Application of transcranial electric stimulation (tDCS, tACS, tRNS): From motor-evoked potentials towards modulation of behaviour

European Psychologist

Volumn 21, Issue 1, 2016, Pages 4-14

  Paulus, Walter ^a   Nitsche, Michael A ^b   Antal, Andrea ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b LEIBNIZ RESEARCH CENTRE FOR WORKING ENVIRONMENT AND HUMAN FACTORS   (Germany)

Author keywords

Alternating current; Direct current; Human; Transcranial stimulation

Indexed keywords

EID: 84962092828     PISSN: 10169040     EISSN: 1878531X     Source Type: Journal    
DOI: 10.1027/1016-9040/a000242     Document Type: Review

References (109)

1. Ali, M. M., Sellers, K. K., & Frohlich, F. (2013). Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance [Research Support, Non-U. S. Gov't]. Journal of Neuroscience, 33, 11262-11275. doi: 10.1523/JNEUROSCI.5867-12.2013
2. Ambrus, G. G., Paulus, W., & Antal, A. (2010). Cutaneous perception thresholds of electrical stimulation methods: Comparison of tDCS and tRNS. Clinical Neurophysiology, 121, 1908-1914. doi: 10.1016/j.clinph.2010.04.020
3. Ambrus, G. G., Zimmer, M., Kincses, Z. T., Harza, I., Kovacs, G., Paulus, W., & Antal, A. (2011). The enhancement of cortical excitability over the DLPFC before and during training impairs categorization in the prototype distortion task. Neuropsychologia, 49, 1974-1980. doi: 10.1016/j.neuropsychologia. 2011.03.026
4. Ambrus, G. G., Zimmer, M., Kincses, Z. T., Harza, I., Kovacs, G., Paulus, W., & Antal, A. (2011). The enhancement of cortical excitability over the DLPFC before and during training impairs categorization in the prototype distortion task. Neuropsychologia, 49, 1974-1980. doi: 10.1016/j.neuropsychologia.2011.03.026
5. Antal, A., Boros, K., Poreisz, C., Chaieb, L., Terney, D., & Paulus, W. (2008). Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans. Brain Stimulation, 1, 97-105. doi: 10.1016/j.brs.2007.10.001
6. Antal, A., Chaieb, L., Moliadze, V., Monte-Silva, K., Poreisz, C., Thirugnanasambandam, N.,... Paulus, W. (2010). Brainderived neurotrophic factor (BDNF) gene polymorphisms shape cortical plasticity in humans. Brain Stimulation, 3, 230-237. doi: 10.1016/j.brs.2009.12.003
7. Antal, A., Kincses, T. Z., Nitsche, M. A., Bartfai, O., & Paulus, W. (2004). Excitability changes induced in the human primary visual cortex by transcranial direct current stimulation: Direct electrophysiological evidence. Investigative Ophthalmology and Visual Science, 45, 702-707.
8. Antal, A., Kincses, T. Z., Nitsche, M. A., & Paulus, W. (2003a). Manipulation of phosphene thresholds by transcranial direct current stimulation in man. Experimental Brain Research, 150, 375-378. doi: 10.1007/s00221-003-1459-8
9. Antal, A., Kincses, T. Z., Nitsche, M. A., & Paulus, W. (2003b). Modulation of moving phosphene thresholds by transcranial direct current stimulation of V1 in human. Neuropsychologia, 41, 1802-1807. doi: 10.1016/S0028-3932 (03) 00181-7
10. Antal, A., Nitsche, M. A., Kincses, T. Z., Kruse, W., Hoffmann, K. P., & Paulus, W. (2004). Facilitation of visuo-motor learning by transcranial direct current stimulation of the motor and extrastriate visual areas in humans. European Journal of Neuroscience, 19, 2888-2892. doi: 10.1111/j.1460-9568.2004.03367.x
11. Antal, A., Nitsche, M. A., & Paulus, W. (2003). Transcranial magnetic and direct current stimulation of the visual cortex. Supplement Clinical Neurophysiolology, 56, 291-304.
12. Antal, A., Terney, D., Poreisz, C., & Paulus, W. (2007). Towards unravelling task-related modulations of neuroplastic changes induced in the human motor cortex. European Journal of Neuroscience, 26, 2687-2691. doi: 10.1111/j.1460-9568.2007.05896.x
13. Ardolino, G., Bossi, B., Barbieri, S., & Priori, A. (2005). Nonsynaptic mechanisms underlie the after-effects of cathodal transcutaneous direct current stimulation of the human brain. Journal of Physiology, 568, 653-663.
