OpenLB
Open Library of Bioscience
Advanced Search
Neurosurgical review
Aug, 2022;45 (4): 2593-2613.

Novel targets in deep brain stimulation for movement disorders.

Alexander J Baumgartner, John A Thompson, Drew S Kern, Steven G Ojemann
Author Information
  1. Alexander J Baumgartner: Department of Neurology, University of Colorado School of Medicine, Aurora, CO, USA. ORCID
  2. John A Thompson: Department of Neurology, University of Colorado School of Medicine, Aurora, CO, USA. ORCID
  3. Drew S Kern: Department of Neurology, University of Colorado School of Medicine, Aurora, CO, USA.
  4. Steven G Ojemann: Department of Neurology, University of Colorado School of Medicine, Aurora, CO, USA. steven.ojemann@cuanschutz.edu. ORCID
PMID: 35511309 DOI: 10.1007/s10143-022-01770-y

Abstract

The neurosurgical treatment of movement disorders, primarily via deep brain stimulation (DBS), is a rapidly expanding and evolving field. Although conventional targets including the subthalamic nucleus (STN) and internal segment of the globus pallidus (GPi) for Parkinson's disease and ventral intermediate nucleus of the thalams (VIM) for tremor provide substantial benefit in terms of both motor symptoms and quality of life, other targets for DBS have been explored in an effort to maximize clinical benefit and also avoid undesired adverse effects associated with stimulation. These novel targets primarily include the rostral zona incerta (rZI), caudal zona incerta (cZI)/posterior subthalamic area (PSA), prelemniscal radiation (Raprl), pedunculopontine nucleus (PPN), substantia nigra pars reticulata (SNr), centromedian/parafascicular (CM/PF) nucleus of the thalamus, nucleus basalis of Meynert (NBM), dentato-rubro-thalamic tract (DRTT), dentate nucleus of the cerebellum, external segment of the globus pallidus (GPe), and ventral oralis (VO) complex of the thalamus. However, reports of outcomes utilizing these targets are scattered and disparate. In order to provide a comprehensive resource for researchers and clinicians alike, we have summarized the existing literature surrounding these novel targets, including rationale for their use, neurosurgical techniques where relevant, outcomes and adverse effects of stimulation, and future directions for research.

Keywords

Ataxia Deep brain stimulation Dystonia Movement disorders Novel targets Parkinson’s disease Tremor

References

  1. Bronstein JM, Tagliati M, Alterman RL, Lozano AM, Volkmann J, Stefani A, Horak FB, Okun MS, Foote KD, Krack P, Pahwa R, Henderson JM, Hariz MI, Bakay RA, Rezai A, Marks WJ, Moro E, Vitek JL, Weaver FM, Gross RE, DeLong MR (2011) Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch Neurol 68. https://doi.org/10.1001/archneurol.2010.260
  2. Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks WJ, Rothlind J, Sagher O, Reda D, Moy CS, Pahwa R, Burchiel K, Hogarth P, Lai EC, Duda JE, Holloway K, Samii A, Horn S, Bronstein J, Stoner G, Heemskerk J, Huang GD, CSP 468 Study Group (2009) Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA 301(63):73. https://doi.org/10.1001/jama.2008.929 [DOI: 10.1001/jama.2008.929]
  3. Koller WC, Lyons KE, Wilkinson SB, Troster AI, Pahwa R (2001) Long-term safety and efficacy of unilateral deep brain stimulation of the thalamus in essential tremor. Mov Disord 16:464–468. https://doi.org/10.1002/mds.1089 [DOI: 10.1002/mds.1089]
  4. Sun B, Chen S, Zhan S, Le W, Krahl SE (2007) Subthalamic nucleus stimulation for primary dystonia and tardive dystonia. Acta Neurochir Suppl 97:207–214. https://doi.org/10.1007/978-3-211-33081-4_23 [DOI: 10.1007/978-3-211-33081-4_23]
  5. Vidailhet M, Vercueil L, Houeto J-L, Krystkowiak P, Benabid A-L, Cornu P, Lagrange C, Tézenas du Montcel S, Dormont D, Grand S, Blond S, Detante O, Pillon B, Ardouin C, Agid Y, Destée A, Pollak P, French Stimulation du Pallidum Interne dans la Dystonie (SPIDY) Study Group (2005) Bilateral deep-brain stimulation of the globus pallidus in primary generalized dystonia. N Engl J Med 352(459):467. https://doi.org/10.1056/NEJMoa042187 [DOI: 10.1056/NEJMoa042187]
  6. Cury RG, Fraix V, Castrioto A, Pérez Fernández MA, Krack P, Chabardes S, Seigneuret E, Alho EJL, Benabid A-L, Moro E (2017) Thalamic deep brain stimulation for tremor in Parkinson disease, essential tremor, and dystonia. Neurology 89:1416–1423. https://doi.org/10.1212/WNL.0000000000004295 [DOI: 10.1212/WNL.0000000000004295]
  7. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, Koudsie A, Limousin PD, Benazzouz A, LeBas JF, Benabid A-L, Pollak P (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934. https://doi.org/10.1056/NEJMoa035275 [DOI: 10.1056/NEJMoa035275]
  8. van Nuenen BFL, Esselink RAJ, Munneke M, Speelman JD, van Laar T, Bloem BR (2008) Postoperative gait deterioration after bilateral subthalamic nucleus stimulation in Parkinson’s disease. Mov Disord 23:2404–2406. https://doi.org/10.1002/mds.21986 [DOI: 10.1002/mds.21986]
  9. Picillo M, Fasano A (2016) Recent advances in essential tremor: surgical treatment. Parkinsonism Relat Disord 22(Suppl 1):S171-175. https://doi.org/10.1016/j.parkreldis.2015.09.012 [DOI: 10.1016/j.parkreldis.2015.09.012]
  10. Benabid AL, Pollak P, Gao D, Hoffmann D, Limousin P, Gay E, Payen I, Benazzouz A (1996) Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J Neurosurg 84:203–214. https://doi.org/10.3171/jns.1996.84.2.0203 [DOI: 10.3171/jns.1996.84.2.0203]
  11. Pahwa R, Lyons KL, Wilkinson SB, Carpenter MA, Tröster AI, Searl JP, Overman J, Pickering S, Koller WC (1999) Bilateral thalamic stimulation for the treatment of essential tremor. Neurology 53:1447–1450. https://doi.org/10.1212/wnl.53.7.1447 [DOI: 10.1212/wnl.53.7.1447]
  12. Forel A (1877) Untersuchungen über die Haubenregion und ihre oberen Verknüpfungen im Gehirne des Menschen und einiger Säugethiere, mit Beiträgen zu den Methoden der Gehirnuntersuchung. Arch Für Psychiatr Nervenkrankh 7:393–495. https://doi.org/10.1007/BF02041873 [DOI: 10.1007/BF02041873]
  13. Mitrofanis J (2005) Some certainty for the “zone of uncertainty”? Exploring the function of the zona incerta. Neuroscience 130:1–15. https://doi.org/10.1016/j.neuroscience.2004.08.017 [DOI: 10.1016/j.neuroscience.2004.08.017]
  14. Kolmac C, Mitrofanis J (1999) Distribution of various neurochemicals within the zona incerta: an immunocytochemical and histochemical study. Anat Embryol (Berl) 199:265–280. https://doi.org/10.1007/s004290050227 [DOI: 10.1007/s004290050227]
