A meta-analytical review of transcranial direct current stimulation parameters on upper limb motor learning in healthy older adults and people with Parkinson’s disease
-
Jessie Siew-Pin Leuk
, Kai-En Yow , Clenyce Zi-Xin Tan , Ashlee M. Hendy , Mika Kar-Wing Tan , Tommy Hock-Beng Ng and Wei-Peng Teo
Abstract
Current literature lacks consolidated evidence for the impact of stimulation parameters on the effects of transcranial direct current stimulation (tDCS) in enhancing upper limb motor learning. Hence, we aim to synthesise available methodologies and results to guide future research on the usage of tDCS on upper limb motor learning, specifically in older adults and Parkinson’s disease (PD). Thirty-two studies (Healthy older adults, N = 526, M = 67.25, SD = 4.30 years; PD, N = 216, M = 66.62, SD = 6.25 years) were included in the meta-analysis. All included studies consisted of active and sham protocols. Random effect meta-analyses were conducted for (i) subjects (healthy older adults and PD); (ii) intensity (1.0, 1.5, 2 mA); (iii) electrode montage (unilateral anodal, bilateral anodal, unilateral cathodal); (iv) stimulation site (cerebellum, frontal, motor, premotor, SMA, somatosensory); (v) protocol (online, offline). Significant tDCS effect on motor learning was reported for both populations, intensity 1.0 and 2.0 mA, unilateral anodal and cathodal stimulation, stimulation site of the motor and premotor cortex, and both online and offline protocols. Regression showed no significant relationship between tDCS effects and density. The efficacy of tDCS is also not affected by the number of sessions. However, studies that reported only single session tDCS found significant negative association between duration with motor learning outcomes. Our findings suggest that different stimulation parameters enhanced upper limb motor learning in older adults and PD. Future research should combine tDCS with neuroimaging techniques to help with optimisation of the stimulation parameters, considering the type of task and population.
Acknowledgements
All co-authors are thanked for the conduct of this systematic review and meta-analysis.
-
Author contribution: Conceptualisation-JSPL; Methodology-JSPL, KEY, CZXT, AH, MKWT; Analysis-JSPL, WPT; Manuscript Preparation and Interpretation-JSPL, THBN, WPT; All authors have read and agreed to this version of the manuscript.
-
Research funding: JSPL is supported by Nanyang Technological University (NTU) Research Scholarship.
-
Conflict of interest: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Aloi, D., Jalali, R., Tilsley, P., Miall, R.C., and Fernández-Espejo, D. (2022). tDCS modulates effective connectivity during motor command following; a potential therapeutic target for disorders of consciousness. Neuroimage 247: 118781. https://doi.org/10.1016/j.neuroimage.2021.118781.Search in Google Scholar PubMed PubMed Central
Alonzo, A., Brassil, J., Taylor, J.L., Martin, D., and 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 Stimul. 5: 208–213. https://doi.org/10.1016/j.brs.2011.04.006.Search in Google Scholar PubMed
Barron, H.C. (2021). Neural inhibition for continual learning and memory. Curr. Opin. Neurobiol. 67: 85–94. https://doi.org/10.1016/j.conb.2020.09.007.Search in Google Scholar PubMed PubMed Central
Benninger, D.H., Lomarev, M., Lopez, G., Wassermann, E.M., Li, X., Considine, E., and Hallett, M. (2010). Transcranial direct current stimulation for the treatment of Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 81: 1105–1111. https://doi.org/10.1136/jnnp.2009.202556.Search in Google Scholar PubMed PubMed Central
Beretta, V.S., Conceição, N.R., Nóbrega-Sousa, P., Orcioli-Silva, D., Dantas, L.K.B.F., Gobbi, L.T.B., and Vitório, R. (2020). Transcranial direct current stimulation combined with physical or cognitive training in people with Parkinson’s disease: a systematic review. J. NeuroEng. Rehabil. 17: 1–15. https://doi.org/10.1186/s12984-020-00701-6.Search in Google Scholar PubMed PubMed Central
Berghuis, K.M., Semmler, J.G., Opie, G.M., Post, A.K., and Hortobágyi, T. (2017). Age-related changes in corticospinal excitability and intracortical inhibition after upper extremity motor learning: a systematic review and meta-analysis. Neurobiol. Aging 55: 61–71. https://doi.org/10.1016/j.neurobiolaging.2017.03.024.Search in Google Scholar PubMed
Bhandari, A., Radhu, N., Farzan, F., Mulsant, B.H., Rajji, T.K., Daskalakis, Z.J., and Blumberger, D.M. (2016). A meta-analysis of the effects of aging on motor cortex neurophysiology assessed by transcranial magnetic stimulation. Clin. Neurophysiol. 127: 2834–2845. https://doi.org/10.1016/j.clinph.2016.05.363.Search in Google Scholar PubMed PubMed Central
