Skip to main content

Advertisement

SpringerLink
Log in

Update on the clinical application of deep brain stimulation in sleep dysfunction of Parkinson’s disease

  • Review
  • Published:
Acta Neurologica Belgica Aims and scope Submit manuscript

Abstract

Sleep dysfunctions, including rapid eye movement sleep behavior disorder, sleep fragmentation, excessive daytime sleepiness and various other dysfunctions, can seriously affect quality of life in patients with Parkinson’s disease (PD). Emerging evidence suggests that deep brain stimulation (DBS) exerts a substantial effect when used to treat sleep dysfunctions, which are common nonmotor symptoms experienced by patients with PD. However, far less is known about the specific mechanisms underlying the effects of DBS on sleep processes and the factors that potentially influence these effects. These issues therefore need to be further clarified. Intriguingly, a number of recent studies have evaluated the effects of applying DBS to various brain targets on sleep in patients with PD. Deeper research into the efficacy of applying DBS to each brain target may help determine which region should be targeted during surgery in PD patients. Furthermore, compared with pharmacological therapy, DBS had more beneficial effects on sleep symptoms, and appropriate management involving the joint application of dopamine replacement therapy and DBS might accelerate the effects of treatment. Here, we review the potential roles DBS may play and provide clinical guidance for the use of DBS in treating sleep dysfunctions in PD patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Schrempf W, Brandt MD, Storch A, Reichmann H (2014) Sleep disorders in Parkinson’s disease. J Parkinsons Dis 4:211–221

    PubMed  Google Scholar 

  2. Olanow CW, Watts RL, Koller WC (2001) An algorithm (decision tree) for the management of Parkinson’s disease (2001): treatment guidelines. Neurology 56:S1–S88

    Article  PubMed  CAS  Google Scholar 

  3. Simuni T, Sethi K (2008) Nonmotor manifestations of Parkinson’s disease. Ann Neurol 64(Suppl 2):S65–S80

    PubMed  Google Scholar 

  4. Tandberg E, Larsen JP, Karlsen K (1998) A community-based study of sleep disorders in patients with Parkinson’s disease. Mov Disord 13:895–899

    Article  PubMed  CAS  Google Scholar 

  5. Borek LL, Kohn R, Friedman JH (2006) Mood and sleep in Parkinson’s disease. J Clin Psychiatry 67:958–963

    Article  PubMed  Google Scholar 

  6. Scaravilli T, Gasparoli E, Rinaldi F, Polesello G, Bracco F (2003) Health-related quality of life and sleep disorders in Parkinson’s disease. Neurol Sci 24:209–210

    Article  PubMed  CAS  Google Scholar 

  7. Olanow CW, Stern MB, Sethi K (2009) The scientific and clinical basis for the treatment of Parkinson disease. Neurology 72:S1–S136

    Article  PubMed  Google Scholar 

  8. Pillai JA, Leverenz JB (2017) Sleep and neurodegeneration: a critical appraisal. Chest 151:1375–1386

    Article  PubMed  Google Scholar 

  9. Xie L, Kang H, Xu Q et al (2013) Sleep drives metabolite clearance from the adult brain. Science 342:373–377

    Article  PubMed  CAS  Google Scholar 

  10. Pahapill PA, Lozano AM (2000) The pedunculopontine nucleus and Parkinson’s disease. Brain 123:1767–1783

    Article  PubMed  Google Scholar 

  11. Braak H, Ghebremedhin E, Rüb U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318:121–134

    Article  PubMed  Google Scholar 

  12. Wetter TC, Collado-Seidel V, Pollmächer T, Yassouridis A, Trenkwalder C (2000) Sleep and periodic leg movement patterns in drug-free patients with Parkinson’s disease and multiple system atrophy. Sleep 23:361–367

    Article  PubMed  CAS  Google Scholar 

  13. Adler CH (2005) Nonmotor complications in Parkinson’s disease. Mov Disord 20:S23–S29

    Article  PubMed  Google Scholar 

  14. Kales A, Ansel RD, Markham CH, Scharf MB, Tan TL (1971) Sleep in patients with Parkinson’s disease and normal subjects prior to and following levodopa administration. Clin Pharmacol Ther 12:397–406

    Article  PubMed  CAS  Google Scholar 

  15. Brunner H, Wetter TC, Hogl B, Yassouridis A, Trenkwalder C, Friess E (2002) Microstructure of the non-rapid eye movement sleep electroencephalogram in patients with newly diagnosed Parkinson’s disease: effects of dopaminergic treatment. Mov Disord 17:928–933

