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Review

Subthalamic nucleus deep brain stimulation for Parkinson’s disease: current trends and future directions

, , , &
Pages 1063-1074 | Received 19 Nov 2019, Accepted 23 Mar 2020, Published online: 06 Apr 2020

References

  • Mahlknecht P, Limousin P, Foltynie T. Deep brain stimulation for movement disorders: update on recent discoveries and outlook on future developments. J Neurol. 2015;262(11):2583–2595.
  • Foerster O. Zur Analyse und Pathophysiologie der striären Bewegungsstörungen. Z Ges Neurol Psychiatry. 1921;73(1):1–169.
  • Meyers R. Surgical experiments in the therapy of certain ‘extrapyramidal’ diseases: a current evaluation. Acta Psychiatr Neurol Suppl. 1951;67:1–42.
  • Cooper IS. Ligation of the anterior choroidal artery for involuntary movements; parkinsonism. Psychiatr Q. 1953;27(2):317–319.
  • Hanieh A, Maloney AF. Localization of stereotaxic lesions in the treatment of Parkinsonism: a clinico-pathological comparison. J Neurosurg. 1969;31(4):393–399.
  • Cooper IS. Clinical results and follow-up studies in a personal series of 300 operations for parkinsonism. J Am Geriatr Soc. 1956;4(12):1171–1181.
  • Wycis HT, Spiegel EA. Parkinsonism with oculogyric crises; stimulation and partial elimination of periaqueductal grey and mesencephalic tegmentum (tegmentotomy). Confin Neurol. 1958;18(6):385–393.
  • Blomstedt P, Hariz MI. Deep brain stimulation for movement disorders before DBS for movement disorders. Parkinsonism Relat Disord. 2010;16(7):429–433.
  • Bechtereva NP, Hughes HK. Implanted electrodes: experimentation on humans? Am J Psychiatry. 1971;127(10):1422–1423.
  • Bechtereva NP, Bondartchuk AN, Smirnov VM, et al. Method of electrostimulation of the deep brain structures in treatment of some chronic diseases. Confin Neurol. 1975;37(1–3):136–140. .
  • Benabid AL, Pollak P, Louveau A, et al. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol. 1987;50(1–6):344–346.
  • Benabid AL, Pollak P, Seigneuret E, et al. Chronic VIM thalamic stimulation in Parkinson’s disease, essential tremor and extra-pyramidal dyskinesias. Acta Neurochir Suppl (Wien). 1993;58:39–44.
  • Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989;12(10):366–375.
  • Simonyan K. Recent advances in understanding the role of the basal ganglia. F1000Res. 2019;8:122.
  • Aquino CC, Fox SH. Clinical spectrum of levodopa-induced complications. Mov Disord. 2015;30(1):80–89.
  • Laitinen LV, Bergenheim AT, Hariz MI. Leksell’s posteroventral pallidotomy in the treatment of Parkinson’s disease. J Neurosurg. 1992;76(1):53–61.
  • Bergman H, Wichmann T, DeLong MR. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science. 1990;249(4975):1436–1438.
  • Aziz TZ, Peggs D, Agarwal E, et al. Subthalamic nucleotomy alleviates parkinsonism in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-exposed primate. Br J Neurosurg. 1992;6(6):575–582. .
  • Benazzouz A, Gross C, Féger J, et al. Reversal of rigidity and improvement in motor performance by subthalamic high-frequency stimulation in MPTP-treated monkeys. Eur J Neurosci. 1993;5(4):382–389. .
  • Parent A, Hazrati LN. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev. 1995;20(1):128–154.
  • Pollak P, Benabid AL, Limousin P, et al. Subthalamic nucleus stimulation alleviates akinesia and rigidity in parkinsonian patients. Adv Neurol. 1996;69:591–594.
  • Benabid AL, Pollak P, Gross C, et al. Acute and long-term effects of subthalamic nucleus stimulation in Parkinson’s disease. Stereotact Funct Neurosurg. 1994;62(1–4):76–84. .
  • Limousin P, Pollak P, Benazzouz A, et al. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet. 1995;345(8942):91–95.
  • Limousin P, Krack P, Pollak P, et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 1998;339(16):1105–1111.
