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| Advance of Transcranial Electrical Stimulation for the Improvement of Motor Performance |
| Zhang Na1, Liu Hui2, Miao Yu1, Qi Fengxue1* |
1(Sports, Exercise and Brain Sciences Laboratory, Beijing Sport University, Beijing 100084, China)
2(China Institute of Sport and Health Science, Beijing Sport University, Beijing 100084, China) |
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Abstract Transcranial electrical stimulation (TES) includes transcranial direct current stimulation, transcranial alternating current stimulation and transcranial random noise stimulation. It is a non-invasive brain stimulation technique using electrodes of different sizes over specific brain regions to modulate cortical neural activity and/or excitability by specific patterns of low-intensity electrical current, thereby strengthen the connections between brain, nerve, and muscle, and improve motor performance. At present, TES technology is going to be utilized to the investigations of sports scientific research. This study first described the neural mechanism of TES over the cerebral cortex, and reviewed the research progress in improving human motor performance of TES over the last two decades in terms of body balance ability, endurance performance muscle fatigue, muscle strength and motor learning. We also reviewed the effects of TES on brain networks functionally connection and discussed the significance of this field in improving motor performance. Finally, we proposed the research perspectives and directions of the TES application in the improvement of motor performance.
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Received: 19 October 2020
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Corresponding Authors:
*E-mail:fengxue.qi@hotmail.com
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[1] Priori A. Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability [J]. Clin Neurophysiol, 2003, 114(4): 589-595.
[2] Merton PA, Morton HB. Stimulation of the cerebral cortex in the intact human subject [J]. Nature, 1980,285: 227-227.
[3] 王静,万有,李小俚. 一种疼痛调控的新手段:经颅直流电刺激 [J]. 中国疼痛医学杂志, 2015, 21(1): 51-55.
[4] Nitsche M A, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation [J]. J Physiol, 2000, 527(3): 633-639.
[5] Antal A, Alekseichuk I, Bikson M, et al. Low intensity transcranial electric stimulation: safety, ethical, legal regulatory and application guidelines [J]. Clin Neurophysiol, 2017, 128(9): 1774-1809.
[6] Paneri B, Adair D, Thomas C, et al. Tolerability of repeated application of transcranial electrical stimulation with limited outputs to healthy subjects [J]. Brain Stimul, 2016, 9(5): 740-754.
[7] 王开元,刘宇. “神经启动”技术增强运动表现 [J]. 体育科学, 2018, 38(1): 96-97.
[8] Reardon S. Neuroscience performance boost paves way for 'brain doping' [J]. Nature, 2016, 531(7594): 283-284.
[9] Mansfield A. Do the warriors owe some of their success to these “brain-zapping” headphones? [DB/OL]. https://www.complex.com/sports/2016/06/warriors-owe-success-brain-zapping-headphones, 2016-06-16/2021-08-15.
[10] Reed T, Cohen KR. Transcranial electrical stimulation (tES) mechanisms and its effects on cortical excitability and connectivity [J]. J Inherit Metab Dis, 2018, 41(6): 1123-1130.
[11] Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans [J]. Neurology, 2001, 57(10): 1899-1901.
[12] Jamil A, Batsikadze G, Kuo H-I, et al. Systematic evaluation of the impact of stimulation intensity on neuroplastic after-effects induced by transcranial direct current stimulation [J]. J Physiol, 2017, 595(4): 1273-1288.
[13] Batsikadze G, Moliadze V, Paulus W, et al. Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans [J]. J Physiol, 2013, 591(7): 1987-2000.
[14] Fertonani A, Miniussi C. Transcranial electrical stimulation: what we know and do not know about mechanisms [J]. Neuroscientist, 2017, 23(2): 109-123.
[15] Monte-Silva K, Kuo MinFang, Hessenthaler S, et al. Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation [J]. Brain Stimul, 2013, 6(3): 424-432.
[16] Liebetanz D, Nitsche MA, Tergau F, et al. Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability [J]. Brain, 2002, 125(10): 2238-2247.
[17] Nitsche MA, Nitsche MS, Klein CC, et al. Level of action of cathodal DC polarisation induced inhibition of the human motor cortex [J]. Clin Neurophysiol, 2003, 114(4): 600-604.
[18] Mosayebi Samani M, Agboada D, Jamil A, et al. Titrating the neuroplastic effects of cathodal transcranial direct current stimulation (tDCS) over the primary motor cortex [J]. Cortex, 2019, 119: 350-361.