  15. Plaha P, Ben-Shlomo Y, Patel NK, Gill SS (2006) Stimulation of the caudal zona incerta is superior to stimulation of the subthalamic nucleus in improving contralateral parkinsonism. Brain 129:1732–1747. https://doi.org/10.1093/brain/awl127 [DOI: 10.1093/brain/awl127]
  16. Ramirez-Zamora A, Smith H, Kumar V, Prusik J, Phookan S, Pilitsis JG (2016) Evolving concepts in posterior subthalamic area deep brain stimulation for treatment of tremor: surgical neuroanatomy and practical considerations. Stereotact Funct Neurosurg 94:283–297. https://doi.org/10.1159/000449007 [DOI: 10.1159/000449007]
  17. Ferraye MU, Gerardin P, Debû B, Chabardès S, Fraix V, Seigneuret E, LeBas J-F, Benabid A-L, Tilikete C, Pollak P (2009) Pedunculopontine nucleus stimulation induces monocular oscillopsia. J Neurol Neurosurg Psychiatry 80:228–231. https://doi.org/10.1136/jnnp.2008.146472 [DOI: 10.1136/jnnp.2008.146472]
  18. Zrinzo L, Zrinzo LV, Tisch S, Limousin PD, Yousry TA, Afshar F, Hariz MI (2008) Stereotactic localization of the human pedunculopontine nucleus: Atlas-based coordinates and validation of a magnetic resonance imaging protocol for direct localization. Brain J Neurol 131:1588–1598. https://doi.org/10.1093/brain/awn075 [DOI: 10.1093/brain/awn075]
  19. Shimamoto SA, Larson PS, Ostrem JL, Glass GA, Turner RS, Starr PA (2010) Physiological identification of the human pedunculopontine nucleus. J Neurol Neurosurg Psychiatry 81:80–86. https://doi.org/10.1136/jnnp.2009.179069 [DOI: 10.1136/jnnp.2009.179069]
  20. Weiss D, Walach M, Meisner C, Fritz M, Scholten M, Breit S, Plewnia C, Bender B, Gharabaghi A, Wächter T, Krüger R (2013) Nigral stimulation for resistant axial motor impairment in Parkinson’s disease? A randomized controlled trial. Brain 136:2098–2108. https://doi.org/10.1093/brain/awt122 [DOI: 10.1093/brain/awt122]
  21. Sharma VD, Mewes K, Wichmann T, Buetefisch C, Willie JT, DeLong M (2017) Deep brain stimulation of the centromedian thalamic nucleus for essential tremor: a case report. Acta Neurochir (Wien) 159:789–793. https://doi.org/10.1007/s00701-017-3143-y [DOI: 10.1007/s00701-017-3143-y]
  22. Gratwicke J, Zrinzo L, Kahan J, Peters A, Beigi M, Akram H, Hyam J, Oswal A, Day B, Mancini L, Thornton J, Yousry T, Limousin P, Hariz M, Jahanshahi M, Foltynie T (2018) Bilateral deep brain stimulation of the nucleus basalis of Meynert for Parkinson disease dementia: a randomized clinical trial. JAMA Neurol 75:169–178. https://doi.org/10.1001/jamaneurol.2017.3762 [DOI: 10.1001/jamaneurol.2017.3762]
  23. Fenoy AJ, Schiess MC (2017) Deep brain stimulation of the dentato-rubro-thalamic tract: outcomes of direct targeting for tremor. Neuromodulation J Int Neuromodulation Soc 20:429–436. https://doi.org/10.1111/ner.12585 [DOI: 10.1111/ner.12585]
  24. Houeto J-L, Yelnik J, Bardinet E, Vercueil L, Krystkowiak P, Mesnage V, Lagrange C, Dormont D, Le Bas J-F, Pruvo J-P, Tézenas du Montcel S, Pollak P, Agid Y, Destée A, Vidailhet M (2007) Acute deep-brain stimulation of the internal and external globus pallidus in primary dystonia: functional mapping of the pallidum. Arch Neurol 64:1281. https://doi.org/10.1001/archneur.64.9.1281 [DOI: 10.1001/archneur.64.9.1281]
  25. Cho CB, Park HK, Lee KJ, Rha HK (2009) Thalamic deep brain stimulation for writer’s cramp. J Korean Neurosurg Soc 46:52. https://doi.org/10.3340/jkns.2009.46.1.52 [DOI: 10.3340/jkns.2009.46.1.52]
  26. Ghika J, Villemure JG, Miklossy J, Temperli P, Pralong E, Christen-Zaech S, Pollo C, Maeder P, Bogousslavsky J, Vingerhoets F (2002) Postanoxic generalized dystonia improved by bilateral Voa thalamic deep brain stimulation. Neurology 58:311–313. https://doi.org/10.1212/WNL.58.2.311 [DOI: 10.1212/WNL.58.2.311]
  27. Katsakiori PF, Kefalopoulou Z, Markaki E, Paschali A, Ellul J, Kagadis GC, Chroni E, Constantoyannis C (2009) Deep brain stimulation for secondary dystonia: Results in 8 patients. Acta Neurochir (Wien) 151:473–478. https://doi.org/10.1007/s00701-009-0281-x [DOI: 10.1007/s00701-009-0281-x]
  28. Merello M, Tenca E, Cerquetti D (2006) Neuronal activity of the zona incerta in Parkinson’s disease patients. Mov Disord 21:937–943. https://doi.org/10.1002/mds.20834 [DOI: 10.1002/mds.20834]
  29. Kerl HU, Gerigk L, Brockmann MA, Huck S, Al-Zghloul M, Groden C, Hauser T, Nagel AM, Nölte IS (2013) Imaging for deep brain stimulation: The zona incerta at 7 Tesla. World J Radiol 5:5–16. https://doi.org/10.4329/wjr.v5.i1.5 [DOI: 10.4329/wjr.v5.i1.5]
  30. Thaker AA, Reddy KM, Thompson JA, Gerecht PD, Brown MS, Abosch A, Ojemann SG, Kern DS (2021) Coronal gradient echo MRI to visualize the zona incerta for deep brain stimulation targeting in Parkinson’s disease. Stereotact Funct Neurosurg 1–8. https://doi.org/10.1159/000515772
  31. Burrows AM, Ravin PD, Novak P, Peters MLB, Dessureau B, Swearer J, Pilitsis JG (2012) Limbic and motor function comparison of deep brain stimulation of the zona incerta and subthalamic nucleus. Neurosurgery 70:125–130. https://doi.org/10.1227/NEU.0b013e318232fdac (discussion 130-131) [DOI: 10.1227/NEU.0b013e318232fdac]
  32. Garcia-Garcia D, Guridi J, Toledo JB, Alegre M, Obeso JA, Rodríguez-Oroz MC (2016) Stimulation sites in the subthalamic nucleus and clinical improvement in Parkinson’s disease: a new approach for active contact localization. J Neurosurg 125:1068–1079. https://doi.org/10.3171/2015.9.JNS15868 [DOI: 10.3171/2015.9.JNS15868]
  33. Maks CB, Butson CR, Walter BL, Vitek JL, McIntyre CC (2009) Deep brain stimulation activation volumes and their association with neurophysiological mapping and therapeutic outcomes. J Neurol Neurosurg Psychiatry 80:659–666. https://doi.org/10.1136/jnnp.2007.126219 [DOI: 10.1136/jnnp.2007.126219]
  34. Aquino CC, Duffley G, Hedges DM, Vorwerk J, House PA, Ferraz HB, Rolston JD, Butson CR, Schrock LE (2019) Interleaved deep brain stimulation for dyskinesia management in Parkinson’s disease. Mov Disord 34:1722–1727. https://doi.org/10.1002/mds.27839 [DOI: 10.1002/mds.27839]
  35. Kern DS, Picillo M, Thompson JA, Sammartino F, di Biase L, Munhoz RP, Fasano A (2018) Interleaving stimulation in Parkinson’s disease, tremor, and dystonia. Stereotact Funct Neurosurg 96:379–391. https://doi.org/10.1159/000494983 [DOI: 10.1159/000494983]