  • Fraix V, Pollak P, Van Blercom N, et al. Effect of subthalamic nucleus stimulation on levodopa-induced dyskinesia in Parkinson’s disease. Neurology. 2000;55(12):1921–1923. .
  • Krack P, Batir A, Van Blercom N, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 2003;349(20):1925–1934. .
  • Funkiewiez A, Ardouin C, Caputo E, et al. Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2004;75(6):834–839. .
  • Hamani C, Richter E, Schwalb JM, et al. Bilateral subthalamic nucleus stimulation for Parkinson’s disease: a systematic review of the clinical literature. Neurosurgery. 2005;56(6):1313–1321. discussion 1321-4. .
  • Deuschl G, Schade-Brittinger C, Krack P, et al. A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med. 2006;355(9):896–908.
  • Kleiner-Fisman G, Herzog J, Fisman DN, et al. Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord. 2006;21(Suppl 14):S290–S304. .
  • Benabid AL, Chabardes S, Mitrofanis J, et al. Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson’s disease. Lancet Neurol. 2009;8(1):67–81. .
  • Thevathasan W, Debu B, Aziz T, et al. Pedunculopontine nucleus deep brain stimulation in Parkinson’s disease: a clinical review. Mov Disord. 2018;33(1):10–20. .
  • Gratwicke J, Zrinzo L, Kahan J, et al. Bilateral deep brain stimulation of the nucleus basalis of meynert for parkinson disease dementia: a randomized clinical trial. JAMA Neurol. 2018;75(2):169–178. .
  • Weiss D, Milosevic L, Gharabaghi A. Deep brain stimulation of the substantia nigra for freezing of gait in Parkinson’s disease: is it about stimulation frequency? Parkinsonism Relat Disord.
  • Chastan N, Westby GWM, Yelnik J, et al. Effects of nigral stimulation on locomotion and postural stability in patients with Parkinson’s disease. Brain. 2009;132(Pt 1):172–184. .
  • Williams A, Gill S, Varma T, et al. Deep brain stimulation plus best medical therapy versus best medical therapy alone for advanced Parkinson’s disease (PD SURG trial): a randomised, open-label trial. Lancet Neurol. 2010;9(6):581–591. .
  • Schupbach WM, Maltete D, Houeto JL, et al. Neurosurgery at an earlier stage of Parkinson disease: a randomized, controlled trial. Neurology. 2007;68(4):267–271.
  • Schuepbach WM, Rau J, Knudsen K, et al. Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med. 2013;368(7):610–622. .
  • Deuschl G, Schüpbach M, Knudsen K, et al. Stimulation of the subthalamic nucleus at an earlier disease stage of Parkinson’s disease: concept and standards of the EARLYSTIM-study. Parkinsonism Relat Disord. 2013;19(1):56–61.
  • Schuepbach WMM, Tonder L, Schnitzler A, et al. Quality of life predicts outcome of deep brain stimulation in early Parkinson disease. Neurology. 2019;92(10):e1109–e1120. .
  • Dulski J, Schinwelski M, Konkel A, et al. The impact of subthalamic deep brain stimulation on sleep and other non-motor symptoms in Parkinson’s disease. Parkinsonism Relat Disord. 2019;64:138–144.
  • Liu FT, Lang L-Q, Yang Y-J, et al. Predictors to quality of life improvements after subthalamic stimulation in Parkinson’s disease. Acta Neurol Scand. 2019;139(4):346–352. .
  • Lau B, Meier N, Serra G, et al. Axial symptoms predict mortality in patients with Parkinson disease and subthalamic stimulation. Neurology. 2019;92(22):e2559–e2570. .
  • Defer GL, Widner H, Marié R.M, et al. Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Mov Disord. 1999;14(4):572–584. .
  • Mestre TA, Espay AJ, Marras C, et al. Subthalamic nucleus-deep brain stimulation for early motor complications in Parkinson’s disease-the EARLYSTIM trial: early is not always better. Mov Disord. 2014;29(14):1751–1756. .
  • Spieles-Engemann AL, Steece-Collier K, Behbehani MM, et al. Subthalamic nucleus stimulation increases brain derived neurotrophic factor in the nigrostriatal system and primary motor cortex. J Parkinsons Dis. 2011;1(1):123–136. .
  • Fischer DL, Sortwell CE. BDNF provides many routes toward STN DBS-mediated disease modification. Mov Disord. 2019;34(1):22–34.