Boggio, P.S., Castro, L.O., Savagim, E.A., Braite, R., Cruz, V.C., Rocha, R.R., Rigonatti, S.P., Silva, M.T., and Fregni, F. (2006). Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation. Neurosci. Lett. 404: 232–236. https://doi.org/10.1016/j.neulet.2006.05.051.Search in Google Scholar PubMed
Bolognini, N., Vallar, G., Casati, C., Latif, L.A., El-Nazer, R., Williams, J., Banco, E., Macea, D.D., Tesio, L., and Chessa, C. (2011). Neurophysiological and behavioral effects of tDCS combined with constraint-induced movement therapy in poststroke patients. Neurorehabil Neural Repair 25: 819–829. https://doi.org/10.1177/1545968311411056.Search in Google Scholar PubMed
Borenstein, M. (2022). Comprehensive meta-analysis software. Systematic reviews in health research: meta Analysis in context. Biostat, Englewood, NJ 2013, pp. 535–548.10.1002/9781119099369.ch27Search in Google Scholar
Broeder, S., Nackaerts, E., Cuypers, K., Meesen, R., Verheyden, G., and Nieuwboer, A. (2019a). tDCS-enhanced consolidation of writing skills and its associations with cortical excitability in Parkinson disease: a pilot study. Neurorehabil Neural Repair 33: 1050–1060. https://doi.org/10.1177/1545968319887684.Search in Google Scholar PubMed
Broeder, S., Heremans, E., Pereira, M.P., Nackaerts, E., Meesen, R., Verheyden, G., and Nieuwboer, A. (2019b). Does transcranial direct current stimulation during writing alleviate upper limb freezing in people with Parkinson’s disease? A pilot study. Hum. Mov. Sci. 65: 142–153. https://doi.org/10.1016/j.humov.2018.02.012.Search in Google Scholar PubMed
Brown, K.E., Neva, J.L., Ledwell, N.M., and Boyd, L.A. (2014). Use of transcranial magnetic stimulation in the treatment of selected movement disorders. Degener. Neurol. Neuromuscul. Dis. 4: 133. https://doi.org/10.2147/DNND.S70079.Search in Google Scholar PubMed PubMed Central
Buch, E.R., Santarnecchi, E., Antal, A., Born, J., Celnik, P.A., Classen, J., Gerloff, C., Hallett, M., Hummel, F.C., and Nitsche, M.A. (2017). Effects of tDCS on motor learning and memory formation: a consensus and critical position paper. Clin. Neurophysiol. 128: 589–603. https://doi.org/10.1016/j.clinph.2017.01.004.Search in Google Scholar PubMed
Cashin, A.G., Lee, H., Bagg, M.K., O’Hagan, E., Traeger, A.C., Kamper, S.J., and McAuley, J.H. (2020). A systematic review highlights the need to improve the quality and applicability of trials of physical therapy interventions for low back pain. Journal of Clinical Epidemiology 126: 106–115.10.1016/j.jclinepi.2020.06.025Search in Google Scholar PubMed
Chadman, K.K., Watson, D.J., and Stanton, M.E. (2006). NMDA receptor antagonism impairs reversal learning in developing rats. Behav. Neurosci. 120: 1071. https://doi.org/10.1037/0735-7044.120.5.1071.Search in Google Scholar PubMed PubMed Central
Chai, Z., Ma, C., and Jin, X. (2019). Homeostatic activity regulation as a mechanism underlying the effect of brain stimulation. Bioelectron Med 5: 1–9. https://doi.org/10.1186/s42234-019-0032-0.Search in Google Scholar PubMed PubMed Central
Chan, M.M., Yau, S.S., and Han, Y.M. (2021). The neurobiology of prefrontal transcranial direct current stimulation (tDCS) in promoting brain plasticity: a systematic review and meta-analyses of human and rodent studies. Neurosci. Biobehav. Rev. 125: 392–416. https://doi.org/10.1016/j.neubiorev.2021.02.035.Search in Google Scholar PubMed
Clark, B. and Taylor, J. (2011). Age-related changes in motor cortical properties and voluntary activation of skeletal muscle. Curr. Aging Sci. 4: 192–199. https://doi.org/10.2174/1874609811104030192.Search in Google Scholar PubMed PubMed Central
Clark, V.P., Coffman, B.A., Trumbo, M.C., and Gasparovic, C. (2011). Transcranial direct current stimulation (tDCS) produces localized and specific alterations in neurochemistry: a 1H magnetic resonance spectroscopy study. Neurosci. Lett. 500: 67–71. https://doi.org/10.1016/j.neulet.2011.05.244.Search in Google Scholar PubMed
Cosentino, G., Valentino, F., Todisco, M., Alfonsi, E., Davì, R., Savettieri, G., Fierro, B., D’Amelio, M., and Brighina, F. (2017). Effects of more-affected vs. less-affected motor cortex tDCS in Parkinson’s disease. Front. Hum. Neurosci. 11: 309. https://doi.org/10.3389/fnhum.2017.00309.Search in Google Scholar PubMed PubMed Central
Cuypers, K., Leenus, D.J., van den Berg, F.E., Nitsche, M.A., Thijs, H., Wenderoth, N., and Meesen, R.L. (2013). Is motor learning mediated by tDCS intensity? PLoS One 8: e67344. https://doi.org/10.1371/journal.pone.0067344.Search in Google Scholar PubMed PubMed Central
Dayan, E. and Cohen, L.G. (2011). Neuroplasticity subserving motor skill learning. Neuron 72: 443–454. https://doi.org/10.1016/j.neuron.2011.10.008.Search in Google Scholar PubMed PubMed Central
