The Impact of Transcranial Direct Current Stimulation on Upper-Limb Motor Performance in Healthy Adults: A Systematic Review and Meta-Analysis

Ronak Patel, James Ashcroft, Ashish Patel, Hutan Ashrafian, Adam J Woods, Harsimrat Singh, Ara Darzi, Daniel Richard Leff, Ronak Patel, James Ashcroft, Ashish Patel, Hutan Ashrafian, Adam J Woods, Harsimrat Singh, Ara Darzi, Daniel Richard Leff

Abstract

Background: Transcranial direct current stimulation (tDCS) has previously been reported to improve facets of upper limb motor performance such as accuracy and strength. However, the magnitude of motor performance improvement has not been reviewed by contemporaneous systematic review or meta-analysis of sham vs. active tDCS. Objective: To systematically review and meta-analyse the existing evidence regarding the benefits of tDCS on upper limb motor performance in healthy adults. Methods: A systematic search was conducted to obtain relevant articles from three databases (MEDLINE, EMBASE, and PsycINFO) yielding 3,200 abstracts. Following independent assessment by two reviewers, a total of 86 articles were included for review, of which 37 were deemed suitable for meta-analysis. Results: Meta-analyses were performed for four outcome measures, namely: reaction time (RT), execution time (ET), time to task failure (TTF), and force. Further qualitative review was performed for accuracy and error. Statistically significant improvements in RT (effect size -0.01; 95% CI -0.02 to 0.001, p = 0.03) and ET (effect size -0.03; 95% CI -0.05 to -0.01, p = 0.017) were demonstrated compared to sham. In exercise tasks, increased force (effect size 0.10; 95% CI 0.08 to 0.13, p < 0.001) and a trend towards improved TTF was also observed. Conclusions: This meta-analysis provides evidence attesting to the impact of tDCS on upper limb motor performance in healthy adults. Improved performance is demonstrable in reaction time, task completion time, elbow flexion tasks and accuracy. Considerable heterogeneity exists amongst the literature, further confirming the need for a standardised approach to reporting tDCS studies.

Keywords: healthy; meta-analysis; motor; performance; systematic review; transcranial direct-current stimulation (tDCS).

Copyright © 2019 Patel, Ashcroft, Patel, Ashrafian, Woods, Singh, Darzi and Leff.

Figures

Figure 1
Figure 1
Prisma Flow diagram detailing exclusions throughout each stage of study selection to yield a total of 86 articles for systematic review, 37 of which were meta-analysable. *2 studies (Waters-Metenier et al., ; Apšvalka et al., 2018) provided data for both reaction time and execution time.
Figure 2
Figure 2
Methodological heterogeneity of selected studies showing variability in (A) current density, (B) stimulation duration, and (C) montage arrangement. Bottom left pie chart illustrates the spread of the target area for stimulation. Bottom right pie chart illustrates the corresponding reference electrode location during motor cortex stimulation. PPC, Posterior Parietal Cortex; SMA, Supplementary Motor Area; PMC, Pre-motor Cortex; PFC, Prefrontal Cortex; SOR, Supraorbital Region; HD, High-Definition.
Figure 3
Figure 3
Forest Plot illustrating effect sizes from the comparison in reaction time between tDCS vs. sham. Positive values indicate an increase in reaction time following anodal tDCS whilst negative values indicate a decrease in reaction time. Grey boxes represent the weight given to each study. Error bars represent 95% confidence intervals.
Figure 4
Figure 4
Forest Plot illustrating effect sizes from the comparison in total task time between tDCS vs. sham. Positive values indicate an increase in time taken following anodal tDCS whilst negative values indicate a decrease in time taken. Grey boxes represent the weight given to each study. Error bars represent 95% confidence intervals.
Figure 5
Figure 5
Forest Plot illustrating effect sizes from the comparison in time to elbow flexion task failure between anodal tDCS vs. sham tDCS. Positive values indicate an increase in time to failure following tDCS whilst negative values indicate a decrease in time. Grey boxes represent the weight given to each study. Error bars represent 95% confidence intervals.
Figure 6
Figure 6
Forest Plot illustrating effect sizes from the comparison in strength between (A) anodal tDCS and (B) sham tDCS vs. baseline. Positive values indicate an increase strength following each intervention whilst negative values indicate a decrease in strength. Grey boxes represent the weight given to each study. Error bars represent 95% confidence intervals.
Figure 7
Figure 7
Risk of bias in all 37 studies included for quantitative analysis.

