Advertisement

Transcranial Direct Current Stimulation Modulation of Neurophysiological Functional Outcomes: Neurophysiological Principles and Rationale

  • Helena Knotkova
  • Michael A. Nitsche
  • Rafael PolaniaEmail author
Chapter

Abstract

For exploring physiological effects of tDCS in humans, numerous tools are available, spanning from measures allowing to monitor regional alterations of brain excitability and activity, to network alterations including modulation of remote areas. The most important tools to explore physiological effects in humans include transcranial magnetic stimulation, evoked potential measures, magnetic resonance tomography, electroencephalography and positron emission tomography. Although the main bulk of studies during the last years have explored tDCS effects on motor cortex excitability and activity, research has extended to other cortical areas, including association cortices, and interaction between remote cortices. This chapter will give a state of the art overview about regional physiological effects of tDCS on motor, sensory and multimodal brain areas, as well as about network effects of tDCS. Overall, the concept of tDCS modulation of functional outcomes in health and disease build on evidence suggesting that (i) the human neural system can undergo neuroplastic changes that may be associated with altered functional outcomes or pathological conditions, (ii) tDCS can induce neuroplasticity in the means of enduring alterations of neural activity and connectivity and thus can be used to attempt prevention or reversal of maladaptive neuroplastic changes or to enhance adaptive neuroplasticity.

Keywords

tDCS Physiological effects Functional outcomes Brain excitability Motor cortex Sensory cortex Neuroplasticity MEP, TMS, functional connectivity 

