Login Register Cart 0
Generic placeholder image

Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

The Multifactorial Role of Pre-supplementary Motor Area Stimulation in the Freezing of Gait: An Alternative Strategy to the Classical Drug-Target Approach

Author(s): Mevhibe Saricaoglu, Lutfu Hanoglu, Guven Toprak, Nesrin Helvaci Yilmaz and Burak Yulug*

Volume 22, Issue 5, 2022

Published on: 03 February, 2022

Page: [518 - 524] Pages: 7

DOI: 10.2174/1871530321666211014170107

Price: $65

Abstract

Introduction: The pre-supplementary motor area (Pre-SMA) plays a pivotal role in the control of voluntary motor control and freezing of gait (FOG) pathophysiological mechanism. Here, we aimed to modulate if the pre-SMA would have beneficial effects on motor and behavioural outcomes in freezing of gait. To test this hypothesis, we examined the left pre-SMA stimulating effect of repetitive Transcranial Magnetic Stimulation (rTMS) on motor, cognitive and behavioural parameters in Parkinson’s patients with FOG.

Methods: The study included 20 Parkinson’s patients with FOG (3 females, 17 males) who received the left Pre-SMA rTMS procedure. The clinical assessments were performed on all patients at the baseline and the patients were re-evaluated under the same clinical conditions one week after the end of the sessions.

Results & Discussion: We found significant improvements in motor, cognitive and behavioural symptoms (p<0.05). The main finding of our study is that Pre-SMA is an attractive stimulation area leading to critical improvement of symptoms of Parkinson’s patients with FOG.

Conclusion: The high-frequency rTMS stimulation over the left preSMA has a restorative effect on the motor, cognitive and behavioural symptoms of Parkinson’s patients with FOG.

Keywords: Freezing of gait, parkinson’s disease, presupplementary area, repetitive transcranial magnetic stimulation, motor symptoms, cognitive symptoms, behavioural symptoms.