14. Bastani, A., & Jaberzadeh, S. (2013). Differential modulation of corticospinal excitability by different current densities of anodal transcranial direct current stimulation. PLoS One, 8, e72254. doi: 10.1371/journal.pone.0072254
15. Batsikadze, G., Moliadze, V., Paulus, W., Kuo, M. F., & Nitsche, M. A. (2013). Partially non-linear stimulation intensitydependent effects of direct current stimulation on motor cortex excitability in humans. Journal of Physiology, 591, 1987-2000. doi: 10.1113/jphysiol.2012.249730
16. Berryhill, M. E., Wencil, E. B., Branch Coslett, H., & Olson, I. R. (2010). A selective working memory impairment after transcranial direct current stimulation to the right parietal lobe [Research Support, N. I. H., Extramural]. Neuroscience Letters, 479, 312-316. doi: 10.1016/j.neulet.2010.05.087
17. Bikson, M., Datta, A., Rahman, A., & Scaturro, J. (2010). Electrode montages for tDCS and weak transcranial electrical stimulation: Role of "return" electrode's position and size. Clinical Neurophysiology, 121, 1976-1978. doi: 10.1016/j.clinph.2010.05.020
18. Bindman, L. J., Lippold, O. C., & Redfearn, J. W. (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. The Journal of Physiology, 172, 369-382.
19. Boros, K., Poreisz, C., Munchau, A., Paulus, W., & Nitsche, M. A. (2008). Premotor transcranial direct current stimulation (tDCS) affects primary motor excitability in humans. The European Journal of Neuroscience, 27, 1292-1300. doi: 10.1111/j.1460-9568.2008.06090.x
20. Brignani, D., Ruzzoli, M., Mauri, P., & Miniussi, C. (2013). Is transcranial alternating current stimulation effective in modulating brain oscillations? PLoS One, 8, e56589. doi: 10.1371/journal.pone.0056589
21. Butts, D. A., Weng, C., Jin, J., Yeh, C. I., Lesica, N. A., Alonso, J. M., & Stanley, G. B. (2007). Temporal precision in the neural code and the timescales of natural vision [Research Support, N. I. H.]. Nature, 449, 92-95. doi: 10.1038/nature06105
22. Cappelletti, M., Gessaroli, E., Hithersay, R., Mitolo, M., Didino, D., Kanai, R.,... Walsh, V. (2013). Transfer of cognitive training across magnitude dimensions achieved with concurrent brain stimulation of the parietal lobe. Journal of Neuroscience, 33, 14899-14907. doi: 10.1523/JNEUROSCI.1692-13.2013
23. Cecere, R., Rees, G., & Romei, V. (2015). Individual differences in alpha frequency drive crossmodal illusory perception [Research Support, Non-U. S. Gov't]. Current Biology, 25, 231-235. doi: 10.1016/j.cub.2014.11.034
24. Chaieb, L., Antal, A., Ambrus, G. G., & Paulus, W. (2014). Brain-derived neurotrophic factor: Its impact upon neuroplasticity and neuroplasticity inducing transcranial brain stimulation protocols. Neurogenetics, 15, 1-11. doi: 10.1007/s10048-014-0393-1
25. Chaieb, L., Antal, A., & Paulus, W. (2008). Gender-specific modulation of short-term neuroplasticity in the visual cortex induced by transcranial direct current stimulation. Visual Neuroscience, 25, 77-81. doi: 10.1017/S0952523808080097
26. Chaieb, L., Antal, A., & Paulus, W. (2011). Transcranial alternating current stimulation in the low kHz range increases motor cortex excitability. Restorative Neurology and Neuroscience, 29, 167-175. doi: 10.3233/RNN-2011-0589
27. Chaieb, L., Antal, A., & Paulus, W. (2015). Transcranial random noise stimulation-induced plasticity is NMDA-receptor independent but sodium-channel blocker and benzodiazepines sensitive. Frontiers in Neuroscience, 9, 125. doi: 10.3389/fnins.2015.00125
28. Citri, A., & Malenka, R. C. (2008). Synaptic plasticity: Multiple forms, functions, and mechanisms. Neuropsychopharmacology, 33, 18-41. doi: 10.1038/sj.npp. 1301559
29. Creutzfeldt, O. D., Fromm, G. H., & Kapp, H. (1962). Influence of transcortical d-c currents on cortical neuronal activity. Experimental Neurology, 5, 436-452.
