Immediate Effects of High-Frequency Repetitive Transcranial Magnetic Stimulation Combined with Task-Specific Training in Individuals with Parkinson’s Disease: a Preliminary Study

Authors

  • Thanakamchokchai J Motor Control and Neural Plasticity Laboratory, Faculty of Physical Therapy
  • Tretriluxana J Motor Control and Neural Plasticity Laboratory, Faculty of Physical Therapy
  • Pakaprot N Department of Physiology
  • Pisarnpong A Movement Disorder Clinic, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Thailand
  • Fisher BE Division of Biokinesiology and Physical Therapy, Southern California University, USA

Keywords:

transcranial magnetic stimulation, brain stimulation, bradykinesia, Parkinson’s disease, task performance

Abstract

Objectives: This study examined the immediate effects of a single-session of high-frequency repetitive transcranial magnetic stimulation (HF-rTMS) combined with task-specific training (TST) on reach-to-grasp (RTG) performance in individuals with Parkinson’s disease (PD).

Study design: Matched-pair experimental design

Setting: Motor Control and Neural Plasticity Laboratory, Faculty of Physical Therapy, Mahidol University

Subjects: Twenty patients with mild to moderate severity of PD (Hoehn &Yahr stage I-III) participated in the study.

Methods: Participants were allocated into two groups. The experimental group received HF-rTMS to the left-primary motor cortex (M1) combined with TST of RTG, while the control group received only HF-rTMS to left-M1. Before and immediately post intervention, right-hand RTG performance was measured under no barrier and barrier conditions. Additionally, cortical silent period (CSP) was determined to verify the effects of HF-rTMS.

Results: There were no significant differences between the two groups for both RTG performance and CSP duration.  In the control group, there was a significant decrease (p = 0.03) in movement time immediately after HF-rTMS for a barrier condition.  Moreover, significant differences in absolute time to maximum aperture (TAmax) (p = 0.04) and temporal transport-grasp coordination (Tmax) (p = 0.04) were observed. A significantly longer CSP in the control group (p = 0.02) confirmed the effects of HF-rTMS. In contrast, the experimental group showed a significant prolonged in TAmax (p = 0.04) and Tmax (p = 0.05).

Conclusion: The findings in the experimental group indicated that the TST of RTG was not sufficient to augment the effects of HF-rTMS that may be the results of the complex task of RTG performance covering the aspect of RTG execution, planning, and transport-grasp coordination.

Keywords: transcranial magnetic stimulation, brain stimulation, bradykinesia, Parkinson’s disease, task performance

Author Biographies

Thanakamchokchai J, Motor Control and Neural Plasticity Laboratory, Faculty of Physical Therapy

+66 2 441 5450; Fax: +66 2 441 5454

Tretriluxana J, Motor Control and Neural Plasticity Laboratory, Faculty of Physical Therapy

 



Pakaprot N, Department of Physiology


Faculty of MedicineSiriraj Hospital, Mahidol University, 2 Wanglang Road Bangkoknoi, Bangkok 10700, Thailand
Email: narawut.pak@mahidol.ac.th
Phone: +66 868864334

Pisarnpong A, Movement Disorder Clinic, Division of Neurology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Thailand

Movement Disorder Clinic, Division of Neurology, Department of Medicine, Faculty of MedicineSiriraj Hospital
Faculty of MedicineSiriraj Hospital, Mahidol University, 2 Wanglang Road Bangkoknoi, Bangkok 10700, Thailand
Email: apisarnpong@yahoo.com
Phone: +66 818454143

Fisher BE, Division of Biokinesiology and Physical Therapy, Southern California University, USA

Division of Biokinesiology and Physical Therapy, Southern California University
1540 Alcazar St., CHP 155, Los Angeles, CA 90089-9006, USA.
Email: bfisher@pt.usc.edu
Phone: (323) 442-2796

References

Janicak PG, Dokucu ME. Transcranial magnetic stimulation for the treatment of major depression. Neuropsychiatr Dis Treat. 2015; 11:1549-60.

Thanakamchokchai J, Tretriluxana J, Pakaprot N, Pisarnpong A, Fisher BE. Effects of high-frequency repetitive transcranial magnetic stimulation on reach-to-grasp performance in individuals with Parkinson’s disease: a preliminary study. Exp Brain Res. 2020; 238:1827–37.

Tung YC, Lai CH, Liao CD, Huang SW, Liou TH, Chen HC. Repetitive transcranial magnetic stimulation of lower limb motor function in patients with stroke: a systematic review and meta-analysis of randomized controlled trials. Clin Rehabil. 2019;33:1102-12.

Tretriluxana J, Kantak S, Tretriluxana S, Wu AD, Fisher BE. Improvement in paretic arm reach-to-grasp following low frequency repetitive transcranial magnetic stimulation depends on object size: a pilot study. Stroke Res Treat. 2015:498169. doi: 10.1155/2015/498169.

Lefaucheur JP, Drouot X, Von Raison F, Menard-Lefaucheur I, Cesaro P, Nguyen JP. Improvement of motor performance and modulation of cortical excitability by repetitive transcranial magnetic stimulation of the motor cortex in Parkinson’s disease. Clin Neurophysiol. 2004;115:2530-41.

Avenanti A, Coccia M, Ladavas E, Provinciali L, Ceravolo MG. Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke: a randomized trial. Neurology. 2012;78:256-64.

Thanakamchokchai J, Tretriluxana J, Jalayondeja C, Pakaprot N. Immediate effects of low-frequency repetitive transcranial magnetic stimulation to augment task-specific training in sub-acute stroke. KKU Res J. 2015;20:89-100.