  36. Merello M, Cavanagh S, Perez-Lloret S, Roldan E, Bruno V, Tenca E, Leiguarda R (2009) Irritability, psychomotor agitation and progressive insomnia induced by bilateral stimulation of the area surrounding the dorsal subthalamic nucleus (zona incerta) in Parkinson’s disease patients. J Neurol 256:2091–2093. https://doi.org/10.1007/s00415-009-5285-1 [DOI: 10.1007/s00415-009-5285-1]
  37. Blomstedt P, Fytagoridis A, Åström M, Linder J, Forsgren L, Hariz MI (2012) Unilateral caudal zona incerta deep brain stimulation for Parkinsonian tremor. Parkinsonism Relat Disord 18:1062–1066. https://doi.org/10.1016/j.parkreldis.2012.05.024 [DOI: 10.1016/j.parkreldis.2012.05.024]
  38. Blomstedt P, Stenmark Persson R, Hariz G-M, Linder J, Fredricks A, Häggström B, Philipsson J, Forsgren L, Hariz M (2018) Deep brain stimulation in the caudal zona incerta versus best medical treatment in patients with Parkinson’s disease: a randomised blinded evaluation. J Neurol Neurosurg Psychiatry 89:710–716. https://doi.org/10.1136/jnnp-2017-317219 [DOI: 10.1136/jnnp-2017-317219]
  39. Kitagawa M, Murata J, Uesugi H, Kikuchi S, Saito H, Tashiro K, Sawamura Y (2005) Two-year follow-up of chronic stimulation of the posterior subthalamic white matter for tremor-dominant Parkinson’s disease. Neurosurgery 56:281–289. https://doi.org/10.1227/01.NEU.0000148167.49105.A3 [DOI: 10.1227/01.NEU.0000148167.49105.A3]
  40. Blomstedt P (2017) Hyperhidrosis caused by deep brain stimulation in the posterior subthalamic area. J Neurol Sci 380:277–279. https://doi.org/10.1016/j.jns.2017.07.021 [DOI: 10.1016/j.jns.2017.07.021]
  41. Fytagoridis A, Blomstedt P (2010) Complications and side effects of deep brain stimulation in the posterior subthalamic area. Stereotact Funct Neurosurg 88:88–93. https://doi.org/10.1159/000271824 [DOI: 10.1159/000271824]
  42. Carrillo-Ruiz JD, Velasco F, Jimènez F, Castro G, Velasco AL, Hernández JA, Ceballos J, Velasco M (2008) Bilateral electrical stimulation of prelemniscal radiations in the treatment of advanced Parkinson’s Disease. Neurosurgery 62:347–359. https://doi.org/10.1227/01.neu.0000316001.03765.e8 [DOI: 10.1227/01.neu.0000316001.03765.e8]
  43. Jiménez F, Velasco F, Velasco M, Brito F, Morel C, Márquez I, Pérez ML (2000) Subthalamic prelemniscal radiation stimulation for the treatment of Parkinson’s disease: Electrophysiological characterization of the area. Arch Med Res 31:270–281. https://doi.org/10.1016/s0188-4409(00)00066-7 [DOI: 10.1016/s0188-4409(00)00066-7]
  44. Velasco F, Jiménez F, Pérez ML, Carrillo-Ruiz JD, Velasco AL, Ceballos J, Velasco M (2001) Electrical stimulation of the prelemniscal radiation in the treatment of Parkinson’s disease: an old target revised with new techniques. Neurosurgery 49:293–306. https://doi.org/10.1097/00006123-200108000-00009 (discussion 306-308) [DOI: 10.1097/00006123-200108000-00009]
  45. Takakusaki K, Kitai ST (1997) Ionic mechanisms involved in the spontaneous firing of tegmental pedunculopontine nucleus neurons of the rat. Neuroscience 78:771–794. https://doi.org/10.1016/s0306-4522(96)00540-4 [DOI: 10.1016/s0306-4522(96)00540-4]
  46. Lavoie B, Parent A (1994) Pedunculopontine nucleus in the squirrel monkey: projections to the basal ganglia as revealed by anterograde tract-tracing methods. J Comp Neurol 344:210–231. https://doi.org/10.1002/cne.903440204 [DOI: 10.1002/cne.903440204]
  47. Winn P (2006) How best to consider the structure and function of the pedunculopontine tegmental nucleus: evidence from animal studies. J Neurol Sci 248:234–250. https://doi.org/10.1016/j.jns.2006.05.036 [DOI: 10.1016/j.jns.2006.05.036]
  48. Matsumura M (2005) The pedunculopontine tegmental nucleus and experimental parkinsonism. A review. J Neurol 252(Suppl 4):IV5–IV12. https://doi.org/10.1007/s00415-005-4003-x [DOI: 10.1007/s00415-005-4003-x]
  49. Nandi D, Aziz TZ, Giladi N, Winter J, Stein JF (2002) Reversal of akinesia in experimental parkinsonism by GABA antagonist microinjections in the pedunculopontine nucleus. Brain 125:2418–2430. https://doi.org/10.1093/brain/awf259 [DOI: 10.1093/brain/awf259]
  50. Jenkinson N, Nandi D, Miall RC, Stein JF, Aziz TZ (2004) Pedunculopontine nucleus stimulation improves akinesia in a Parkinsonian monkey. NeuroReport 15:2621–2624. https://doi.org/10.1097/00001756-200412030-00012 [DOI: 10.1097/00001756-200412030-00012]
  51. Jenkinson N, Nandi D, Oram R, Stein JF, Aziz TZ (2006) Pedunculopontine nucleus electric stimulation alleviates akinesia independently of dopaminergic mechanisms. NeuroReport 17:639–641. https://doi.org/10.1097/00001756-200604240-00016 [DOI: 10.1097/00001756-200604240-00016]
  52. Hamani C, Lozano AM, Mazzone PAM, Moro E, Hutchison W, Silburn PA, Zrinzo L, Alam M, Goetz L, Pereira E, Rughani A, Thevathasan W, Aziz T, Bloem BR, Brown P, Chabardes S, Coyne T, Foote K, Garcia-Rill E, Hirsch EC, Okun MS, Krauss JK (2016) Pedunculopontine nucleus region deep brain stimulation in Parkinson disease: surgical techniques, side effects, and postoperative imaging. Stereotact Funct Neurosurg 94:307–319. https://doi.org/10.1159/000449011 [DOI: 10.1159/000449011]
  53. Thevathasan W, Pogosyan A, Hyam JA, Jenkinson N, Foltynie T, Limousin P, Bogdanovic M, Zrinzo L, Green AL, Aziz TZ, Brown P (2012) Alpha oscillations in the pedunculopontine nucleus correlate with gait performance in parkinsonism. Brain 135:148–160 [DOI: 10.1093/brain/awr315]
  54. Yelnik J (2007) PPN or PPD, what is the target for deep brain stimulation in Parkinson’s disease? Brain 130:e79–e79 [DOI: 10.1093/brain/awm138]
  55. Zrinzo L, Zrinzo L, Hariz M (2007) The peripeduncular nucleus: A novel target for deep brain stimulation? NeuroReport 18:1301–1302 [DOI: 10.1097/WNR.0b013e3282638603]
  56. Thevathasan W, Debu B, Aziz T, Bloem BR, Blahak C, Butson C, Czernecki V, Foltynie T, Fraix V, Grabli D, Joint C, Lozano AM, Okun MS, Ostrem J, Pavese N, Schrader C, Tai C-H, Krauss JK, Moro E (2018) Pedunculopontine nucleus deep brain stimulation in Parkinson’s disease: a clinical review. Mov Disord 33:10–20. https://doi.org/10.1002/mds.27098 [DOI: 10.1002/mds.27098]
  57. Goetz L, Maineri C, Piallat B, David O, Ferraye M, Torres N, Debu B, Seigneuret E, Fraix V, Lebas J, Pollak P (2010) A normalized per-operatory microstimulation mapping of the rostral brainstem as a tool to delineate PPNa target
  58. Wilcox RA, Cole MH, Wong D, Coyne T, Silburn P, Kerr G (2011) Pedunculopontine nucleus deep brain stimulation produces sustained improvement in primary progressive freezing of gait. J Neurol Neurosurg Psychiatry 82:1256–1259. https://doi.org/10.1136/jnnp.2010.213462 [DOI: 10.1136/jnnp.2010.213462]