30. Datta, A., Bansal, V., Diaz, J., Patel, J., Reato, D., & Bikson, M. (2009). Gyri-precise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimulation, 2, 201-207. doi: 10.1016/j.brs.2009.03.005
31. de Vries, M. H., Barth, A. C., Maiworm, S., Knecht, S., Zwitserlood, P., & Floel, A. (2010). Electrical stimulation of Broca's area enhances implicit learning of an artificial grammar. Journal of Cognitive Neuroscience, 22, 2427-2436. doi: 10.1162/jocn. 2009.21385
32. Dockery, C. A., Hueckel-Weng, R., Birbaumer, N., & Plewnia, C. (2009). Enhancement of planning ability by transcranial direct current stimulation. Journal of Neuroscience, 29, 7271-7277. doi: 10.1523/JNEUROSCI.0065-09.2009
33. Dundas, J. E., Thickbroom, G. W., & Mastaglia, F. L. (2007). Perception of comfort during transcranial DC stimulation: Effect of NaCl solution concentration applied to sponge electrodes. Clinical Neurophysiology, 118, 1166-1170. doi: 10.1016/j.clinph.2007.01.010
34. Fertonani, A., Ferrari, C., & Miniussi, C. (2015). What do you feel if I apply transcranial electric stimulation? Safety, sensations and secondary induced effects. Clinical Neurophysiology, 126, 2181-2188. doi: 10.1016/j.clinph.2015.03.015
35. Fertonani, A., Pirulli, C., & Miniussi, C. (2011). Random noise stimulation improves neuroplasticity in perceptual learning. Journal of Neuroscience, 31, 15416-15423. doi: 10.1523/JNEUROSCI.2002-11.2011
36. Feurra, M., Paulus, W., Walsh, V., & Kanai, R. (2011). Frequency specific modulation of human somatosensory cortex. Frontiers in Psychology, 2, 13. doi: 10.3389/fpsyg.2011.00013
37. Fregni, F., & Pascual-Leone, A. (2007). Technology insight: Noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nature Clinical Practice in Neurology, 3, 383-393. doi: 10.1038/ncpneuro0530
38. Fröhlich, F., & McCormick, D. A. (2010). Endogenous electric fields may guide neocortical network activity. Neuron, 67, 129-143. doi: 10.1016/j.neuron. 2010.06.005
39. Gandiga, P. C., Hummel, F. C., & Cohen, L. G. (2006). Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation. Clinical Neurophysiology, 117, 845-850.
40. Guleyupoglu, B., Schestatsky, P., Edwards, D., Fregni, F., & Bikson, M. (2013). Classification of methods in transcranial electrical stimulation (tES) and evolving strategy from historical approaches to contemporary innovations. Journal of Neuroscience Methods, 219, 297-311. doi: 10.1016/j.jneumeth.2013.07.016
41. Helfrich, R. F., Knepper, H., Nolte, G., Struber, D., Rach, S., Herrmann, C. S.,... Engel, A. K. (2014). Selective modulation of interhemispheric functional connectivity by HD-tACS shapes perception. PLoS Biology, 12, e1002031, doi: 10.1371/journal.pbio.1002031.