    Article  PubMed  Google Scholar 

  16. Adler CH, Thorpy MJ (2005) Sleep issues in Parkinson’s disease. Neurology 64:S12–S20

    Article  PubMed  Google Scholar 

  17. Schrag A, Sauerbier A, Chaudhuri KR (2015) New clinical trials for nonmotor manifestations of Parkinson’s disease. Mov Disord Sep 30:1490–1504

    Article  CAS  Google Scholar 

  18. Dong J, Cui Y, Li S, Le W (2016) Current pharmaceutical treatments and alternative therapies of Parkinson’s disease. Curr Neuropharmacol 14:339–355

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Volkmann J, Albanese A, Kulisevsky J et al (2009) Long-term effects of pallidal or subthalamic deep brain stimulation on quality of life in Parkinson’s disease. Mov Disord 24:1154–1161

    Article  PubMed  Google Scholar 

  20. Rodrigues JP, Walters SE, Watson P, Stell R, Mastaglia FL (2007) Globus pallidus stimulation improves both motor and nonmotor aspects of quality of life in advanced Parkinson’s disease. Mov Disord 22:866–870

    Article  Google Scholar 

  21. Arnulf I, Bejjani BP, Garma L et al (2000) Improvement of sleep architecture in PD with subthalamic nucleus stimulation. Neurology 55:1732–1734

    Article  PubMed  CAS  Google Scholar 

  22. Litvinenko IV, Krasakov IV, Tikhomirova OV (2012) Sleep disorders in Parkinson’s disease without dementia: a comparative randomized controlled study of melatonin and clonazepam. Zh Nevrol Psikhiatr Im S S Korsakova 112:26–30

    PubMed  CAS  Google Scholar 

  23. Trenkwalder C, Kies B, Rudzinska M et al (2011) Rotigotine effects on early morning motor function and sleep in Parkinson’s Disease: a double-blind, Randomized, Placebo-Controlled Study (RECOVER). Mov Disord 26:90–99

    Article  PubMed  Google Scholar 

  24. Eggert K, Öhlwein C, Kassubek J et al (2014) Influence of the nonergot dopamine agonist piribedil on vigilance in patients with Parkinson disease and excessive daytime sleepiness. Clin Neuropharmacol 37:116–122

    Article  PubMed  CAS  Google Scholar 

  25. Zibetti M, Rizzone M, Merola A et al (2013) Sleep improvement with levodopa/carbidopa intestinal gel infusion in Parkinson disease. Acta Neurol Scand 127:e28–e32

    Article  PubMed  CAS  Google Scholar 

  26. Kulua TK, Fedorova NV, Popovkina OA (2011) Nocturnal motor symptoms of Parkinson’s disease and their treatment with the three-component drug levodopa/carbidopa/entacapone. Zh Nevrol Psikhiatr Im S S Korsakova 111:45–50

    PubMed  CAS  Google Scholar 

  27. Rios Romenets S, Creti L, Fichten C et al (2013) Doxepin and cognitive behavioural therapy for insomnia in patients with Parkinson’s disease—a randomized study. Parkinsonism Relat Disord 19:670–675

    Article  PubMed  CAS  Google Scholar 

  28. Di Giacopo R, Fasano A, Quaranta D, Della Marca G, Bove F, Bentivoglio AR (2012) Rivastigmine as alternative treatment for refractory REM behavior disorder in Parkinson’s disease. Mov Disord 27:559–561

    Article  PubMed  CAS  Google Scholar 

  29. Lotan I, Treves TA, Roditi Y, Djaldetti R (2014) Cannabis (medical marijuana) treatment for motor and non-motor symptoms of Parkinson disease. Clin Neuropharmacol 37:41–44

    Article  PubMed  Google Scholar 

  30. Ricciardi L, De Nigris F, Specchia A, Fasano A (2015) Homotaurine in Parkinson’s disease. Neurol Sci 36:1581–1587

    Article  PubMed  Google Scholar 

  31. Gallagher DA, Lees AJ, Schrag A (2010) What are the most important nonmotor symptoms in patients with Parkinson’s disease and are we missing them? Mov Disord 25:2493–2500