[19] Nitsche M A, Bikson M. Extending the parameter range for tDCS: safety and tolerability of 4 mA stimulation [J]. Brain Stimul, 2017, 10(3): 541-542.
[20] Paquette C, Sidel M, Radinska B A, et al. Bilateral transcranial direct current stimulation modulates activation-induced regional blood flow changes during voluntary movement [J]. J Cereb Blood Flow Metab, 2011, 31(10): 2086-2095.
[21] Zheng Xin, Alsop DC, Schlaug G. Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow [J]. NeuroImage, 2011, 58(1): 26-33.
[22] Stagg CJ, Lin RL, Mezue M, et al. Widespread modulation of cerebral perfusion induced during and after transcranial direct current stimulation applied to the left dorsolateral prefrontal cortex [J]. J Neurosci, 2013, 33(28): 11425-11431.
[23] 林博荣,何勍,赵金,等. 经颅电刺激与视功能调控 [J]. 心理科学进展, 2018, 26(9): 1632-1641.
[24] Helfrich RF, Schneider TR, Rach S, et al. Entrainment of brain oscillations by transcranial alternating current stimulation [J]. Curr Biol, 2014, 24(3): 333-339.
[25] Tavakoli AV, Yun K. Transcranial alternating current stimulation (tACS) mechanisms and protocols [J]. Front Cell Neurosci, 2017, 11:214.
[26] 张雪,袁佩君,王莹,等. 知觉相关的神经振荡-外界节律同步化现象 [J]. 生物化学与生物物理进展, 2016, 43(4): 308-315.
[27] Kortuem V, Kadish N E, Siniatchkin M, et al. Efficacy of tRNS and 140 Hz tACS on motor cortex excitability seemingly dependent on sensitivity to sham stimulation [J]. Exp Brain Res, 2019, 237(11): 2885-2895.
[28] Moliadze V, Atalay D, Antal A, et al. Close to threshold transcranial electrical stimulation preferentially activates inhibitory networks before switching to excitation with higher intensities [J]. Brain Stimul, 2012, 5(4): 505-511.
[29] Chaieb L, Antal A, Paulus W. Transcranial alternating current stimulation in the low kHz range increases motor cortex excitability [J]. Restor Neurol Neurosci, 2011, 29(3): 167-175.
[30] Antal A, Paulus W. Transcranial alternating current stimulation (tACS) [J]. Front Hum Neurosci, 2013, 7: 317.
[31] Feurra M, Bianco G, Santarnecchi E, et al. Frequency-dependent tuning of the human motor system induced by transcranial oscillatory potentials [J]. J Neurosci, 2011, 31(34): 12165-12170.
[32] Cappon D, Cappon K, Garraux G, et al. Effects of 10 Hz and 20 Hz transcranial alternating current stimulation on automatic motor control [J]. Brain Stimul, 2016, 9(4): 518-524.
[33] Zaghi S, De Freitas Rezende L, De Oliveira LM, et al. Inhibition of motor cortex excitability with 15 Hz transcranial alternating current stimulation (tACS) [J]. Neurosci Lett, 2010, 479(3): 211-214.
[34] Nowak M, Hinson E, Ede FV, et al. Driving human motor cortical oscillations leads to behaviorally relevant changes in local GABAA inhibition: A tACS-TMS study. [J]. J Neurosci, 2017, 37(17): 4481-4492.
[35] Antal A, Herrmann CS. Transcranial alternating current and random noise stimulation: possible mechanisms [J]. Neural Plasticity, 2016, 2016: 3616807.
[36] Terney D, Chaieb L, Moliadze V, et al. Increasing human brain excitability by transcranial high-frequency random noise stimulation [J]. J Neurosci, 2008, 28(52): 14147-14155.
[37] Moliadze V, Fritzsche G, Antal A. Comparing the efficacy of excitatory transcranial stimulation methods measuring motor evoked potentials [J]. Neural Plasticity, 2014, 2014: 837141.
[38] Laczó B, Antal A, Rothkegel H, et al. Increasing human leg motor cortex excitability by transcranial high frequency random noise stimulation [J]. Restor Neurol Neurosci, 2014, 32(3): 403-410.
[39] Remedios L, Mabil P, Flores-Hernández J, et al. Effects of short-term random noise electrical stimulation on dissociated pyramidal neurons from the cerebral cortex [J]. Neuroscience, 2019, 404: 371-386.