de Moura, M.C.D.S., Hazime, F.A., Marotti Aparicio, L.V., Grecco, L.A., Brunoni, A.R., and Hasue, R.H. (2019). Effects of transcranial direct current stimulation (tDCS) on balance improvement: a systematic review and meta-analysis. Somatosens. Mot. Res. 36: 122–135. https://doi.org/10.1080/08990220.2019.1624517.Search in Google Scholar PubMed
Deroost, N., Baetens, K., Vandenbossche, J., and Kerckhofs, E. (2018). Anodal tDCS of the primary motor cortex and motor sequence learning in a large sample of patients with Parkinson’s disease. Neuropsychiatry 8: 35–46.10.4172/Neuropsychiatry.1000323Search in Google Scholar
Doyon, J., Gaudreau, D., Laforce, R.Jr, Castonguay, M., Bedard, P., Bedard, F., and Bouchard, J. (1997). Role of the striatum, cerebellum, and frontal lobes in the learning of a visuomotor sequence. Brain Cogn 34: 218–245. https://doi.org/10.1006/brcg.1997.0899.Search in Google Scholar PubMed
Dumel, G., Bourassa, M.-E., Desjardins, M., Voarino, N., Charlebois-Plante, C., Doyon, J., and De Beaumont, L. (2016). Multisession anodal tDCS protocol improves motor system function in an aging population. Neural Plast. 2016: 5961362., https://doi.org/10.1155/2016/5961362.Search in Google Scholar PubMed PubMed Central
Dumel, G., Bourassa, M.-È., Charlebois-Plante, C., Desjardins, M., Doyon, J., Saint-Amour, D., and De Beaumont, L. (2017). Multisession anodal transcranial direct current stimulation induces motor cortex plasticity enhancement and motor learning generalization in an aging population. Clin. Neurophysiol. 129: 494–502. https://doi.org/10.1016/j.clinph.2017.10.041.Search in Google Scholar PubMed
Dumel, G., Bourassa, M.-E., Charlebois-Plante, C., Desjardins, M., Doyon, J., Saint-Amour, D., and De Beaumont, L. (2018). Motor learning improvement remains 3 months after a multisession anodal tDCS intervention in an aging population. Front. Aging Neurosci. 10: 1–9, https://doi.org/10.3389/fnagi.2018.00335.Search in Google Scholar PubMed PubMed Central
Festini, S.B., Zahodne, L., and Reuter-Lorenz, P.A. (2018). Theoretical perspectives on age differences in brain activation: Harold, pasa, crunch—How do they stac up? Oxford Research Encyclopedia of Psychology. https://doi.org/10.1093/acrefore/9780190236557.013.400.Search in Google Scholar
Filmer, H.L., Dux, P.E., and Mattingley, J.B. (2014). Applications of transcranial direct current stimulation for understanding brain function. Trends Neurosci. 37: 742–753. https://doi.org/10.1016/j.tins.2014.08.003.Search in Google Scholar PubMed
Firouzi, M., Van Herk, K., Kerckhofs, E., Swinnen, E., Baeken, C., Van Overwalle, F., and Deroost, N. (2021a). Transcranial direct- current stimulation enhances implicit motor sequence learning in persons with Parkinson’s disease with mild cognitive impairment. J. Neuropsychol. 15: 363–378. https://doi.org/10.1111/jnp.12231.Search in Google Scholar PubMed
Firouzi, M., Baetens, K., Swinnen, E., Duta, C., Baeken, C., Van Overwalle, F., and Deroost, N. (2021b). Implicit learning of perceptual sequences is preserved in Parkinson’s disease. Neuropsychology. 35: 679–690. https://doi.org/10.1037/neu0000749.Search in Google Scholar PubMed
Floyer-Lea, A., Wylezinska, M., Kincses, T., and Matthews, P.M. (2006). Rapid modulation of GABA concentration in human sensorimotor cortex during motor learning. J. Neurophysiol. 95: 1639–1644. https://doi.org/10.1152/jn.00346.2005.Search in Google Scholar PubMed
Foerster, Á., Rocha, S., Araújo, M.d. G.R., Lemos, A., and Monte-Silva, K. (2015). Effects of transcranial direct current stimulation on motor learning in healthy individuals: a systematic review. Fisioterapia em Movimento 28: 159–167. https://doi.org/10.1590/0103-5150.028.001.ar01.Search in Google Scholar
Fregni, F., Boggio, P.S., Santos, M.C., Lima, M., Vieira, A.L., Rigonatti, S.P., Silva, M.T.A., Barbosa, E.R., Nitsche, M.A., and Pascual Leone, A. (2006). Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov. Disord. 21: 1693–1702. https://doi.org/10.1002/mds.21012.Search in Google Scholar PubMed
Gálvez, V., Alonzo, A., Martin, D., and Loo, C.K. (2013). Transcranial direct current stimulation treatment protocols: should stimulus intensity be constant or incremental over multiple sessions? Int. J. Neuropsychopharmacol. 16: 13–21. https://doi.org/10.1017/S1461145712000041.Search in Google Scholar PubMed
Gilat, M., Bell, P.T., Martens, K.A.E., Georgiades, M.J., Hall, J.M., Walton, C.C., Lewis, S.J., and Shine, J.M. (2017). Dopamine depletion impairs gait automaticity by altering cortico-striatal and cerebellar processing in Parkinson’s disease. Neuroimage 152: 207–220. https://doi.org/10.1016/j.neuroimage.2017.02.073.Search in Google Scholar PubMed
