-6736(95)90062-4. [DOI] [PubMed] [Google Scholar]
  22. Marconi R., Lefebvre-Caparros D., Bonnet A. M., Vidailhet M., Dubois B., Agid Y. Levodopa-induced dyskinesias in Parkinson's disease phenomenology and pathophysiology. Mov Disord. 1994 Jan;9(1):2–12. doi: 10.1002/mds.870090103. [DOI] [PubMed] [Google Scholar]
  23. Mouroux M., Hassani O. K., Féger J. Electrophysiological study of the excitatory parafascicular projection to the subthalamic nucleus and evidence for ipsi- and contralateral controls. Neuroscience. 1995 Jul;67(2):399–407. doi: 10.1016/0306-4522(95)00032-e. [DOI] [PubMed] [Google Scholar]
  24. Narabayashi H., Yokochi F., Nakajima Y. Levodopa-induced dyskinesia and thalamotomy. J Neurol Neurosurg Psychiatry. 1984 Aug;47(8):831–839. doi: 10.1136/jnnp.47.8.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nauta W. J., Mehler W. R. Projections of the lentiform nucleus in the monkey. Brain Res. 1966 Jan;1(1):3–42. doi: 10.1016/0006-8993(66)90103-x. [DOI] [PubMed] [Google Scholar]
  26. Ohye C., Maeda T., Narabayashi H. Physiologically defined VIM nucleus. Its special reference to control of tremor. Appl Neurophysiol. 1976;39(3-4):285–295. [PubMed] [Google Scholar]
  27. Ohye C., Narabayashi H. Physiological study of presumed ventralis intermedius neurons in the human thalamus. J Neurosurg. 1979 Mar;50(3):290–297. doi: 10.3171/jns.1979.50.3.0290. [DOI] [PubMed] [Google Scholar]
  28. Ohye C., Shibazaki T., Hirai T., Wada H., Hirato M., Kawashima Y. Further physiological observations on the ventralis intermedius neurons in the human thalamus. J Neurophysiol. 1989 Mar;61(3):488–500. doi: 10.1152/jn.1989.61.3.488. [DOI] [PubMed] [Google Scholar]
  29. Parker F., Tzourio N., Blond S., Petit H., Mazoyer B. Evidence for a common network of brain structures involved in parkinsonian tremor and voluntary repetitive movement. Brain Res. 1992 Jul 3;584(1-2):11–17. doi: 10.1016/0006-8993(92)90872-7. [DOI] [PubMed] [Google Scholar]
  30. Percheron G., François C., Talbi B., Yelnik J., Fénelon G. The primate motor thalamus. Brain Res Brain Res Rev. 1996 Aug;22(2):93–181. [PubMed] [Google Scholar]
  31. Percheron G., Yelnik J., François C., Fénelon G., Talbi B. Analyse informationnelle du système lié aux ganglions de la base. Rev Neurol (Paris) 1994 Aug-Sep;150(8-9):614–626. [PubMed] [Google Scholar]
  32. Ranck J. B., Jr Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 1975 Nov 21;98(3):417–440. doi: 10.1016/0006-8993(75)90364-9. [DOI] [PubMed] [Google Scholar]
  33. Siegfried J. Therapeutic stereotactic procedures on the thalamus for motor movement disorders. Acta Neurochir (Wien) 1993;124(1):14–18. doi: 10.1007/BF01400708. [DOI] [PubMed] [Google Scholar]
  34. Sugimoto T., Hattori T. Organization and efferent projections of nucleus tegmenti pedunculopontinus pars compacta with special reference to its cholinergic aspects. Neuroscience. 1984 Apr;11(4):931–946. doi: 10.1016/0306-4522(84)90204-5. [DOI] [PubMed] [Google Scholar]
  35. Tasker R. R., Organ L. W., Hawrylyshyn P. Investigation of the surgical target for alleviation of involuntary movement disorders. Appl Neurophysiol. 1982;45(3):261–274. doi: 10.1159/000101610. [DOI] [PubMed] [Google Scholar]
  36. Woolf N. J. Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol. 1991;37(6):475–524. doi: 10.1016/0301-0082(91)90006-m. [DOI] [PubMed] [Google Scholar]
  37. Yelnik J., Percheron G., François C., Garnier A. Cholinergic neurons of the rat and primate striatum are morphologically different. Prog Brain Res. 1993;99:25–34. doi: 10.1016/s0079-6123(08)61336-9. [DOI] [PubMed] [Google Scholar]

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