References

  1. Accornero, N., Voti, P. L., La Riccia, M., & Gregori, B. (2007). Visual evoked potentials modulation during direct current cortical polarization. Experimental Brain Research, 178(2), 261–266.PubMedPubMedCentralGoogle Scholar
  2. Albert, J., López-Martín, S., & Carretié, L. (2010). Emotional context modulates response inhibition: Neural and behavioral data. NeuroImage, 49(1), 914–921.PubMedCrossRefPubMedCentralGoogle Scholar
  3. Antal, A., Brepohl, N., Poreisz, C., Boros, K., Csifcsak, G., & Paulus, W. (2008). Transcranial direct current stimulation over somatosensory cortex decreases experimentally induced acute pain perception. The Clinical Journal of Pain, 24(1), 56–63.PubMedCrossRefPubMedCentralGoogle Scholar
  4. Antal, A., Chaieb, L., Moliadze, V., Monte-Silva, K., Poreisz, C., Thirugnanasambandam, N., & Paulus, W. (2010). Brain-derived neurotrophic factor (BDNF) gene polymorphisms shape cortical plasticity in humans. Brain Stimulation, 3(4), 230–237.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 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(3), 375–378.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 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(13), 1802–1807.PubMedCrossRefPubMedCentralGoogle Scholar
  7. Antal, A., Nitsche, M. A., Kincses, T. Z., Kruse, W., Hoffmann, K. P., & Paulus, W. (2004a). Facilitation of visuo-motor learning by transcranial direct current stimulation of the motor and extrastriate visual areas in humans. European Journal of Neuroscience, 19(10), 2888–2892.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Antal, A., Nitsche, M. A., Kruse, W., Kincses, T. Z., Hoffmann, K. P., & Paulus, W. (2004b). Direct current stimulation over V5 enhances visuomotor coordination by improving motion perception in humans. Journal of Cognitive Neuroscience, 16(4), 521–527.PubMedPubMedCentralGoogle Scholar
  9. Antal, A., Nitsche, M. A., & Paulus, W. (2001). External modulation of visual perception in humans. Neuroreport, 12(16), 3553–3555.PubMedCrossRefPubMedCentralGoogle Scholar
  10. Antal, A., Polania, R., Schmidt-Samoa, C., Dechent, P., & Paulus, W. (2011). Transcranial direct current stimulation over the primary motor cortex during fMRI. NeuroImage, 55(2), 590–596.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 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(9), 2687–2691.PubMedCrossRefPubMedCentralGoogle Scholar
  12. Ardolino, G., Bossi, B., Barbieri, S., & Priori, A. (2005). Non-synaptic mechanisms underlie the after-effects of cathodal transcutaneous direct current stimulation of the human brain. The Journal of Physiology, 568(2), 653–663.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Azanon, E., & Haggard, P. (2009). Somatosensory processing and the body representation. Cortex, 45(9), 1078–1084.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Barron, H. C., Vogels, T. P., Emir, U. E., Makin, T. R., O’Shea, J., Clare, S., … Behrens, T. E. J. (2016). Unmasking latent inhibitory connections in human cortex to reveal dormant cortical memories. Neuron, 90, 191–203.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Batsikadze, G., Moliadze, V., Paulus, W., Kuo, M. F., & Nitsche, M. A. (2013). Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. The Journal of Physiology, 591(7), 1987–2000.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Baudewig, J., Nitsche, M. A., Paulus, W., & Frahm, J. (2001). Regional modulation of BOLD MRI responses to human sensorimotor activation by transcranial direct current stimulation. Magnetic Resonance in Medicine, 45(2), 196–201.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Benninger, D. H., Lomarev, M., Lopez, G., Wassermann, E. M., Li, X., Considine, E., & Hallett, M. (2010). Transcranial direct current stimulation for the treatment of Parkinson’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 81(10), 1105–1111.CrossRefGoogle Scholar
  18. Bolzoni, F., Pettersson, L. G., & Jankowska, E. (2013). Evidence for long-lasting subcortical facilitation by transcranial direct current stimulation in the cat. The Journal of Physiology, 591(13), 3381–3399.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Boros, K., Poreisz, C., Münchau, A., Paulus, W., & Nitsche, M. A. (2008). Premotor transcranial direct current stimulation (tDCS) affects primary motor excitability in humans. European Journal of Neuroscience, 27(5), 1292–1300.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bradnam, L. V., Stinear, C. M., & Byblow, W. D. (2011). Cathodal transcranial direct current stimulation suppresses ipsilateral projections to presumed propriospinal neurons of the proximal upper limb. Journal of Neurophysiology, 105(5), 2582–2589.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10(3), 186–198.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Campanella, S., Schroder, E., Monnart, A., Vanderhasselt, M. A., Duprat, R., Rabijns, M., … Baeken, C. (2017). Transcranial direct current stimulation over the right frontal inferior cortex decreases neural activity needed to achieve inhibition: A double-blind ERP study in a male population. Clinical EEG and Neuroscience, 48(3), 176–188.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Chen, J. C., Hämmerer, D., D’Ostilio, K., Casula, E. P., Marshall, L., Tsai, C. H., … Edwards, M. J. (2014a). Bi-directional modulation of somatosensory mismatch negativity with transcranial direct current stimulation: An event related potential study. The Journal of Physiology, 592(4), 745–757.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Chen, J. C., Hämmerer, D., Strigaro, G., Liou, L. M., Tsai, C. H., Rothwell, J. C., & Edwards, M. J. (2014b). Domain-specific suppression of auditory mismatch negativity with transcranial direct current stimulation. Clinical Neurophysiology, 125(3), 585–592.PubMedCrossRefPubMedCentralGoogle Scholar
