Advertisement

Parkinson’s Disease: Deep Brain Stimulation

  • Donald J. Crammond
  • R. Mark RichardsonEmail author
Chapter
  • 98 Downloads

Abstract

Deep brain stimulation (DBS) is the gold standard therapy for Parkinson’s disease when medications no longer provide adequate and consistent benefit with respect to motor symptoms. In conjunction with ever-accumulating evidence for the safety, clinical effectiveness, and cost-effectiveness of DBS, our understanding of the neurophysiology of surgical targets has evolved substantially over the last two decades. This chapter focuses significant attention on these details, as they provide the foundation for understanding both how to target DBS leads in the absence of neurophysiological guidance and how the use of neurophysiological signals may evolve in the future, intraoperatively and in chronically implanted devices.

Keywords

Parkinson’s disease Deep brain stimulation Basal ganglia Subthalamic nucleus Globus pallidus Microelectrode recording Local field potentials Beta oscillations Gamma oscillations 

References

  1. 1.
    Benabid A, 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;50:344–6.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Limousin P, Pollak P, Benazzouz A, Hoffmann D, Bas LJ, Broussolle E, et al. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet (London, England). 1995;345:91–5.CrossRefGoogle Scholar
  3. 3.
    Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks WJ, et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA. 2009;301:63–73.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Jiang L-LL, Liu J-LL FX-LL, Xian W-BB GJ, Liu Y-MM, et al. Long-term efficacy of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a 5-year follow-up study in China. Chin Med J. 2015;128:2433–8.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Merola A, Romagnolo A, Bernardini A, Rizzi L, Artusi CA, Lanotte M, et al. Earlier versus later subthalamic deep brain stimulation in Parkinson’s disease. Parkinsonism Relat Disord. 2015;21:972–5.CrossRefGoogle Scholar
  6. 6.
    Follett KA, Weaver FM, Stern M, Hur K, Harris CL, Luo P, et al. Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease. N Engl J Med. 2010;362:2077–91.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Rodriguez-Oroz M, Obeso J, Lang A, Houeto J-LL, Pollak P, Rehncrona S, et al. Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain J Neurol. 2005;128:2240–9.CrossRefGoogle Scholar
  8. 8.
    Lilleeng B, Gjerstad M, Baardsen R, Dalen I, Larsen J. The long-term development of non-motor problems after STN-DBS. Acta Neurol Scand. 2015;132:251–8.CrossRefGoogle Scholar
  9. 9.
    Zibetti M, Merola A, Rizzi L, Ricchi V, Angrisano S, Azzaro C, et al. Beyond nine years of continuous subthalamic nucleus deep brain stimulation in Parkinson’s disease. Mov Disord. 2011;26:2327–34.CrossRefGoogle Scholar
  10. 10.
    Lin HY, Hasegawa H, Mundil N, Samuel M, Ashkan K. Patients’ expectations and satisfaction in subthalamic nucleus deep brain stimulation for Parkinson disease: 6-year follow-up. World Neurosurg. 2019;121:e654–60.CrossRefGoogle Scholar
  11. 11.
    Castrioto A, Lozano AM, Poon Y-YY, Lang AE, Fallis M, Moro E. Ten-year outcome of subthalamic stimulation in Parkinson disease: a blinded evaluation. Arch Neurol. 2011;68:1550–6.CrossRefGoogle Scholar
  12. 12.
    Henriksen BM, Johnsen E, Sunde N, Vase A, Gjelstrup M, Østergaard K. Surviving 10 years with deep brain stimulation for Parkinson’s disease – a follow-up of 79 patients. Eur J Neurol. 2016;23:53–61.CrossRefGoogle Scholar
  13. 13.
    Janssen ML, Duits AA, Turaihi AH, Ackermans L, Leentjens AF, Leentjes AF, et al. Subthalamic nucleus high-frequency stimulation for advanced Parkinson’s disease: motor and neuropsychological outcome after 10 years. Stereotact Funct Neurosurg. 2014;92:381–7.CrossRefGoogle Scholar
  14. 14.
    Limousin P, Foltynie T. Long-term outcomes of deep brain stimulation in Parkinson disease. Nat Rev Neurol. 2019;15:234–42.CrossRefGoogle Scholar
  15. 15.