References

    1. Abdelmoula A., Baudry S., Duchateau J. (2016). Anodal transcranial direct current stimulation enhances time to task failure of a submaximal contraction of elbow flexors without changing corticospinal excitability. Neuroscience 322, 94–103. 10.1016/j.neuroscience.2016.02.025
    1. Ambrus G. G., Chaieb L., Stilling R., Rothkegel H., Antal A., Paulus W. (2016). Monitoring transcranial direct current stimulation induced changes in cortical excitability during the serial reaction time task. Neurosci. Lett. 616, 98–104. 10.1016/j.neulet.2016.01.039
    1. Andrade C. (2013). Once- to twice-daily, 3-year domiciliary maintenance transcranial direct current stimulation for severe, disabling, clozapine-refractory continuous auditory hallucinations in schizophrenia. J. ECT 29, 239–242. 10.1097/YCT.0b013e3182843866
    1. Angius L., Hopker J., Mauger A. R. (2017). The ergogenic effects of transcranial direct current stimulation on exercise performance. Front. Physiol. 8:90. 10.3389/fphys.2017.00090
    1. Antal A., Keeser D., Priori A., Padberg F., Nitsche M. A. (2015). Conceptual and procedural shortcomings of the systematic review Evidence That Transcranial Direct Current Stimulation (tDCS) generates little-to-no reliable neurophysiologic effect beyond MEP amplitude modulation in healthy human subjects: a systematic review. Brain Stimul. 8, 846–849. 10.1016/j.brs.2015.05.010
    1. Apšvalka D., Ramsey R., Cross E. S. (2018). Anodal tDCS over primary motor cortex provides no advantage to learning motor sequences via observation. Neural Plast. 2018:1237962. 10.1155/2018/1237962
    1. Arias P., Corral-Bergantiños Y., Robles-García V., Madrid A., Oliviero A., Cudeiro J. (2016). Bilateral tDCS on primary motor cortex: effects on fast arm reaching tasks. PLoS ONE 11:e0160063. 10.1371/journal.pone.0160063
    1. Baker J. M., Rorden C., Fridriksson J. (2010). Using transcranial direct-current stimulation to treat stroke patients with Aphasia. Stroke 41, 1229–1236. 10.1161/STROKEAHA.109.576785
    1. Bandeira I. D., Guimarães R. S. Q., Jagersbacher J. G., Barretto T. L., de Jesus-Silva J. R., Santos S. N., et al. . (2016). Transcranial direct current stimulation in children and adolescents with attention-deficit/hyperactivity disorder (ADHD). J. Child Neurol. 31, 918–924. 10.1177/0883073816630083
    1. Bastani A., Jaberzadeh S. (2012). Does anodal transcranial direct current stimulation enhance excitability of the motor cortex and motor function in healthy individuals and subjects with stroke: a systematic review and meta-analysis. Clin. Neurophysiol. 123, 644–657. 10.1016/j.clinph.2011.08.029
    1. Bikson M., Grossman P., Thomas C., Zannou A. L., Jiang J., Adnan T., et al. . (2016). Safety of transcranial direct current stimulation: evidence based update 2016. Brain Stimul. 9, 641–661. 10.1016/j.brs.2016.06.004
    1. Bindman L. J., Lippold O. C. J., Redfearn J. W. T. (1964). The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long-lasting after-effects. J. Physiol. 172, 369–382. 10.1113/jphysiol.1964.sp007425
    1. Block H., Celnik P. (2013). Stimulating the cerebellum affects visuomotor adaptation but not intermanual transfer of learning. Cereblleum 12, 781–793. 10.1007/s12311-013-0486-7
    1. Boggio P. S., Castro L. O., Savagim E. A., Braite R., Cruz V. C., Rocha R. R., et al. . (2006). Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation. Neurosci. Lett. 404, 232–236. 10.1016/j.neulet.2006.05.051
    1. Breitling C., Zaehle T., Dannhauer M., Bonath B., Tegelbeckers J., Flechtner H. H., et al. . (2016). Improving interference control in ADHD patients with transcranial direct current stimulation (tDCS). Front. Cell. Neurosci. 10:72. 10.3389/fncel.2016.00072
    1. Brunoni A. R., Amadera J., Berbel B., Volz M. S., Rizzerio B. G., Fregni F. (2011). A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. Int. J. Neuropsychopharmacol. 14, 1133–1145. 10.1017/S1461145710001690
    1. Brunoni A. R., Nitsche M. A., Bolognini N., Bikson M., Wagner T., Merabet L., et al. . (2012). Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul. 5, 175–195. 10.1016/j.brs.2011.03.002
    1. Buch E. R., Santarnecchi E., Antal A., Born J., Celnik P. A., Classen J., et al. . (2017). Effects of tDCS on motor learning and memory formation: a consensus and critical position paper. Clin. Neurophysiol. 128, 589–603. 10.1016/j.clinph.2017.01.004
    1. Cantarero G., Spampinato D., Reis J., Ajagbe L., Thompson T., Kulkarni K., et al. . (2015). Cerebellar direct current stimulation enhances on-line motor skill acquisition through an effect on accuracy. J. Neurosci. 35, 3285–3290. 10.1523/JNEUROSCI.2885-14.2015
    1. Carlsen A. N., Eagles J. S., MacKinnon C. D. (2015). Transcranial direct current stimulation over the supplementary motor area modulates the preparatory activation level in the human motor system. Behav. Brain Res. 279, 68–75. 10.1016/j.bbr.2014.11.009
    1. Carter M. J., Maslovat D., Carlsen A. N. (2017). Intentional switches between coordination patterns are faster following anodal-tDCS applied over the supplementary motor area. Brain Stimul. 10, 162–164. 10.1016/j.brs.2016.11.002