Goodwill, A.M., Daly, R.M., and Kidgell, D.J. (2015). The effects of anodal-tDCS on cross-limb transfer in older adults. Clin. Neurophysiol. 126: 2189–2197. https://doi.org/10.1016/j.clinph.2015.01.006.Search in Google Scholar PubMed
Goodwill, A.M., Reynolds, J., Daly, R.M., and Kidgell, D.J. (2013). Formation of cortical plasticity in older adults following tDCS and motor training. Front. Aging Neurosci. 5: 87. https://doi.org/10.3389/fnagi.2013.00087.Search in Google Scholar PubMed PubMed Central
Halakoo, S., Ehsani, F., Hosnian, M., Zoghi, M., and Jaberzadeh, S. (2020). The comparative effects of unilateral and bilateral transcranial direct current stimulation on motor learning and motor performance: a systematic review of literature and meta-analysis. J. Clin. Neurosci. 72: 8–14. https://doi.org/10.1016/j.jocn.2019.12.022.Search in Google Scholar PubMed
Hardwick, R.M. and Celnik, P.A. (2014). Cerebellar direct current stimulation enhances motor learning in older adults. Neurobiol. Aging 35: 2217–2221. https://doi.org/10.1016/j.neurobiolaging.2014.03.030.Search in Google Scholar PubMed PubMed Central
Hashemirad, F., Zoghi, M., Fitzgerald, P.B., and 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 Cognit. 102: 1–12. https://doi.org/10.1016/j.bandc.2015.11.005.Search in Google Scholar PubMed
Higgins, E.S. and George, M.S. (2019). Brain stimulation therapies for clinicians. American Psychiatric Pub, Washington, DC.Search in Google Scholar
Horiba, M., Ueki, Y., Nojima, I., Shimizu, Y., Sahashi, K., Itamoto, S., Suzuki, A., Yamada, G., Matsukawa, N., and Wada, I. (2019). Impaired motor skill acquisition using mirror visual feedback improved by transcranial direct current stimulation (tDCS) in patients with Parkinson’s disease. Front. Neurosci. 13: 602. https://doi.org/10.3389/fnins.2019.00602.Search in Google Scholar PubMed PubMed Central
Hummel, F., Celnik, P., Giraux, P., Floel, A., Wu, W.-H., Gerloff, C., and Cohen, L.G. (2005). Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain 128: 490–499. https://doi.org/10.1093/brain/awh369.Search in Google Scholar PubMed
Hummel, F.C., Heise, K., Celnik, P., Floel, A., Gerloff, C., and 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. https://doi.org/10.1016/j.neurobiolaging.2008.12.008.Search in Google Scholar PubMed PubMed Central
Ishikuro, K., Dougu, N., Nukui, T., Yamamoto, M., Nakatsuji, Y., Kuroda, S., Matsushita, I., Nishimaru, H., Araujo, M.F., and Nishijo, H. (2018). Effects of transcranial direct current stimulation (tDCS) over the frontal polar area on motor and executive functions in Parkinson’s disease; a pilot study. Front. Aging Neurosci. 10: 1–9, https://doi.org/10.3389/fnagi.2018.00231.Search in Google Scholar PubMed PubMed Central
Izawa, J., Criscimagna-Hemminger, S.E., and Shadmehr, R. (2012). Cerebellar contributions to reach adaptation and learning sensory consequences of action. J. Neurosci. 32: 4230–4239. https://doi.org/10.1523/jneurosci.6353-11.2012.Search in Google Scholar
Jacobson, L., Koslowsky, M., and Lavidor, M. (2012). tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp. Brain Res. 216: 1–10. https://doi.org/10.1007/s00221-011-2891-9.Search in Google Scholar PubMed
Johnson, J.F., Belyk, M., Schwartze, M., Pinheiro, A.P., and Kotz, S.A. (2019). The role of the cerebellum in adaptation: ALE meta‐analyses on sensory feedback error. Hum. Brain Mapp. 40: 3966–3981. https://doi.org/10.1002/hbm.24681.Search in Google Scholar PubMed PubMed Central
Kadosh, R.C., Soskic, S., Iuculano, T., Kanai, R., and Walsh, V. (2010). Modulating neuronal activity produces specific and long-lasting changes in numerical competence. Curr. Biol. 20: 2016–2020. https://doi.org/10.1016/j.cub.2010.10.007.Search in Google Scholar PubMed PubMed Central
Kida, H., Tsuda, Y., Ito, N., Yamamoto, Y., Owada, Y., Kamiya, Y., and Mitsushima, D. (2016). Motor training promotes both synaptic and intrinsic plasticity of layer II/III pyramidal neurons in the primary motor cortex. Cerebr. Cortex 26: 3494–3507. https://doi.org/10.1093/cercor/bhw134.Search in Google Scholar PubMed PubMed Central
Krakauer, J.W. and Mazzoni, P. (2011). Human sensorimotor learning: adaptation, skill, and beyond. Curr. Opin. Neurobiol. 21: 636–644.10.1016/j.conb.2011.06.012Search in Google Scholar PubMed
Laakso, I., Tanaka, S., Mikkonen, M., Koyama, S., Sadato, N., and Hirata, A. (2016). Electric fields of motor and frontal tDCS in a standard brain space: a computer simulation study. Neuroimage 137: 140–151. https://doi.org/10.1016/j.neuroimage.2016.05.032.Search in Google Scholar PubMed
Lee, H.K., Ahn, S.J., Shin, Y.M., Kang, N., and Cauraugh, J.H. (2019). Does transcranial direct current stimulation improve functional locomotion in people with Parkinson’s disease? A systematic review and meta-analysis. J. NeuroEng. Rehabil. 16: 1–13. https://doi.org/10.1186/s12984-019-0582-0.Search in Google Scholar PubMed PubMed Central
