DOI QR코드

DOI QR Code

Effects of Acute Transcranial Direct Current Stimulation on Muscle Endurance of the Lower Extremities for Young Healthy Adults

일회성 경두개 직류전기자극(tDCS) 적용이 젊은 성인의 하지 근지구력에 미치는 영향

  • Park, Shin-Young (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Ko, Do-Kyung (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Jeong, Hyeong Do (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Lee, Hanall (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Lee, Hyungwoo (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Kim, Chanki (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • An, Seungho (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Kim, Jiyoung (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Moon, Bosung (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Son, Jee-Soo (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Lee, Dohyeon (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Lee, Eui-Young (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Lee, Ju Hak (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Im, Seungbin (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Tan, Yuan (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Jeon, Kyoungkyu (Department of Human Movement Science, Graduate School of Incheon National University) ;
  • Kang, Nyeonju (Department of Human Movement Science, Graduate School of Incheon National University)
  • Received : 2022.08.29
  • Accepted : 2022.09.19
  • Published : 2022.09.30

Abstract

Objective: The purpose of this study was to investigate the effect of acute transcranial direct current stimulation (tDCS) on the isokinetic muscular endurance of the lower extremity for young adults. Method: Thirteen young adults performed isokinetic fatigue tasks for two experimental conditions including real tDCS and sham stimulation protocols. Before and after the task, the tensiomyography was used for evaluating muscle contraction characteristics of vastus medialis and semitendinosus. Paired t-test was performed to compare the fatigue index, changes in maximum radial displacement (∆Dm), delay time (∆Tc), and velocity of contraction (∆Vc) between tDCS conditions. Results: We found no significant differences in the fatigue index between real and sham conditions. In addition, the analyses identified no significant different values of ∆Dm, ∆Tc, and ∆Vc in the vastus medialis and semitendinosus between real and sham conditions. Conclusion: These findings suggest that the tDCS protocols may have no acute effect on lower limb muscle endurance for young adults. Future studies should consider the long-term effects of repetitive tDCS sessions, various stimulation positions, exercise tasks, and participant characteristics to more clearly understand the effect of tDCS on muscle endurance of lower extremities.

Keywords

References

  1. Alix-Fages, C., Romero-Arenas, S., Castro-Alonso, M., Colomer-Poveda, D., Rio-Rodriguez, D., Jerez-Martinez, A. ... & Marquez, G. (2019). Short-term effects of anodal transcranial direct current stimulation on endurance and maximal force production: A systematic review and meta-analysis. Journal of Clinical Medicine, 8(4), 536. https://doi.org/10.3390/jcm8040536
  2. Alonzo, A., Brassil, J., Taylor, J. L., Martin, D. & Loo, C. K. (2012). Daily transcranial direct current stimulation (tDCS) leads to greater increases in cortical excitability than second daily transcranial direct current stimulation. Brain Stimulation, 5(3), 208-213. https://doi.org/10.1016/j.brs.2011.04.006
  3. Angius, L., Hopker, J. & Mauger, A. R. (2017). The ergogenic effects of transcranial direct current stimulation on exercise performance. Frontiers in Physiology, 8, 90.