42. Helfrich, R. F., Schneider, T. R., Rach, S., Trautmann-Lengsfeld, S. A., Engel, A. K., & Herrmann, C. S. (2014). Entrainment of brain oscillations by transcranial alternating current stimulation. Current Biology, 24, 333-339. doi: 10.1016/j.cub.2013.12.041
43. Iyer, M. B., Mattu, U., Grafman, J., Lomarev, M., Sato, S., & Wassermann, E. M. (2005). Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology, 64, 872-875. doi: 10.1212/01. WNL.0000152986. 07469. E9
44. Jacobson, L., Koslowsky, M., & Lavidor, M. (2012). tDCS polarity effects in motor and cognitive domains: A metaanalytical review. Experimental Brain Research, 216, 1-10. doi: 10.1007/s00221-011-2891-9
45. Javadi, A. H., & Walsh, V. (2012). Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory. Brain Stimulation, 5, 231-241. doi: 10.1016/j.brs.2011.06.007
46. Joundi, R. A., Jenkinson, N., Brittain, J. S., Aziz, T. Z., & Brown, P. (2012). Driving oscillatory activity in the human cortex enhances motor performance. Current Biology, 22, 403-407. doi: 10.1016/j.cub.2012.01.024
47. Kabakov, A. Y., Muller, P. A., Pascual-Leone, A., Jensen, F. E., & Rotenberg, A. (2012). Contribution of axonal orientation to pathway-dependent modulation of excitatory transmission by direct current stimulation in isolated rat hippocampus. Journal of Neurophysiology, 107, 1881-1889. doi: 10.1152/jn. 00715.2011
48. Kanai, R., Paulus, W., & Walsh, V. (2010). Transcranial alternating current stimulation (tACS) modulates cortical excitability as assessed by TMS-induced phosphene thresholds. Clinical Neurophysiology, 121, 1551-1554. doi: 10.1016/j.clinph.2010.03.022
49. Kar, K., & Krekelberg, B. (2014). Transcranial alternating current stimulation attenuates visual motion adaptation. Journal of Neuroscience, 34, 7334-7340. doi: 10.1523/JNEUROSCI.5248-13.2014
50. Kuo, M. F., Paulus, W., & Nitsche, M. A. (2006). Sex differences in cortical neuroplasticity in humans. Neuroreport, 17, 1703-1707. doi: 10.1097/01.wnr.0000239955. 68319.c2
51. Kuo, M. F., Paulus, W., & Nitsche, M. A. (2008). Boosting focally-induced brain plasticity by dopamine. Cerebral Cortex, 18, 648-651. doi: 10.1093/cercor/bhm098
52. Kuo, M. F., Unger, M., Liebetanz, D., Lang, N., Tergau, F., Paulus, W., & Nitsche, M. A. (2008). Limited impact of homeostatic plasticity on motor learning in humans. Neuropsychologia, 46, 2122-2128. doi: 10.1016/j. neuropsychologia.2008.02.023
53. Laczó, B., Antal, A., Niebergall, R., Treue, S., & Paulus, W. (2012). Transcranial alternating stimulation in a high gamma frequency range applied over V1 improves contrast perception but does not modulate spatial attention. Brain Stimulation, 5, 484-491. doi: 10.1016/j.brs.2011.08.008
54. Lang, N., Siebner, H. R., Ward, N. S., Lee, L., Nitsche, M. A., Paulus, W.,... Frackowiak, R. S. (2005). How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? The European Journal of Neuroscience, 22, 495-504.
55. López-Alonso, V., Cheeran, B., Río-Rodríguez, D., & Fernández-Del-Olmo, M. (2014). Inter-individual variability in response to noninvasive brain stimulation paradigms. Brain Stimulation, 7, 372-380. doi: 10.1016/j.brs.2014.02.004
56. Marshall, L., Molle, M., Siebner, H. R., & Born, J. (2005). Bifrontal transcranial direct current stimulation slows reaction time in a working memory task. BMC Neuroscience, 6, 23. doi: 10.1186/1471-2202-6-23
57. Mei, F., Nagappan, G., Ke, Y., Sacktor, T. C., & Lu, B. (2011). BDNF facilitates L-LTP maintenance in the absence of protein synthesis through PKMzeta. PLoS One, 6, e21568. doi: 10.1371/journal.pone.0021568
58. Miniussi, C., Harris, J. A., & Ruzzoli, M. (2013). Modelling non-invasive brain stimulation in cognitive neuroscience. Neuroscience and Biobehavioral Reviews, 37, 1702-1712. doi: 10.1016/j.neubiorev. 2013.06.014
59. Miranda, P. C., Mekonnen, A., Salvador, R., & Ruffini, G. (2013). The electric field in the cortex during transcranial current stimulation. NeuroImage, 70, 48-58. doi: 10.1016/j.neuroimage.2012.12.034
