The site of the Media Sphera Publishers contains materials intended solely for healthcare professionals.
By closing this message, you confirm that you are a certified medical professional or a student of a medical educational institution.

Aftanas L.I.

Research Institute of Physiology and Fundamental Medicine;
Novosibirsk State University, Department of Neurosciences

Brack I.V.

Research Institute of Physiology and Fundamental Medicine

Kulikova K.I.

Research Institute of Physiology and Fundamental Medicine

Filimonova E.A.

Research Institute of Physiology and Fundamental Medicine

Dzemidovich S.S.

Research Institute of Physiology and Fundamental Medicine

Piradov M.A.

Research Center of Neurology

Suponeva N.A.

Research Center of Neurology

Poidasheva A.G.

Research Center of Neurology

Clinical and neurophysiological effects of dual-target high-frequency rTMS over the primary motor and prefrontal cortex in Parkinson’s disease

Authors:

Aftanas L.I., Brack I.V., Kulikova K.I., Filimonova E.A., Dzemidovich S.S., Piradov M.A., Suponeva N.A., Poidasheva A.G.

More about the authors

Read: 4339 times


To cite this article:

Aftanas LI, Brack IV, Kulikova KI, et al. Clinical and neurophysiological effects of dual-target high-frequency rTMS over the primary motor and prefrontal cortex in Parkinson’s disease. S.S. Korsakov Journal of Neurology and Psychiatry. 2020;120(5):29‑36. (In Russ.)
https://doi.org/10.17116/jnevro202012005129

Recommended articles:
Effect of uric acid on the progression of Parkinson’s disease: Myth or reality?. S.S. Korsakov Journal of Neurology and Psychiatry. 2025;(7):7-14
Oxidative stress and depression in Parkinson’s disease. S.S. Korsakov Journal of Neurology and Psychiatry. 2025;(9):131-138
Musculoskeletal diso­rders in patients with Parkinson’s disease. S.S. Korsakov Journal of Neurology and Psychiatry. 2025;(11-2):6-10
«Brain—gut—microbiome» axis in patients with Parkinson’s disease. S.S. Korsakov Journal of Neurology and Psychiatry. 2025;(11-2):18-23

References:

  1. Pringsheim T, Jette N, Frolkis A, Steeves TD. The prevalence of Parkinson’s disease: A systematic review and meta‐analysis. Movement Disorders. 2014;29:1583-1590. https://doi.org/10.1002/mds.25945
  2. Aarsland D, Creese B, Chaudhuri KR. A new tool to identify patients with Parkinson’s disease at increased risk of dementia. The Lancet Neurology. 2017;16(8):576-578.  https://doi.org/10.1016/S1474-4422(17)30170-9
  3. He W, Fong PY, Leung TWH, Huang YZ. Protocols of non-invasive brain stimulation for neuroplasticity induction. Neuroscience letters. 2020 Feb 6;719:133437  https://doi.org/10.1016/j.neulet.2018.02.045
  4. Chervyakov AV, Chernyavsky AY, Sinitsyn DO, Piradov MA. Possible Mechanisms Underlying the Therapeutic Effects of Transcranial Magnetic Stimulation. Front Hum Neurosci. 2015;9:303.  https://doi.org/10.3389/fnhum.2015.00303
  5. Peng Z, Zhou C, Xue S, Bai J, Yu S, Li X, Wang H, Tan Q. Mechanism of Repetitive Transcranial Magnetic Stimulation for Depression. Shanghai Arch Psychiatry. 2018;30(2):84-92.  https://doi.org/10.11919/j.issn.1002-0829.217047
  6. Yulug B, Hanoglu L, Kilic E, Polat B, Schabitz WR. The Neuroprotective Role of Repetitive Transcranial Magnetic Stimulation (rTMS) for Neurodegenerative Diseases: A Short Review on Experimental Studies. Mini-Reviews in Medicinal Chemistry. 2016;16:1269. https://doi.org/10.2174/1389557516666160523145154
  7. Dinkelbach L, Brambilla M, Manenti R, Brem AK. Non-invasive brain stimulation in Parkinson’s disease: Exploiting crossroads of cognition and mood. Neuroscience&Biobehavioral Reviews. 2017;75:407-418.  https://doi.org/10.1016/j.neubiorev.2017.01.021
  8. Boggio PS, Fregni F, Bermpohl F, Mansur CG, Rosa M, Rumi DO, Barbosa ER, Odebrecht Rosa M, Pascual-Leone A, Rigonatti SP, Marcolin MA, Araujo Silva MT. Effect of repetitive TMS and fluoxetine on cognitive function in patients with Parkinson’s disease and concurrent depression. Movement Disorders. 2005;20(9):1178-1184. https://doi.org/10.1002/mds.20508
  9. Kimura H, Kurimura M, Kurokawa K, Nagaoka U, Arawaka S, Wada M, Kawanami T, Kurita K, Kato T. A Comprehensive Study of Repetitive Transcranial Magnetic Stimulation in Parkinson’s Disease. ISRN Neurology. 2011;2011:845453. https://doi.org/10.5402/2011/845453
  10. Manenti R, Brambilla M, Benussi A, Rosini S, Cobelli C, Ferrari C, Petesi M, Orizio I, Padovani A, Borroni B, Cotelli M. Mild cognitive impairment in Parkinson’s disease is improved by transcranial direct current stimulation combined with physical therapy. Movement Disorders. 2016;31:715-724.  https://doi.org/10.1002/mds.26561
  11. Benninger DH, Iseki K, Kranick S, Luckenbaugh DA, Houdayer E, Hallett M. Controlled study of 50-Hz repetitive transcranial magnetic stimulation for the treatment of Parkinson disease. Neurorehabilitation and neural repair. 2012;26(9):1096-1105. https://doi.org/10.1177/1545968312445636
  12. Cocchi L, Zalesky A, Nott Z, Whybird G, Fitzgerald PB, Breakspear M. Transcranial magnetic stimulation in obsessive-compulsive disorder: A focus on network mechanisms and state dependence. Neuroimage Clin. 2018;19:661-674.  https://doi.org/10.1016/j.nicl.2018.05.029
  13. Lefaucheur JP, André-Obadia N, Antal A, Ayache SS, Baeken C, Benninger DH, Cantello RM, Cincotta M, de Carvalho M, De Ridder D, Devanne H, Di Lazzaro V, Filipović SR, Hummel FC, Jääskeläinen SK, Kimiskidis VK, Koch G, Langguth B, Nyffeler T, Oliviero A, Padberg F, Poulet E, Rossi S, Rossini PM, Rothwell JC, Schönfeldt-Lecuona C, Siebner HR, Slotema CW, Stagg CJ, Valls-Sole J, Ziemann U, Paulus W, Garcia-Larrea L. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS), Clinical Neurophysiology. 2014;125(11):2150-2206. https://doi.org/10.1016/j.clinph.2014.05.021
  14. Shirota Y, Ohtsu H, Hamada M, Enomoto H, Ugawa Y. Supplementary motor area stimulation for Parkinson disease A randomized controlled study. Neurology. 2013;80(15):1400-1405. https://doi.org/10.1212/WNL.0b013e31828c2f66