[40] Chaieb L, Antal A, Paulus W. Transcranial random noise stimulation-induced plasticity is NMDA-receptor independent but sodium-channel blocker and benzodiazepines sensitive [J]. Front Neurosci, 2015, 9: 125.
[41] Rostami M, Mosallanezhad Z, Ansari S, et al. Multi-session anodal transcranial direct current stimulation enhances lower extremity functional performance in healthy older adults [J]. Exp Brain Res, 2020, 238(9): 1925-1936.
[42] Xiao Songlin, Wang Baofeng, Zhang Xini, et al. Acute effects of high-definition transcranial direct current stimulation on foot muscle strength, passive ankle kinesthesia, and static balance: a pilot study [J]. J Brain Sci, 2020, 10(4): 246.
[43] Cogiamanian F, Marceglia S, Ardolino G, et al. Improved isometric force endurance after transcranial direct current stimulation over the human motor cortical areas [J]. Eur J Neurosci, 2007, 26(1): 242-249.
[44] Abdelmoula A, Baudry S, Duchateau J. Anodal transcranial direct current stimulation enhances time to task failure of a submaximal contraction of elbow flexors without changing corticospinal excitability [J]. Neuroscience, 2016, 322: 94-103.
[45] Roberto C, Rosario A, Luca F, et al. Ergogenic effects of bihemispheric transcranial direct current stimulation on fitness: a randomized cross-over trial [J]. Int J Sports Med, 2020, 42(1): 66-73.
[46] Sasada S, Endoh T, Ishii T, et al. Differential effects of transcranial direct current stimulation on sprint and endurance cycling [J]. Transl Sports Med, 2020, 3(3): 204-212.
[47] Seidel-Marzi O, Ragert P. Anodal transcranial direct current stimulation reduces motor slowing in athletes and non-athletes [J]. BMC Neurosci, 2020, 21(1): 26.
[48] Faria VLA, Eduardo L, Antônio DJAM, et al. Transcranial direct current stimulation (tDCS) improves back-squat performance in intermediate resistance-training men. [J]. Res Q Exerc Sport, 2020(4): 1-9.
[49] Angius L, Pageaux B, Hopker J, et al. Transcranial direct current stimulation improves isometric time to exhaustion of the knee extensors [J]. Neuroscience, 2016, 339: 363-375.
[50] Angius L, Mauger AR, Hopker J, et al. Bilateral extracephalic transcranial direct current stimulation improves endurance performance in healthy individuals [J]. Brain Stimul, 2018, 11(1): 108-117.
[51] Muthalib M, Kan B, Nosaka K, et al. Effects of transcranial direct current stimulation of the motor cortex on prefrontal cortex activation during a neuromuscular fatigue task: an fNIRS study [J]. Adv Exp Med Biol, 2013, 789: 73-79.
[52] Kan B, Dundas JE, Nosaka K. Effect of transcranial direct current stimulation on elbow flexor maximal voluntary isometric strength and endurance [J]. Appl Physiol Nutr Metab, 2013, 38(7): 734-739.
[53] Wrightson JG, Twomey R, Yeung STY, et al. No effect of tDCS of the primary motor cortex on isometric exercise performance or perceived fatigue [J]. Eur J Neurosci, 2020, 52(2): 2905-2914.
[54] Byrne R, Flood A. The influence of transcranial direct current stimulation on pain affect and endurance exercise [J]. Psychol Sport Exerc, 2019, 45: 101554.
[55] Workman CD, Fietsam AC, Rudroff T. Transcranial direct current stimulation at 4 mA induces greater leg muscle fatigability in women compared to men [J]. J Brain Sci, 2020, 10(4): 244.
[56] Valenzuela PL, Amo C, Sánchez-Martínez G, et al. Transcranial direct current stimulation enhances mood but not performance in elite athletes [J]. Int J Sports Physiol Perform, 2018, 14(3): 310-316.
[57] Mesquita PHC, Lage GM, Franchini E, et al. Bi-hemispheric anodal transcranial direct current stimulation worsens taekwondo-related performance [J]. Hum Mov Sci, 2019, 66: 578-586.
[58] Satoshi T, Takashi H, Manabu H, et al. Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation [J]. Exp Brain Res, 2009, 196(3): 459-465.
[59] Chandramouli K, Rajiv R, Kantak SS, et al. Anodal transcranial direct current stimulation alters elbow flexor muscle recruitment strategies [J]. Brain Stimul, 2014, 7(3): 443-450.