« Previous Next »
Graphical Abstract

[1]
Nachev, P.; Wydell, H.; O'neill, K.; Husain, M.; Kennard, C. The role of the pre-supplementary motor area in the control of action. Neuroimage, 2007, 36 Suppl 2(3-3), 155-163.
[http://dx.doi.org/10.1016/j.neuroimage.2007.03.034]
[2]
Brass, M.; Haggard, P. The what, when, whether model of intentional action. Neuroscientist, 2008, 14(4), 319-325.
[http://dx.doi.org/10.1177/1073858408317417] [PMID: 18660462]
[3]
Forstmann, B.U.; Dutilh, G.; Brown, S.; Neumann, J.; von Cramon, D.Y.; Ridderinkhof, K.R.; Wagenmakers, E.J. Striatum and pre-SMA facilitate decision-making under time pressure. Proc. Natl. Acad. Sci. USA, 2008, 105(45), 17538-17542.
[http://dx.doi.org/10.1073/pnas.0805903105] [PMID: 18981414]
[4]
Escobar Sanabria, D.; Johnson, L.A.; Nebeck, S.D.; Zhang, J.; Johnson, M.D.; Baker, K.B.; Molnar, G.F.; Vitek, J.L. Parkinsonism and vigilance: Alteration in neural oscillatory activity and phase-amplitude coupling in the basal ganglia and motor cortex. J. Neurophysiol., 2017, 118(5), 2654-2669.
[http://dx.doi.org/10.1152/jn.00388.2017] [PMID: 28835526]
[5]
Galvan, A.; Wichmann, T. Pathophysiology of parkinsonism. Clin. Neurophysiol., 2008, 119(7), 1459-1474.
[http://dx.doi.org/10.1016/j.clinph.2008.03.017] [PMID: 18467168]
[6]
Hendrix, C.M.; Campbell, B.A.; Tittle, B.J.; Johnson, L.A.; Baker, K.B.; Johnson, M.D.; Molnar, G.F.; Vitek, J.L. Predictive encoding of motor behavior in the supplementary motor area is disrupted in parkinsonism. J. Neurophysiol., 2018, 120(3), 1247-1255.
[http://dx.doi.org/10.1152/jn.00306.2018] [PMID: 29873615]
[7]
Wang, J.; Johnson, L.A.; Jensen, A.L.; Baker, K.B.; Molnar, G.F.; Johnson, M.D.; Vitek, J.L. Network-wide oscillations in the parkinsonian state: Alterations in neuronal activities occur in the premotor cortex in parkinsonian nonhuman primates. J. Neurophysiol., 2017, 117(6), 2242-2249.
[http://dx.doi.org/10.1152/jn.00011.2017] [PMID: 28228579]
[8]
Linkenkaer-Hansen, K.; Nikulin, V.V.; Palva, S.; Ilmoniemi, R.J.; Palva, J.M. Prestimulus oscillations enhance psychophysical performance in humans. J. Neurosci., 2004, 24(45), 10186-10190.
[http://dx.doi.org/10.1523/JNEUROSCI.2584-04.2004] [PMID: 15537890]
[9]
Yulug, B.; Hanoglu, L.; Tavli, AM.; Yılmaz, NH.; Kılıc, E. The brain protective effect of rtms (repetitive transcranial magnetic stimulation) in depression: a mini-review in animal studies. Med. Chem., 2016, 12(6 ), 500-550.
[http://dx.doi.org/10.2174/1573406411666151005110321]
[10]
Caglayan, A.B.; Beker, M.C.; Caglayan, B.; Yalcin, E.; Caglayan, A.; Yulug, B.; Hanoglu, L.; Kutlu, S.; Doeppner, T.R.; Hermann, D.M.; Kilic, E. Acute and post-acute neuromodulation induces stroke recovery by promoting survival signaling, neurogenesis, and pyramidal tract plasticity. Front. Cell. Neurosci., 2019, 13, 144.
[http://dx.doi.org/10.3389/fncel.2019.00144] [PMID: 31031599]
[11]
Yulug, B.; Hanoglu, L.; Khanmammadov, E.; Duz, O.A.; Polat, B.; Hanoglu, T.; Gunal, M.Y.; Kilic, E. Beyond The Therapeutic Effect of rTMS in Alzheimer’s Disease: A Possible Neuroprotective Role of Hippocampal BDNF?: A Minireview. Mini Rev. Med. Chem., 2018, 18(17), 1479-1485.
[http://dx.doi.org/10.2174/1389557517666170927162537] [PMID: 28971775]
[12]
Lapchak, P.A.; Zhang, J.H. Neuroprotective therapy for stroke and ischemic disease; Springer International Publishing, 2017.
[http://dx.doi.org/10.1007/978-3-319-45345-3]
[13]
Velioglu, H.A.; Hanoglu, L.; Bayraktaroglu, Z.; Toprak, G.; Guler, E.M.; Bektay, M.Y.; Mutlu-Burnaz, O.; Yulug, B. Left lateral parietal rTMS improves cognition and modulates resting brain connectivity in patients with Alzheimer’s disease: Possible role of BDNF and oxidative stress. Neurobiol. Learn. Mem., 2021, 180, 107410.