    Volkmann J, Albanese A, Kulisevsky J, Tornqvist A-LL, Houeto J-LL, Pidoux B, et al. Long-term effects of pallidal or subthalamic deep brain stimulation on quality of life in Parkinson’s disease. Mov Disord. 2009;24:1154–61.CrossRefGoogle Scholar
  16. 16.
    Moro E, Lozano AM, Pollak P, Agid Y, Rehncrona S, Volkmann J, et al. Long-term results of a multicenter study on subthalamic and pallidal stimulation in Parkinson’s disease. Mov Disord. 2010;25:578–86.CrossRefGoogle Scholar
  17. 17.
    Defer G, Widner H, Marié R, Rémy P, Levivier M. Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Mov Disord. 1999;14:572–84.CrossRefGoogle Scholar
  18. 18.
    Kleiner-Fisman G, Herzog J, Fisman DN, Tamma F, Lyons KE, Pahwa R, et al. Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord. 2006;21(Suppl 14):S290–304.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Galati S, Stefani A. Deep brain stimulation of the subthalamic nucleus: all that glitters isn’t gold? Mov Disord. 2015;30:632–7.CrossRefGoogle Scholar
  20. 20.
    deSouza R, Akram H, Low H, Green A, Ashkan K, Schapira A. The timing of deep brain stimulation for Parkinson disease in the UK from 1997 to 2012. Eur J Neurol. 2015;22:1415–7.CrossRefGoogle Scholar
  21. 21.
    DeLong MR, Huang KT, Gallis J, Lokhnygina Y, Parente B, Hickey P, et al. Effect of advancing age on outcomes of deep brain stimulation for Parkinson disease. JAMA Neurol. 2014;71:1290–5.CrossRefGoogle Scholar
  22. 22.
    Shalash A, Alexoudi A, Knudsen K, Volkmann J, Mehdorn M, Deuschl G. The impact of age and disease duration on the long term outcome of neurostimulation of the subthalamic nucleus. Parkinsonism Relat Disord. 2014;20:47–52.CrossRefGoogle Scholar
  23. 23.
    Schuepbach WMM, Rau J, Knudsen K, Volkmann J, Krack P, Timmermann L, et al. Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med. 2013;368:610–22.CrossRefGoogle Scholar
  24. 24.
    Charles D, Konrad PE, Neimat JS, Molinari AL, Tramontana MG, Finder SG, et al. Subthalamic nucleus deep brain stimulation in early stage Parkinson’s disease. Parkinsonism Relat Disord. 2014;20:731–7.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Spieles-Engemann AL, Steece-Collier K, Behbehani MM, Collier TJ, Wohlgenant SL, Kemp CJ, et al. Subthalamic nucleus stimulation increases brain derived neurotrophic factor in the nigrostriatal system and primary motor cortex. J Park Dis. 2011;1:123–36.Google Scholar
  26. 26.
    Fischer D, Kemp CJ, Cole-Strauss A, Polinski NK, Paumier KL, Lipton JW, et al. Subthalamic nucleus deep brain stimulation employs trkB signaling for neuroprotection and functional restoration. J Neurosci Off J Soc Neurosci. 2017;37:6786–96.CrossRefGoogle Scholar
  27. 27.
    Kim SJ, Udupa K, Ni Z, Moro E, Gunraj C, Mazzella F, et al. Effects of subthalamic nucleus stimulation on motor cortex plasticity in Parkinson disease. Neurology. 2015;85:425–32.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    de Hemptinne C, Swann NC, Ostrem JL, Ryapolova-Webb ES, Luciano M, Galifianakis NB, et al. Therapeutic deep brain stimulation reduces cortical phase-amplitude coupling in Parkinson’s disease. Nat Neurosci. 2015;18:779–86.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Alhourani A, Well MM, Randazzo MJ, Wozny TA, Kondylis ED, Lipski WJ, et al. Network effects of deep brain stimulation. J Neurophysiol. 2015;114:2105–17.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Vasques X, Cif L, Hess O, Gavarini S, Mennessier G, Coubes P. Prognostic value of globus pallidus internus volume in primary dystonia treated by deep brain stimulation. J Neurosurg. 2009;110:220–8.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Ngoga D, Mitchell R, Kausar J, Hodson J, Harries A, Pall H. Deep brain stimulation improves survival in severe Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2014;85:17–22.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Eggington S, Brandt A, Rasmussen RE, Grifi M, Nyberg J. Cost-effectiveness of deep brain stimulation (Dbs) in the management of advanced Parkinson’s disease: a Swedish Payer Perspective. Value Health. 2015;18:A352.CrossRefGoogle Scholar
  33. 33.