  15. Goodwill AM, Lum JAG, Hendy AM, Muthalib M, Johnson L, Albein-Urios N, Teo WP. Using non-invasive transcranial stimulation to improve motor and cognitive function in Parkinson’s disease: a systematic review and meta-analysis. Scientific Reports.2017;7:14840. https://doi.org/10.1038/s41598-017-13260-z
  16. Maruo T, Hosomi K, Shimokawa T, Kishima H, Oshino S, Morris S, Kageyama Y, Yokoe M, Yoshimine T, Saitoh Y. High-frequency repetitive transcranial magnetic stimulation over the primary foot motor area in Parkinson’s disease. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation. 2013;6(6):884-891.  https://doi.org/10.1016/j.brs.2013.05.002
  17. Lanoue AC, Blatt GJ, Soghomonian JJ. Decreased parvalbumin mRNA expression in dorsolateral prefrontal cortex in Parkinson′ s disease. Brain research. 2013;1531:37-47.  https://doi.org/10.1016/j.brainres.2013.07.025
  18. Huang C, Tang C, Feigin A, Lesser M, Ma Y, Pourfar M, Ma Y, Pourfar M, Dhawan V, Eidelberg D. Changes in network activity with the progression of Parkinson’s disease. Brain: A Journal of Neurology. 2007;130(07):1834-1846. https://doi.org/10.1093/brain/awm086
  19. Hosokai Y, Nishio Y, Hirayama K, Takeda A, Ishioka T, Sawada Y, Suzuki K, Itoyama Y, Takahashi S, Fukuda H, Mori E. Distinct patterns of regional cerebral glucose metabolism in Parkinson’s disease with and without mild cognitive impairment. Movement Disorders. 2009;24(6):854-862.  https://doi.org/10.1002/mds.22444
  20. Hattori T, Orimo S, Aoki S, Ito K, Abe O, Amano A, Sato R, Sakai K, Mizusawa H. Cognitive status correlates with white matter alteration in Parkinson’s disease. Human brain mapping. 2012;33(3):727-739.  https://doi.org/10.1002/hbm.21245
  21. Melzer TR, Watts R, MacAskill MR, Pitcher TL, Livingston L, Keenan RJ, Dalrymple-Alford JC, Anderson TJ. Grey matter atrophy in cognitively impaired Parkinson’s disease. Journal of Neurology, Neurosurgery & Psychiatry. 2012;83(2):188-194.  https://doi.org/10.1136/jnnp-2011-300828
  22. Pal E, Nagy F, Aschermann Z, Balazs E, Kovacs N. The impact of left prefrontal repetitive transcranial magnetic stimulation on depression in Parkinson’s disease: A randomized, double‐blind, placebo‐controlled study. Movement Disorders. 2010;25(14):2311-2317. https://doi.org/10.1002/mds.23270
  23. Yokoe M, Mano T, Maruo T, Hosomi K, Shimokawa T, Kishima H, Oshino S, Morris S, Kageyama Y, Goto Y, Shimizu T, Mochizuki H, Yoshimine T, Saitoh Y. The optimal stimulation site for high-frequency repetitive transcranial magnetic stimulation in Parkinson’s disease: A double-blind crossover pilot study. Journal of Clinical Neuroscience. 2018;47:72-78.  https://doi.org/10.1016/j.jocn.2017.09.023
  24. Lomarev MP, Kanchana S, Bara-Jimenez W, Iyer M, Wassermann EM, Hallett M. Placebo‐controlled study of rTMS for the treatment of Parkinson’s disease. Movement Disorders. 2006;21(3):325-331.  https://doi.org/10.1002/mds.20713
  25. Brys M, Fox MD, Agarwal S, Biagioni M, Dacpano G, Kumar P, Shukla AW. Multifocal repetitive TMS for motor and mood symptoms of Parkinson disease: a randomized trial. Neurology. 2016;10: 1108-1212. https://doi.org/10.1212/WNL.0000000000003279
  26. Chou YH, Hickey PT, Sundman M, Song AW, Chen NK. Effects of repetitive transcranial magnetic stimulation on motor symptoms in Parkinson disease: a systematic review and meta-analysis. JAMA Neurol. 2015;72(4):432-440.  https://doi.org/10.1001/jamaneurol.2014.4380
  27. Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. Journal of Neurology, Neurosurgery & Psychiatry. 1992;55(3):181-184.  https://doi.org/10.1136/jnnp.55.3.181
  28. Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality. Neurology. 1967;17(5):427-442.  https://doi.org/10.1212/01.wnl.0000405146.06300.91
  29. Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE. Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Movement Disorders. 2010;25(15):2649-2653. https://doi.org/10.1002/mds.23429