  4. Angius, L., Mauger, A., Hopker, J., Pascual-Leone, A., Santarnecchi, E. & Marcora, S. (2018). Bilateral extracephalic transcranial direct current stimulation improves endurance performance in healthy individuals. Brain Stimulation, 11(1), 108-117. https://doi.org/10.1016/j.brs.2017.09.017
  5. Barwood, M. J., Butterworth, J., Goodall, S., House, J. R., Laws, R., Nowicky, A. & Corbett, J. (2016). The effects of direct current stimulation on exercise performance, pacing and perception in temperate and hot environments. Brain Stimulation, 9(6), 842-849. https://doi.org/10.1016/j.brs.2016.07.006
  6. Bornheim, S., Thibaut, A., Beaudart, C., Maquet, P., Croisier, J. L. & Kaux, J. F. (2022). Evaluating the effects of tDCS in stroke patients using functional outcomes: a systematic review. Disability and Rehabilitation, 44(1), 13-23. https://doi.org/10.1080/09638288.2020.1759703
  7. Brunoni, A. R., Nitsche, M. A., Bolognini, N., Bikson, M., Wagner, T., Merabet, L. ... & Pascual-Leone, A. (2012). Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimulation, 5(3), 175-195. https://doi.org/10.1016/j.brs.2011.03.002
  8. Callahan, D. M. & Kent-Braun, J. A. (2010). Neural Activation Does Not Mediate Age-Related Reductions in the Torque-Velocity Relationship in Healthy Older Adults. Medicine & Science in Sports & Exercise, 42(10), 108-109. https://doi.org/10.1249/01.MSS.0000389487.85057.31
  9. Chaieb, L., Antal, A. & Paulus, W. (2008). Gender-specific modulation of short-term neuroplasticity in the visual cortex induced by transcranial direct current stimulation. Visual Neuroscience, 25(1), 77-81. https://doi.org/10.1017/S0952523808080097
  10. Chinzara, T., Buckingham, G. & Harris, D. (2021). Transcranial direct current stimulation (tDCS) and sporting performance: A systematic review and meta-analysis of tDCS effects on physical endurance, muscular strength, and visuomotor skills. The European Journal of Neuroscience.
  11. Cogiamanian, F., Marceglia, S., Ardolino, G., Barbieri, S. & Priori, A. (2007). Improved isometric force endurance after transcranial direct current stimulation over the human motor cortical areas. European Journal of Neuroscience, 26(1), 242-249. https://doi.org/10.1111/j.1460-9568.2007.05633.x
  12. Colzato, L. S., Nitsche, M. A. & Kibele, A. (2017). Noninvasive brain stimulation and neural entrainment enhance athletic performance -a review. Journal of Cognitive Enhancement, 1(1), 73-79. https://doi.org/10.1007/s41465-016-0003-2
  13. de Moura, M. C. D. S., Hazime, F. A., Marotti Aparicio, L. V., Grecco, L. A., Brunoni, A. R. & Hasue, R. H. (2019). Effects of transcranial direct current stimulation (tDCS) on balance improvement: a systematic review and meta-analysis. Somatosensory & Motor Research, 36(2), 122-135. https://doi.org/10.1080/08990220.2019.1624517
  14. de Paula Simola, R. A., Raeder, C., Wiewelhove, T., Kellmann, M., Meyer, T., Pfeiffer, M. & Ferrauti, A. (2016). Muscle mechanical properties of strength and endurance athletes and changes after one week of intensive training. Journal of Electromyography and Kinesiology, 30, 73-80. https://doi.org/10.1016/j.jelekin.2016.05.005
  15. de Souza, L. M. L., Cabral, H. V., de Oliveira, L. F. & Vieira, T. M. (2018). Motor units in vastus lateralis and in different vastus medialis regions show different firing properties during low-level, isometric knee extension contraction. Human Movement Science, 58, 307-314. https://doi.org/10.1016/j.humov.2017.12.012
  16. Dumel, G., Bourassa, M. E., Charlebois-Plante, C., Desjardins, M., Doyon, J., Saint-Amour, D. & De Beaumont, L. (2018). Motor learning improvement remains 3 months after a multisession anodal tDCS intervention in an aging population. Frontiers in Aging Neuroscience, 335.
  17. Dutta, A., Krishnan, C., Kantak, S. S., Ranganathan, R. & Nitsche, M. A. (2015). Recurrence quantification analysis of surface electromyogram supports alterations in motor unit recruitment strategies by anodal transcranial direct current stimulation. Restorative Neurology and Neuroscience, 33(5), 663-669. https://doi.org/10.3233/RNN-140469
  18. Enoka, R. M. & Duchateau, J. (2016). Translating fatigue to human performance. Medicine and Science in Sports and Exercise, 48(11), 2228. https://doi.org/10.1249/MSS.0000000000000929
  19. Eo, E. & Hwang, B. (2017). The Comparison of Contractile Properties between Knee Flexor and Extensor Muscles in Highschool Basketball Players using Tensiomyography (TMG). Journal of Sport and Leisure Studies, 387-394.