    Article  PubMed  Google Scholar 

  32. Iranzo A, Valldeoriola F, Santamaria J, Tolosa E, Rumia J (2002) Sleep symptoms and polysomnographic architecture in advanced Parkinson’s disease after chronic bilateral subthalamic stimulation. J Neurol Neurosurg Psychiatry 72:661–664

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Hwynn N, Ul Haq I, Malaty IA, Resnick AS, Dai Y, Foote KD (2011) Effect of deep brain stimulation on Parkinson’s nonmotor symptoms following unilateral DBS: a pilot study. Parkinsons Dis 2011:507416

    PubMed  PubMed Central  Google Scholar 

  34. Amara AW, Standaert DG, Guthrie S, Cutter G, Watts RL, Walker HC (2012) Unilateral subthalamic nucleus deep brain stimulation improves sleep quality in Parkinson’s disease. Parkinsonism Relat Disord 18:63–68

    Article  PubMed  Google Scholar 

  35. Lyons KE, Pahwa R (2006) Effects of bilateral subthalamic nucleus stimulation on sleep, daytime sleepiness, and early morning dystonia in patients with Parkinson disease. J Neurosurg 104:502–505

    Article  PubMed  Google Scholar 

  36. Monaca C, Ozsancak C, Jacquesson JM et al (2004) Effects of bilateral subthalamic stimulation on sleep in Parkinson’s disease. J Neurol 251:214–218

    Article  PubMed  CAS  Google Scholar 

  37. Arnulf I, Bejjani BP, Garma L et al (2000) Effect of low and high frequency thalamic stimulation on sleep in patients with Parkinson’s disease and essential tremor. J Sleep Res 9:55–62

    Article  PubMed  CAS  Google Scholar 

  38. Chahine LM, Ahmed A, Sun Z (2011) Effects of STN DBS for Parkinson’s disease on restless legs syndrome and other sleep-related measures. Parkinsonism Relat Disord 17:208–211

    Article  PubMed  CAS  Google Scholar 

  39. Aravamuthan BR, Muthusamy KA, Stein JF, Aziz TZ, Johansen-Berg H (2007) Topography of cortical and subcortical connections of the human pedunculopontine and subthalamic nuclei. Neuroimage 37:694–705

    Article  PubMed  CAS  Google Scholar 

  40. Lu J, Sherman D, Devor M, Saper CB (2006) A putative flip-flop switch for control of REM sleep. Nature 441:589–594

    Article  PubMed  CAS  Google Scholar 

  41. Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev 20:128–154

    Article  PubMed  CAS  Google Scholar 

  42. Bevan MD, Bolam JP (1995) Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J Neurosci 15:7105–7120

    Article  PubMed  CAS  Google Scholar 

  43. Amara AW, Watts RL, Walker HC (2011) The effects of deep brain stimulation on sleep in Parkinson’s disease. Ther Adv Neurol Disord 4:15–24

    Article  PubMed  PubMed Central  Google Scholar 

  44. Azmi H, Gupta F, Vukic M et al (2016) Interventional magnetic resonance imaging-guided subthalamic nucleus deep brain stimulation for Parkinson’s disease: patient selection. Surg Neurol Int 7:S557–S563

    Article  PubMed  PubMed Central  Google Scholar 

  45. Profice P, Mazzone P, Pilato F et al (2011) Neurophysiological evaluation of the pedunculopontine nucleus in humans. J Neural Transm (Vienna) 118:1423–1429

    Article  CAS  Google Scholar 

  46. Wang XH, Zhang L, Sperry L et al (2015) Target selection recommendations based on impact of deep brain stimulation surgeries on nonmotor symptoms of Parkinson’s disease. Chin Med J (Engl) 128:3371–3380

    Article  Google Scholar 

  47. Qiu MH, Yao QL, Vetrivelan R, Chen MC, Lu J (2016) Nigrostriatal dopamine acting on globus pallidus regulates sleep. Cereb Cortex 26:1430–1439

    Article  PubMed  Google Scholar 

  48. Kovac S, Wright MA, Eriksson SH, Zrinzo L, Matharu M, Walker MC (2014) The effect of posterior hypothalamus region deep brain stimulation on sleep. Cephalalgia 34:219–223

    Article  PubMed  Google Scholar 

  49. Lim AS, Moro E, Lozano AM et al (2009) Selective enhancement of rapid eye movement sleep by deep brain stimulation of the human pons. Ann Neurol 66:110–114