    1. Chhatbar P. Y., Chen R., Deardorff R., Dellenbach B., Kautz S. A., George M. S., et al. . (2017). Safety and tolerability of transcranial direct current stimulation to stroke patients - A phase I current escalation study. Brain Stimul. 10, 553–559. 10.1016/j.brs.2017.02.007
    1. Chothia M., Doeltgen S., Bradnam L. V. (2016). Anodal cerebellar direct current stimulation reduces facilitation of propriospinal neurons in healthy humans. Brain Stimul. 9, 364–371. 10.1016/j.brs.2016.01.002
    1. Ciechanski P., Cheng A., Lopushinsky S., Hecker K., Gan L. S., Lang S., et al. . (2017). Effects of transcranial direct-current stimulation on neurosurgical skill acquisition: a randomized controlled trial. World Neurosurg. 108, 876–884.e4. 10.1016/j.wneu.2017.08.123
    1. 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. Eur. J. Neurosci. 26, 242–249. 10.1111/j.1460-9568.2007.05633.x
    1. Convento S., Bolognini N., Fusaro M., Lollo F., Vallar G. (2014). Neuromodulation of parietal and motor activity affects motor planning and execution. CORTEX 57, 51–59. 10.1016/j.cortex.2014.03.006
    1. Cuypers K., Leenus D. J. F., van den Berg F. E., Nitsche M. A., Thijs H., Wenderoth N., et al. . (2013). Is motor learning mediated by tDCS intensity? PLoS ONE 8:e67344. 10.1371/journal.pone.0067344
    1. Dedoncker J., Brunoni A. R., Baeken C., Vanderhasselt M. A. (2016). A systematic review and meta-analysis of the effects of transcranial direct current stimulation (tDCS) over the dorsolateral prefrontal cortex in healthy and neuropsychiatric samples: influence of stimulation parameters. Brain Stimul. 9, 501–517. 10.1016/j.brs.2016.04.006
    1. Doppelmayr M., Pixa N. H., Steinberg F. (2016). Cerebellar, but not motor or parietal, high-density anodal transcranial direct current stimulation facilitates motor adaptation. J. Int. Neuropsychol. Soc. 22, 928–936. 10.1017/S1355617716000345
    1. Doyon J., Bellec P., Amsel R., Penhune V., Monchi O., Carrier J., et al. . (2009). Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav. Brain Res. 199, 61–75. 10.1016/j.bbr.2008.11.012
    1. Doyon J., Song A. W., Karni A., Lalonde F., Adams M. M., Ungerleider L. G. (2002). Experience-dependent changes in cerebellar contributions to motor sequence learning. Proc. Natl. Acad. Sci. U.S.A. 99, 1017–1022. 10.1073/pnas.022615199
    1. Dumel G., Bourassa M.-È., Charlebois-Plante C., Desjardins M., Doyon J., Saint-Amour D., et al. . (2018). Multisession anodal transcranial direct current stimulation induces motor cortex plasticity enhancement and motor learning generalization in an aging population. Clin. Neurophysiol. 129, 494–502. 10.1016/j.clinph.2017.10.041
    1. Dumel G., Bourassa M. E., Desjardins M., Voarino N., Charlebois-Plante C., Doyon J., et al. . (2016). Multisession anodal tDCS protocol improves motor system function in an aging population. Neural Plast. 2016, 15–18. 10.1155/2016/5961362
    1. Edwards D. J., Cortes M., Wortman-Jutt S., Putrino D., Bikson M., Thickbroom G., et al. . (2017). Transcranial direct current stimulation and sports performance. Front. Hum. Neurosci. 11:243. 10.3389/fnhum.2017.00243
    1. Ehsani F., Bakhtiary A. H., Jaberzadeh S., Talimkhani A., Hajihasani A. (2016). Differential effects of primary motor cortex and cerebellar transcranial direct current stimulation on motor learning in healthy individuals: a randomized double-blind sham-controlled study. Neurosci. Res. 112, 10–19. 10.1016/j.neures.2016.06.003
    1. Fagerlund A. J., Hansen O. A., Aslaksen P. M. (2015). Transcranial direct current stimulation as a treatment for patients with fibromyalgia. Pain 156, 62–71. 10.1016/j.pain.0000000000000006
    1. Fenton B. W., Palmieri P. A., Boggio P., Fanning J., Fregni F. (2009). A preliminary study of transcranial direct current stimulation for the treatment of refractory chronic pelvic pain. Brain Stimul. 2, 103–107. 10.1016/j.brs.2008.09.009
    1. Ferrucci R., Brunoni A. R., Parazzini M., Vergari M., Rossi E., Fumagalli M., et al. (2013). Modulating human procedural learning by cerebellar transcranial direct current stimulation centro clinico per la neurostimolazione, le neurotecnologie ed i disordini del movimento, fondazione IRCCS Ca' granda. Cerebellum 12, 485–492. 10.1007/s12311-012-0436-9
    1. Floyer-Lea A., Matthews P. M. (2005). Distinguishable brain activation networks for short- and long-term motor skill learning. J. Neurophysiol. 94, 512–518. 10.1152/jn.00717.2004
    1. Focke J., Kemmet S., Krause V., Keitel A., Pollok B. (2017). Cathodal transcranial direct current stimulation (tDCS) applied to the left premotor cortex (PMC) stabilizes a newly learned motor sequence. Behav. Brain Res. 316, 87–93. 10.1016/j.bbr.2016.08.032
    1. Frazer A., Williams J., Spittles M., Rantalainen T., Kidgell D. (2016). Anodal transcranial direct current stimulation of the motor cortex increases cortical voluntary activation and neural plasticity. Muscle Nerve 54, 903–913. 10.1002/mus.25143