    Eggington S, Valldeoriola F, Chaudhuri K, Ashkan K, Annoni E, Deuschl G. The cost-effectiveness of deep brain stimulation in combination with best medical therapy, versus best medical therapy alone, in advanced Parkinson’s disease. J Neurol. 2014;261:106–16.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Dams J, Balzer-Geldsetzer M, Siebert U, Deuschl G, Uepbach W, Krack P, et al. Cost-effectiveness of neurostimulation in Parkinson’s disease with early motor complications. Mov Disord. 2016;31:1183–91.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Liu Y, Li W, Tan C, Liu X, Wang X, Gui Y, et al. Meta-analysis comparing deep brain stimulation of the globus pallidus and subthalamic nucleus to treat advanced Parkinson disease. J Neurosurg. 2014;121:709–18.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Peng L, Fu J, Ming Y, Zeng S, He H, Chen L. The long-term efficacy of STN vs GPi deep brain stimulation for Parkinson disease: a meta-analysis. Medicine. 2018;97:e12153.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Mansouri A, Taslimi S, Badhiwala JH, Witiw CD, Nassiri F, Odekerken VJ, et al. Deep brain stimulation for Parkinson’s disease: meta-analysis of results of randomized trials at varying lengths of follow-up. J Neurosurg. 2018;128:1199–213.CrossRefGoogle Scholar
  38. 38.
    Rodriguez-Oroz MC, Moro E, Krack P. Long-term outcomes of surgical therapies for Parkinson’s disease. Mov Disord. 2012;27:1718–28.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Odekerken VJ, van Laar T, Staal MJ, Mosch A, Hoffmann CF, Nijssen PC, et al. Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson’s disease (NSTAPS study): a randomised controlled trial. Lancet Neurol. 2013;12:37–44.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Odekerken VJ, Boel JA, Schmand BA, de Haan RJ, Figee M, van den Munckhof P, et al. GPi vs STN deep brain stimulation for Parkinson disease: three-year follow-up. Neurology. 2016;86:755–61.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Okun MS, Fernandez HH, Wu SS, Kirsch-Darrow L, Bowers D, Bova F, et al. Cognition and mood in Parkinson’s disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: the COMPARE trial. Ann Neurol. 2009;65:586–95.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Voon V, Krack P, Lang AE, Lozano AM, Dujardin K, Schüpbach M, et al. A multicentre study on suicide outcomes following subthalamic stimulation for Parkinson’s disease. Brain J Neurol. 2008;131:2720–8.CrossRefGoogle Scholar
  43. 43.
    Weintraub D, Duda JE, Carlson K, Luo P, Sagher O, Stern M, et al. Suicide ideation and behaviours after STN and GPi DBS surgery for Parkinson’s disease: results from a randomised, controlled trial. J Neurol Neurosurg Psychiatry. 2013;84:1113–8.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Lhommée E, Klinger H, Thobois S, Schmitt E, Ardouin C, Bichon A, et al. Subthalamic stimulation in Parkinson’s disease: restoring the balance of motivated behaviours. Brain J Neurol. 2012;135:1463–77.CrossRefGoogle Scholar
  45. 45.
    Israel Z, Burchiel KJ. Microelectrode recording in movement disorders surgery. New York: Thieme; 2004.CrossRefGoogle Scholar
  46. 46.