Lima de Albuquerque, L., Pantovic, M., Clingo, M., Fischer, K., Jalene, S., Landers, M., Mari, Z., and Poston, B. (2020). An acute application of cerebellar transcranial direct current stimulation does not improve motor performance in Parkinson’s disease. Brain Sci. 10: 735. https://doi.org/10.3390/brainsci10100735.Search in Google Scholar PubMed PubMed Central
Lima de Albuquerque, L.L., Pantovic, M., Clingo, M.G., Fischer, K.M., Jalene, S., Landers, M.R., Mari, Z., and Poston, B. (2021). Long-term application of cerebellar transcranial direct current stimulation does not improve motor learning in Parkinson’s disease. Cerebellum 21: 333–349.10.1007/s12311-021-01297-wSearch in Google Scholar PubMed PubMed Central
Lindenberg, R., Nachtigall, L., Meinzer, M., Sieg, M.M., and Flöel, A. (2013). Differential effects of dual and unihemispheric motor cortex stimulation in older adults. J. Neurosci. 33: 9176–9183. https://doi.org/10.1523/jneurosci.0055-13.2013.Search in Google Scholar PubMed PubMed Central
Ljubisavljevic, M.R., Oommen, J., Filipovic, S., Bjekic, J., Szolics, M., and Nagelkerke, N. (2019). Effects of tDCS of dorsolateral prefrontal cortex on dual-task performance involving manual dexterity and cognitive task in healthy older adults. Front. Aging Neurosci. 11: 144. https://doi.org/10.3389/fnagi.2019.00144.Search in Google Scholar PubMed PubMed Central
Marinelli, L., Quartarone, A., Hallett, M., Frazzitta, G., and Ghilardi, M.F. (2017). The many facets of motor learning and their relevance for Parkinson’s disease. Clin. Neurophysiol. 128: 1127–1141. https://doi.org/10.1016/j.clinph.2017.03.042.Search in Google Scholar PubMed PubMed Central
Meinzer, M., Lindenberg, R., Antonenko, D., Flaisch, T., and Flöel, A. (2013). Anodal transcranial direct current stimulation temporarily reverses age-associated cognitive decline and functional brain activity changes. J. Neurosci. 33: 12470–12478. https://doi.org/10.1523/jneurosci.5743-12.2013.Search in Google Scholar PubMed PubMed Central
Minarik, T., Berger, B., Althaus, L., Bader, V., Biebl, B., Brotzeller, F., Fusban, T., Hegemann, J., Jesteadt, L., and Kalweit, L. (2016). The importance of sample size for reproducibility of tDCS effects. Front. Hum. Neurosci. 10: 453. https://doi.org/10.3389/fnhum.2016.00453.Search in Google Scholar PubMed PubMed Central
Moher, D., Altman, D.G., Liberati, A., and Tetzlaff, J. (2011). PRISMA statement. Epidemiology 22: 128. https://doi.org/10.1097/ede.0b013e3181fe7825.Search in Google Scholar PubMed
Monte-Silva, K., Kuo, M.-F., Hessenthaler, S., Fresnoza, S., Liebetanz, D., Paulus, W., and Nitsche, M.A. (2013). Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul. 6: 424–432. https://doi.org/10.1016/j.brs.2012.04.011.Search in Google Scholar PubMed
Mooney, R.A., Cirillo, J., and Byblow, W.D. (2019). Neurophysiological mechanisms underlying motor skill learning in young and older adults. Exp. Brain Res. 237: 2331–2344. https://doi.org/10.1007/s00221-019-05599-8.Search in Google Scholar PubMed
Morya, E., Monte-Silva, K., Bikson, M., Esmaeilpour, Z., Biazoli, C.E., Fonseca, A., Bocci, T., Farzan, F., Chatterjee, R., and Hausdorff, J.M. (2019). Beyond the target area: an integrative view of tDCS-induced motor cortex modulation in patients and athletes. J. NeuroEng. Rehabil. 16: 1–29. https://doi.org/10.1186/s12984-019-0581-1.Search in Google Scholar PubMed PubMed Central
Muffel, T., Kirsch, F., Shih, P.-C., Kalloch, B., Schaumberg, S., Villringer, A., and Sehm, B. (2019). Anodal transcranial direct current stimulation over S1 differentially modulates proprioceptive accuracy in young and old adults. Front. Aging Neurosci. 264, https://doi.org/10.3389/fnagi.2019.00264.Search in Google Scholar PubMed PubMed Central
Nitsche, M.A., Jaussi, W., Liebetanz, D., Lang, N., Tergau, F., and Paulus, W. (2004). Consolidation of human motor cortical neuroplasticity by D-cycloserine. Neuropsychopharmacology 29: 1573–1578. https://doi.org/10.1038/sj.npp.1300517.Search in Google Scholar PubMed
Nitsche, M.A., Fricke, K., Henschke, U., Schlitterlau, A., Liebetanz, D., Lang, N., Henning, S., Tergau, F., and Paulus, W. (2003). Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J. Physiol. 553: 293–301. https://doi.org/10.1113/jphysiol.2003.049916.Search in Google Scholar PubMed PubMed Central
O’Shea, J., Boudrias, M.-H., Stagg, C.J., Bachtiar, V., Kischka, U., Blicher, J.U., and Johansen-Berg, H. (2014). Predicting behavioural response to TDCS in chronic motor stroke. Neuroimage 85: 924–933. https://doi.org/10.1016/j.neuroimage.2013.05.096.Search in Google Scholar PubMed PubMed Central