60. Moliadze, V., Antal, A., & Paulus, W. (2010a). Boosting brain excitability by transcranial high frequency stimulation in the ripple range. Journal of Physiology, 588, 4891-4904. doi: 10.1113/jphysiol.2010.196998
61. Moliadze, V., Antal, A., & Paulus, W. (2010b). Electrodedistance dependent after-effects of transcranial direct and random noise stimulation with extracephalic reference electrodes. [Research Support, Non-U. S. Gov't]. Clinical Neurophysiology, 121, 2165-2171. doi: 10.1016/j.clinph.2010.04.033
62. Moliadze, V., Atalay, D., Antal, A., & Paulus, W. (2012). Close to threshold transcranial electrical stimulation preferentially activates inhibitory networks before switching to excitation with higher intensities. Brain Stimulation, 5, 505-511. doi: 10.1016/j.brs.2011.11.004
63. Monte-Silva, K., Kuo, M. F., Thirugnanasambandam, N., Liebetanz, D., Paulus, W., & Nitsche, M. A. (2009). Dosedependent inverted U-shaped effect of dopamine (D2-like) receptor activation on focal and nonfocal plasticity in humans. Jounral of Neuroscience, 29, 6124-6131. doi: 10.1523/JNEUROSCI.0728-09.2009
64. Monte-Silva, K., Liebetanz, D., Grundey, J., Paulus, W., & Nitsche, M. A. (2010). Dosage-dependent non-linear effect of L-dopa on human motor cortex plasticity. Journal of Physiology, 588, 3415-3424. doi: 10.1113/jphysiol.2010. 190181
65. Moss, F., Ward, L. M., & Sannita, W. G. (2004). Stochastic resonance and sensory information processing: A tutorial and review of application. Clinical Neurophysiology, 115, 267-281.
66. Mulquiney, P. G., Hoy, K. E., Daskalakis, Z. J., & Fitzgerald, P. B. (2011). Improving working memory: Exploring the effect of transcranial random noise stimulation and transcranial direct current stimulation on the dorsolateral prefrontal cortex. Clinical Neurophysiology, 122, 2384-2389. doi: 10.1016/j.clinph.2011.05.009
67. Neuling, T., Rach, S., & Herrmann, C. S. (2013). Orchestrating neuronal networks: Sustained after-effects of transcranial alternating current stimulation depend upon brain states. Frontiers in Human Neuroscience, 7, 161. doi: 10.3389/fnhum.2013.00161
68. Neuling, T., Rach, S., Wagner, S., Wolters, C. H., & Herrmann, C. S. (2012). Good vibrations: Oscillatory phase shapes perception. NeuroImage, 63, 771-778. doi: 10.1016/j.neuroimage.2012.07.024
69. Nitsche, M. A., Doemkes, S., Karakose, T., Antal, A., Liebetanz, D., Lang, N.,... Paulus, W. (2007). Shaping the effects of transcranial direct current stimulation of the human motor cortex. Journal of Neurophysiology, 97, 3109-3117. doi: 10.1152/jn. 01312.2006
70. Nitsche, M. A., Fricke, K., Henschke, U., Schlitterlau, A., Liebetanz, D., Lang, N.,... Paulus, W. (2003). Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. Journal of Physiology, 553, 293-301.
71. Nitsche, M. A., Grundey, J., Liebetanz, D., Lang, N., Tergau, F., & Paulus, W. (2004). Catecholaminergic consolidation of motor cortical neuroplasticity in humans. Cerebral Cortex, 14, 1240-1245.
72. Nitsche, M. A., Jakoubkova, M., Thirugnanasambandam, N., Schmalfuss, L., Hullemann, S., Sonka, K.,... Happe, S. (2010). Contribution of the premotor cortex to consolidation of motor sequence learning in humans during sleep. Journal of Neurophysiology, 104, 2603-2614. doi: 10.1152/jn. 00611.2010
73. Nitsche, M. A., Kuo, M. F., Karrasch, R., Wachter, B., Liebetanz, D., & Paulus, W. (2009). Serotonin affects transcranial direct current-induced neuroplasticity in humans. Biological Psychiatry, 66, 503-508. doi: 10.1016/j.biopsych. 2009.03.022
74. Nitsche, M. A., Liebetanz, D., Schlitterlau, A., Henschke, U., Fricke, K., Frommann, K.,... Tergau, F. (2004). GABAergic modulation of DC stimulation-induced motor cortex excitability shifts in humans. European Journal of Neuroscience, 19, 2720-2726.
75. Nitsche, M. A., Nitsche, M. S., Klein, C. C., Tergau, F., Rothwell, J. C., & Paulus, W. (2003). Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clinical Neurophysiology, 114, 600-604.