  30. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dobel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N; Movement Diorder Society UPDRS Devision Task Force. Movement Disorder Society‐sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS‐UPDRS): Scale presentation and clinimetric testing results. Movement disorders. 2008;23(15):2129-2170. https://doi.org/10.1002/mds.22340
  31. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry. 1961;4(6):561-571.  https://doi.org/10.1001/archpsyc.1961.01710120031004
  32. Hamilton M. A rating scale for depression. Journal of Neurology, Neurosurgery&Psychiatry. 1960;23(1):56.  https://doi.org/10.1136/jnnp.23.1.56
  33. Lovibond PF, Lovibond SH. The structure of negative emotional states: Comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behaviour Research and Therapy. 1995;33(3):335-343.  https://doi.org/10.1016/0005-7967(94)00075-U
  34. Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, Di Iorio R, Di Lazzaro V, Ferreri F, Fitzgerald PB, George MS, Hallett M, Lefaucheur JP, Langguth B, Matsumoto H, Miniussi C, Nitsche MA, Pascual-Leone A, Paulus W, Rossi S, Rothwell JC, Siebner HR, Ugawa Y, Walsh V, Ziemann U. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clinical Neurophysiology. 2015;126(6):1071-1107. https://doi.org/10.1016/j.clinph.2015.02.001
  35. Chervyakov AV, Piradov MA, Nazarova MA, Savitskaya NG, Chernikova LA, Konovalov RN. Mapping of motor representation of m. abductor pollicis brevis in healthy volunteers using navigational transcranial magnetic stimulation NBS eXima Nexstim. Annaly klinicheskoi i eksperimental’noi nevrologii. 2012;6(3):14-17. (In Russ.).
  36. Groppa S, Oliviero A, Eisen A, Quartarone A, Cohen LG, Mall V, Kaelin-Lang A, Mima T, Rossi S, Thickbroom GW, Rossini PM, Ziemann U, Valls-Solé J, Siebner HR. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clinical Neurophysiology. 2012;123(5):858-882.  https://doi.org/10.1016/j.clinph.2012.01.010
  37. Gao LL, Wu T. The study of brain functional connectivity in Parkinson’s disease. Transl Neurodegener. 2016;5:18.  https://doi.org/10.1186/s40035-016-0066-0
  38. Ghabra MB, Hallett M, Wassermann EM. Simultaneous repetitive transcranial magnetic stimulation does not speed fine movement in PD. Neurology. 1999;52(4):768-768.  https://doi.org/10.1212/WNL.52.4.768
  39. Tergau F, Wassermann EM, Paulus W, Ziemann U. Lack of clinical improvement in patients with Parkinson’s disease after low and high frequency repetitive transcranial magnetic stimulation. Electroencephalography and Clinical Neurophysiology. 1999;51:281-288. 
  40. Pallanti S, Marras A. Transcranial Magnetic Stimulation Treatment for Motor Symptoms in Parkinson’s Disease: A Review of Two Decades of Studies. Alzheimers Disease & Parkinsonism. 2015;5:191.  https://doi.org/10.4172/2161-0460.1000191
  41. Koch G, Brusa L, Caltagirone C, Olivieri M, Peppe A, Tiraboschi P, Stanzione P. Subthalamic deep brain stimulation improves time perception in Parkinson’s disease. NeuroReport. 2004;15(6):1071-1073. https://doi.org/10.1097/00001756-200404290-00028
  42. Benninger DH, Berman BD, Houdayer E, Pal N, Luckenbaugh DA, Schneider L, Miranda S, Hallett M. Intermittent theta-burst transcranial magnetic stimulation for treatment of Parkinson disease. Neurology. 2011;76(7):601-609.  https://doi.org/10.1212/WNL.0b013e31820ce6bb
  43. Rektorova I, Sedlackova S, Telecka S, Hlubocky A, Rektor I. Dorsolateral Prefrontal Cortex: A Possible Target for Modulating Dyskinesias in Parkinson’s Disease by Repetitive Transcranial Magnetic Stimulation. International Journal of Biomedical Imaging. 2008;2008:372125. https://doi.org/10.1155/2008/372125

Email Confirmation

An email was sent to test@gmail.com with a confirmation link. Follow the link from the letter to complete the registration on the site.

Email Confirmation

We use cооkies to improve the performance of the site. By staying on our site, you agree to the terms of use of cооkies. To view our Privacy and Cookie Policy, please. click here.