Olson, M., Lockhart, T.E., and Lieberman, A. (2019). Motor learning deficits in Parkinson’s disease (PD) and their effect on training response in gait and balance: a narrative review. Front. Neurol. 62, https://doi.org/10.3389/fneur.2019.00062.Search in Google Scholar PubMed PubMed Central
Panouillères, M.T., Joundi, R.A., Brittain, J.S., and Jenkinson, N. (2015). Reversing motor adaptation deficits in the ageing brain using non-invasive stimulation. J. Physiol. 593: 3645–3655. https://doi.org/10.1113/JP270484.Search in Google Scholar PubMed PubMed Central
Parikh, P.J. and Cole, K.J. (2014). Effects of transcranial direct current stimulation in combination with motor practice on dexterous grasping and manipulation in healthy older adults. Phys. Rep. 2: e00255. https://doi.org/10.1002/phy2.255.Search in Google Scholar PubMed PubMed Central
Parikh, P.J. and Cole, K.J. (2015). Effects of transcranial direct current stimulation on the control of finger force during dexterous manipulation in healthy older adults. PLoS One 10: e0124137. https://doi.org/10.1371/journal.pone.0124137.Search in Google Scholar PubMed PubMed Central
Patel, R., Ashcroft, J., Patel, A., Ashrafian, H., Woods, A.J., Singh, H., Darzi, A., and Leff, D.R. (2019). The impact of transcranial direct current stimulation on upper-limb motor performance in healthy adults: a systematic review and meta-analysis. Front. Neurosci. 13: 1213., https://doi.org/10.3389/fnins.2019.01213.Search in Google Scholar PubMed PubMed Central
Paul, S.S., Dibble, L.E., Olivier, G.N., Walter, C., Duff, K., and Schaefer, S.Y. (2020). Dopamine replacement improves motor learning of an upper extremity task in people with Parkinson disease. Behav. Brain Res. 377: 112213. https://doi.org/10.1016/j.bbr.2019.112213.Search in Google Scholar PubMed PubMed Central
Pendt, L.K., Reuter, I., and Müller, H. (2011). Motor skill learning, retention, and control deficits in Parkinson’s disease. PLoS One 6: e21669. https://doi.org/10.1371/journal.pone.0021669.Search in Google Scholar PubMed PubMed Central
Peters, R. (2006). Ageing and the brain. Postgrad. Med. 82: 84–88. https://doi.org/10.1136/pgmj.2005.036665.Search in Google Scholar PubMed PubMed Central
Prehn, K. and Flöel, A. (2015). Potentials and limits to enhance cognitive functions in healthy and pathological aging by tDCS. Front. Cell. Neurosci. 9: 355. https://doi.org/10.3389/fncel.2015.00355.Search in Google Scholar PubMed PubMed Central
Raw, R.K., Allen, R.J., Mon-Williams, M., and Wilkie, R.M. (2016). Motor sequence learning in healthy older adults is not necessarily facilitated by transcranial direct current stimulation (tDCS). Geriatrics 1: 32. https://doi.org/10.3390/geriatrics1040032.Search in Google Scholar PubMed PubMed Central
Raw, R.K., Wilkie, R.M., Allen, R.J., Warburton, M., Leonetti, M., Williams, J.H., and Mon-Williams, M. (2019). Skill acquisition as a function of age, hand and task difficulty: interactions between cognition and action. PLoS One 14: e0211706. https://doi.org/10.1371/journal.pone.0211706.Search in Google Scholar PubMed PubMed Central
Rawji, V., Ciocca, M., Zacharia, A., Soares, D., Truong, D., Bikson, M., Rothwell, J., and Bestmann, S. (2018). tDCS changes in motor excitability are specific to orientation of current flow. Brain Stimul. 11: 289–298. https://doi.org/10.1016/j.brs.2017.11.001.Search in Google Scholar PubMed PubMed Central
Reeve, A., Simcox, E., and Turnbull, D. (2014). Ageing and Parkinson’s disease: why is advancing age the biggest risk factor? Ageing Res. Rev. 14: 19–30. https://doi.org/10.1016/j.arr.2014.01.004.Search in Google Scholar PubMed PubMed Central
Reis, J. and Fritsch, B. (2011). Modulation of motor performance and motor learning by transcranial direct current stimulation. Curr. Opin. Neurol. 24: 590–596. https://doi.org/10.1097/wco.0b013e32834c3db0.Search in Google Scholar
Reis, J., Schambra, H.M., Cohen, L.G., Buch, E.R., Fritsch, B., Zarahn, E., Celnik, P.A., and Krakauer, J.W. (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. https://doi.org/10.1073/pnas.0805413106.Search in Google Scholar PubMed PubMed Central
Rezvani, A.H. (2006). Involvement of the NMDA System in Learning and Memory. Animal models of cognitive impairment. CRC Press, Boca Raton, Florida, USA, pp. 37–48.10.1201/9781420004335.ch4Search in Google Scholar
Ridding, M., Rothwell, J., and Inzelberg, R. (1995). Changes in excitability of motor cortical circuitry in patients with Parkinson’s disease. Ann. Neurol. 37: 181–188. https://doi.org/10.1002/ana.410370208.Search in Google Scholar PubMed