  • Rodriguez-Oroz MC, Zamarbide I, Guridi J, et al. Efficacy of deep brain stimulation of the subthalamic nucleus in Parkinson’s disease 4 years after surgery: double blind and open label evaluation. J Neurol Neurosurg Psychiatry. 2004;75(10):1382–1385. .
  • Rodriguez-Oroz MC, Obeso JA, Lang AE, et al. Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain. 2005;128(Pt 10):2240–2249. .
  • Tagliati M, Martin C, Alterman R. Lack of motor symptoms progression in Parkinson’s disease patients with long-term bilateral subthalamic deep brain stimulation. Int J Neurosci. 2010;120(11):717–723.
  • Hilker R, Portman A.T, Voges J, et al. Disease progression continues in patients with advanced Parkinson’s disease and effective subthalamic nucleus stimulation. J Neurol Neurosurg Psychiatry. 2005;76(9):1217–1221.
  • Musacchio T, Rebenstorff M, Fluri F, et al. Subthalamic nucleus deep brain stimulation is neuroprotective in the A53T alpha-synuclein Parkinson’s disease rat model. Ann Neurol. 2017;81(6):825–836. .
  • Volkmann J, Moro E, Pahwa R. Basic algorithms for the programming of deep brain stimulation in Parkinson’s disease. Mov Disord. 2006;21(Suppl 14):S284–S289.
  • Burchiel KJ, Anderson VC, Favre J, et al. Comparison of pallidal and subthalamic nucleus deep brain stimulation for advanced Parkinson’s disease: results of a randomized, blinded pilot study. Neurosurgery. 1999;45(6):1375–1382. discussion 1382-4.
  • McIntyre CC, Mori S, Sherman DL, et al. Electric field and stimulating influence generated by deep brain stimulation of the subthalamic nucleus. Clin Neurophysiol. 2004;115(3):589–595. .
  • Krack P, Fraix V, Mendes A, et al. Postoperative management of subthalamic nucleus stimulation for Parkinson’s disease. Mov Disord. 2002;17(Suppl 3):S188–97. .
  • Miocinovic S, Khemani P, Whiddon R, et al. Outcomes, management, and potential mechanisms of interleaving deep brain stimulation settings. Parkinsonism Relat Disord. 2014;20(12):1434–1437. .
  • Wodarg F, Herzog J, Reese R, et al. Stimulation site within the MRI-defined STN predicts postoperative motor outcome. Mov Disord. 2012;27(7):874–879. .
  • Akram H, Sotiropoulos SN, Jbabdi S, et al. Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease. Neuroimage. 2017;158:332–345.
  • Timmermann L, Jain R, Chen L, et al. Multiple-source current steering in subthalamic nucleus deep brain stimulation for Parkinson’s disease (the VANTAGE study): a non-randomised, prospective, multicentre, open-label study. Lancet Neurol. 2015;14(7):693–701. .
  • van Dijk KJ, Verhagen R, Bour LJ, et al. Avoiding internal capsule stimulation with a new eight-channel steering deep brain stimulation lead. Neuromodulation. 2018;21(6):553–561. .
  • Moreau C, Pennel‐Ployart O, Pinto S, et al. Modulation of dysarthropneumophonia by low-frequency STN DBS in advanced Parkinson’s disease. Mov Disord. 2011;26(4):659–663. .
  • Knowles T, Adams S, Abeyesekera A, et al. Deep brain stimulation of the subthalamic nucleus parameter optimization for vowel acoustics and speech intelligibility in parkinson’s disease. J Speech Lang Hear Res. 2018;61(3):510–524. .
  • Morello A, Beber BC, Fagundes VC, et al. Dysphonia and dysarthria in people with parkinson’s disease after subthalamic nucleus deep brain stimulation: effect of frequency modulation. J Voice. 2018.
  • Tripoliti E, Zrinzo L, Martinez-Torres I, et al. Effects of subthalamic stimulation on speech of consecutive patients with Parkinson disease. Neurology. 2011;76(1):80–86. .
  • Fabbri M, Zibetti M, Ferrero G, et al. Is lowering stimulation frequency a feasible option for subthalamic deep brain stimulation in Parkinson’s disease patients with dysarthria? Parkinsonism Relat Disord. 2019;64:242–248.