  20. Galvez, V., Alonzo, A., Martin, D. & Loo, C. K. (2013). Transcranial direct current stimulation treatment protocols: should stimulus intensity be constant or incremental over multiple sessions? International Journal of Neuropsychopharmacology, 16(1), 13-21. https://doi.org/10.1017/S1461145712000041
  21. Gandevia, S. C. (2001). Spinal and supraspinal factors in human muscle fatigue. Physiological Reviews.
  22. Garcia-Manso, J. M., Rodriguez-Ruiz, D., Rodriguez-Matoso, D., de Saa, Y., Sarmiento, S. & Quiroga, M. (2011). Assessment of muscle fatigue after an ultra-endurance triathlon using tensiomyography (TMG). Journal of Sports Sciences, 29(6), 619-625. https://doi.org/10.1080/02640414.2010.548822
  23. Gualano, A., Bozza, T., Lopes De Campos, P., Roschel, H., Dos Santos Costa, A., Luiz Marquezi, M. ... & Herbert Lancha Junior, A. (2011). Branched-chain amino acids supplementation enhances exercise capacity and lipid oxidation during endurance exercise after muscle glycogen depletion. The Journal of Sports Medicine and Physical Fitness, 51(1), 82-88.
  24. Han, G. & Kim, H. (2003). Isokinetic Evaluation of Knee Muscles in Female Youth Group. Korean Journal of Sport Biomechanics, 1-12.
  25. Kan, B., Dundas, J. E. & Nosaka, K. (2013). Effect of transcranial direct current stimulation on elbow flexor maximal voluntary isometric strength and endurance. Applied Physiology, Nutrition, and Metabolism, 38(7), 734-739. https://doi.org/10.1139/apnm-2012-0412
  26. Krause, B. & Cohen Kadosh, R. (2014). Not all brains are created equal: the relevance of individual differences in responsiveness to transcranial electrical stimulation. Frontiers in Systems Neuroscience, 8, 25.
  27. Lattari, E., Budde, H., Paes, F., Neto, G. A. M., Appolinario, J. C., Nardi, A. E. ... & Machado, S. (2018). Effects of aerobic exercise on anxiety symptoms and cortical activity in patients with panic disorder: a pilot study. Clinical Practice and Epidemiology in Mental Health: CP & EMH, 14, 11. https://doi.org/10.2174/1745017901814010011
  28. Liu, J. Z., Zhang, L., Yao, B., Sahgal, V. & Yue, G. H. (2005). Fatigue induced by intermittent maximal voluntary contractions is associated with significant losses in muscle output but limited reductions in functional MRI-measured brain activation level. Brain Research, 1040(1-2), 44-54. https://doi.org/10.1016/j.brainres.2005.01.059
  29. Lohr, C., Braumann, K. M., Reer, R., Schroeder, J. & Schmidt, T. (2018). Reliability of tensiomyography and myotonometry in detecting mechanical and contractile characteristics of the lumbar erector spinae in healthy volunteers. European Journal of Applied Physiology, 118(7), 1349-1359. https://doi.org/10.1007/s00421-018-3867-2
  30. Loturco, I., Pereira, L. A., Kobal, R., Kitamura, K., Ramirez-Campillo, R., Zanetti, V. ... & Nakamura, F. Y. (2016). Muscle contraction velocity: a suitable approach to analyze the functional adaptations in elite soccer players. Journal of Sports Science & Medicine, 15(3), 483.