76. Nitsche, M. A., & Paulus, W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. Journal of Physiology, 527, 633-639.
77. Nitsche, M. A., & Paulus, W. (2001). Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology, 57, 1899-1901.
78. Nitsche, M. A., Schauenburg, A., Lang, N., Liebetanz, D., Exner, C., Paulus, W., & Tergau, F. (2003). Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. Journal of Cognitive Neuroscience, 15, 619-626.
79. Opitz, A., Paulus, W., Will, S., Antunes, A., & Thielscher, A. (2015). Determinants of the electric field during transcranial direct current stimulation. NeuroImage, 109 C, 140-150. doi: 10.1016/j.neuroimage.2015.01.033
80. Paulus, W. (2010). On the difficulties of separating retinal from cortical origins of phosphenes when using transcranial alternating current stimulation (tACS). Clinical Neurophysiology, 121, 987-991. doi: 10.1016/j.clinph.2010.01.029
81. Paulus, W. (2011). Transcranial electrical stimulation (tES - tDCS; tRNS, tACS) methods. Neuropsychology and Rehabilitaion, 21, 602-617. doi: 10.1080/09602011.2011.557292
82. Pirulli, C., Fertonani, A., & Miniussi, C. (2014). Is neural hyperpolarization by cathodal stimulation always detrimental at the behavioral level? Frontiers in Behavioral Neuroscience, 8, 226. doi: 10.3389/fnbeh.2014.00226
83. Pogosyan, A., Gaynor, L. D., Eusebio, A., & Brown, P. (2009). Boosting cortical activity at Beta-band frequencies slows movement in humans. Current Biology, 19, 1637-1641. doi: 10.1016/j.cub.2009.07.074
84. Polania, R., Nitsche, M. A., Korman, C., Batsikadze, G., & Paulus, W. (2012). The importance of timing in segregated theta phase-coupling for cognitive performance [Research Support, Non-U. S. Gov't]. Current Biology, 22, 1314-1318. doi: 10.1016/j.cub.2012.05.021
85. Polania, R., Nitsche, M. A., & Paulus, W. (2011). Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation [Research Support, Non-U. S. Gov't]. Human Brain Mapping, 32, 1236-1249. doi: 10.1002/hbm.21104
86. Poreisz, C., Boros, K., Antal, A., & Paulus, W. (2007). Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Research Bulletin, 72, 208-214.
87. Radman, T., Datta, A., Ramos, R. L., Brumberg, J. C., & Bikson, M. (2009). One-dimensional representation of a neuron in a uniform electric field. In Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, USA (pp. 6481-6484). doi: 10.1109/IEMBS.2009.5333586
88. Reato, D., Gasca, F., Datta, A., Bikson, M., Marshall, L., & Parra, L. C. (2013). Transcranial electrical stimulation accelerates human sleep homeostasis. PLoS Computational Biology, 9, e1002898. doi: 10.1371/journal.pcbi.1002898
89. Reato, D., Rahman, A., Bikson, M., & Parra, L. C. (2010). Lowintensity electrical stimulation affects network dynamics by modulating population rate and spike timing. Journal of Neuroscience, 30, 15067-15079. doi: 10.1523/JNEURO-SCI.2059-10.2010
90. Reis, J., Schambra, H. M., Cohen, L. G., Buch, E. R., Fritsch, B., Zarahn, E.,... Krakauer, J. W. (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proceedings of the National Academy of Sciences of USA, 106, 1590-1595. doi: 10.1073/pnas.0805413106
91. Reymann, K. G., & Frey, J. U. (2007). The late maintenance of hippocampal LTP: Requirements, phases, 'synaptic tagging', 'late-associativity' and implications. Neuropharmacology, 52, 24-40. doi: 10.1016/j.neuropharm.2006.07.026
92. Ruffini, G., Fox, M. D., Ripolles, O., Miranda, P. C., & Pascual-Leone, A. (2014). Optimization of multifocal transcranial current stimulation for weighted cortical pattern targeting from realistic modeling of electric fields. Neuroimage, 89, 216-225. doi: 10.1016/j.neuroimage.2013.12.002
93. Ruohonen, J., & Karhu, J. (2012). tDCS possibly stimulates glial cells. Clinical Neurophysiology, 123, 2006-2009. doi: 10.1016/j.clinph.2012.02.082
94. Schinder, A. F., & Poo, M. (2000). The neurotrophin hypothesis for synaptic plasticity. Trends in Neuroscience, 23, 639-645.