  59. Khan S, Mooney L, Plaha P, Javed S, White P, Whone AL, Gill SS (2011) Outcomes from stimulation of the caudal zona incerta and pedunculopontine nucleus in patients with Parkinson’s disease. Br J Neurosurg 25:273–280. https://doi.org/10.3109/02688697.2010.544790 [DOI: 10.3109/02688697.2010.544790]
  60. Mazzone P, Sposato S, Insola A, Dilazzaro V, Scarnati E (2008) Stereotactic surgery of nucleus tegmenti pedunculopontine [corrected]. Br J Neurosurg 22(Suppl 1):S33-40. https://doi.org/10.1080/02688690802448327 [DOI: 10.1080/02688690802448327]
  61. Moro E, Hamani C, Poon Y-Y, Al-Khairallah T, Dostrovsky JO, Hutchison WD, Lozano AM (2010) Unilateral pedunculopontine stimulation improves falls in Parkinson’s disease. Brain 133:215–224. https://doi.org/10.1093/brain/awp261 [DOI: 10.1093/brain/awp261]
  62. Thevathasan W, Cole MH, Graepel CL, Hyam JA, Jenkinson N, Brittain J-S, Coyne TJ, Silburn PA, Aziz TZ, Kerr G, Brown P (2012) A spatiotemporal analysis of gait freezing and the impact of pedunculopontine nucleus stimulation. Brain 135:1446–1454. https://doi.org/10.1093/brain/aws039 [DOI: 10.1093/brain/aws039]
  63. Welter M-L, Demain A, Ewenczyk C, Czernecki V, Lau B, El Helou A, Belaid H, Yelnik J, François C, Bardinet E, Karachi C, Grabli D (2015) PPNa-DBS for gait and balance disorders in Parkinson’s disease: a double-blind, randomised study. J Neurol 262:1515–1525. https://doi.org/10.1007/s00415-015-7744-1 [DOI: 10.1007/s00415-015-7744-1]
  64. Mestre TA, Sidiropoulos C, Hamani C, Poon Y-Y, Lozano AM, Lang AE, Moro E (2016) Long-term double-blinded unilateral pedunculopontine area stimulation in Parkinson’s disease. Mov Disord 31:1570–1574. https://doi.org/10.1002/mds.26710 [DOI: 10.1002/mds.26710]
  65. Thevathasan W, Silburn PA, Brooker H, Coyne TJ, Khan S, Gill SS, Aziz TZ, Brown P (2010) The impact of low-frequency stimulation of the pedunculopontine nucleus region on reaction time in parkinsonism. J Neurol Neurosurg Psychiatry 81:1099–1104. https://doi.org/10.1136/jnnp.2009.189324 [DOI: 10.1136/jnnp.2009.189324]
  66. Galazky I, Kaufmann J, Lorenzl S, Ebersbach G, Gandor F, Zaehle T, Specht S, Stallforth S, Sobieray U, Wirkus E, Casjens F, Heinze H-J, Kupsch A, Voges J (2018) Deep brain stimulation of the pedunculopontine nucleus for treatment of gait and balance disorder in progressive supranuclear palsy: Effects of frequency modulations and clinical outcome. Parkinsonism Relat Disord 50:81–86. https://doi.org/10.1016/j.parkreldis.2018.02.027 [DOI: 10.1016/j.parkreldis.2018.02.027]
  67. Peppe A, Pierantozzi M, Chiavalon C, Marchetti F, Caltagirone C, Musicco M, Stanzione P, Stefani A (2010) Deep brain stimulation of the pedunculopontine tegmentum and subthalamic nucleus: effects on gait in Parkinson’s disease. Gait Posture 32:512–518. https://doi.org/10.1016/j.gaitpost.2010.07.012 [DOI: 10.1016/j.gaitpost.2010.07.012]
  68. Stefani A, Lozano AM, Peppe A, Stanzione P, Galati S, Tropepi D, Pierantozzi M, Brusa L, Scarnati E, Mazzone P (2007) Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson’s disease. Brain 130:1596–1607. https://doi.org/10.1093/brain/awl346 [DOI: 10.1093/brain/awl346]
  69. Khan S, Gill SS, Mooney L, White P, Whone A, Brooks DJ, Pavese N (2012) Combined pedunculopontine-subthalamic stimulation in Parkinson disease. Neurology 78:1090–1095. https://doi.org/10.1212/WNL.0b013e31824e8e96 [DOI: 10.1212/WNL.0b013e31824e8e96]
  70. Schrader C, Seehaus F, Capelle HH, Windhagen A, Windhagen H, Krauss JK (2013) Effects of pedunculopontine area and pallidal DBS on gait ignition in Parkinson’s disease. Brain Stimulat 6:856–859. https://doi.org/10.1016/j.brs.2013.05.005 [DOI: 10.1016/j.brs.2013.05.005]
  71. Lim AS, Moro E, Lozano AM, Hamani C, Dostrovsky JO, Hutchison WD, Lang AE, Wennberg RA, Murray BJ (2009) Selective enhancement of rapid eye movement sleep by deep brain stimulation of the human pons. Ann Neurol 66:110–114. https://doi.org/10.1002/ana.21631 [DOI: 10.1002/ana.21631]
  72. Romigi A, Placidi F, Peppe A, Pierantozzi M, Izzi F, Brusa L, Galati S, Moschella V, Marciani MG, Mazzone P, Stanzione P, Stefani A (2008) Pedunculopontine nucleus stimulation influences REM sleep in Parkinson’s disease. Eur J Neurol 15:e64-65. https://doi.org/10.1111/j.1468-1331.2008.02167.x [DOI: 10.1111/j.1468-1331.2008.02167.x]
  73. Aviles-Olmos I, Foltynie T, Panicker J, Cowie D, Limousin P, Hariz M, Fowler CJ, Zrinzo L (2011) Urinary incontinence following deep brain stimulation of the pedunculopontine nucleus. Acta Neurochir (Wien) 153:2357–2360. https://doi.org/10.1007/s00701-011-1155-6 [DOI: 10.1007/s00701-011-1155-6]
  74. Nosko D, Ferraye MU, Fraix V, Goetz L, Chabardès S, Pollak P, Debû B (2015) Low-frequency versus high-frequency stimulation of the pedunculopontine nucleus area in Parkinson’s disease: A randomised controlled trial. J Neurol Neurosurg Psychiatry 86:674–679. https://doi.org/10.1136/jnnp-2013-307511 [DOI: 10.1136/jnnp-2013-307511]
  75. Massey LA, Yousry TA (2010) Anatomy of the substantia nigra and subthalamic nucleus on MR imaging. Neuroimaging Clin N Am 20:7–27. https://doi.org/10.1016/j.nic.2009.10.001 [DOI: 10.1016/j.nic.2009.10.001]
  76. Zhou F-M, Lee CR (2011) Intrinsic and integrative properties of substantia nigra pars reticulata neurons. Neuroscience 198:69–94. https://doi.org/10.1016/j.neuroscience.2011.07.061 [DOI: 10.1016/j.neuroscience.2011.07.061]
  77. Ilinsky IA, Tourtellotte WG, Kultas-Ilinsky K (1993) Anatomical distinctions between the two basal ganglia afferent territories in the primate motor thalamus. Stereotact Funct Neurosurg 60:62–69. https://doi.org/10.1159/000100590 [DOI: 10.1159/000100590]
  78. Beninato M, Spencer RF (1987) A cholinergic projection to the rat substantia nigra from the pedunculopontine tegmental nucleus. Brain Res 412:169–174. https://doi.org/10.1016/0006-8993(87)91455-7 [DOI: 10.1016/0006-8993(87)91455-7]
  79. Garcia-Rill E, Hyde J, Kezunovic N, Urbano FJ, Petersen E (2015) The physiology of the pedunculopontine nucleus: Implications for deep brain stimulation. J Neural Transm 122:225–235. https://doi.org/10.1007/s00702-014-1243-x [DOI: 10.1007/s00702-014-1243-x]
  80. Inglis WL, Winn P (1995) The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation. Prog Neurobiol 47:1–29. https://doi.org/10.1016/0301-0082(95)00013-l [DOI: 10.1016/0301-0082(95)00013-l]