    Brahimaj B, Kochanski RB, Sani S. Microelectrode accuracy in deep brain stimulation surgery. J Clin Neurosci. 2018;50:58–61.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Reck C, Maarouf M, Wojtecki L, Groiss SJ, Florin E, Sturm V, et al. Clinical outcome of subthalamic stimulation in Parkinson’s disease is improved by intraoperative multiple trajectories microelectrode recording. J Neurol Surg A Cent Eur Neurosurg. 2012;73:377–86.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Temel Y, Wilbrink P, Duits A, Boon P, Tromp S, Ackermans L, et al. Single electrode and multiple electrode guided electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. Neurosurgery. 2007;61:346–55; discussion 355–7.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Bjerknes S, Toft M, Konglund AE, Pham U, Waage TR, Pedersen L, et al. Multiple microelectrode recordings in STN-DBS surgery for Parkinson’s disease: a randomized study. Mov Disord Clin Pract. 2018;5:296–305.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Bour LJ, Contarino M, Foncke EM, de Bie RM, van den Munckhof P, Speelman JD, et al. Long-term experience with intraoperative microrecording during DBS neurosurgery in STN and GPi. Acta Neurochir. 2010;152:2069–77.CrossRefGoogle Scholar
  51. 51.
    Lozano CS, Ranjan M, Boutet A, Xu DS, Kucharczyk W, Fasano A, et al. Imaging alone versus microelectrode recording-guided targeting of the STN in patients with Parkinson’s disease. J Neurosurg. 2018:1–6.Google Scholar
  52. 52.
    Shenai MB, Patel DM, Romeo A, Whisenhunt J, Walker HC, Guthrie S, et al. The relationship of electrophysiologic subthalamic nucleus length as a predictor of outcomes in deep brain stimulation for Parkinson disease. Stereotact Funct Neurosurg. 2017;95:341–7.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Boëx C, Tyrand R, Horvath J, Fleury V, Sadri S, Corniola M, et al. What is the best electrophysiologic marker of the outcome of subthalamic nucleus stimulation in Parkinson disease? World Neurosurg. 2018;120:e1217–24.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Hamel W, Köppen JA, Alesch F, Antonini A, Barcia JA, Bergman H, et al. Targeting of the subthalamic nucleus for deep brain stimulation: a survey among Parkinson disease specialists. World Neurosurg. 2017;99:41–6.CrossRefGoogle Scholar
  55. 55.
    Garcia-Garcia D, Guridi J, Toledo JB, Alegre M, Obeso JA, Rodríguez-Oroz MC. Stimulation sites in the subthalamic nucleus and clinical improvement in Parkinson’s disease: a new approach for active contact localization. J Neurosurg. 2016;125:1068–79.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Bot M, Schuurman P, Odekerken VJ, Verhagen R, Contarino FM, Bie RM, et al. Deep brain stimulation for Parkinson’s disease: defining the optimal location within the subthalamic nucleus. J Neurol Neurosurg Psychiatry. 2018;89:493–8.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Hutchison W, Allan R, Opitz H, Levy R, Dostrovsky J, Lang A, et al. Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson’s disease. Ann Neurol. 1998;44:622–8.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Seifried C, Weise L, Hartmann R, Gasser T, Baudrexel S, Szelényi A, et al. Intraoperative microelectrode recording for the delineation of subthalamic nucleus topography in Parkinson’s disease. Brain Stimul. 2012;5:378–87.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Lourens M, Meijer H, Contarino M, van den Munckhof P, Schuurman P, van Gils S, et al. Functional neuronal activity and connectivity within the subthalamic nucleus in Parkinson’s disease. Clin Neurophysiol. 2013;124:967–81.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Steigerwald F, Pötter M, Herzog J, Pinsker M, Kopper F, Mehdorn H, et al. Neuronal activity of the human subthalamic nucleus in the parkinsonian and nonparkinsonian state. J Neurophysiol. 2008;100:2515–24.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Deffains M, Holland P, Moshel S, de Noriega F, Bergman H, Israel Z. Higher neuronal discharge rate in the motor area of the subthalamic nucleus of Parkinsonian patients. J Neurophysiol. 2014;112:1409–20.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Pozzi NG, Arnulfo G, Canessa A, Steigerwald F, Nickl R, Homola GA, et al. Distinctive neuronal firing patterns in subterritories of the subthalamic nucleus. Clin Neurophysiol. 2016;127:3387–93.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Guo S, Zhuang P, Zheng Z, Zhang Y, Li J, Li Y. Neuronal firing patterns in the subthalamic nucleus in patients with akinetic-rigid-type Parkinson’s disease. J Clin Neurosci. 2012;19:1404–7.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Guo S, Zhuang P, Hallett M, Zheng Z, Zhang Y, Li J, et al. Subthalamic deep brain stimulation for Parkinson’s disease: correlation between locations of oscillatory activity and optimal site of stimulation. Parkinsonism Relat Disord. 2013;19:109–14.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Lazzaro DV. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J Neurosci Off J Soc Neurosci. 2001;21:1033–8.CrossRefGoogle Scholar
  66. 66.