    Article  PubMed  Google Scholar 

  50. Peppe A, Pierantozzi M, Baiamonte V et al (2012) Deep brain stimulation of pedunculopontine tegmental nucleus: role in sleep modulation in advanced Parkinson disease patients: one-year follow-up. Sleep 35:1637–1642

    Article  PubMed  PubMed Central  Google Scholar 

  51. Garcia-Rill E, Luster B, D’Onofrio S, Mahaffey S, Bisagno V, Urbano FJ (2015) Pedunculopontine arousal system physiology-Deep brain stimulation (DBS). Sleep Sci 8:153–161

    Article  PubMed  PubMed Central  Google Scholar 

  52. Deuschl G, Schade-Brittinger C, Krack P et al (2006) A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med 355:896–908

    Article  PubMed  CAS  Google Scholar 

  53. Hjort N, Østergaard K, Dupont E (2004) Improvement of sleep quality in patients with advanced Parkinson’s disease treated with deep brain stimulation of the subthalamic nucleus. Mov Disord 19:196–199

    Article  PubMed  Google Scholar 

  54. Rye DB (1997) Contributions of the pedunculopontine region to normal and altered REM sleep. Sleep 20:757–788

    Article  PubMed  CAS  Google Scholar 

  55. Kedia S, Moro E, Tagliati M, Lang AE, Kumar R (2004) Emergence of restless legs syndrome during subthalamic stimulation for Parkinson disease. Neurology 63:2410–2412

    Article  PubMed  CAS  Google Scholar 

  56. Cicolin A, Lopiano L, Zibetti M et al (2004) Effects of deep brain stimulation of the subthalamic nucleus on sleep architecture in parkinsonian patients. Sleep Med 5:207–210

    Article  PubMed  Google Scholar 

  57. Baumann-Vogel H, Imbach LL, Sürücü O et al (2017) The impact of subthalamic deep brain stimulation on sleep-wake behavior: a prospective electrophysiological study in 50 Parkinson patients. Sleep 40:zsx033

    Google Scholar 

  58. Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL (2003) Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci 23:1916–1923

    Article  PubMed  CAS  Google Scholar 

  59. Kita H, Tachibana Y, Nambu A, Chiken S (2005) Balance of monosynaptic excitatory and disynaptic inhibitory responses of the globus pallidus induced after stimulation of the subthalamic nucleus in the monkey. J Neurosci 25:8611–8619

    Article  PubMed  CAS  Google Scholar 

  60. Miocinovic S, Parent M, Butson CR et al (2006) Computational analysis of subthalamic nucleus and lenticular fasciculus activation during therapeutic deep brain stimulation. J Neurophysiol 96:1569–1580

    Article  PubMed  Google Scholar 

  61. Hahn PJ, Russo GS, Hashimoto T et al (2008) Pallidal burst activity during therapeutic deep brain stimulation. Exp Neurol 211:243–251

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Qiu MH, Chen MC, Wu J, Nelson D, Lu J (2016) Deep brain stimulation in the globus pallidus externa promotes sleep. Neuroscience 322:115–120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Qiu MH, Vetrivelan R, Fuller PM, Lu J (2010) Basal ganglia control of sleep-wake behavior and cortical activation. Eur J Neurosci 31:499–507

    Article  PubMed  PubMed Central  Google Scholar 

  64. Chen MC, Ferrari L, Sacchet MD et al (2015) Identification of a direct GABAergic pallidocortical pathway in rodents. Eur J Neurosci 41:748–759

    Article  PubMed  PubMed Central  Google Scholar 

  65. Borgohain R, Kandadai RM, Jabeen A, Kannikannan MA (2012) Nonmotor outcomes in Parkinson’s disease: is deep brain stimulation better than dopamine replacement therapy? Ther Adv Neurol Disord 5:23–41

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Pahwa R, Stacy MA, Factor SA et al (2007) EASE-PD Adjunct Study Investigators. Ropinirole 24-hour prolonged release: randomized, controlled study in advanced Parkinson disease. Neurology 68:1108–1115

    Article  PubMed  CAS  Google Scholar 

  67. Vignatelli L, Billiard M, Clarenbach P et al (2006) EFNS guidelines on management of restless legs syndrome and periodic limb movement disorder in sleep. Eur J Neurol 13:1049–1065

    Article  PubMed  CAS  Google Scholar 

  68. Winkelman JW, Sethi KD, Kushida CA et al (2006) Efficacy and safety of pramipexole in restless legs syndrome. Neurology 67:1034–1039