  31. Lu, P., Hanson, N. J., Wen, L., Guo, F. & Tian, X. (2021). Transcranial Direct Current Stimulation Enhances Muscle Strength of Non-dominant Knee in Healthy Young Males. Frontiers in Physiology, 12.
  32. Macgregor, L. J., Ditroilo, M., Smith, I. J., Fairweather, M. M. & Hunter, A. M. (2016). Reduced radial displacement of the gastrocnemius medialis muscle after electrically elicited fatigue. Journal of Sport Rehabilitation, 25(3), 241-247. https://doi.org/10.1123/jsr.2014-0325
  33. Macgregor, L. J., Hunter, A. M., Orizio, C., Fairweather, M. M. & Ditroilo, M. (2018). Assessment of skeletal muscle contractile properties by radial displacement: the case for tensiomyography. Sports Medicine, 48(7), 1607-1620. https://doi.org/10.1007/s40279-018-0912-6
  34. Machado, D. G. d. S., Unal, G., Andrade, S. M., Moreira, A., Altimari, L. R., Brunoni, A. R. ... & Okano, A. H. (2019). Effect of transcranial direct current stimulation on exercise performance: a systematic review and meta-analysis. Brain Stimulation, 12(3), 593-605. https://doi.org/10.1016/j.brs.2018.12.227
  35. Martin-Rodriguez, S., Loturco, I., Hunter, A. M., Rodriguez-Ruiz, D. & Munguia-Izquierdo, D. (2017). Reliability and measurement error of tensiomyography to assess mechanical muscle function: A systematic review. The Journal of Strength & Conditioning Research, 31(12), 3524-3536. https://doi.org/10.1519/JSC.0000000000002250
  36. Martin-San Agustin, R., Medina-Mirapeix, F., Casana-Granell, J., GarciaVidal, J. A., Lillo-Navarro, C. & Benitez-Martinez, J. C. (2020). Tensiomyographical responsiveness to peripheral fatigue in quadriceps femoris. PeerJ, 8, e8674. doi:10.7717/peerj.8674
  37. Mauger, A. R. (2013). Fatigue is a pain-the use of novel neurophysiological techniques to understand the fatigue-pain relationship. In (Vol. 4, pp. 104): Frontiers Media SA.
  38. Mendes, B., Firmino, T., Oliveira, R., Neto, T., Cruz-Montecinos, C., Cerda, M. ... & Freitas, S. R. (2020). Effects of knee flexor submaximal isometric contraction until exhaustion on semitendinosus and biceps femoris long head shear modulus in healthy individuals. Scientific Reports, 10(1), 1-8. https://doi.org/10.1038/s41598-019-56847-4
  39. Muthalib, M., Kan, B., Nosaka, K. & Perrey, S. (2013). Effects of transcranial direct current stimulation of the motor cortex on prefrontal cortex activation during a neuromuscular fatigue task: an fNIRS study. In Oxygen Transport to Tissue XXXV (pp. 73-79): Springer.