    Giannicola G, Marceglia S, Rossi L, Mrakic-Sposta S, Rampini P, Tamma F, et al. The effects of levodopa and ongoing deep brain stimulation on subthalamic beta oscillations in Parkinson’s disease. Exp Neurol. 2010;226:120–7.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Eusebio A, Thevathasan W, Gaynor DL, Pogosyan A, Bye E, Foltynie T, et al. Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. J Neurol Neurosurg Psychiatry. 2011;82:569.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO. Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson’s disease. Brain J Neurol. 2002;125:1196–209.CrossRefGoogle Scholar
  69. 69.
    Cassidy M, Mazzone P, Oliviero A, Insola A, Tonali P, Lazzaro V, et al. Movement-related changes in synchronization in the human basal ganglia. Brain J Neurol. 2002;125:1235–46.CrossRefGoogle Scholar
  70. 70.
    Tan H, Pogosyan A, Anzak A, Foltynie T, Limousin P, Zrinzo L, et al. Frequency specific activity in subthalamic nucleus correlates with hand bradykinesia in Parkinson’s disease. Exp Neurol. 2013;240:122–9.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Quinn EJ, Blumenfeld Z, Velisar A, Koop MM, Shreve LA, Trager MH, et al. Beta oscillations in freely moving Parkinson’s subjects are attenuated during deep brain stimulation. Mov Disord. 2015;30:1750–8.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Neumann W-JJ, Degen K, Schneider G-HH, Brücke C, Huebl J, Brown P, et al. Subthalamic synchronized oscillatory activity correlates with motor impairment in patients with Parkinson’s disease. Mov Disord. 2016;31:1748–51.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Neumann W-JJ, Kühn AA. Subthalamic beta power-Unified Parkinson’s disease rating scale III correlations require akinetic symptoms. Mov Disord. 2017;32:175–6.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Beudel M, Oswal A, Jha A, Foltynie T, Zrinzo L, Hariz M, et al. Oscillatory beta power correlates with akinesia-rigidity in the parkinsonian subthalamic nucleus. Mov Disord. 2017;32:174–5.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Geng X, Xu X, Horn A, Li N, Ling Z, Brown P, et al. Intra-operative characterisation of subthalamic oscillations in Parkinson’s disease. Clin Neurophysiol. 2018;129(5):1001–10.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Alegre M, López-Azcárate J, Alonso-Frech F, Rodríguez-Oroz MC, Valencia M, Guridi J, et al. Subthalamic activity during diphasic dyskinesias in Parkinson’s disease. Mov Disord. 2012;27:1178–81.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Hirschmann J, Butz M, Hartmann CJ, Hoogenboom N, Özkurt TE, Vesper J, et al. Parkinsonian rest tremor is associated with modulations of subthalamic high-frequency oscillations. Mov Disord. 2016;31:1551–9.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Lofredi R, Neumann W-JJ, Bock A, Horn A, Huebl J, Siegert S, et al. Dopamine-dependent scaling of subthalamic gamma bursts with movement velocity in patients with Parkinson’s disease. elife. 2018;7.Google Scholar
  79. 79.
    Kühn AA, Trottenberg T, Kivi A, Kupsch A, Schneider G-HH, Brown P. The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson’s disease. Exp Neurol. 2005;194:212–20.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Weinberger M, Mahant N, Hutchison WD, Lozano AM, Moro E, Hodaie M, et al. Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson’s disease. J Neurophysiol. 2006;96:3248–56.CrossRefGoogle Scholar
  81. 81.
    Moran A, Bergman H, Israel Z, Bar-Gad I. Subthalamic nucleus functional organization revealed by parkinsonian neuronal oscillations and synchrony. Brain. 2008;131:3395–409.CrossRefGoogle Scholar
  82. 82.