  81. Herkenham M (1979) The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J Comp Neurol 183:487–517. https://doi.org/10.1002/cne.901830304 [DOI: 10.1002/cne.901830304]
  82. Nishimura Y, Takada M, Mizuno N (1997) Topographic distribution and collateral projections of the two major populations of nigrothalamic neurons. A retrograde labeling study in the rat. Neurosci Res 28:1–9. https://doi.org/10.1016/s0168-0102(97)01171-1 [DOI: 10.1016/s0168-0102(97)01171-1]
  83. Deniau JM, Chevalier G (1985) Disinhibition as a basic process in the expression of striatal functions. II. The striato-nigral influence on thalamocortical cells of the ventromedial thalamic nucleus. Brain Res 334:227–233. https://doi.org/10.1016/0006-8993(85)90214-8 [DOI: 10.1016/0006-8993(85)90214-8]
  84. MacLeod NK, James TA, Kilpatrick IC, Starr MS (1980) Evidence for a GABAergic nigrothalamic pathway in the rat. II Electrophysiological studies Exp Brain Res 40:55–61. https://doi.org/10.1007/BF00236662 [DOI: 10.1007/BF00236662]
  85. Schultz W (1986) Activity of pars reticulata neurons of monkey substantia nigra in relation to motor, sensory, and complex events. J Neurophysiol 55:660–677. https://doi.org/10.1152/jn.1986.55.4.660 [DOI: 10.1152/jn.1986.55.4.660]
  86. Walters JR, Hu D, Itoga CA, Parr-Brownlie LC, Bergstrom DA (2007) Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine. Neuroscience 144:762–776. https://doi.org/10.1016/j.neuroscience.2006.10.006 [DOI: 10.1016/j.neuroscience.2006.10.006]
  87. Wichmann T, Bergman H, Starr PA, Subramanian T, Watts RL, DeLong MR (1999) Comparison of MPTP-induced changes in spontaneous neuronal discharge in the internal pallidal segment and in the substantia nigra pars reticulata in primates. Exp Brain Res 125:397–409. https://doi.org/10.1007/s002210050696 [DOI: 10.1007/s002210050696]
  88. DeLong MR, Crutcher MD, Georgopoulos AP (1983) Relations between movement and single cell discharge in the substantia nigra of the behaving monkey. J Neurosci Off J Soc Neurosci 3:1599–1606 [DOI: 10.1523/JNEUROSCI.03-08-01599.1983]
  89. Hikosaka O, Wurtz RH (1983) Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J Neurophysiol 49:1285–1301. https://doi.org/10.1152/jn.1983.49.5.1285 [DOI: 10.1152/jn.1983.49.5.1285]
  90. Brown P (2003) Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson’s disease. Mov Disord 18:357–363. https://doi.org/10.1002/mds.10358 [DOI: 10.1002/mds.10358]
  91. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281–285. https://doi.org/10.1016/0166-2236(90)90110-v [DOI: 10.1016/0166-2236(90)90110-v]
  92. Milosevic L, Kalia SK, Hodaie M, Lozano AM, Fasano A, Popovic MR, Hutchison WD (2018) Neuronal inhibition and synaptic plasticity of basal ganglia neurons in Parkinson’s disease. Brain 141:177–190. https://doi.org/10.1093/brain/awx296 [DOI: 10.1093/brain/awx296]
  93. Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: Moving forward on a mysterious clinical phenomenon. Lancet Neurol 10:734–744. https://doi.org/10.1016/S1474-4422(11)70143-0 [DOI: 10.1016/S1474-4422(11)70143-0]
  94. Zibetti M, Merola A, Rizzi L, Ricchi V, Angrisano S, Azzaro C, Artusi CA, Arduino N, Marchisio A, Lanotte M, Rizzone M, Lopiano L (2011) Beyond nine years of continuous subthalamic nucleus deep brain stimulation in Parkinson’s disease. Mov Disord 26:2327–2334. https://doi.org/10.1002/mds.23903 [DOI: 10.1002/mds.23903]
  95. Pötter-Nerger M, Ilic TV, Siebner HR, Deuschl G, Volkmann J (2008) Subthalamic nucleus stimulation restores corticospinal facilitation in Parkinson’s disease. Mov Disord 23:2210–2215. https://doi.org/10.1002/mds.22284 [DOI: 10.1002/mds.22284]
  96. Thevathasan W, Pogosyan A, Hyam JA, Jenkinson N, Bogdanovic M, Coyne TJ, Silburn PA, Aziz TZ, Brown P (2011) A block to pre-prepared movement in gait freezing, relieved by pedunculopontine nucleus stimulation. Brain 134:2085–2095. https://doi.org/10.1093/brain/awr131 [DOI: 10.1093/brain/awr131]
  97. Hamel W, Fietzek U, Morsnowski A, Schrader B, Herzog J, Weinert D, Pfister G, Müller D, Volkmann J, Deuschl G, Mehdorn HM (2003) Deep brain stimulation of the subthalamic nucleus in Parkinson’s disease: evaluation of active electrode contacts. J Neurol Neurosurg Psychiatry 74:1036–1046. https://doi.org/10.1136/jnnp.74.8.1036 [DOI: 10.1136/jnnp.74.8.1036]
  98. Hidding U, Gulberti A, Horn A, Buhmann C, Hamel W, Koeppen JA, Westphal M, Engel AK, Gerloff C, Weiss D, Moll CKE, Pötter-Nerger M (2017) Impact of combined subthalamic nucleus and substantia nigra stimulation on neuropsychiatric symptoms in Parkinson’s disease patients. Park Dis 2017:7306192. https://doi.org/10.1155/2017/7306192 [DOI: 10.1155/2017/7306192]
  99. Weiss D, Breit S, Wächter T, Plewnia C, Gharabaghi A, Krüger R (2011) Combined stimulation of the substantia nigra pars reticulata and the subthalamic nucleus is effective in hypokinetic gait disturbance in Parkinson’s disease. J Neurol 258:1183–1185. https://doi.org/10.1007/s00415-011-5906-3 [DOI: 10.1007/s00415-011-5906-3]
  100. Groenewegen HJ, Berendse HW (1994) The specificity of the “nonspecific” midline and intralaminar thalamic nuclei. Trends Neurosci 17:52–57. https://doi.org/10.1016/0166-2236(94)90074-4 [DOI: 10.1016/0166-2236(94)90074-4]
  101. Moruzzi G, Magoun HW (1949) Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1:455–473 [DOI: 10.1016/0013-4694(49)90219-9]
  102. Sadikot AF, Parent A, Smith Y, Bolam JP (1992) Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: A light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity. J Comp Neurol 320:228–242. https://doi.org/10.1002/cne.903200207 [DOI: 10.1002/cne.903200207]
  103. Sadikot AF, Rymar VV (2009) The primate centromedian-parafascicular complex: anatomical organization with a note on neuromodulation. Brain Res Bull 78:122–130. https://doi.org/10.1016/j.brainresbull.2008.09.016 [DOI: 10.1016/j.brainresbull.2008.09.016]
  104. Thomas TM, Smith Y, Levey AI, Hersch SM (2000) Cortical inputs to m2-immunoreactive striatal interneurons in rat and monkey. Synapse 37:252–261. https://doi.org/10.1002/1098-2396(20000915)37:4%3c252::AID-SYN2%3e3.0.CO;2-A [DOI: 10.1002/1098-2396(20000915)37]
  105. Sidibé M, Paré J-F, Smith Y (2002) Nigral and pallidal inputs to functionally segregated thalamostriatal neurons in the centromedian/parafascicular intralaminar nuclear complex in monkey. J Comp Neurol 447:286–299. https://doi.org/10.1002/cne.10247 [DOI: 10.1002/cne.10247]