  40. Napadow, V., Dhond, R., Conti, G., Makris, N., Brown, E. N. & Barbieri, R. (2008). Brain correlates of autonomic modulation: combining heart rate variability with fMRI. Neuroimage, 42(1), 169-177. https://doi.org/10.1016/j.neuroimage.2008.04.238
  41. Nitsche, M. A., Fricke, K., Henschke, U., Schlitterlau, A., Liebetanz, D., Lang, N. ... & Paulus, W. (2003). Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. The Journal of Physiology, 553(1), 293-301. https://doi.org/10.1113/jphysiol.2003.049916
  42. Okano, A. H., Fontes, E. B., Montenegro, R. A., Farinatti, P. D. T. V., Cyrino, E. S., Li, L. M. ... & Noakes, T. D. (2015). Brain stimulation modulates the autonomic nervous system, rating of perceived exertion and performance during maximal exercise. British Journal of Sports Medicine, 49(18), 1213-1218. https://doi.org/10.1136/bjsports-2012-091658
  43. Pageaux, B. (2014). The psychobiological model of endurance performance: an effort-based decision-making theory to explain selfpaced endurance performance. Sports Medicine, 44(9), 1319. https://doi.org/10.1007/s40279-014-0198-2
  44. Paillard, T. & Noe, F. (2020). Does monopedal postural balance differ between the dominant leg and the non-dominant leg? A review. Human Movement Science, 74, 102686. https://doi.org/10.1016/j.humov.2020.102686
  45. Papale, A. E. & Hooks, B. M. (2018). Circuit changes in motor cortex during motor skill learning. Neuroscience, 368, 283-297. https://doi.org/10.1016/j.neuroscience.2017.09.010
  46. Park, S., Ryu, Y. & Kim, K. (2014). Correlation between Balance Ability, Muscle Strength, and Muscle Endurance, in Taekwondo, Soccer, and Gymnastics Athletes. Korean Journal of Sport Biomechanics, 24(1), 85-93. https://doi.org/10.5103/KJSB.2014.24.1.085
  47. Perotto, A. O. (2011). Anatomical guide for the electromyographer: the limbs and trunk: Charles C Thomas Publisher.
  48. Pincivero, D., Lephart, S. & Karunakara, R. (1997). Reliability and precision of isokinetic strength and muscular endurance for the quadriceps and hamstrings. International Journal of Sports Medicine, 18(02), 113-117. https://doi.org/10.1055/s-2007-972605
  49. Pol, F., Salehinejad, M. A., Baharlouei, H. & Nitsche, M. A. (2021). The effects of transcranial direct current stimulation on gait in patients with Parkinson's disease: a systematic review. Translational Neurodegeneration, 10(1), 1-19. https://doi.org/10.1186/s40035-020-00225-y
  50. Raeder, C., Wiewelhove, T., Simola, R. A. D. P., Kellmann, M., Meyer, T., Pfeiffer, M. & Ferrauti, A. (2016). Assessment of fatigue and recovery in male and female athletes after 6 days of intensified strength training. The Journal of Strength & Conditioning Research, 30(12), 3412-3427. https://doi.org/10.1519/JSC.0000000000001427
  51. Reis, J., Schambra, H. M., Cohen, L. G., Buch, E. R., Fritsch, B., Zarahn, E. ... & Krakauer, J. W. (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proceedings of the National Academy of Sciences, 106(5), 1590-1595. https://doi.org/10.1073/pnas.0805413106
  52. Robertson, C. V. & Marino, F. E. (2016). A role for the prefrontal cortex in exercise tolerance and termination. Journal of Applied Physiology, 120(4), 464-466. https://doi.org/10.1152/japplphysiol.00363.2015
  53. Rostami, M., Mosallanezhad, Z., Ansari, S., Ehsani, F., Kidgell, D., Nourbakhsh, M. R. ... & Jaberzadeh, S. (2020). Multi-session anodal transcranial direct current stimulation enhances lower extremity functional performance in healthy older adults. Experimental Brain Research, 238(9), 1925-1936. https://doi.org/10.1007/s00221-020-05827-6
  54. Russell, M., Goodman, T., Wang, Q., Groshong, B. & Lyeth, B. G. (2014). Gender differences in current received during transcranial electrical stimulation. Frontiers in Psychiatry, 5, 104.