    Zaidel A, Spivak A, Grieb B, Bergman H, Israel Z. Subthalamic span of beta oscillations predicts deep brain stimulation efficacy for patients with Parkinson’s disease. Brain J Neurol. 2010;133:2007–21.CrossRefGoogle Scholar
  83. 83.
    Verhagen R, Zwartjes DG, Heida T, Wiegers EC, Contarino M, de Bie RM, et al. Advanced target identification in STN-DBS with beta power of combined local field potentials and spiking activity. J Neurosci Methods. 2015;253:116–25.CrossRefGoogle Scholar
  84. 84.
    Telkes I, Ince N, Onaran I, Abosch A. Spatio-spectral characterization of local field potentials in the subthalamic nucleus via multitrack microelectrode recordings. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Annual Conference. 2015;2015:5561–4.Google Scholar
  85. 85.
    Kostoglou K, Michmizos KP, Stathis P, Sakas D, Nikita KS, Mitsis GD. Classification and prediction of clinical improvement in deep brain stimulation from intraoperative microelectrode recordings. IEEE Trans Biomed Eng. 2017;64:1123–30.CrossRefGoogle Scholar
  86. 86.
    Wan KR, Maszczyk T, See AA, Dauwels J, King NK. A review on microelectrode recording selection of features for machine learning in deep brain stimulation surgery for Parkinson’s disease. Clin Neurophysiol. 2019;130:145–54.CrossRefGoogle Scholar
  87. 87.
    Nambu A, Takada M, Inase M, Tokuno H. Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area. J Neurosci Off J Soc Neurosci. 1996;16:2671–83.CrossRefGoogle Scholar
  88. 88.
    Miocinovic S, de Hemptinne C, Chen W, Isbaine F, Willie JT, Ostrem JL, et al. Cortical potentials evoked by subthalamic stimulation demonstrate a short latency hyperdirect pathway in humans. J Neurosci Off J Soc Neurosci. 2018;38:9129.CrossRefGoogle Scholar
  89. 89.
    Whitmer D, de Solages C, Hill B, Yu H, Henderson JM, Bronte-Stewart H. High frequency deep brain stimulation attenuates subthalamic and cortical rhythms in Parkinson’s disease. Front Hum Neurosci. 2012;6:155.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    McCairn KW, Turner RS. Deep brain stimulation of the globus pallidus internus in the parkinsonian primate: local entrainment and suppression of low-frequency oscillations. J Neurophysiol. 2009;101:1941–60.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Johnson LA, Xu W, Baker KB, Zhang J, Vitek JL. Modulation of motor cortex neuronal activity and motor behavior during subthalamic nucleus stimulation in the normal primate. J Neurophysiol. 2015;113:2549–54.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Yang AI, Vanegas N, Lungu C, Zaghloul KA. Beta-coupled high-frequency activity and beta-locked neuronal spiking in the subthalamic nucleus of Parkinson’s disease. J Neurosci Off J Soc Neurosci. 2014;34:12816–27.CrossRefGoogle Scholar
  93. 93.
    Wang DD, de Hemptinne C, Miocinovic S, Qasim SE, Miller AM, Ostrem JL, et al. Subthalamic local field potentials in Parkinson’s disease and isolated dystonia: an evaluation of potential biomarkers. Neurobiol Dis. 2016;89:213–22.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    de Hemptinne C, Ryapolova-Webb ES, Air EL, Garcia PA, Miller KJ, Ojemann JG, et al. Exaggerated phase-amplitude coupling in the primary motor cortex in Parkinson disease. Proc Natl Acad Sci U S A. 2013;110:4780–5.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Kondylis ED, Randazzo MJ, Alhourani A, Lipski WJ, Wozny TA, Pandya Y, et al. Movement-related dynamics of cortical oscillations in Parkinson’s disease and essential tremor. Brain J Neurol. 2016;139:2211–23.CrossRefGoogle Scholar
  96. 96.