  106. Smith Y, Raju D, Nanda B, Pare J-F, Galvan A, Wichmann T (2009) The thalamostriatal systems: anatomical and functional organization in normal and parkinsonian states. Brain Res Bull 78:60–68. https://doi.org/10.1016/j.brainresbull.2008.08.015 [DOI: 10.1016/j.brainresbull.2008.08.015]
  107. Kerkerian-Le Goff L, Bacci J-J, Jouve L, Melon C, Salin P (2009) Impact of surgery targeting the caudal intralaminar thalamic nuclei on the pathophysiological functioning of basal ganglia in a rat model of Parkinson’s disease. Brain Res Bull 78:80–84. https://doi.org/10.1016/j.brainresbull.2008.08.010 [DOI: 10.1016/j.brainresbull.2008.08.010]
  108. Henderson JM, Carpenter K, Cartwright H, Halliday GM (2000) Degeneration of the centré median-parafascicular complex in Parkinson’s disease. Ann Neurol 47:345–352 [DOI: 10.1002/1531-8249(200003)47]
  109. Andy OJ (1980) Parafascicular-center median nuclei stimulation for intractable pain and dyskinesia (painful-dyskinesia). Appl Neurophysiol 43:133–144. https://doi.org/10.1159/000102247 [DOI: 10.1159/000102247]
  110. Krauss JK, Simpson RK, Ondo WG, Pohle T, Burgunder JM, Jankovic J (2001) Concepts and methods in chronic thalamic stimulation for treatment of tremor: technique and application. Neurosurgery 48:535–541. https://doi.org/10.1097/00006123-200103000-00015 (discussion 541-543) [DOI: 10.1097/00006123-200103000-00015]
  111. Velasco F, Velasco M, Velasco AL, Jimenez F, Marquez I, Rise M (1995) Electrical stimulation of the centromedian thalamic nucleus in control of seizures: long-term studies. Epilepsia 36:63–71. https://doi.org/10.1111/j.1528-1157.1995.tb01667.x [DOI: 10.1111/j.1528-1157.1995.tb01667.x]
  112. Krauss JK, Pohle T, Weigel R, Burgunder J-M (2002) Deep brain stimulation of the centre median-parafascicular complex in patients with movement disorders. J Neurol Neurosurg Psychiatry 72:546–548. https://doi.org/10.1136/jnnp.72.4.546 [DOI: 10.1136/jnnp.72.4.546]
  113. Caparros-Lefebvre D, Pollak P, Feltin MP, Blond S, Benabid AL (1999) The effect of thalamic stimulation on levodopa induced dyskinesias–evaluation of a new target: the center parafascicular median. Rev Neurol (Paris) 155:543–550
  114. Mazzone P, Stocchi F, Galati S, Insola A, Altibrandi MG, Modugno N, Tropepi D, Brusa L, Stefani A (2006) Bilateral implantation of centromedian-parafascicularis complex and GPi: a new combination of unconventional targets for deep brain stimulation in severe Parkinson disease. Neuromodulation 9:221–228. https://doi.org/10.1111/j.1525-1403.2006.00063.x [DOI: 10.1111/j.1525-1403.2006.00063.x]
  115. Stefani A, Peppe A, Pierantozzi M, Galati S, Moschella V, Stanzione P, Mazzone P (2009) Multi-target strategy for Parkinsonian patients: the role of deep brain stimulation in the centromedian–parafascicularis complex. Brain Res Bull 78:113–118. https://doi.org/10.1016/j.brainresbull.2008.08.007 [DOI: 10.1016/j.brainresbull.2008.08.007]
  116. Peppe A, Gasbarra A, Stefani A, Chiavalon C, Pierantozzi M, Fermi E, Stanzione P, Caltagirone C, Mazzone P (2008) Deep brain stimulation of CM/PF of thalamus could be the new elective target for tremor in advanced Parkinson’s Disease? Parkinsonism Relat Disord 14:501–504. https://doi.org/10.1016/j.parkreldis.2007.11.005 [DOI: 10.1016/j.parkreldis.2007.11.005]
  117. Schrock LE, Mink JW, Woods DW, Porta M, Servello D, Visser-Vandewalle V, Silburn PA, Foltynie T, Walker HC, Shahed-Jimenez J, Savica R, Klassen BT, Machado AG, Foote KD, Zhang J-G, Hu W, Ackermans L, Temel Y, Mari Z, Changizi BK, Lozano A, Auyeung M, Kaido T, Agid Y, Welter ML, Khandhar SM, Mogilner AY, Pourfar MH, Walter BL, Juncos JL, Gross RE, Kuhn J, Leckman JF, Neimat JA, Okun MS, Tourette Syndrome Association International Deep Brain Stimulation (DBS) Database and Registry Study Group (2015) Tourette syndrome deep brain stimulation: A review and updated recommendations. Mov Disord 30(448):471. https://doi.org/10.1002/mds.26094 [DOI: 10.1002/mds.26094]
  118. Servello D, Galbiati TF, Balestrino R, Iess G, Zekaj E, Michele SD, Porta M (2020) Deep brain stimulation for Gilles de la Tourette syndrome: Toward limbic targets. Brain Sci 10. https://doi.org/10.3390/brainsci10050301
  119. Cernera S, Okun MS, Gunduz A (2019) A review of cognitive outcomes across movement disorder patients undergoing deep brain stimulation. Front Neurol 10:419. https://doi.org/10.3389/fneur.2019.00419 [DOI: 10.3389/fneur.2019.00419]
  120. Ackermans L, Duits A, van der Linden C, Tijssen M, Schruers K, Temel Y, Kleijer M, Nederveen P, Bruggeman R, Tromp S, van Kranen-Mastenbroek V, Kingma H, Cath D, Visser-Vandewalle V (2011) Double-blind clinical trial of thalamic stimulation in patients with Tourette syndrome. Brain J Neurol 134:832–844. https://doi.org/10.1093/brain/awq380 [DOI: 10.1093/brain/awq380]
  121. Schoenberg MR, Maddux BN, Riley DE, Whitney CM, Ogrocki PK, Gould D, Maciunas RJ (2015) Five-months-postoperative neuropsychological outcome from a pilot prospective randomized clinical trial of thalamic deep brain stimulation for Tourette syndrome. Neuromodulation J Int Neuromodulation Soc 18:97–104. https://doi.org/10.1111/ner.12233 [DOI: 10.1111/ner.12233]
  122. Watkins LH, Sahakian BJ, Robertson MM, Veale DM, Rogers RD, Pickard KM, Aitken MRF, Robbins TW (2005) Executive function in Tourette’s syndrome and obsessive–compulsive disorder. Psychol Med 35:571–582. https://doi.org/10.1017/S0033291704003691 [DOI: 10.1017/S0033291704003691]
  123. Mesulam M-M, Mufson EJ, Levey AI, Wainer BH (1983) Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (Substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214:170–197. https://doi.org/10.1002/cne.902140206 [DOI: 10.1002/cne.902140206]
  124. Goard M, Dan Y (2009) Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12:1444–1449. https://doi.org/10.1038/nn.2402 [DOI: 10.1038/nn.2402]
  125. Ray NJ, Bradburn S, Murgatroyd C, Toseeb U, Mir P, Kountouriotis GK, Teipel SJ, Grothe MJ (2018) In vivo cholinergic basal forebrain atrophy predicts cognitive decline in de novo Parkinson’s disease. Brain 141:165–176. https://doi.org/10.1093/brain/awx310 [DOI: 10.1093/brain/awx310]
  126. Bot M, van Rootselaar F, Contarino MF, Odekerken V, Dijk J, de Bie R, Schuurman R, van den Munckhof P (2018) Deep brain stimulation for essential tremor: aligning thalamic and posterior subthalamic targets in 1 surgical trajectory. Oper Neurosurg 15:144–152. https://doi.org/10.1093/ons/opx232 [DOI: 10.1093/ons/opx232]