Rumpf, J.-J., Wegscheider, M., Hinselmann, K., Fricke, C., King, B.R., Weise, D., Klann, J., Binkofski, F., Buccino, G., and Karni, A. (2017). Enhancement of motor consolidation by post-training transcranial direct current stimulation in older people. Neurobiol. Aging 49: 1–8. https://doi.org/10.1016/j.neurobiolaging.2016.09.003.Search in Google Scholar PubMed
Russo, R., Twyman, P., Cooper, N.R., Fitzgerald, P.B., and Wallace, D. (2017). When you can, scale up: large-scale study shows no effect of tDCS in an ambiguous risk-taking task. Neuropsychologia 104: 133–143. https://doi.org/10.1016/j.neuropsychologia.2017.08.008.Search in Google Scholar PubMed
Ryan, K., Schranz, A.L., Duggal, N., and Bartha, R. (2019). Differential effects of transcranial direct current stimulation on antiphase and inphase motor tasks: a pilot study. Behav. Brain Res. 366: 13–18. https://doi.org/10.1016/j.bbr.2019.03.014.Search in Google Scholar PubMed
Samaei, A., Ehsani, F., Zoghi, M., Hafez Yosephi, M., and 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. https://doi.org/10.1111/ejn.13559.Search in Google Scholar PubMed
Saucedo Marquez, C.M., Zhang, X., Swinnen, S.P., Meesen, R., and Wenderoth, N. (2013). Task-specific effect of transcranial direct current stimulation on motor learning. Front. Hum. Neurosci. 7: 333. https://doi.org/10.3389/fnhum.2013.00333.Search in Google Scholar PubMed PubMed Central
Schiavo, J.H. (2019). PROSPERO: An International Register of Systematic Review Protocols. Med. Ref. Serv. Quart. 38: 171–180, https://doi.org/10.1080/02763869.2019.1588072.Search in Google Scholar PubMed
Schmidt, R.A. and Lee, T.D. (2005). Motor control and learning: A behavioral emphasis, 4th ed. Champaign: Human Kinetics.Search in Google Scholar
Schroeder, P.A., Schwippel, T., Wolz, I., and Svaldi, J. (2020). Meta-analysis of the effects of transcranial direct current stimulation on inhibitory control. Brain Stimul. 13: 1159–1167. https://doi.org/10.1016/j.brs.2020.05.006.Search in Google Scholar PubMed
Sehm, B., Kipping, J.A., Schäfer, A., Villringer, A., and Ragert, P. (2013). A comparison between uni-and bilateral tDCS effects on functional connectivity of the human motor cortex. Front. Hum. Neurosci. 7: 183. https://doi.org/10.3389/fnhum.2013.00183.Search in Google Scholar PubMed PubMed Central
Seidler, R., Erdeniz, B., Koppelmans, V., Hirsiger, S., Mérillat, S., and Jäncke, L. (2015). Associations between age, motor function, and resting state sensorimotor network connectivity in healthy older adults. Neuroimage 108: 47–59. https://doi.org/10.1016/j.neuroimage.2014.12.023.Search in Google Scholar PubMed
Seidler, R.D. (2006). Differential effects of age on sequence learning and sensorimotor adaptation. Brain Res. Bull. 70: 337–346. https://doi.org/10.1016/j.brainresbull.2006.06.008.Search in Google Scholar PubMed
Seidler, R.D. (2007). Older adults can learn to learn new motor skills. Behav. Brain Res. 183: 118–122. https://doi.org/10.1016/j.bbr.2007.05.024.Search in Google Scholar PubMed PubMed Central
Seidler, R.D., Bernard, J.A., Burutolu, T.B., Fling, B.W., Gordon, M.T., Gwin, J.T., Kwak, Y., and Lipps, D.B. (2010). Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci. Biobehav. Rev. 34: 721–733. https://doi.org/10.1016/j.neubiorev.2009.10.005.Search in Google Scholar PubMed PubMed Central
Shea, C.H., Park, J.-H., and Wilde Braden, H. (2006). Age-related effects in sequential motor learning. Phys. Ther. 86: 478–488. https://doi.org/10.1093/ptj/86.4.478.Search in Google Scholar
Simpson, M.W. and Mak, M. (2022). Single session transcranial direct current stimulation to the primary motor cortex fails to enhance early motor sequence learning in Parkinson’s disease. Behav. Brain Res. 418: 113624. https://doi.org/10.1016/j.bbr.2021.113624.Search in Google Scholar PubMed
Stagg, C., O’shea, J., Kincses, Z., Woolrich, M., Matthews, P., and Johansen-Berg, H. (2009a). Modulation of movement-associated cortical activation by transcranial direct current stimulation. Eur. J. Neurosci. 30: 1412–1423. https://doi.org/10.1111/j.1460-9568.2009.06937.x.Search in Google Scholar PubMed
Stagg, C.J., Bachtiar, V., and Johansen-Berg, H. (2011). The role of GABA in human motor learning. Curr. Biol. 21: 480–484. https://doi.org/10.1016/j.cub.2011.01.069.Search in Google Scholar PubMed PubMed Central
Stagg, C.J., Best, J.G., Stephenson, M.C., O’Shea, J., Wylezinska, M., Kincses, Z.T., Morris, P.G., Matthews, P.M., and Johansen-Berg, H. (2009b). Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J. Neurosci. 29: 5202–5206. https://doi.org/10.1523/jneurosci.4432-08.2009.Search in Google Scholar PubMed PubMed Central
Summers, J.J., Kang, N., and Cauraugh, J.H. (2016). Does transcranial direct current stimulation enhance cognitive and motor functions in the ageing brain? A systematic review and meta-analysis. Ageing Res. Rev. 25: 42–54. https://doi.org/10.1016/j.arr.2015.11.004.Search in Google Scholar PubMed