    Lipski WJ, Wozny TA, Alhourani A, Kondylis ED, Turner RS, Crammond DJ, et al. Dynamics of human subthalamic neuron phase-locking to motor and sensory cortical oscillations during movement. J Neurophysiol. 2017;118:1472–87.CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Rafferty MR, Prodoehl J, Robichaud JA, David FJ, Poon C, Goelz LC, et al. Effects of 2 years of exercise on gait impairment in people with Parkinson disease: the PRET-PD randomized trial. J Neurol Phys Ther. 2017;41:21–30.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    DeLong M, Crutcher MD, Georgopoulos A. Primate globus pallidus and subthalamic nucleus: functional organization. J Neurophysiol. 1985;53:530–43.CrossRefGoogle Scholar
  99. 99.
    Bergman H, Wichmann T, Karmon B, MR DL. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol. 1994;72(2):507–20.CrossRefGoogle Scholar
  100. 100.
    Vitek J, Bakay R, Hashimoto T, Kaneoke Y, et al. Microelectrode-guided pallidotomy: technical approach and its application in medically intractable Parkinson’s disease. J Neurosurg. 1998;88(6):1027–43.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Vayssiere N, van der Gaag N, Cif L, Hemm S, et al. Deep brain stimulation for dystonia confirming a somatotopic organization in the globus pallidus internus. J Neurosurg. 2004;101(2):181–8.CrossRefGoogle Scholar
  102. 102.
    Chang EF, Turner RS, Ostrem JL, Davis VR, Starr PA. Neuronal responses to passive movement in the globus pallidus internus in primary dystonia. J Neurophysiol. 2007;98:3696–707.CrossRefGoogle Scholar
  103. 103.
    Baker KB, Lee JY, Mavinkurve G, Russo GS, Walter B, DeLong MR, et al. Somatotopic organization in the internal segment of the globus pallidus in Parkinson’s disease. Exp Neurol. 2010;222:219–25.CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Ostrem JL, Starr PA. Treatment of dystonia with deep brain stimulation. Neurotherapeutics. 2008;5:320–30.CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    McClelland V, Valentin A, Rey H, Lumsden D, Elze M, Selway R, et al. Differences in globus pallidus neuronal firing rates and patterns relate to different disease biology in children with dystonia. J Neurol Neurosurg Psychiatry. 2016;87:958–67.CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Harries AM, Kausar J, Roberts SA, Mocroft A, Hodson JA, Pall HS, et al. Deep brain stimulation of the subthalamic nucleus for advanced Parkinson disease using general anesthesia: long-term results. J Neurosurg. 2012;116:107–13.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Burchiel KJ, McCartney S, Lee A, Raslan AM. Accuracy of deep brain stimulation electrode placement using intraoperative computed tomography without microelectrode recording. J Neurosurg. 2013;119:301–6.CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Aviles-Olmos I, Kefalopoulou Z, Tripoliti E, Candelario J, Akram H, Martinez-Torres I, et al. Long-term outcome of subthalamic nucleus deep brain stimulation for Parkinson’s disease using an MRI-guided and MRI-verified approach. J Neurol Neurosurg Psychiatry. 2014;85:1419–25.CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Larson PS, Starr PA, Bates G, Tansey L, Richardson R, Martin AJ. An optimized system for interventional magnetic resonance imaging-guided stereotactic surgery: preliminary evaluation of targeting accuracy. Neurosurgery. 2012;70:95–103. discussion 103CrossRefGoogle Scholar
  110. 110.
    Larson PS, Starr PA, Martin AJ. Deep brain stimulation: interventional and intraoperative MRI approaches. Prog Neurol Surg. 2018;33:187–97.CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Lee PS, Richardson RM. Interventional MRI–guided deep brain stimulation lead implantation. Neurosurg Clin N Am [Internet]. 2017;28:535–44. Available from: http://www.sciencedirect.com/science/article/pii/S1042368017300657.CrossRefGoogle Scholar
  112. 112.
    Richardson RM, Golby AJ. Chapter 13: Functional neurosurgery: deep brain stimulation and gene therapy. In: Image guided neurosurgery [Internet]. Cambridge, Massachusetts, USA: Academic Press; 2015. p. 297–323. Available from: https://www.sciencedirect.com/science/article/pii/B9780128008706000133.
  113. 113.