  • Grover T, Georgiev D, Kalliola R, et al. Effect of low versus high frequency subthalamic deep brain stimulation on speech intelligibility and verbal fluency in parkinson’s disease: a double-blind study. J Parkinsons Dis. 2019;9(1):141–151. .
  • Fasano A, Aquino CC, Krauss JK, et al. Axial disability and deep brain stimulation in patients with Parkinson disease. Nat Rev Neurol. 2015;11(2):98–110.
  • Eusebio A, Chen CC, Lu CS, et al. Effects of low-frequency stimulation of the subthalamic nucleus on movement in Parkinson’s disease. Exp Neurol. 2008;209(1):125–130. .
  • Sidiropoulos C, Walsh R, Meaney C, et al. Low-frequency subthalamic nucleus deep brain stimulation for axial symptoms in advanced Parkinson’s disease. J Neurol. 2013;260(9):2306–2311. .
  • Moreau C, Defebvre L, Destee A, et al. STN-DBS frequency effects on freezing of gait in advanced Parkinson disease. Neurology. 2008;71(2):80–84. .
  • Xie T, Vigil J, MacCracken E, et al. Low-frequency stimulation of STN-DBS reduces aspiration and freezing of gait in patients with PD. Neurology. 2015;84(4):415–420. .
  • Reich MM, Steigerwald F, Sawalhe A.D, et al. Short pulse width widens the therapeutic window of subthalamic neurostimulation. Ann Clin Transl Neurol. 2015;2(4):427–432. .
  • Bouthour W, Wegrzyk J, Momjian S, et al. Short pulse width in subthalamic stimulation in Parkinson’s disease: a randomized, double-blind study. Mov Disord. 2018;33(1):169–173. .
  • Dayal V, Grover T, Limousin P, et al. The effect of short pulse width settings on the therapeutic window in subthalamic nucleus deep brain stimulation for parkinson’s disease. J Parkinsons Dis. 2018;8(2):273–279. .
  • Moro E, Poon Y-YW, Lozano AM, et al. Subthalamic nucleus stimulation: improvements in outcome with reprogramming. Arch Neurol. 2006;63(9):1266–1272. .
  • Dembek TA, Reker P, Visser-Vandewalle V, et al. Directional DBS increases side-effect thresholds-A prospective, double-blind trial. Mov Disord. 2017;32(10):1380–1388. .
  • Steigerwald F, Matthies C, Volkmann J. Directional deep brain stimulation. Neurotherapeutics. 2019;16(1):100–104.
  • Pollo C, Kaelin-Lang A, Oertel MF, et al. Directional deep brain stimulation: an intraoperative double-blind pilot study. Brain. 2014;137(Pt 7):2015–2026. .
  • Contarino MF, Bour LJ, Verhagen R, et al. Directional steering: a novel approach to deep brain stimulation. Neurology. 2014;83(13):1163–1169. .
  • Sheshadri V, Rowland NC, Mehta J, et al. Comparison of general and local anesthesia for deep brain stimulator insertion: a systematic review. Can J Neurol Sci. 2017;44(6):697–704.
  • Chen T, Mirzadeh Z, Chapple KM, et al. Clinical outcomes following awake and asleep deep brain stimulation for Parkinson disease. J Neurosurg. 2018;130(1):109–120. .
  • Brodsky MA, Anderson S, Murchison C, et al. Clinical outcomes of asleep vs awake deep brain stimulation for Parkinson disease. Neurology. 2017;89(19):1944–1950. .
  • Ho AL, Ali R, Connolly ID, et al. Awake versus asleep deep brain stimulation for Parkinson’s disease: a critical comparison and meta-analysis. J Neurol Neurosurg Psychiatry. 2018;89(7):687–691. .
  • Kochanski RB, Sani S. Awake versus asleep deep brain stimulation surgery: technical considerations and critical review of the literature. Brain Sci. 2018;8(1):17.
  • Halim A, Baumgartner L, Binder DK. Effect of deep brain stimulation on autonomic dysfunction in patients with Parkinson’s disease. J Clin Neurosci. 2011;18(6):804–806.
  • Finazzi-Agro E, PEPPE A, D’AMICO A, et al. Effects of subthalamic nucleus stimulation on urodynamic findings in patients with Parkinson’s disease. J Urol. 2003;169(4):1388–1391. .