Tretriluxana J, Thanakamchokchai J, Jalayondeja C, Pakaprot N, Tretriluxana S. The persisted effects of low-frequency repetitive transcranial magnetic stimulation to augment task-specific induced hand recovery following subacute stroke: extended study. Ann Rehabil Med. 2018;42:777-87.

Jankovic J. Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry. 2008;79:368-76.

Khacharoen S, Tretriluxana J, Chaiyawat P, Pisarnpong A. Impaired reach-to-grasp actions during barrier avoidance in individuals with Parkinson’s disease. J Med Assoc Thai. 2015;98:889-95.

Petzinger GM, Holschneider DP, Fisher BE, McEwen S, Kintz N, Halliday M, et al. The effects of exercise on dopamine neurotransmission in Parkinson’s disease: targeting neuroplasticity to modulate basal ganglia circuitry. Brain Plast. 2015;1:29-39.

Ridding MC, Inzelberg R, Rothwell JC. Changes in excitability of motor cortical circuitry in patients with Parkinson’s disease. Ann Neurol. 1995;37:181-8.

Cantello R, Gianelli M, Bettucci D, Civardi C, De Angelis MS, Mutani R. Parkinson’s disease rigidity: magnetic motor evoked potentials in a small hand muscle. Neurology. 1991;41:1449-56.

Harris-Love ML, Cohen LG. Noninvasive cortical stimulation in neurorehabilitation: a review. Arch Phys Med Rehabil. 2006;87: S84-93.

Randhawa BK, Farley BG, and Boyd LA. Repetitive transcranial magnetic stimulation improves handwriting in Parkinson’s disease. Parkinson’s Dis. 2013:1-9. http://dx.doi.org/10.1155/2013/751925.

Boylan LS, Pullmanb SL, Lisanbyc SH, Spicknalld KE, Sackeimd HA. Repetitive transcranial magnetic stimulation to SMA worsens complex movements in Parkinson’s disease. Clin Neurophysiol. 2001;112:259-64.

lez-Garcı´a NG, Armony JL, Soto J, Trejo D, Alegrı´a MA, Drucker-Colı´n R. Effects of rTMS on Parkinson’s disease: a longitudinal fMRI study. J Neurol. 2011;258:1268-80.

Sullivan GM, Feinn R. Using effect size-or why the p value is not enough. J Grad Med Educ. 2012;4:279-82.

Strafella AP, Ko JH, Grant J, Fraraccio M, Monchi O. Corticostriatal functional interactions in Parkinson’s disease: a rTMS/[11C]raclopride PET study. Eur J Neurosci. 2005;22:2946-52.

Strafella AP, Paus T, Fraraccio M, Dagher A. Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain. 2003;126:2609-15.

Chandharohit T. Effects of amplitude-speed training strategy on reach-to-grasp actions in individuals with Parkinson’s disease [Master’s thesis]. Thailand: [Thailand]: Mahidol University; 2017. p. 30-1.

Goebel S, Mehdorn HM, Leplow B. Strategy instruction in Parkinson’s disease: influence on cognitive performance. Neuropsychologia. 2010;48:574-80.

Yang YR, Tseng CY, Chiou SY, Liao KK, Cheng SJ, Lai KL, et al. Combination of rTMS and treadmill training modulates corticomotor inhibition and improves walking in Parkinson disease: a randomized trial. Neurorehabil Neural Repair. 2013;27:79-86.

Behrmana AL, Cauraughb JH, Lighta KE. Practice as an intervention to improve speeded motor performance and motor learning in Parkinson’s disease. Neurological Sci. 2000;174:127-36.

Jeannerod M. Intersegmental coordination during reaching at natural visual objects. In: Long J, Baddeley A, editors. Attention and performance IX Hillsdale, NJ: Erlbaum; 1981. p.153-69.

Jeannerod M, Arbib MA, Rizzolatti G, Sakata H. Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci. 1995;18:314-20.

Haber SN. Neuroanatomy of reward: a view from the ventral striatum. In: Gottfried JA, editor. Neurobiology of sensation and reward. Boca Raton (FL): CRC Press/Taylor & Francis; 2011. https://www.ncbi.nlm.nih.gov/books/NBK92777/.

Ballard IC, Murty VP, Carter RM, MacInnes JJ, Huettel SA, Adcock RA. Dorsolateral prefrontal cortex drives mesolimbic dopaminergic regions to initiate motivated behavior. J Neurosci. 2011;31:10340-6.

Halsband U, Lange RK. Motor learning in man: a review of functional and clinical studies. J Physiol Paris. 2006;99:414-24.

Petrides M. The role of the mid-dorsolateral prefrontal cortex in working memory. Exp Brain Res. 2000;133:44-54.

Leh SE, Petrides M, Strafella AP. The neural circuitry of executive functions in healthy subjects and Parkinson’s disease. Neuropsychopharmacol. 2010;35:70-85.

McKinlay A, Grace RC, Dalrymple-Alford JC, Roger D. Characteristics of executive function impairment in Parkinson’s disease patients without dementia. J Int Neuropsychol Soc. 2010;16:268-77.

Desmurget M, Grafton ST, Vindras P, Grea H, Turner RS. The basal ganglia network mediates the planning of movement amplitude. Eur J Neurosci. 2004;19:2871-80.

Mouthon A, Taube W. Intracortical inhibition increases during postural task execution in response to balance training. Neuroscience. 2019;401:35-42.

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Published

2020-10-28