[60] Hendy AM, Kidgell DJ. Anodal-tDCS applied during unilateral strength training increases strength and corticospinal excitability in the untrained homologous muscle [J]. Exp Brain Res, 2014, 232(10): 3243-3252.
[61] Dos Santos GAC, Cavalcante PGL, Sousa TBDS, et al. Effects of peripheral and cerebral electrical stimulation on maximal isometric strength of knee extensors: a randomized clinical trial [J]. Revista Pesquisa em Fisioterapia, 2019, 9(3): 321-330.
[62] Eduardo L, Carlos C, Khede LM, et al. Can Transcranial direct current stimulation improve muscle power in individuals with advanced weight-training experience? [J]. J Strength Cond Res, 2020, 34(1): 97-103.
[63] Vargas VZ, Baptista AF, Pereira GOC, et al. Modulation of isometric quadriceps strength in soccer players with transcranial direct current stimulation: a crossover study [J]. J Strength Cond Res, 2018, 32(5): 1336-1341.
[64] Ahmad HF, Alves DCR, Rozenblit SR, et al. Anodal transcranial direct current stimulation (tDCS) increases isometric strength of shoulder rotators muscles in handball players [J]. Int J Sports Phys Ther, 2017, 12(3): 402-407.
[65] Ali-Mohammad K, Kheradmand SZ, Seyedeh-Saeedeh Y, et al. Transcranial direct current stimulation to enhance athletic performance outcome in experienced bodybuilders [J]. PLoS ONE, 2019, 14(8): e0220363.
[66] Alix- Fages C, García-Ramos A, Calderón-Nadal G, et al. Anodal transcranial direct current stimulation enhances strength training volume but not the force-velocity profile [J]. Eur J Appl Physiol, 2020, 120(8): 1881-1891.
[67] Kazuhei M, Tomofumi Y, Tsuyoshi T, et al. Transcranial direct current stimulation does not affect lower extremity muscle strength training in healthy individuals: a triple-blind, sham-controlled study [J]. Front Neurosci, 2017, 11: 179.
[68] Fan J, Voisin J, Milot MH, et al. Transcranial direct current stimulation over multiple days enhances motor performance of a grip task [J]. Ann Phys Rehabil Med, 2017, 60(5): 329-333.
[69] Ali-Mohammad K, Mohammad N, Seyedeh-Saeedeh Y, et al. Transcranial direct current stimulation to assist experienced pistol shooters in gaining even-better performance scores [J]. Cerebellum, 2019, 18(1): 119-127.
[70] Máximo Z, Kirstin FH, Christian G, et al. Disrupting the ipsilateral motor cortex interferes with training of a complex motor task in older adults. [J]. Cereb Cortex, 2014, 24(4): 1030-1036.
[71] Qi FengXue, Nitsche MA, Zschorlich VR. Modulating observation-execution-related motor cortex activity by cathodal transcranial direct current stimulation [J]. J Brain Sci, 2019, 9(5): 121.
[72] Oliver S, Patrick R. Effects of transcranial direct current stimulation of primary motor cortex on reaction time and tapping performance: A comparison between athletes and non-athletes [J]. Front Hum Neurosci, 2019, 13: 103.
[73] Foerster Á, Dutta A, Kuo MinFang, et al. Effects of anodal transcranial direct current stimulation over lower limb primary motor cortex on motor learning in healthy individuals [J]. Eur J Neurosci, 2018, 47(7): 779-789.
[74] Jin Y, Lee J, Kim S, et al. Noninvasive brain stimulation over M1 and DLPFC cortex enhances the learning of bimanual isometric force control [J]. Hum Mov Sci, 2019, 66: 73-83.
[75] Yamaguchi T, Moriya K, Tanabe S, et al. Transcranial direct-current stimulation combined with attention increases cortical excitability and improves motor learning in healthy volunteers [J]. J Neuroeng Rehabilitation, 2020, 17(1): 23.
[76] Debarnot U, Neveu R, Samaha Y, et al. Acquisition and consolidation of implicit motor learning with physical and mental practice across multiple days of anodal tDCS [J]. Neurobiol Learn Mem, 2019, 164: 107062.
[77] Pollok B, Boysen A-C, Krause V. The effect of transcranial alternating current stimulation (tACS) at alpha and beta frequency on motor learning [J]. Behav Brain Res, 2015, 293: 234-240.
[78] Vanessa K, Anna M, Lars D, et al. Beta band transcranial alternating (tACS) and direct current stimulation (tDCS) applied after initial learning facilitate retrieval of a motor sequence [J]. Front Behav Neurosci, 2016, 2016:10.