  • Herzog J, Weiss PH, Assmus A, et al. Subthalamic stimulation modulates cortical control of urinary bladder in Parkinson’s disease. Brain. 2006;129(Pt 12):3366–3375. .
  • Arnulf I, Bejjani BP, Garma L, et al. Improvement of sleep architecture in PD with subthalamic nucleus stimulation. Neurology. 2000;55(11):1732–1734. .
  • Kim HJ, Paek SH, Kim J-Y, et al. Chronic subthalamic deep brain stimulation improves pain in Parkinson disease. J Neurol. 2008;255(12):1889–1894. .
  • Witjas T, Kaphan E, Régis J, et al. Effects of chronic subthalamic stimulation on nonmotor fluctuations in Parkinson’s disease. Mov Disord. 2007;22(12):1729–1734. .
  • Trachani E, Constantoyannis C, Sirrou V, et al. Effects of subthalamic nucleus deep brain stimulation on sweating function in Parkinson’s disease. Clin Neurol Neurosurg. 2010;112(3):213–217. .
  • Zrinzo L, Foltynie T, Limousin P, et al. Reducing hemorrhagic complications in functional neurosurgery: a large case series and systematic literature review. J Neurosurg. 2012;116(1):84–94. .
  • Bjerknes S, Skogseid IM, Sæhle T, et al. Surgical site infections after deep brain stimulation surgery: frequency, characteristics and management in a 10-year period. PLoS One. 2014;9(8):e105288. .
  • Pepper J, Zrinzo L, Mirza B, et al. The risk of hardware infection in deep brain stimulation surgery is greater at impulse generator replacement than at the primary procedure. Stereotact Funct Neurosurg. 2013;91(1):56–65. .
  • Pepper J, Meliak L, Akram H, et al. Changing of the guard: reducing infection when replacing neural pacemakers. J Neurosurg. 2017;126(4):1165–1172. .
  • Morishita T, Hilliard JD, Okun MS, et al. Postoperative lead migration in deep brain stimulation surgery: incidence, risk factors, and clinical impact. PLoS One. 2017;12(9):e0183711. .
  • Bronstein JM, Tagliati M, Alterman RL, et al. Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch Neurol. 2011;68(2):165. .
  • Piboolnurak P, Lang AE, Lozano AM, et al. Levodopa response in long-term bilateral subthalamic stimulation for Parkinson’s disease. Mov Disord. 2007;22(7):990–997. .
  • Wertheimer J, Gottuso AY, Nuno M, et al. The impact of STN deep brain stimulation on speech in individuals with Parkinson’s disease: the patient’s perspective. Parkinsonism Relat Disord. 2014;20(10):1065–1070. .
  • Moro E. Let’s listen to patients with PD after deep brain stimulation. Nat Rev Neurol. 2014;10(10):550–552.
  • Schupbach M, Gargiulo M, Welter ML, et al. Neurosurgery in Parkinson disease: a distressed mind in a repaired body? Neurology. 2006;66(12):1811–1816. .
  • Houeto JL, Mesnage V, Mallet L, et al. Behavioural disorders, Parkinson’s disease and subthalamic stimulation. J Neurol Neurosurg Psychiatry. 2002;72(6):701–707. .
  • Kulisevsky J, Berthier ML, Gironell A, et al. Mania following deep brain stimulation for Parkinson’s disease. Neurology. 2002;59(9):1421–1424. .
  • Voon V, Krack P, Lang AE, et al. A multicentre study on suicide outcomes following subthalamic stimulation for Parkinson’s disease. Brain. 2008;131(Pt 10):2720–2728. .
  • Cyron D. Mental side effects of deep brain stimulation (DBS) for movement disorders: the futility of denial. Front Integr Neurosci. 2016;10:17.
  • Gee L, Smith H, De La Cruz P, et al. The influence of bilateral subthalamic nucleus deep brain stimulation on impulsivity and prepulse inhibition in parkinson’s disease patients. Stereotact Funct Neurosurg. 2015;93(4):265–270. .
  • Kim YE, Kim HJ, Kim H-J, et al. Impulse control and related behaviors after bilateral subthalamic stimulation in patients with Parkinson’s disease. J Clin Neurosci. 2013;20(7):964–969. .