    1. Frazer A. K., Williams J., Spittle M., Kidgell D. J. (2017). Cross-education of muscular strength is facilitated by homeostatic plasticity. Eur. J. Appl. Physiol. 117, 665–677. 10.1007/s00421-017-3538-8
    1. Fregni F., Boggio P. S., Lima M. C., Ferreira M. J. L., Wagner T., Rigonatti S. P., et al. . (2006). A sham-controlled, phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Pain 122, 197–209. 10.1016/j.pain.2006.02.023
    1. Fregni F., Nitsche M., Loo C., Brunoni A., Marangolo P., Leite J., et al. . (2016). Regulatory considerations for the clinical and research use of transcranial direct current stimulation (tDCS): review and recommendations from an expert panel. Clin. Res. Regul. Aff. 32, 22–35. 10.3109/10601333.2015.980944
    1. Furuya S., Klaus M., Nitsche M. A., Paulus W., Altenmüller E. (2014). Ceiling effects prevent further improvement of transcranial stimulation in skilled musicians. J. Neurosci. 34, 13834–13839. 10.1523/JNEUROSCI.1170-14.2014
    1. Galea J. M., Vazquez A., Pasricha N., de Xivry J.-J. O., Celnik P. (2011). Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb. Cortex 21, 1761–1770. 10.1093/cercor/bhq246
    1. Giordano J., Bikson M., Kappenman E. S., Clark V. P., Branch Coslett H., Hamblin M. R., et al. . (2017). Mechanisms and effects of transcranial direct current stimulation. Dose-Response 15:1559325816685467. 10.1177/1559325816685467
    1. Gomes-Osman J., Field-Fote E. C. (2013). Bihemispheric anodal corticomotor stimulation using transcranial direct current stimulation improves bimanual typing task performance. J. Mot. Behav. 45, 361–367. 10.1080/00222895.2013.808604
    1. Goodwill A. M., Reynolds J., Daly R. M., Kidgell D. J. (2013). Formation of cortical plasticity in older adults following tDCS and motor training. Front. Aging Neurosci. 5:87. 10.3389/fnagi.2013.00087
    1. Hardwick R. M., Celnik P. A. (2014). Cerebellar direct current stimulation enhances motor learning in older adults. Neurobiol. Aging 35, 2217–2221. 10.1016/j.neurobiolaging.2014.03.030
    1. Hardwick R. M., Rottschy C., Miall R. C., Eickhoff S. B. (2013). A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 67, 283–297. 10.1016/j.neuroimage.2012.11.020
    1. Hashemirad F., Fitzgerald P. B., Zoghi M., Jaberzadeh S. (2017). Single-session anodal tDCS with small-size stimulating electrodes over frontoparietal superficial sites does not affect motor sequence learning. Front. Hum. Neurosci. 11:153 10.3389/fnhum.2017.00153
    1. Hashemirad F., Zoghi M., Fitzgerald P. B., Jaberzadeh S. (2016). The effect of anodal transcranial direct current stimulation on motor sequence learning in healthy individuals: a systematic review and meta-analysis. Brain Cogn. 102, 1–12. 10.1016/j.bandc.2015.11.005
    1. Heise K.-F., Niehoff M., Feldheim J.-F., Liuzzi G., Gerloff C., Hummel F. C. (2014). Differential behavioral and physiological effects of anodal transcranial direct current stimulation in healthy adults of younger and older age. Front. Aging Neurosci. 6:146. 10.3389/fnagi.2014.00146
    1. Hendy A. M., Kidgell D. J. (2013). Anodal tDCS applied during strength training enhances motor cortical plasticity. Med. Sci. Sport. Exerc. 45, 1721–1729. 10.1249/MSS.0b013e31828d2923
    1. Hendy A. M., Kidgell D. J. (2014). Anodal-tDCS applied during unilateral strength training increases strength and corticospinal excitability in the untrained homologous muscle. Exp. Brain Res. 232:3243. 10.1007/s00221-014-4016-8
    1. Hendy A. M., Teo W., Kidgell D. J. (2015). Anodal transcranial direct current stimulation prolongs the cross-education of strength and corticomotor plasticity. Med. Sci. Sport. Exerc. 47, 1788–1797. 10.1249/MSS.0000000000000600
    1. Herzfeld D. J., Pastor D., Haith A. M., Rossetti Y., Shadmehr R., O'Shea J. (2014). Contributions of the cerebellum and the motor cortex to acquisition and retention of motor memories. Neuroimage 98, 147–158. 10.1016/j.neuroimage.2014.04.076
    1. Higgins J. P. T., Green S. (eds). (2011). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration. Available online at:
    1. Horvath J. C., Carter O., Forte J. D. (2016). No significant effect of transcranial direct current stimulation (tDCS) found on simple motor reaction time comparing 15 different simulation protocols. Neuropsychologia 91, 544–552. 10.1016/j.neuropsychologia.2016.09.017
    1. Huang L., Deng Y., Zheng X., Liu Y. (2019). Transcranial direct current stimulation with halo sport enhances repeated sprint cycling and cognitive performance. Front. Physiol. 10:118. 10.3389/fphys.2019.00118
    1. Hummel F. C., Heise K., Celnik P., Floel A., Gerloff C., Cohen L. G. (2010). Facilitating skilled right hand motor function in older subjects by anodal polarization over the left primary motor cortex. Neurobiol. Aging 31, 2160–2168. 10.1016/j.neurobiolaging.2008.12.008
    1. Jadad A., Moore R., Carroll D., Jenkinson C., Reynolds J., Gavaghan D., et al. . (1996). Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control. Clin. Trials 17, 1–12. 10.1016/0197-2456(95)00134-4