[79] Giustiniani A, Tarantino V, Bonaventura R E, et al. Effects of low-gamma tACS on primary motor cortex in implicit motor learning [J]. Behav Brain Res, 2019, 376: 112170.
[80] Sugata H, Yagi K, Yazawa S, et al. Modulation of motor learning capacity by transcranial alternating current stimulation [J]. Neuroscience, 2018, 391: 131-139.
[81] Bologna M, Guerra A, Paparella G, et al. Transcranial alternating current stimulation has frequency-dependent effects on motor learning in healthy humans [J]. Neuroscience, 2019, 411: 130-139.
[82] Berntsen MB, Cooper NR, Hughes G, et al. Prefrontal transcranial alternating current stimulation improves motor sequence reproduction [J]. Behav Brain Res, 2019, 361: 39-49.
[83] Andreas J, Linus H, Arvid K, et al. Motor task-dependent dissociated effects of transcranial random noise stimulation in a finger-tapping task versus a Go/No-Go task on corticospinal excitability and task performance [J]. Front Neurosci, 2019, 13: 161.
[84] Abe T, Miyaguchi S, Otsuru N, et al. The effect of transcranial random noise stimulation on corticospinal excitability and motor performance [J]. Neurosci Lett, 2019, 705: 138-142.
[85] Albuquerque LLD, Fischer KM, Pauls AL, et al. An acute application of transcranial random noise stimulation does not enhance motor skill acquisition or retention in a golf putting task [J]. Hum Mov Sci, 2019, 66: 241-248.
[86] Heuvel MPVD, Sporns O. Network hubs in the human brain [J]. Trends Cogn Sci, 2013, 17(12): 683-696.
[87] Ting TW, Dirk DR, John H, et al. Changing brain networks through non-invasive neuromodulation [J]. Front Hum Neurosci, 2018, 12: 128.
[88] Kunze T, Hunold A, Haueisen J, et al. Transcranial direct current stimulation changes resting state functional connectivity: a large-scale brain network modeling study [J]. NeuroImage, 2016, 140: 174-187.
[89] Krishnamurthy V, Gopinath K, Brown G S, et al. Resting-state fMRI reveals enhanced functional connectivity in spatial navigation networks after transcranial direct current stimulation [J]. Neurosci Lett, 2015, 604: 80-85.
[90] Velicia B, Jamie N, Heidi JB, et al. Modulation of GABA and resting state functional connectivity by transcranial direct current stimulation [J]. eLife, 2015, 4: 28.
[91] Stagg CJ, Bachtiar V, Amadi U, et al. Local GABA concentration is related to network-level resting functional connectivity [J]. eLife, 2014, 3: e01465.
[92] 孟献龙,罗志增,史红斐,等. 经颅直流电刺激对运动脑功能网络特征的影响 [J]. 航天医学与医学工程, 2020, 33(4): 298-305.
[93] Polanía R, Nitsche MA, Paulus W. Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation [J]. Hum Brain Mapp, 2011, 32(8): 1236-1249.
[94] Bernhard S, Alexander S, Judy K, et al. Dynamic modulation of intrinsic functional connectivity by transcranial direct current stimulation [J]. J Neurophysiol, 2012, 108(12): 3253-3263.
[95] Bernhard S, Judy K, Alexander S, et al. A comparison between uni- and bilateral tDCS effects on functional connectivity of the human motor cortex [J]. Front Hum Neurosci, 2013, 7: 183.
[96] Moisa M, Polania R, Grueschow M, et al. Brain network mechanisms underlying motor enhancement by transcranial entrainment of gamma oscillations [J]. J Neurosci, 2016, 36(47): 12053-12065.
[97] Yaqub MA, Woo SW, Hong KS, et al. Effects of HD-tDCS on resting-state functional connectivity in the prefrontal cortex: An fNIRS study [J]. Complexity, 2018, 2018:1-13.
[98] Hunter MA, Coffman BA, Gasparovic C, et al. Baseline effects of transcranial direct current stimulation on glutamatergic neurotransmission and large-scale network connectivity [J]. Brain Res, 2015, 1594: 92-107.
[99] Mencarelli L, Menardi A, Neri F, et al. Impact of network-targeted multichannel transcranial direct current stimulation on intrinsic and network-to-network functional connectivity [J]. J Neurosci Res, 2020, 98(10): 1843-1856. |
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