  • Lim SY, O’Sullivan SS, Kotschet K, et al. Dopamine dysregulation syndrome, impulse control disorders and punding after deep brain stimulation surgery for Parkinson’s disease. J Clin Neurosci. 2009;16(9):1148–1152. .
  • Moum SJ, Price CC, Limotai N, et al. Effects of STN and GPi deep brain stimulation on impulse control disorders and dopamine dysregulation syndrome. PLoS One. 2012;7(1):e29768. .
  • Amami P, Dekker I, Piacentini S, et al. Impulse control behaviours in patients with Parkinson’s disease after subthalamic deep brain stimulation: de novo cases and 3-year follow-up. J Neurol Neurosurg Psychiatry. 2015;86(5):562–564. .
  • Merola A, Romagnolo A, Rizzi L, et al. Impulse control behaviors and subthalamic deep brain stimulation in Parkinson disease. J Neurol. 2017;264(1):40–48. .
  • Mosley PE, Marsh R. The psychiatric and neuropsychiatric symptoms after subthalamic stimulation for Parkinson’s disease. J Neuropsychiatry Clin Neurosci. 2015;27(1):19–26.
  • Seppi K, Weintraub D, Coelho M, et al. The movement disorder society evidence-based medicine review update: treatments for the non-motor symptoms of Parkinson’s disease. Mov Disord. 2011;26(Suppl 3):S42–80. .
  • Bannier S, Montaurier C, Derost PP, et al. Overweight after deep brain stimulation of the subthalamic nucleus in Parkinson disease: long term follow-up. J Neurol Neurosurg Psychiatry. 2009;80(5):484–488. .
  • Limousin P, Foltynie T. Long-term outcomes of deep brain stimulation in Parkinson disease. Nat Rev Neurol. 2019;15(4):234–242.
  • Zibetti M, Merola A, Rizzi L, et al. Beyond nine years of continuous subthalamic nucleus deep brain stimulation in Parkinson’s disease. Mov Disord. 2011;26(13):2327–2334. .
  • Obeso JA, Olanow W. Deep brain stimulation for Parkinson’s disease: thinking about the long-term in the short-term. Mov Disord. 2011;26(13):2303–2304.
  • Di Giulio I, Kalliolia E, Georgiev D, et al. Chronic subthalamic nucleus stimulation in parkinson’s disease: optimal frequency for gait depends on stimulation site and axial symptoms. Front Neurol. 2019;10:29.
  • Karachi C, Cormier-Dequaire F, Grabli D, et al. Clinical and anatomical predictors for freezing of gait and falls after subthalamic deep brain stimulation in Parkinson’s disease patients. Parkinsonism Relat Disord. 2019;62:91–97.
  • Beudel M, Brown P. Adaptive deep brain stimulation in Parkinson’s disease. Parkinsonism Relat Disord. 2016;22(Suppl 1):S123–6.
  • Hammond C, Bergman H, Brown P. Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci. 2007;30(7):357–364.
  • Azodi-Avval R, Gharabaghi A. Phase-dependent modulation as a novel approach for therapeutic brain stimulation. Front Comput Neurosci. 2015;9:26.
  • Swann NC, de Hemptinne C, Thompson MC, et al. Adaptive deep brain stimulation for Parkinson’s disease using motor cortex sensing. J Neural Eng. 2018;15(4):046006. .
  • Swann NC, de Hemptinne C, Miocinovic S, et al. Chronic multisite brain recordings from a totally implantable bidirectional neural interface: experience in 5 patients with Parkinson’s disease. J Neurosurg. 2018;128(2):605–616. .
  • Hamani C, Florence G, Heinsen H, et al. Subthalamic nucleus deep brain stimulation: basic concepts and novel perspectives. eNeuro. 2017;4(5):ENEURO.0140–17.2017.
  • Brown P, Oliviero A, Mazzone P, et al. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J Neurosci. 2001;21(3):1033–1038. .
  • Williams D, Tijssen M, Vanv Get al. Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain. 2002;125(Pt 7):1558–1569. .
  • Mahlknecht P, Akram H, Georgiev D, et al. Pyramidal tract activation due to subthalamic deep brain stimulation in Parkinson’s disease. Mov Disord. 2017;32(8):1174–1182. .

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