95. Schmidt, S. L., Iyengar, A. K., Foulser, A. A., Boyle, M. R., & Fröhlich, F. (2014). Endogenous cortical oscillations constrain neuromodulation by weak electric fields. Brain Stimulation, 7, 878-889. doi: 10.1016/j.brs.2014.07.033
96. Schoen, I., & Fromherz, P. (2008). Extracellular stimulation of mammalian neurons through repetitive activation of Na+ channels by weak capacitive currents on a silicon chip. Journal of Neurophysiology, 100, 346-357. doi: 10.1152/jn. 90287.2008
97. Schutter, D. J. L. G., & Hortensius, R. (2010). Retinal origin of phosphenes to transcranial alternating current stimulation. Clinical Neurophysiology, 121, 1080-1084.
98. Silvanto, J., Muggleton, N., & Walsh, V. (2008). State-dependency in brain stimulation studies of perception and cognition. Trends in Cognitive Science, 12, 447-454. doi: 10.1016/j.tics.2008.09.004
99. Snowball, A., Tachtsidis, I., Popescu, T., Thompson, J., Delazer, M., Zamarian, L.,... Cohen Kadosh, R. (2013). Long-term enhancement of brain function and cognition using cognitive training and brain stimulation. Current Biology, 23, 987-992. doi: 10.1016/j.cub.2013.04.045
100. Stacey, W. C., & Durand, D. M. (2000). Stochastic resonance improves signal detection in hippocampal CA1 neurons. Journal of Neurophysiology, 83, 1394-1402.
101. Stagg, C. J., Jayaram, G., Pastor, D., Kincses, Z. T., Matthews, P. M., & Johansen-Berg, H. (2011). Polarity and timingdependent effects of transcranial direct current stimulation in explicit motor learning. Neuropsychologia, 49, 800-804. doi: 10.1016/j.neuropsychologia.2011.02.009
102. Struber, D., Rach, S., Trautmann-Lengsfeld, S. A., Engel, A. K., & Herrmann, C. S. (2014). Antiphasic 40 Hz oscillatory current stimulation affects bistable motion perception. Brain Topography, 27, 158-171. doi: 10.1007/s10548-013-0294-x
103. Terney, D., Chaieb, L., Moliadze, V., Antal, A., & Paulus, W. (2008). Increasing human brain excitability by transcranial high-frequency random noise stimulation. Journal of Neuroscience, 28, 14147-14155. doi: 10.1523/JNEUROSCI. 4248-08.2008
104. Turi, Z., Ambrus, G. G., Janacsek, K., Emmert, K., Hahn, L., Paulus, W., & Antal, A. (2013). Both the cutaneous sensation and phosphene perception are modulated in a frequencyspecific manner during transcranial alternating current stimulation. Restorative Neurology and Neuroscience, 31, 275-285. doi: 10.3233/RNN-120297
105. Voss, U., Holzmann, R., Hobson, A., Paulus, W., Koppehele-Gossel, J., Klimke, A., & Nitsche, M. A. (2014). Induction of self awareness in dreams through frontal low current stimulation of gamma activity. Nature Neuroscience, 17, 810-812. doi: 10.1038/nn. 3719
106. Wiethoff, S., Hamada, M., & Rothwell, J. C. (2014). Variability in response to transcranial direct current stimulation of the motor cortex. Brain Stimulation, 7, 468-475. doi: 10.1016/j.brs.2014.02.003
107. Zaehle, T., Rach, S., & Herrmann, C. S. (2010). Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS One, 5, e13766. doi: 10.1371/journal.pone.0013766
108. Zaehle, T., Sandmann, P., Thorne, J. D., Jancke, L., & Herrmann, C. S. (2011). Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: Combined behavioural and electrophysiological evidence. BMC Neuroscience, 12, 2. doi: 10.1186/1471-2202-12-2
109. Zwissler, B., Sperber, C., Aigeldinger, S., Schindler, S., Kissler, J., & Plewnia, C. (2014). Shaping memory accuracy by left prefrontal transcranial direct current stimulation. Journal of Neuroscience, 34, 4022-4026. doi: 10.1523/JNEUROSCI. 5407-13.2014