    Lee PS, Weiner GM, Corson D, Kappel J, Chang Y-FF, Suski VR, et al. Outcomes of interventional-MRI versus microelectrode recording-guided subthalamic deep brain stimulation. Front Neurol. 2018;9:241.CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Ostrem JL, Ziman N, Galifianakis NB, Starr PA, Luciano MS, Katz M, et al. Clinical outcomes using ClearPoint interventional MRI for deep brain stimulation lead placement in Parkinson’s disease. J Neurosurg. 2016;124:908–16.CrossRefGoogle Scholar
  115. 115.
    Ostrem JL, Galifianakis NB, Markun LC, Grace JK, Martin AJ, Starr PA, et al. Clinical outcomes of PD patients having bilateral STN DBS using high-field interventional MR-imaging for lead placement. Clin Neurol Neurosurg. 2013;115:708–12.CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Sidiropoulos C, Rammo R, Merker B, Mahajan A, LeWitt P, Kaminski P, et al. Intraoperative MRI for deep brain stimulation lead placement in Parkinson’s disease: 1 year motor and neuropsychological outcomes. J Neurol. 2016;263:1226–31.CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Conway ZJ, Silburn PA, Thevathasan W, Maley KO, Naughton GA, Cole MH. Alternate subthalamic nucleus deep brain stimulation parameters to manage motor symptoms of Parkinson’s disease: systematic review and meta-analysis. Mov Disord Clin Pract. 2019;6:17–26.CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Brocker DT, Swan BD, Turner DA, Gross RE, Tatter SB, Koop MM, et al. Improved efficacy of temporally non-regular deep brain stimulation in Parkinson’s disease. Exp Neurol. 2013;239:60–7.CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Tass PA, Qin L, Hauptmann C, Dovero S, Bezard E, Boraud T, et al. Coordinated reset has sustained aftereffects in Parkinsonian monkeys. Ann Neurol. 2012;72:816–20.CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Adamchic I, Hauptmann C, Barnikol UB, Pawelczyk N, Popovych O, Barnikol TT, et al. Coordinated reset neuromodulation for Parkinson’s disease: proof-of-concept study. Mov Disord. 2014;29:1679–84.CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Dembek TA, Reker P, Visser-Vandewalle V, Wirths J, Treuer H, Klehr M, et al. Directional DBS increases side-effect thresholds-A prospective, double-blind trial. Mov Disord. 2017;32:1380–8.CrossRefGoogle Scholar
  122. 122.
    Tinkhauser G, Pogosyan A, Debove I, Nowacki A, Shah S, Seidel K, et al. Directional local field potentials: a tool to optimize deep brain stimulation. Mov Disord. 2018;33(1):159–64.CrossRefGoogle Scholar
  123. 123.
    Bour L, Lourens M, Verhagen R, de Bie R, van den Munckhof P, Schuurman P, et al. Directional recording of subthalamic spectral power densities in Parkinson’s disease and the effect of steering deep brain stimulation. Brain Stimul. 2015;8:730–41.CrossRefGoogle Scholar
  124. 124.
    Velisar A, Syrkin-Nikolau J, Blumenfeld Z, Trager MH, Afzal MF, Prabhakar V, et al. Dual threshold neural closed loop deep brain stimulation in Parkinson disease patients. Brain Stimul. 2019;12(4):868–76.CrossRefGoogle Scholar
  125. 125.
    Arlotti M, Marceglia S, Foffani G, Volkmann J, Lozano AM, Moro E, et al. Eight-hours adaptive deep brain stimulation in patients with Parkinson disease. Neurology. 2018;90:e971–6.CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Habets JG, Heijmans M, Kuijf ML, Janssen ML, Temel Y, Kubben PL. An update on adaptive deep brain stimulation in Parkinson’s disease. Mov Disord. 2018;33:1834–43.CrossRefPubMedPubMedCentralGoogle Scholar
  127. 127.
    Neumann W-JJ, Turner RS, Blankertz B, Mitchell T, Kühn AA, Richardson R. Toward electrophysiology-based intelligent adaptive deep brain stimulation for movement disorders. Neurotherapeutics. 2019;16:105–18.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Neurological SurgeryUniversity of Pittsburgh School of MedicinePittsburghUSA
  2. 2.Department of NeurosurgeryMassachusetts General Hospital, Harvard Medical SchoolBostonUSA

Personalised recommendations