    1. Jenkins I. H., Brooks D. J., Nixon P. D., Frackowiak R. S. J., Passingham F. E. (1994). Motor sequence learning: a study with positron emission tomography. J. Neurosci. 14, 3775–3790. 10.1523/JNEUROSCI.14-06-03775.1994
    1. Kaminski E., Steele C. J., Hoff M., Gundlach C., Rjosk V., Sehm B., et al. . (2016). Transcranial direct current stimulation (tDCS) over primary motor cortex leg area promotes dynamic balance task performance. Clin. Neurophysiol. 127, 2455–2462. 10.1016/j.clinph.2016.03.018
    1. Kan B., Dundas J. E., Nosaka K. (2013). Effect of transcranial direct current stimulation on elbow flexor maximal voluntary isometric strength and endurance. Appl. Physiol. Nutr. Metab. 38, 734–739. 10.1139/apnm-2012-0412
    1. Kang E. K., Paik N.-J. (2011). Effect of a tDCS electrode montage on implicit motor sequence learning in healthy subjects. Exp. Transl. Stroke Med. 3:4. 10.1186/2040-7378-3-4
    1. Kantak S. S., Mummidisetty C. K., Stinear J. W. (2012). Primary motor and premotor cortex in implicit sequence learning - evidence for competition between implicit and explicit human motor memory systems. Eur. J. Neurosci. 36, 2710–2715. 10.1111/j.1460-9568.2012.08175.x
    1. Karni A., Meyer G., Jezzard P., Adams M. M., Turner R., Ungerleider L. G. (1995). Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155–158. 10.1038/377155a0
    1. Karok S., Fletcher D., Witney A. G. (2017). Task-specificity of unilateral anodal and dual-M1 tDCS effects on motor learning. Neuropsychologia 94, 84–95. 10.1016/j.neuropsychologia.2016.12.002
    1. Karok S., Witney A. G. (2013). Enhanced motor learning following task-concurrent dual transcranial direct current stimulation. PLoS ONE 8:e85693. 10.1371/journal.pone.0085693
    1. Kaski D., Dominguez R., Allum J., Islam A., Bronstein A. (2014). Combining physical training with transcranial direct current stimulation to improve gait in Parkinson's disease: a pilot randomized controlled study. Clin. Rehabil. 28, 1115–1124. 10.1177/0269215514534277
    1. Kidgell D. J., Goodwill A. M., Frazer A. K., Daly R. M. (2013). Induction of cortical plasticity and improved motor performance following unilateral and bilateral transcranial direct current stimulation of the primary motor cortex. BMC Neurosci. 14:64. 10.1186/1471-2202-14-64
    1. Koyama S., Tanaka S., Tanabe S., Sadato N. (2015). Dual-hemisphere transcranial direct current stimulation over primary motor cortex enhances consolidation of a ballistic thumb movement. Neurosci. Lett. 588, 49–53. 10.1016/j.neulet.2014.11.043
    1. Krishnan C., Ranganathan R., Kantak S. S., Dhaher Y. Y., Rymer W. Z. (2014). Anodal transcranial direct current stimulation alters elbow flexor muscle recruitment strategies. Brain Stimul. 7, 443–450. 10.1016/j.brs.2014.01.057
    1. Krishnan C., Santos L., Peterson M. D., Ehinger M. (2015). Safety of noninvasive brain stimulation in children and adolescents. Brain Stimul. 8, 76–87. 10.1016/j.brs.2014.10.012
    1. Lampropoulou S. I., Nowicky A. V. (2013). The effect of transcranial direct current stimulation on perception of effort in an isolated isometric elbow flexion task. Motor Control 17, 412–426. 10.1123/mcj.17.4.412
    1. Lang N., Siebner H. R., Ward N. S., Lee L., Nitsche M. A., Paulus W., et al. (2005). How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Europe PMC funders group. Eur. J. Neurosci. 22, 495–504. 10.1111/j.1460-9568.2005.04233.x
    1. Lattari E., Oliveira B. R. R., Monteiro Júnior R. S., Marques Neto S. R., Oliveira A. J., Maranhão Neto G. A., et al. . (2018). Acute effects of single dose transcranial direct current stimulation on muscle strength: a systematic review and meta-analysis. PLoS ONE 13:e0209513. 10.1371/journal.pone.0209513
    1. Leite J., Carvalho S., Fregni F., Gonçalves Ó. F. (2011). Task-specific effects of tDCS-induced cortical excitability changes on cognitive and motor sequence set shifting performance. PLoS ONE 6:e24140. 10.1371/journal.pone.0024140
    1. Liebetanz D., Nitsche M. A., Tergau F., Paulus W. (2002). Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain 125, 2238–2247. 10.1093/brain/awf238
    1. Lindenberg R., Nachtigall L., Meinzer M., Sieg M. M., Flöel A. (2013). Differential effects of dual and unihemispheric motor cortex stimulation in older adults. J. Neurosci. 33, 9176–9183. 10.1523/JNEUROSCI.0055-13.2013
    1. Lindenberg R., Sieg M. M., Meinzer M., Nachtigall L., Flöel A. (2016). Neural correlates of unihemispheric and bihemispheric motor cortex stimulation in healthy young adults. Neuroimage 140, 141–149. 10.1016/j.neuroimage.2016.01.057
    1. Loo C. K., Alonzo A., Martin D., Mitchell P. B., Galvez V., Sachdev P. (2012). Transcranial direct current stimulation for depression: 3-week, randomised, sham-controlled trial. Br. J. Psychiatry 200, 52–59. 10.1192/bjp.bp.111.097634
    1. Lopez-Alonso V., del Olmo F. M., Liew S.-L., Fernández del Olmo M., Cheeran B. (2018). A preliminary comparison of motor learning across different non-invasive brain stimulation paradigms shows no consistent modulations. Front. Neurosci. 1:253 10.3389/fnins.2018.00253