[http://dx.doi.org/10.1016/j.nlm.2021.107410] [PMID: 33610772]
[14]
Kim, M.S.; Chang, W.H.; Cho, J.W.; Youn, J.; Kim, Y.K.; Kim, S.W.; Kim, Y.H. Efficacy of cumulative high-frequency rTMS on freezing of gait in Parkinson’s disease. Restor. Neurol. Neurosci., 2015, 33(4), 521-530.
[http://dx.doi.org/10.3233/RNN-140489] [PMID: 26409410]
[15]
Daniel, S.E.; Lees, A.J. Parkinson’s Disease Society Brain Bank, London: overview and research. J. Neural Transm. Suppl., 1993, 39, 165-172.
[PMID: 8360656]
[16]
Giladi, N.; Tal, J.; Azulay, T.; Rascol, O.; Brooks, D.J.; Melamed, E.; Oertel, W.; Poewe, W.H.; Stocchi, F.; Tolosa, E. Validation of the freezing of gait questionnaire in patients with Parkinson’s disease. Mov. Disord., 2009, 24(5), 655-661.
[http://dx.doi.org/10.1002/mds.21745] [PMID: 19127595]
[17]
Acaröz-Candan, S.; Çatıker, A.; Özcan, T.Ş. Psychometric properties of the Turkish version of the freezing of gait questionnaire for patients with Parkinson’s disease. Neurol. Sci. Neurophysiol., 2019, 36(1), 44-50.
[http://dx.doi.org/10.5152/NSN.2019.11115]
[18]
Akbostancı, M.C.; Balaban, H.; Atbasoglu, C. Interrater reliability of the turkish version of unified parkinson’s disease rating scale-motor examination subscale and abnormal involuntary movements scale. Parkinson Hast. Hareket. Boz. Der., 2000, 3(2), 7-13. [in Turkish].
[19]
Lin, M.R.; Hwang, H.F.; Hu, M.H.; Wu, H.D.; Wang, Y.W.; Huang, F.C. Psychometric comparisons of the timed up and go, one-leg stand, functional reach, and Tinetti balance measures in community-dwelling older people. J. Am. Geriatr. Soc., 2004, 52(8), 1343-1348.
[http://dx.doi.org/10.1111/j.1532-5415.2004.52366.x] [PMID: 15271124]
[20]
Şahin, F.; Yilmaz, F.; Özmaden, A.; Kotevolu, N.; Şahin, T.; Kuran, B. Reliability and validity of the Turkish version of the Berg Balance Scale. J. Geriatr. Phys. Ther., 2008, 31(1), 32-37.
[http://dx.doi.org/10.1519/00139143-200831010-00006] [PMID: 18489806]
[21]
Güngen, C.; Ertan, T.; Eker, E.; Yaşar, R.; Engin, F. Reliability and validity of the standardized Mini Mental State Examination in the diagnosis of mild dementia in Turkish population. Turk Psikiyatr. Derg., 2002, 13(4), 273-281. [Turkish.].
[PMID: 12794644]
[22]
Karakaş, S.; Erdoğan, E.; Soysal, Ş.; Ulusoy, T.; Ulusoy, Yüceyurt, İ.; Alkan, S. Stroop test tbag form: standardisation for turkish culture, reliability and validity. J. Clin. Psy., 1999, 2, 75-88. [in Turkish].
[23]
Karakaş, S.; Eski, R.; Başar, E. A collection of standardized neuropsychological tests for Turkish culture: BILNOT Battery. 32nd National Neurology Congrees book, Turk. J. Neurol; Ufuk Press: Istanbul, Turkey, 1997. in Turkish
[24]
Öktem, Ö. A verbal test of memory processes: A preliminary Study. Arch. Neuropsychiatry, 1992, 29(4), 196-206. [in Turkish].
[25]
Akça, Kalem, Ş.; Hanağası, H.; Cummings, J.L.; Gürvit, H. Validation study of the Turkish translation of the Neuropsychiatric Inventory (NPI). 21st International Conference of Alzheimer’s Disease International, Istanbul, Turkey. Abstract Book, 2005, pp. 47-58.
[26]
Ertan, T.; Eker, E.; Şar, V. Reliability and validity of Geriatric Depression Scale in Turkish elderly population. Archi. Neuropsychiatry, 1997, 34, 62-71. [in Turkish].
[27]
Ulus, Y.; Durmus, D.; Akyol, Y.; Terzi, Y.; Bilgici, A.; Kuru, O. Reliability and validity of the Turkish version of the Falls Efficacy Scale International (FES-I) in community-dwelling older persons. Arch. Gerontol. Geriatr., 2012, 54(3), 429-433.
[http://dx.doi.org/10.1016/j.archger.2011.06.010] [PMID: 21831462]