    Article  PubMed  CAS  Google Scholar 

  69. Stiasny-Kolster K, Kohnen R, Schollmayer E, Moller JC, Oertel WH, Rotigotine Sp 666 Study Group (2004) Patch application of the dopamine agonist rotigotine to patients with moderate to advanced stages of restless legs syndrome: a double-blind, placebo-controlled pilot study. Mov Disord 19:1432–1438

    Article  PubMed  Google Scholar 

  70. Walters AS, Ondo WG, Dreykluft T, Grunstein R, Lee D, Sethi K (2004) Ropinirole is effective in the treatment of restless legs syndrome. TREAT RLS 2: a 12-week, double-blind, randomized, parallel- group, placebo controlled study. Mov Disord 19:1414–1423

    Article  PubMed  Google Scholar 

  71. Micallef J, Rey M, Eusebio A et al (2009) Antiparkinsonian drug-induced sleepiness: a double-blind placebo-controlled study of l-dopa, bromocriptine and pramipexole in healthy subjects. Br J Clin Pharmacol 67:333–340

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Ferreira JJ, Galitzky M, Montastruc JL, Rascol O (2000) Sleep attacks and Parkinson’s disease treatment. Lancet 355:1333–1334

    Article  PubMed  CAS  Google Scholar 

  73. Schapira AHV (2000) Sleep attacks (sleep episodes) with pergolide. Lancet 355:1332–1333

    Article  PubMed  CAS  Google Scholar 

  74. Frucht S, Rogers JD, Greene PE, Gordon MF, Fahn S (1999) Falling asleep at the wheel: motor vehicle mishaps in persons taking pramipexole and ropinirole. Neurology 52:1908–1910

    Article  PubMed  CAS  Google Scholar 

  75. Allen RP, Earley CJ (1996) Augmentation of the restless legs syndrome with carbidopa/levodopa. Sleep 19:205–213

    Article  PubMed  CAS  Google Scholar 

  76. Rukmini Mridula K, Borgohain R et al (2015) Comparison of frequencies of nonmotor symptoms in Indian Parkinson’s disease patients on medical management versus deep brain stimulation: a case–control study. Iran J Neurol 14:86–93

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Program of Individualized Diagnosis and Treatment of Parkinson’s Disease and Related Dyskinesia and Construction of Neural Regulation Platform (LNCCC-C06-2015), and the Integrated Research Project of New Diagnosis and Treatment Technology of Electrical Stimulation of Brain Implantation (2016YFC0105900).

Funding

This study was funded by the Program of Individualized Diagnosis and Treatment of Parkinson’s Disease and Related Dyskinesia and Construction of Neural Regulation Platform (LNCCC-C06-2015), and the Integrated Research Project of New Diagnosis and Treatment Technology of Electrical Stimulation of Brain Implantation (2016YFC0105900).

Author information

Author notes

  1. Shuang Zou, Yu-Long Lan and Ya-Ping Hu contributed equally to this work.

Authors and Affiliations

  1. Department of Neurology, The First Affiliated Hospital of Dalian Medical University, No. 222 Zhong Shan Road, Dalian, 116011, People’s Republic of China

    Shuang Zou, Ya-Ping Hu, Xiao-Xue Yin, Wen-Long Liu, Tao Li & Zhanhua Liang

  2. Department of Neurosurgery, The Second Affiliated Hospital of Dalian Medical University, 467 Zhong Shan Road, Dalian, 116023, People’s Republic of China

    Yu-Long Lan

  3. Department of Physiology, Dalian Medical University, 9 Western District, Lvshun South Road, Dalian, 116044, People’s Republic of China

    Shuang Zou & Yu-Long Lan

  4. Department of Pharmacy, Dalian Medical University, Dalian, 116044, People’s Republic of China

    Yu-Long Lan

Authors
  1. Shuang Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu-Long Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ya-Ping Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiao-Xue Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wen-Long Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhanhua Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Tao Li or Zhanhua Liang.

Ethics declarations

Conflict of interest

The authors declare no competing financial interests.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Informed consent

For this type of study written formal consent is not required.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zou, S., Lan, YL., Hu, YP. et al. Update on the clinical application of deep brain stimulation in sleep dysfunction of Parkinson’s disease. Acta Neurol Belg 118, 351–359 (2018). https://doi.org/10.1007/s13760-018-0971-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13760-018-0971-3

Keywords

Search

Navigation