Tazoe, T., Endoh, T., Kitamura, T., and Ogata, T. (2014). Polarity specific effects of transcranial direct current stimulation on interhemispheric inhibition. PLoS One 9: e114244. https://doi.org/10.1371/journal.pone.0114244.Search in Google Scholar PubMed PubMed Central
Teo, W.-P., Muthalib, M., and Kidgell, D. (2015). Modulation of corticospinal excitability and inhibition of the contralateral M1 during and after ipsilateral anodal tDCS. Brain Stimul. 8: 341. https://doi.org/10.1016/j.brs.2015.01.103.Search in Google Scholar
Teo, W.-P., Rodrigues, J.P., Mastaglia, F.L., and Thickbroom, G.W. (2014). Modulation of corticomotor excitability after maximal or sustainable-rate repetitive finger movement is impaired in Parkinson’s disease and is reversed by levodopa. Clin. Neurophysiol. 125: 562–568. https://doi.org/10.1016/j.clinph.2013.09.004.Search in Google Scholar PubMed
Thair, H., Holloway, A.L., Newport, R., and Smith, A.D. (2017). Transcranial direct current stimulation (tDCS): a beginner’s guide for design and implementation. Front. Neurosci. 11: 641. https://doi.org/10.3389/fnins.2017.00641.Search in Google Scholar PubMed PubMed Central
Truong, D.Q. and Bikson, M. (2018). Physics of transcranial direct current stimulation devices and their history. J. ECT 34: 137–143. https://doi.org/10.1097/yct.0000000000000531.Search in Google Scholar PubMed
Vallesi, A., McIntosh, A.R., Kovacevic, N., Chan, S.C., and Stuss, D.T. (2010). Age effects on the asymmetry of the motor system: evidence from cortical oscillatory activity. Biol. Psychol. 85: 213–218. https://doi.org/10.1016/j.biopsycho.2010.07.003.Search in Google Scholar PubMed
Weightman, M., Brittain, J.-S., Punt, D., Miall, R.C., and Jenkinson, N. (2020). Targeted tDCS selectively improves motor adaptation with the proximal and distal upper limb. Brain Stimul. 13: 707–716. https://doi.org/10.1016/j.brs.2020.02.013.Search in Google Scholar PubMed
Wolpert, D.M., Ghahramani, Z., and Flanagan, J.R. (2001). Perspectives and problems in motor learning. Trends Cogn. Sci. 5: 487–494.10.1016/S1364-6613(00)01773-3Search in Google Scholar
Yamaguchi, T., Moriya, K., Tanabe, S., Kondo, K., Otaka, Y., and Tanaka, S. (2020). Transcranial direct-current stimulation combined with attention increases cortical excitability and improves motor learning in healthy volunteers. J. NeuroEng. Rehabil. 17: 1–13. https://doi.org/10.1186/s12984-020-00665-7.Search in Google Scholar PubMed PubMed Central
Zich, C., Harty, S., Kranczioch, C., Mansfield, K.L., Sella, F., Debener, S., and Cohen Kadosh, R. (2017). Modulating hemispheric lateralization by brain stimulation yields gain in mental and physical activity. Sci. Rep. 7: 1–10. https://doi.org/10.1038/s41598-017-13795-1.Search in Google Scholar PubMed PubMed Central
Zimerman, M., Heise, K.-F., Gerloff, C., Cohen, L.G., and Hummel, F.C. (2014). Disrupting the ipsilateral motor cortex interferes with training of a complex motor task in older adults. Cerebr. Cortex 24: 1030–1036. https://doi.org/10.1093/cercor/bhs385.Search in Google Scholar PubMed
Zimerman, M., Nitsch, M., Giraux, P., Gerloff, C., Cohen, L.G., and Hummel, F.C. (2013). Neuroenhancement of the aging brain: restoring skill acquisition in old subjects. Ann. Neurol. 73: 10. https://doi.org/10.1002/ana.23761.Search in Google Scholar PubMed PubMed Central
© 2022 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Aging, testosterone, and neuroplasticity: friend or foe?
- Mitochondrial fission mediated by Drp1-Fis1 pathway and neurodegenerative diseases
- The limitations of investigating appetite through circuit manipulations: are we biting off more than we can chew?
- The role and mechanism of tryptophan – kynurenine metabolic pathway in depression
- A meta-analytical review of transcranial direct current stimulation parameters on upper limb motor learning in healthy older adults and people with Parkinson’s disease
- A systematic review of transcranial direct current stimulation on eye movements and associated psychological function
Articles in the same Issue
- Frontmatter
- Aging, testosterone, and neuroplasticity: friend or foe?
- Mitochondrial fission mediated by Drp1-Fis1 pathway and neurodegenerative diseases
- The limitations of investigating appetite through circuit manipulations: are we biting off more than we can chew?
- The role and mechanism of tryptophan – kynurenine metabolic pathway in depression
- A meta-analytical review of transcranial direct current stimulation parameters on upper limb motor learning in healthy older adults and people with Parkinson’s disease
- A systematic review of transcranial direct current stimulation on eye movements and associated psychological function