  55. Samani, M. M., Agboada, D., Jamil, A., Kuo, M. F. & Nitsche, M. A. (2019). Titrating the neuroplastic effects of cathodal transcranial direct current stimulation (tDCS) over the primary motor cortex. Cortex, 119, 350-361. https://doi.org/10.1016/j.cortex.2019.04.016
  56. Sanchez-Kuhn, A., Perez-Fernandez, C., Canovas, R., Flores, P. & SanchezSanted, F. (2017). Transcranial direct current stimulation as a motor neurorehabilitation tool: an empirical review. Biomedical Engineering Online, 16(1), 1-22. https://doi.org/10.1186/s12938-016-0292-9
  57. Senefeld, J., Yoon, T. & Hunter, S. K. (2017). Age differences in dynamic fatigability and variability of arm and leg muscles: Associations with physical function. Experimental Gerontology, 87, 74-83. https://doi.org/10.1016/j.exger.2016.10.008
  58. Stagg, C. J. & Nitsche, M. A. (2011). Physiological basis of transcranial direct current stimulation. The Neuroscientist, 17(1), 37-53. https://doi.org/10.1177/1073858410386614
  59. Thongsawang, S., Krataithong, T., ChorCharoenying, S., Norchai, P. & Nokkaew, N. (2021). Applying Cordyceps sinensis to Boost Endurance Performance in Long-Distance Runners. Journal of Exercise Physiology Online, 24(3), 1-13.
  60. Van Cutsem, J., Marcora, S., De Pauw, K., Bailey, S., Meeusen, R. & Roelands, B. (2017). The effects of mental fatigue on physical performance: a systematic review. Sports Medicine, 47(8), 1569-1588. https://doi.org/10.1007/s40279-016-0672-0
  61. Vaseghi, B., Zoghi, M. & Jaberzadeh, S. (2014). Does anodal transcranial direct current stimulation modulate sensory perception and pain? A meta-analysis study. Clinical Neurophysiology, 125(9), 1847-1858. https://doi.org/10.1016/j.clinph.2014.01.020
  62. Vitor-Costa, M., Okuno, N. M., Bortolotti, H., Bertollo, M., Boggio, P. S., Fregni, F. & Altimari, L. R. (2015). Improving cycling performance: transcranial direct current stimulation increases time to exhaustion in cycling. PloS One, 10(12), e0144916. https://doi.org/10.1371/journal.pone.0144916
  63. Wan, J. J., Qin, Z., Wang, P. Y., Sun, Y. & Liu, X. (2017). Muscle fatigue: general understanding and treatment. Experimental & Molecular Medicine, 49(10), e384-e384. https://doi.org/10.1038/emm.2017.194
  64. Wang, L., Wang, C., Yang, H., Shao, Q., Niu, W., Yang, Y. & Zheng, F. (2022). Halo Sport Transcranial Direct Current Stimulation Improved Muscular Endurance Performance and Neuromuscular Efficiency During an Isometric Submaximal Fatiguing Elbow Flexion Task. Frontiers in Human Neuroscience, 16.
  65. Williams, P. S., Hoffman, R. L. & Clark, B. C. (2013). Preliminary evidence that anodal transcranial direct current stimulation enhances time to task failure of a sustained submaximal contraction. PloS One, 8(12), e81418. https://doi.org/10.1371/journal.pone.0081418
  66. Workman, C. D., Fietsam, A. C. & Rudroff, T. (2020). Transcranial direct current stimulation at 4 mA induces greater leg muscle fatigability in women compared to men. Brain Sciences, 10(4), 244. https://doi.org/10.3390/brainsci10040244
  67. Workman, C. D., Kamholz, J. & Rudroff, T. (2019). The tolerability and efficacy of 4 mA transcranial direct current stimulation on leg muscle fatigability. Brain Sciences, 10(1), 12. https://doi.org/10.3390/brainsci10010012
  68. Yavari, F., Jamil, A., Samani, M. M., Vidor, L. P. & Nitsche, M. A. (2018). Basic and functional effects of transcranial electrical stimulation (tES)-an introduction. Neuroscience & Biobehavioral Reviews, 85, 81-92. https://doi.org/10.1016/j.neubiorev.2017.06.015
  69. Zhang, R., Lam, C. L., Peng, X., Zhang, D., Zhang, C., Huang, R. & Lee, T. M. (2021). Efficacy and acceptability of transcranial direct current stimulation for treating depression: A meta-analysis of randomized controlled trials. Neuroscience & Biobehavioral Reviews, 126, 481-490. https://doi.org/10.1016/j.neubiorev.2021.03.026