    1. Machado D. G. D. S., Unal G., Andrade S. M., Moreira A., Altimari L. R. (2019). Effect of transcranial direct current stimulation on exercise performance: a systematic review and meta-analysis. Brain Stimul. 12:593–605. 10.1016/j.brs.2018.12.227
    1. Marquez J., Conley A., Karayanidis F., Lagopoulos J., Parsons M. (2015). Anodal direct current stimulation in the healthy aged: effects determined by the hemisphere stimulated. Restor. Neurol. Neurosci. 33, 509–519. 10.3233/RNN-140490
    1. Matsumoto H., Ugawa Y. (2017). Adverse events of tDCS and tACS: a review. Clin. Neurophysiol. Pract. 2, 19–25. 10.1016/j.cnp.2016.12.003
    1. Matsuo A., Maeoka H., Hiyamizu M., Shomoto K., Morioka S., Seki K. (2011). Enhancement of precise hand movement by transcranial direct current stimulation. Neuroreport 22, 78–82. 10.1097/WNR.0b013e32834298b3
    1. Mccambridge A. B., Stinear J. W., Byblow W. D. (2016). Neurophysiological and behavioural effects of dual-hemisphere transcranial direct current stimulation on the proximal upper limb. Exp. Brain Res. 234, 1419–1428. 10.1007/s00221-015-4547-7
    1. Medina J., Cason S. (2017). No evidential value in samples of transcranial direct current stimulation (tDCS) studies of cognition and working memory in healthy populations. Cortex 94, 131–141. 10.1016/j.cortex.2017.06.021
    1. Mizuguchi N., Katayama T., Kanosue K. (2018). The effect of cerebellar transcranial direct current stimulation on a throwing task depends on individual level of task performance. Neuroscience 371:119–125. 10.1016/j.neuroscience.2017.11.048
    1. Naros G., Geyer M., Koch S., Mayr L., Ellinger T., Grimm F., et al. (2016). Enhanced motor learning with bilateral transcranial direct current stimulation: impact of polarity or current flow direction? Clin. Neurophysiol. 127, 2119–2126. 10.1016/j.clinph.2015.12.020
    1. Nikolin S., Huggins C., Martin D., Alonzo A., Loo C. K. (2018). Safety of repeated sessions of transcranial direct current stimulation: a systematic review. Brain Stimul. 11, 278–288. 10.1016/j.brs.2017.10.020
    1. Nilsson J., Lebedev A. V., Rydström A., Lövdén M. (2017). Direct-current stimulation does little to improve the outcome of working memory training in older adults. Psychol. Sci. 28, 907–920. 10.1177/0956797617698139
    1. Nitsche M. A., Jakoubkova M., Thirugnanasambandam N., Schmalfuss L., Hullemann S., Sonka K., et al. . (2010). Contribution of the premotor cortex to consolidation of motor sequence learning in humans during sleep. J. Neurophysiol. 104, 2603–2614. 10.1152/jn.00611.2010
    1. Nitsche M. A., Niehaus L., Hoffmann K. T., Hengst S., Liebetanz D., Paulus W., et al. . (2004). MRI study of human brain exposed to weak direct current stimulation of the frontal cortex. Clin. Neurophysiol. 115, 2419–2423. 10.1016/j.clinph.2004.05.001
    1. Nitsche M. A., Nitsche M. S., Klein C. C., Tergau F., Rothwell J. C., Paulus W. (2003a). Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin. Neurophysiol. 114, 600–604. 10.1016/S1388-2457(02)00412-1
    1. Nitsche M. A., Paulus W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 527, 633–639. 10.1111/j.1469-7793.2000.t01-1-00633.x
    1. Nitsche M. A., Paulus W. (2001). Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57, 1899–1901. 10.1212/WNL.57.10.1899
    1. Nitsche M. A., Schauenburg A., Lang N., Liebetanz D., Exner C., Paulus W., et al. . (2003b). Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J. Cogn. Neurosci. 15, 619–626. 10.1162/089892903321662994
    1. Okano A. H., Fontes E. B., Montenegro R. A., Farinatti P., de T. V., Cyrino E. S., et al. . (2015). Brain stimulation modulates the autonomic nervous system, rating of perceived exertion and performance during maximal exercise. Br. J. Sports Med. 49, 1213–1218. 10.1136/bjsports-2012-091658
    1. Oki K., Mahato N. K., Nakazawa M., Amano S., France C. R., Russ D. W., et al. . (2016). Preliminary evidence that excitatory transcranial direct current stimulation extends time to task failure of a sustained, submaximal muscular contraction in older adults. J. Gerontol. Biol. Sci. Med. Sci. 71, 1109–1112. 10.1093/gerona/glw011
    1. Palm U., Schiller C., Fintescu Z., Obermeier M., Keeser D., Reisinger E., et al. . (2012). Transcranial direct current stimulation in treatment resistant depression: a randomized double-blind, placebo-controlled study. Brain Stimul. 5, 242–251. 10.1016/j.brs.2011.08.005
    1. Palm U., Segmiller F. M., Epple A. N., Freisleder F.-J., Koutsouleris N., Schulte-Körne G., et al. . (2016). Transcranial direct current stimulation in children and adolescents: a comprehensive review. J. Neural Transm. 123, 1219–1234. 10.1007/s00702-016-1572-z
    1. Paneri B., Khadka N., Patel V., Thomas C., Tyler W., Parra L. C., et al. (2015). The tolerability of transcranial electrical stimulation used across extended periods in a naturalistic context by healthy individuals. PeerJ. 3:e1097v2. 10.7287/peerj.preprints.1097v2
