Immediate Effects of High-Frequency Repetitive Transcranial Magnetic Stimulation Combined with Task-Specific Training in Individuals with Parkinson’s Disease: a Preliminary Study
Keywords:
transcranial magnetic stimulation, brain stimulation, bradykinesia, Parkinson’s disease, task performanceAbstract
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
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.