  127. Herzog J, Hamel W, Wenzelburger R, Pötter M, Pinsker MO, Bartussek J, Morsnowski A, Steigerwald F, Deuschl G, Volkmann J (2007) Kinematic analysis of thalamic versus subthalamic neurostimulation in postural and intention tremor. Brain 130:1608–1625. https://doi.org/10.1093/brain/awm077 [DOI: 10.1093/brain/awm077]
  128. Favilla CG, Ullman D, Wagle Shukla A, Foote KD, Jacobson CE, Okun MS (2012) Worsening essential tremor following deep brain stimulation: Disease progression versus tolerance. Brain 135:1455–1462. https://doi.org/10.1093/brain/aws026 [DOI: 10.1093/brain/aws026]
  129. Barbe MT, Liebhart L, Runge M, Pauls KAM, Wojtecki L, Schnitzler A, Allert N, Fink GR, Sturm V, Maarouf M, Timmermann L (2011) Deep brain stimulation in the nucleus ventralis intermedius in patients with essential tremor: Habituation of tremor suppression. J Neurol 258:434–439. https://doi.org/10.1007/s00415-010-5773-3 [DOI: 10.1007/s00415-010-5773-3]
  130. Chiu SY, Nozile-Firth K, Klassen BT, Adams A, Lee K, Van Gompel JJ, Hassan A (2020) Ataxia and tolerance after thalamic deep brain stimulation for essential tremor. Parkinsonism Relat Disord 80:47–53. https://doi.org/10.1016/j.parkreldis.2020.09.009 [DOI: 10.1016/j.parkreldis.2020.09.009]
  131. Fytagoridis A, Sandvik U, Aström M, Bergenheim T, Blomstedt P (2012) Long term follow-up of deep brain stimulation of the caudal zona incerta for essential tremor. J Neurol Neurosurg Psychiatry 83:258–262. https://doi.org/10.1136/jnnp-2011-300765 [DOI: 10.1136/jnnp-2011-300765]
  132. Plaha P, Javed S, Agombar D, O’ Farrell G, Khan S, Whone A, Gill S (2011) Bilateral caudal zona incerta nucleus stimulation for essential tremor: Outcome and quality of life. J Neurol Neurosurg Psychiatry 82(899):904. https://doi.org/10.1136/jnnp.2010.222992 [DOI: 10.1136/jnnp.2010.222992]
  133. Diaz A, Cajigas I, Cordeiro JG, Mahavadi A, Sur S, Di Luca DG, Shpiner DS, Luca CC, Jagid JR (2020) Individualized anatomy-based targeting for VIM-cZI DBS in essential tremor. World Neurosurg 140:e225–e233. https://doi.org/10.1016/j.wneu.2020.04.240 [DOI: 10.1016/j.wneu.2020.04.240]
  134. Murata J, Kitagawa M, Uesugi H, Saito H, Iwasaki Y, Kikuchi S, Tashiro K, Sawamura Y (2003) Electrical stimulation of the posterior subthalamic area for the treatment of intractable proximal tremor. J Neurosurg 99:708–715. https://doi.org/10.3171/jns.2003.99.4.0708 [DOI: 10.3171/jns.2003.99.4.0708]
  135. Schlaier J, Anthofer J, Steib K, Fellner C, Rothenfusser E, Brawanski A, Lange M (2015) Deep brain stimulation for essential tremor: targeting the dentato-rubro-thalamic tract? Neuromodulation Technol Neural Interface 18:105–112. https://doi.org/10.1111/ner.12238 [DOI: 10.1111/ner.12238]
  136. King NKK, Krishna V, Basha D, Elias G, Sammartino F, Hodaie M, Lozano AM, Hutchison WD (2017) Microelectrode recording findings within the tractography-defined ventral intermediate nucleus. J Neurosurg 126:1669–1675. https://doi.org/10.3171/2016.3.JNS151992 [DOI: 10.3171/2016.3.JNS151992]
  137. Fiechter M, Nowacki A, Oertel MF, Fichtner J, Debove I, Lachenmayer ML, Wiest R, Bassetti CL, Raabe A, Kaelin-Lang A, Schüpbach MW, Pollo C (2017) Deep brain stimulation for tremor: is there a common structure? Stereotact Funct Neurosurg 95:243–250. https://doi.org/10.1159/000478270 [DOI: 10.1159/000478270]
  138. Klein JC, Barbe MT, Seifried C, Baudrexel S, Runge M, Maarouf M, Gasser T, Hattingen E, Liebig T, Deichmann R, Timmermann L, Weise L, Hilker R (2012) The tremor network targeted by successful VIM deep brain stimulation in humans. Neurology 78:787–795. https://doi.org/10.1212/WNL.0b013e318249f702 [DOI: 10.1212/WNL.0b013e318249f702]
  139. Coenen VA, Allert N, Mädler B (2011) A role of diffusion tensor imaging fiber tracking in deep brain stimulation surgery: DBS of the dentato-rubro-thalamic tract (drt) for the treatment of therapy-refractory tremor. Acta Neurochir (Wien) 153:1579–1585. https://doi.org/10.1007/s00701-011-1036-z [DOI: 10.1007/s00701-011-1036-z]
  140. Hegeman DJ, Hong ES, Hernández VM, Chan CS (2016) The external globus pallidus: progress and perspectives. Eur J Neurosci 43:1239–1265. https://doi.org/10.1111/ejn.13196 [DOI: 10.1111/ejn.13196]
  141. Kita H, Kita T (2001) Number, origins, and chemical types of rat pallidostriatal projection neurons. J Comp Neurol 437:438–448. https://doi.org/10.1002/cne.1294 [DOI: 10.1002/cne.1294]
  142. Baron MS, Chaniary KD, Rice AC, Shapiro SM (2011) Multi-neuronal recordings in the basal ganglia in normal and dystonic rats. Front Syst Neurosci 5:67. https://doi.org/10.3389/fnsys.2011.00067 [DOI: 10.3389/fnsys.2011.00067]
  143. Nishibayashi H, Ogura M, Kakishita K, Tanaka S, Tachibana Y, Nambu A, Kita H, Itakura T (2011) Cortically evoked responses of human pallidal neurons recorded during stereotactic neurosurgery. Mov Disord 26:469–476. https://doi.org/10.1002/mds.23502 [DOI: 10.1002/mds.23502]
  144. Starr PA, Rau GM, Davis V, Marks WJ, Ostrem JL, Simmons D, Lindsey N, Turner RS (2005) Spontaneous pallidal neuronal activity in human dystonia: Comparison with Parkinson’s disease and normal macaque. J Neurophysiol 93:3165–3176. https://doi.org/10.1152/jn.00971.2004 [DOI: 10.1152/jn.00971.2004]
  145. Nambu A, Chiken S, Shashidharan P, Nishibayashi H, Ogura M, Kakishita K, Tanaka S, Tachibana Y, Kita H, Itakura T (2011) Reduced pallidal output causes dystonia. Front Syst Neurosci 5:89. https://doi.org/10.3389/fnsys.2011.00089 [DOI: 10.3389/fnsys.2011.00089]
  146. Percheron G, François C, Talbi B, Meder JF, Fenelon G, Yelnik J (1993) The primate motor thalamus analysed with reference to subcortical afferent territories. Stereotact Funct Neurosurg 60:32–41. https://doi.org/10.1159/000100588 [DOI: 10.1159/000100588]
  147. Horisawa S, Taira T, Goto S, Ochiai T, Nakajima T (2013) Long-term improvement of musician’s dystonia after stereotactic ventro-oral thalamotomy. Ann Neurol 74:648–654. https://doi.org/10.1002/ana.23877 [DOI: 10.1002/ana.23877]
  148. Shimizu T, Maruo T, Miura S, Kishima H, Ushio Y, Goto S (2018) Stereotactic lesioning of the thalamic Vo nucleus for the treatment of writer’s cramp (focal hand dystonia). Front Neurol 9:1008. https://doi.org/10.3389/fneur.2018.01008 [DOI: 10.3389/fneur.2018.01008]