    1. Panouilìeres M. T. N., Joundi R. A., Brittain J.-S., Jenkinson N. (2015). The journal of physiology neuroscience C 2015 the authors. J. Physiol. 593, 3645–3655. 10.1113/JP270484
    1. Parikh P. J., Cole K. J. (2014). Effects of transcranial direct current stimulation in combination with motor practice on dexterous grasping and manipulation in healthy older adults. Physiol. Rep. 2:e00255. 10.1002/phy2.255
    1. Park S.-B., Sung D. J., Kim B., Kim S., Han J.-K. (2019). Transcranial direct current Stimulation of motor cortex enhances running performance. PLoS ONE 14:e0211902. 10.1371/journal.pone.0211902
    1. Pixa N. H., Pollok B. (2018). Effects of tDCS on bimanual motor skills: a brief review. Front. Behav. Neurosci. 12:63. 10.3389/fnbeh.2018.00063
    1. Pixa N. H., Steinberg F., Doppelmayr M. (2017a). Effects of high-definition anodal transcranial direct current stimulation applied simultaneously to both primary motor cortices on bimanual sensorimotor performance. Front. Behav. Neurosci. 11:130. 10.3389/fnbeh.2017.00130
    1. Pixa N. H., Steinberg F., Doppelmayr M. (2017b). High-definition transcranial direct current stimulation to both primary motor cortices improves unimanual and bimanual dexterity. Neurosci. Lett. 643, 84–88. 10.1016/j.neulet.2017.02.033
    1. Prichard G., Weiller C., Fritsch B., Reis J. (2014). Effects of different electrical brain stimulation protocols on subcomponents of motor skill learning. Brain Stimul. 7, 532–540. 10.1016/j.brs.2014.04.005
    1. Radel R., Tempest G., Denis G., Besson P., Zory R. (2017). Extending the limits of force endurance: stimulation of the motor or the frontal cortex? Cortex 97, 96–108. 10.1016/j.cortex.2017.09.026
    1. Reis J., Fritsch B. (2011). Modulation of motor performance and motor learning by transcranial direct current stimulation. Curr. Opin. Neurol. 24, 590–596. 10.1097/WCO.0b013e32834c3db0
    1. Reis J., Schambra H. M., Cohen L. G., Buch E. R., Fritsch B., Zarahn E., et al. . (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl. Acad. Sci. U.S.A. 106, 1590–1595. 10.1073/pnas.0805413106
    1. Rroji O., van Kuyck K., Nuttin B., Wenderoth N. (2015). Anodal tDCS over the primary motor cortex facilitates long-term memory formation reflecting use-dependent plasticity. PLoS ONE 10:e0127270. 10.1371/journal.pone.0127270
    1. Rumpf J.-J., Wegscheider M., Hinselmann K., Fricke C., King B. R., Weise D., et al. . (2017). Enhancement of motor consolidation by post-training transcranial direct current stimulation in older people. Neurobiol. Aging 49, 1–8. 10.1016/j.neurobiolaging.2016.09.003
    1. Samaei A., Ehsani F., Zoghi M., Hafez Yosephi M., Jaberzadeh S. (2017). Online and offline effects of cerebellar transcranial direct current stimulation on motor learning in healthy older adults: a randomized double-blind sham-controlled study. Eur. J. Neurosci. 45, 1177–1185. 10.1111/ejn.13559
    1. Saruco E., Di Rienzo F., Nunez-Nagy S., Rubio-Gonzalez M. A., Jackson P. L., Collet C., et al. . (2017). Anodal tDCS over the primary motor cortex improves motor imagery benefits on postural control: a pilot study. Sci. Rep. 7:480. 10.1038/s41598-017-00509-w
    1. Saucedo Marquez C. M., Zhang X., Swinnen S. P., Meesen R., Wenderoth N. (2013). Task-specific effect of transcranial direct current stimulation on motor learning. Front. Hum. Neurosci. 7:333. 10.3389/fnhum.2013.00333
    1. Schambra H. M., Abe M., Luckenbaugh D. A., Reis J., Krakauer J. W., Cohen L. G. (2011). Probing for hemispheric specialization for motor skill learning: a transcranial direct current stimulation study. J. Neurophysiol. 106, 652–661. 10.1152/jn.00210.2011
    1. Schmidt S., Fleischmann R., Bathe-Peters R., Irlbacher K., Brandt S. A. (2013). Evolution of premotor cortical excitability after cathodal inhibition of the primary motor cortex: a sham-controlled serial navigated TMS study. PLoS ONE 8:e57425. 10.1371/journal.pone.0057425
    1. Shimizu R. E., Wu A. D., Samra J. K., Knowlton B. J. (2017). The impact of cerebellar transcranial direct current stimulation (tDCS) on learning fine-motor sequences. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 372:20160050. 10.1098/rstb.2016.0050
    1. Simonsmeier B. A., Grabner R. H., Hein J., Krenz U., Schneider M. (2018). Electrical brain stimulation (tES) improves learning more than performance: a meta-analysis. Neurosci. Biobehav. Rev. 84, 171–181. 10.1016/j.neubiorev.2017.11.001
    1. Sohn M. K., Kim B. O., Song H. T. (2012). Effect of stimulation polarity of transcranial direct current stimulation on non-dominant hand function. Ann. Rehabil. Med. 36, 1–7. 10.5535/arm.2012.36.1.1
    1. Stagg C. J., Jayaram G., Pastor D., Kincses Z. T., Matthews P. M., Johansen-Berg H. (2011). Polarity and timing-dependent effects of transcranial direct current stimulation in explicit motor learning. Neuropsychologia 49, 800–804. 10.1016/j.neuropsychologia.2011.02.009
    1. Summers R. L. S., Chen M., Hatch A., Kimberley T. J., Perrey S., Brighina F., et al. . (2018). Cerebellar transcranial direct current stimulation modulates corticospinal excitability during motor training. Front. Hum. Neurosci. 12:118. 10.3389/fnhum.2018.00118