[28]
Hanoğlu, L.; Saricaoglu, M.; Toprak, G.; Yılmaz, N.H.; Yuluğ, B. Preliminary findings on the role of high-frequency (5Hz) rTMS stimulation on M1 and pre-SMA regions in Parkinson’s disease. Neurosci. Lett., 2020, 724, 134837.
[http://dx.doi.org/10.1016/j.neulet.2020.134837] [PMID: 32057924]
[29]
Tremblay, P.; Gracco, V.L. Contribution of the pre-SMA to the production of words and non-speech oral motor gestures, as revealed by repetitive transcranial magnetic stimulation (rTMS). Brain Res., 2009, 1268, 112-124.
[http://dx.doi.org/10.1016/j.brainres.2009.02.076] [PMID: 19285972]
[30]
Dvorák, J.; Herdmann, J.; Theiler, R.; Grob, D. Magnetic stimulation of motor cortex and motor roots for painless evaluation of central and proximal peripheral motor pathways. Normal values and clinical application in disorders of the lumbar spine. Spine, 1991, 16(8), 955-961.
[http://dx.doi.org/10.1097/00007632-199108000-00016] [PMID: 1948382]
[31]
Rossi, S.; Hallett, M.; Rossini, P.M.; Pascual-Leone, A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol., 2009, 120(12), 2008-2039.
[http://dx.doi.org/10.1016/j.clinph.2009.08.016] [PMID: 19833552]
[32]
Chung, C.L.; Mak, M.K. Effect of repetitive transcranial magnetic stimulation on physical function and motor signs in parkinson’s disease: a systematic review and meta-analysis. Brain Stimul., 2016, 9(4), 475-487.
[http://dx.doi.org/10.1016/j.brs.2016.03.017] [PMID: 27117282]
[33]
Kim, S.J.; Paeng, S.H.; Kang, S.Y. Stimulation in Supplementary Motor Area Versus Motor Cortex for Freezing of Gait in Parkinson’s Disease. J. Clin. Neurol., 2018, 14(3), 320-326.
[http://dx.doi.org/10.3988/jcn.2018.14.3.320] [PMID: 29856153]
[34]
Bluett, B.; Banks, S.; Cordes, D.; Bayram, E.; Mishra, V.; Cummings, J.; Litvan, I. Neuroimaging and neuropsychological assessment of freezing of gait in Parkinson’s disease. Alzheimers Dement. (N. Y.), 2018, 4, 387-394.
[http://dx.doi.org/10.1016/j.trci.2018.04.010] [PMID: 30211293]
[35]
Heremans, E.; Nieuwboer, A.; Spildooren, J.; Vandenbossche, J.; Deroost, N.; Soetens, E.; Kerckhofs, E.; Vercruysse, S. Cognitive aspects of freezing of gait in Parkinson’s disease: A challenge for rehabilitation. J. Neural Transm. (Vienna), 2013, 120(4), 543-557.
[http://dx.doi.org/10.1007/s00702-012-0964-y] [PMID: 23328947]
[36]
Vandenbossche, J.; Deroost, N.; Soetens, E.; Zeischka, P.; Spildooren, J.; Vercruysse, S.; Nieuwboer, A.; Kerckhofs, E. Conflict and freezing of gait in Parkinson’s disease: support for a response control deficit. Neuroscience, 2012, 206, 144-154.
[http://dx.doi.org/10.1016/j.neuroscience.2011.12.048] [PMID: 22265727]
[37]
Giladi, N.; Hausdorff, J.M. The role of mental function in the pathogenesis of freezing of gait in Parkinson’s disease. J. Neurol. Sci., 2006, 248(1-2), 173-176.
[http://dx.doi.org/10.1016/j.jns.2006.05.015] [PMID: 16780886]
[38]
Etkin, A.; Büchel, C.; Gross, J.J. The neural bases of emotion regulation. Nat. Rev. Neurosci., 2015, 16(11), 693-700.
[http://dx.doi.org/10.1038/nrn4044] [PMID: 26481098]
[39]
Herman, T.; Shema-Shiratzky, S.; Arie, L.; Giladi, N.; Hausdorff, J.M. Depressive symptoms may increase the risk of the future development of freezing of gait in patients with Parkinson’s disease: Findings from a 5-year prospective study. Parkinsonism Relat. Disord., 2019, 60, 98-104.
[http://dx.doi.org/10.1016/j.parkreldis.2018.09.013] [PMID: 30236826]
[40]
Witt, I.; Ganjavi, H.; MacDonald, P. Relationship between Freezing of Gait and Anxiety in Parkinson’s Disease Patients: A Systemic Literature Review. Parkinsons Dis., 2019, 2019, 6836082.
[http://dx.doi.org/10.1155/2019/6836082] [PMID: 31428304]