  149. Fukaya C, Katayama Y, Kano T, Nagaoka T, Kobayashi K, Oshima H, Yamamoto T (2007) Thalamic deep brain stimulation for writer’s cramp. J Neurosurg 107:977–982. https://doi.org/10.3171/JNS-07/11/0977 [DOI: 10.3171/JNS-07/11/0977]
  150. Hirt L, Grassia F, Feuerstein J, Thompson JA, Ojemann S, Kern DS (2021) Deep brain stimulation of the ventral intermediate nucleus of the thalamus in writer’s cramp: a case report. Tremor Hyperkinetic Mov 11:46. https://doi.org/10.5334/tohm.645 [DOI: 10.5334/tohm.645]
  151. Goto S, Shimazu H, Matsuzaki K, Tamura T, Murase N, Nagahiro S, Kaji R (2008) Thalamic Vo-complex vs pallidal deep brain stimulation for focal hand dystonia. Neurology 70:1500–1501. https://doi.org/10.1212/01.wnl.0000310430.00743.11 [DOI: 10.1212/01.wnl.0000310430.00743.11]
  152. Tsuboi T, Wong JK, Eisinger RS, Okromelidze L, Burns MR, Ramirez-Zamora A, Almeida L, Wagle Shukla A, Foote KD, Okun MS, Grewal SS, Middlebrooks EH (2021) Comparative connectivity correlates of dystonic and essential tremor deep brain stimulation. Brain 144:1774–1786. https://doi.org/10.1093/brain/awab074 [DOI: 10.1093/brain/awab074]
  153. Poologaindran A, Ivanishvili Z, Morrison MD, Rammage LA, Sandhu MK, Polyhronopoulos NE, Honey CR (2018) The effect of unilateral thalamic deep brain stimulation on the vocal dysfunction in a patient with spasmodic dysphonia: interrogating cerebellar and pallidal neural circuits. J Neurosurg 128:575–582. https://doi.org/10.3171/2016.10.JNS161025 [DOI: 10.3171/2016.10.JNS161025]
  154. de Silva RN, Vallortigara J, Greenfield J, Hunt B, Giunti P, Hadjivassiliou M (2019) Diagnosis and management of progressive ataxia in adults. Pract Neurol 19:196–207. https://doi.org/10.1136/practneurol-2018-002096 [DOI: 10.1136/practneurol-2018-002096]
  155. Diener HC, Dichgans J (1992) Pathophysiology of cerebellar ataxia. Mov Disord 7:95–109. https://doi.org/10.1002/mds.870070202 [DOI: 10.1002/mds.870070202]
  156. Teixeira MJ, Cury RG, Galhardoni R, Barboza VR, Brunoni AR, Alho E, Lepski G, de Andrade DC (2015) Deep brain stimulation of the dentate nucleus improves cerebellar ataxia after cerebellar stroke. Neurology 85:2075–2076. https://doi.org/10.1212/WNL.0000000000002204 [DOI: 10.1212/WNL.0000000000002204]
  157. Cury RG, França C, Barbosa ER, Galhardoni R, Lepski G, Teixeira MJ, Ciampi de Andrade D (2019) Dentate nucleus stimulation in a patient with cerebellar ataxia and tremor after cerebellar stroke: a long-term follow-up. Parkinsonism Relat Disord 60:173–175. https://doi.org/10.1016/j.parkreldis.2018.10.001 [DOI: 10.1016/j.parkreldis.2018.10.001]
  158. Cury RG, França C, Silva V, Barbosa ER, Capato TTC, Lepski G, Duarte KP, Teixeira MJ, Ciampi de Andrade D (2019) Effects of dentate nucleus stimulation in spinocerebellar ataxia type 3. Parkinsonism Relat Disord 69:91–93. https://doi.org/10.1016/j.parkreldis.2019.10.029 [DOI: 10.1016/j.parkreldis.2019.10.029]
  159. Oyama G, Umemura A, Shimo Y, Nishikawa N, Nakajima A, Jo T, Nakajima M, Ishii H, Yamada D, Takanashi M, Arai H, Nanba E, Hattori N (2014) Posterior subthalamic area deep brain stimulation for fragile X-associated tremor/ataxia syndrome. Neuromodulation 17:721–723. https://doi.org/10.1111/ner.12150 [DOI: 10.1111/ner.12150]
  160. Oyama G, Thompson A, Foote KD, Limotai N, Abd-El-Barr M, Maling N, Malaty IA, Rodriguez RL, Subramony SH, Ashizawa T, Okun MS (2014) Deep brain stimulation for tremor associated with underlying ataxia syndromes: A case series and discussion of issues. Tremor Hyperkinetic Mov 4:228. https://doi.org/10.5334/tohm.180 [DOI: 10.5334/tohm.180]
  161. dos Santos Ghilardi MG, Cury RG, dos Ângelos JS, Barbosa DC, Barbosa ER, Teixeira MJ, Fonoff ET (2015) Long-term improvement of tremor and ataxia after bilateral DBS of VoP/zona incerta in FXTAS. Neurology 84:1904–1906. https://doi.org/10.1212/WNL.0000000000001553 [DOI: 10.1212/WNL.0000000000001553]
  162. Bot M, van Rootselaari A-F, Odekerken V, Dijk J, de Bie RMA, Beudel M, van den Munckhof P, Schuurman PR (2021) Evaluating and optimizing dentato-rubro-thalamic-tract deterministic tractography in deep brain stimulation for essential tremor. Oper Neurosurg Hagerstown Md opab324. https://doi.org/10.1093/ons/opab324
  163. Muller J, Alizadeh M, Matias CM, Thalheimer S, Romo V, Martello J, Liang T-W, Mohamed FB, Wu C (2021) Use of probabilistic tractography to provide reliable distinction of the motor and sensory thalamus for prospective targeting during asleep deep brain stimulation. J Neurosurg 1–10. https://doi.org/10.3171/2021.5.JNS21552
  164. Cong F, Liu X, Liu C-SJ, Xu X, Shen Y, Wang B, Zhuo Y, Yan L (2020) Improved depiction of subthalamic nucleus and globus pallidus internus with optimized high-resolution quantitative susceptibility mapping at 7 T. NMR Biomed 33:e4382. https://doi.org/10.1002/nbm.4382 [DOI: 10.1002/nbm.4382]
  165. Isaacs BR, Heijmans M, Kuijf ML, Kubben PL, Ackermans L, Temel Y, Keuken MC, Forstmann BU (2021) Variability in subthalamic nucleus targeting for deep brain stimulation with 3 and 7 Tesla magnetic resonance imaging. NeuroImage Clin 32:102829. https://doi.org/10.1016/j.nicl.2021.102829 [DOI: 10.1016/j.nicl.2021.102829]
  166. Barthel C, Mallia E, Debû B, Bloem BR, Ferraye MU The practicalities of assessing freezing of gait. J Park Dis 6:667–674. https://doi.org/10.3233/JPD-160927

MeSH Term

Deep Brain Stimulation
Humans
Intralaminar Thalamic Nuclei
Parkinson Disease
Quality of Life
Subthalamic Nucleus
Journal Article Review
Article has an altmetric score of 15

Word Cloud

Created with Highcharts 10.0.0targetsnucleusstimulationdisordersbrainneurosurgicalmovementprimarilydeepDBSincludingsubthalamicsegmentglobuspallidusdiseaseventralprovidebenefitadverseeffectsnovelzonaincertathalamusoutcomesNoveltreatmentviarapidlyexpandingevolvingfieldAlthoughconventionalSTNinternalGPiParkinson'sintermediatethalamsVIMtremorsubstantialtermsmotorsymptomsqualitylifeexploredeffortmaximizeclinicalalsoavoidundesiredassociatedincluderostralrZIcaudalcZI/posteriorareaPSAprelemniscalradiationRaprlpedunculopontinePPNsubstantianigraparsreticulataSNrcentromedian/parafascicularCM/PFbasalisMeynertNBMdentato-rubro-thalamictractDRTTdentatecerebellumexternalGPeoralisVOcomplexHoweverreportsutilizingscattereddisparateordercomprehensiveresourceresearcherscliniciansalikesummarizedexistingliteraturesurroundingrationaleusetechniquesrelevantfuturedirectionsresearchAtaxiaDeepDystoniaMovementParkinson’sTremor

Similar Articles

Cited By