    1. Tadini L., El-Nazer R., Brunoni A. R., Williams J., Carvas M., Boggio P., et al. . (2011). Cognitive, mood, and electroencephalographic effects of noninvasive cortical stimulation with weak electrical currents. J. ECT 27, 134–140. 10.1097/YCT.0b013e3181e631a8
    1. Tan A., Ashrafian H., Scott A. J., Mason S. E., Harling L., Athanasiou T., et al. . (2016). Robotic surgery: disruptive innovation or unfulfilled promise? A systematic review and meta-analysis of the first 30 years. Surg. Endosc. 30, 4330–52. 10.1007/s00464-016-4752-x
    1. Taubert M., Stein T., Kreutzberg T., Stockinger C., Hecker L., Focke A., et al. . (2016). Remote effects of non-invasive cerebellar stimulation on error processing in motor re-learning. Brain Stimul. 9, 692–699. 10.1016/j.brs.2016.04.007
    1. Tecchio F., Zappasodi F., Assenza G., Tombini M., Vollaro S., Barbati G., et al. . (2010). Anodal transcranial direct current stimulation enhances procedural consolidation. J. Neurophysiol. 104, 1134–1140. 10.1152/jn.00661.2009
    1. Toni I., Krams M., Turner R., Passingham R. (1998). The time course of changes during motor sequence learning: a whole-brain fMRI study. Neuroimage 8, 50–61. 10.1006/nimg.1998.0349
    1. Ungerleider L. G., Doyon J., Karni A. (2002). Imaging brain plasticity during motor skill learning. Neurobiol. Learn. Mem. 78, 553–564. 10.1006/nlme.2002.4091
    1. van Tulder M., Furlan A., Bombardier C., Bouter L. (2003) Editorial Board of the Cochrane Collaboration Back Review G. Updated Method Guidelines for Systematic Reviews in the Cochrane Collaboration Back Review Group. Spine 28, 1290–1299. 10.1097/
    1. Vergallito A., Romero Lauro L. J., Bonandrini R., Zapparoli L., Danelli L., Berlingeri M. (2018). What is difficult for you can be easy for me. Effects of increasing individual task demand on prefrontal lateralization: a tDCS study. Neuropsychologia 109, 283–294. 10.1016/j.neuropsychologia.2017.12.038
    1. Vines B. W., Cerruti C., Schlaug G. (2008a). Dual-hemisphere tDCS facilitates greater improvements for healthy subjects' non-dominant hand compared to uni-hemisphere stimulation. BMC Neurosci. 9:103. 10.1186/1471-2202-9-103
    1. Vines B. W., Nair D., Schlaug G. (2008b). Modulating activity in the motor cortex affects performance for the two hands differently depending upon which hemisphere is stimulated. Eur. J. Neurosci. 28, 1667–1673. 10.1111/j.1460-9568.2008.06459.x
    1. Vitor-Costa M., Okuno N. M., Bortolotti H., Bertollo M., Boggio P. S., Fregni F., et al. . (2015). Improving cycling performance: transcranial direct current stimulation increases time to exhaustion in cycling. PLoS ONE 10:e0144916. 10.1371/journal.pone.0144916
    1. Vollmann H., Conde V., Sewerin S., Taubert M., Sehm B., Witte O. W., et al. (2013). Anodal transcranial direct current stimulation (tDCS) over supplementary motor area (SMA) but not pre-SMA promotes short-term visuomotor learning. Brain Stimul. 6, 101–107. 10.1016/j.brs.2012.03.018
    1. Waters S., Wiestler T., Diedrichsen J. (2017). Cooperation not competition: bihemispheric tDCS and fMRI show role for ipsilateral hemisphere in motor learning. J. Neurosci. 37, 7500–7512. 10.1523/JNEUROSCI.3414-16.2017
    1. Waters-Metenier S., Husain M., Wiestler T., Diedrichsen J. (2014). Bihemispheric transcranial direct current stimulation enhances effector-independent representations of motor synergy and sequence learning. J. Neurosci. 34, 1037–1050. 10.1523/JNEUROSCI.2282-13.2014
    1. Westwood S. J., Romani C. (2017). Transcranial direct current stimulation (tDCS) modulation of picture naming and word reading: a meta-analysis of single session tDCS applied to healthy participants. Neuropsychologia 104, 234–249. 10.1016/j.neuropsychologia.2017.07.031
    1. Williams J. A., Pascual-Leone A., Fregni F. (2010). Interhemispheric modulation induced by cortical stimulation and motor training. Phys. Ther. 90, 398–410. 10.2522/ptj.20090075
    1. 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:e81418. 10.1371/journal.pone.0081418
    1. Woods A. J., Antal A., Bikson M., Boggio P. S., Brunoni A. R., Celnik P., et al. . (2016). A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin. Neurophysiol. 127, 1031–1048. 10.1016/j.clinph.2015.11.012
    1. Zhu F. F., Yeung A. Y., Poolton J. M., Lee T. M. C., Leung G. K. K., Masters R. S. W. (2015). Cathodal transcranial direct current stimulation over left dorsolateral prefrontal cortex area promotes implicit motor learning in a golf putting task. Brain Stimul. 8, 784–786. 10.1016/j.brs.2015.02.005
    1. Zimerman M., Heise K. F., Gerloff C., Cohen L. G., Hummel F. C. (2014). Disrupting the ipsilateral motor cortex interferes with training of a complex motor task in older adults. Cereb. Cortex 24, 1030–1036. 10.1093/cercor/bhs385
    1. Zimerman M., Nitsch M., Giraux P., Gerloff C., Cohen L. G., Hummel F. C. (2013). Neuroenhancement of the aging brain: restoring skill acquisition in old subjects. Ann. Neurol. 73, 10–15. 10.1002/ana.23761

Source: PubMed

3
Abonnieren