[41]
Hikosaka, O.; Sakai, K.; Miyauchi, S.; Takino, R.; Sasaki, Y.; Pütz, B. Activation of human presupplementary motor area in learning of sequential procedures: A functional MRI study. J. Neurophysiol., 1996, 76(1), 617-621.
[http://dx.doi.org/10.1152/jn.1996.76.1.617] [PMID: 8836248]
[42]
Sakai, K.; Hikosaka, O.; Miyauchi, S.; Sasaki, Y.; Fujimaki, N.; Pütz, B. Presupplementary motor area activation during sequence learning reflects visuo-motor association. J. Neurosci., 1999, 19(10), RC1.
[http://dx.doi.org/10.1523/JNEUROSCI.19-10-j0002.1999] [PMID: 10234047]
[43]
Lewis, S.J.; Shine, J.M. The next step: a common neural mechanism for freezing of gait. Neuroscientist, 2016, 22(1), 72-82.
[http://dx.doi.org/10.1177/1073858414559101] [PMID: 25398230]
[44]
Lau, H.C.; Rogers, R.D.; Passingham, R.E. Manipulating the experienced onset of intention after action execution. J. Cogn. Neurosci., 2007, 19(1), 81-90.
[http://dx.doi.org/10.1162/jocn.2007.19.1.81] [PMID: 17214565]
[45]
Mars, R.B.; Klein, M.C.; Neubert, F.X.; Olivier, E.; Buch, E.R.; Boorman, E.D.; Rushworth, M.F. Short-latency influence of medial frontal cortex on primary motor cortex during action selection under conflict. J. Neurosci., 2009, 29(21), 6926-6931.
[http://dx.doi.org/10.1523/JNEUROSCI.1396-09.2009] [PMID: 19474319]
[46]
Watanabe, T.; Hanajima, R.; Shirota, Y.; Tsutsumi, R.; Shimizu, T.; Hayashi, T.; Terao, Y.; Ugawa, Y.; Katsura, M.; Kunimatsu, A.; Ohtomo, K.; Hirose, S.; Miyashita, Y.; Konishi, S. Effects of rTMS of pre-supplementary motor area on fronto basal ganglia network activity during stop-signal task. J. Neurosci., 2015, 35(12), 4813-4823.
[http://dx.doi.org/10.1523/JNEUROSCI.3761-14.2015] [PMID: 25810512]
[47]
Mantovani, A.; Lisanby, S.H.; Pieraccini, F.; Ulivelli, M.; Castrogiovanni, P.; Rossi, S. Repetitive transcranial magnetic stimulation (rTMS) in the treatment of obsessive-compulsive disorder (OCD) and Tourette’s syndrome (TS). Int. J. Neuropsychopharmacol., 2006, 9(1), 95-100.
[http://dx.doi.org/10.1017/S1461145705005729] [PMID: 15982444]
[48]
Mantovani, A.; Simpson, H.B.; Fallon, B.A.; Rossi, S.; Lisanby, S.H. Randomized sham-controlled trial of repetitive transcranial magnetic stimulation in treatment-resistant obsessive-compulsive disorder. Int. J. Neuropsychopharmacol., 2010, 13(2), 217-227.
[http://dx.doi.org/10.1017/S1461145709990435] [PMID: 19691873]
[49]
Gomes, P.V.; Brasil-Neto, J.P.; Allam, N.; Rodrigues de Souza, E. A randomized, double-blind trial of repetitive transcranial magnetic stimulation in obsessive-compulsive disorder with three-month follow-up. J. Neuropsychiatry Clin. Neurosci., 2012, 24(4), 437-443.
[http://dx.doi.org/10.1176/appi.neuropsych.11100242] [PMID: 23224449]
[50]
Arumugham, S.S.; Vs, S.; Hn, M.; B, V.; Ravi, M.; Sharma, E.; Thirthalli, J.; Reddy, Y.C.J. Augmentation effect of low-frequency repetitive transcranial magnetic stimulation over presupplementary motor area in obsessive-compulsive disorder: a randomized controlled trial. J. ECT, 2018, 34(4), 253-257.
[http://dx.doi.org/10.1097/YCT.0000000000000509] [PMID: 29901496]
[51]
Pelissolo, A.; Harika-Germaneau, G.; Rachid, F.; Gaudeau-Bosma, C.; Tanguy, M.L.; BenAdhira, R.; Bouaziz, N.; Popa, T.; Wassouf, I.; Saba, G.; Januel, D.; Jaafari, N. Repetitive transcranial magnetic stimulation to supplementary motor area in refractory obsessive-compulsive disorder treatment: a sham-controlled trial. Int. J. Neuropsychopharmacol., 2016, 19(8), pyw025.
[http://dx.doi.org/10.1093/ijnp/pyw025] [PMID: 27207923]

Rights & Permissions Print Cite
Article Metrics
37
1
Wayfinder Image
© 2024 Bentham Science Publishers | Privacy Policy