  25. Chib, V. S., Yun, K., Takahashi, H., & Shimojo, S. (2013). Noninvasive remote activation of the ventral midbrain by transcranial direct current stimulation of prefrontal cortex. Translational Psychiatry, 3, e268.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Clithero, J. A., & Rangel, A. (2013). Informatic parcellation of the network involved in the computation of subjective value. Social Cognitive and Affective Neuroscience, 9(9), 1289–1302.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Conti, C. L., Moscon, J. A., Fregni, F., Nitsche, M. A., & Nakamura-Palacios, E. M. (2014). Cognitive related electrophysiological changes induced by non-invasive cortical electrical stimulation in crack-cocaine addiction. The International Journal of Neuropsychopharmacology, 17(9), 1465–1475.PubMedCrossRefPubMedCentralGoogle Scholar
  28. Curio, G. (2000). Linking 600-Hz “spikelike” EEG/MEG wavelets (“sigma-bursts”) to cellular substrates: concepts and caveats. Journal of Clinical Neurophysiology, 17(4), 377–396. 11012041.PubMedCrossRefGoogle Scholar
  29. Curio, G., Mackert, B. M., Burghoff, M., Koetitz, R., Abraham-Fuchs, K., & Härer, W. (1994). Localization of evoked neuromagnetic 600 Hz activity in the cerebral somatosensory system. Electroencephalography and Clinical Neurophysiology, 91(6), 483–487.PubMedCrossRefGoogle Scholar
  30. Curio, G., Mackert, B. M., Burghoff, M., Neumann, J., Nolte, G., Scherg, M., & Marx, P. (1997). Somatotopic source arrangement of 600 Hz oscillatory magnetic fields at the human primary somatosensory hand cortex. Neuroscience Letters, 234(2), 131–134.PubMedCrossRefGoogle Scholar
  31. Daw, N. D., O’Doherty, J. P., Dayan, P., Seymour, B., & Dolan, R. J. (2006). Cortical substrates for exploratory decisions in humans. Nature, 441, 876–879.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Dieckhöfer, A., Waberski, T. D., Nitsche, M., Paulus, W., Buchner, H., & Gobbelé, R. (2006). Transcranial direct current stimulation applied over the somatosensory cortex–differential effect on low and high frequency SEPs. Clinical Neurophysiology, 117(10), 2221–2227.PubMedCrossRefGoogle Scholar
  33. Edwards, D., Cortes, M., Datta, A., Minhas, P., Wassermann, E. M., & Bikson, M. (2013). Physiological and modeling evidence for focal transcranial electrical brain stimulation in humans: A basis for high-definition tDCS. NeuroImage, 74, 266–275.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Faehling, F., & Plewnia, C. (2016). Controlling the emotional bias: Performance, late positive potentials, and the effect of anodal transcranial direct current stimulation (tDCS). Frontiers in Cellular Neuroscience, 10, 159. PubMed PMID: 27378856.Google Scholar
  35. 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 Stimulation, 2(2), 103–107.PubMedCrossRefGoogle Scholar
  36. Fricke, K., Seeber, A. A., Thirugnanasambandam, N., Paulus, W., Nitsche, M. A., & Rothwell, J. C. (2011). Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. Journal of Neurophysiology, 105(3), 1141–1149.PubMedCrossRefGoogle Scholar
  37. Fritsch, B., Reis, J., Martinowich, K., Schambra, H. M., Ji, Y., Cohen, L. G., & Lu, B. (2010). Direct current stimulation promotes BDNF-dependent synaptic plasticity: Potential implications for motor learning. Neuron, 66(2), 198–204.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Grueschow, M., Polania, R., Hare, T. A., & Ruff, C. C. (2015). Automatic versus choice-dependent value representations in the human brain. Neuron, 85(4), 874–885.PubMedCrossRefPubMedCentralGoogle Scholar
  39. Grundey, J., Thirugnanasambandam, N., Kaminsky, K., Drees, A., Skwirba, A. C., Lang, N., … Nitsche, M. A. (2012). Neuroplasticity in cigarette smokers is altered under withdrawal and partially restituted by nicotine exposition. The Journal of Neuroscience, 32(12), 4156–4162.PubMedCrossRefPubMedCentralGoogle Scholar
  40. Grundmann, L., Rolke, R., Nitsche, M. A., Pavlakovic, G., Happe, S., Treede, R. D., … Bachmann, C. G. (2011). Effects of transcranial direct current stimulation of the primary sensory cortex on somatosensory perception. Brain Stimulation, 4(4), 253–260.PubMedCrossRefPubMedCentralGoogle Scholar
  41. Haider, B., & Mccormick, D. A. (2009). Rapid neocortical dynamics: Cellular and network mechanisms. Neuron, 62, 171–189.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hasan, A., Nitsche, M. A., Rein, B., Schneider-Axmann, T., Guse, B., Gruber, O., … Wobrock, T. (2011). Dysfunctional long-term potentiation-like plasticity in schizophrenia revealed by transcranial direct current stimulation. Behavioural Brain Research, 224(1), 15–22.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Huttunen, J., Komssi, S., & Lauronen, L. (2006). Spatial dynamics of population activities at S1 after median and ulnar nerve stimulation revisited: An MEG study. NeuroImage, 32(3), 1024–1031.PubMedCrossRefGoogle Scholar
  44. Iezzi, E., Suppa, A., Conte, A., Li Voti, P., Bologna, M., & Berardelli, A. (2011). Short-term and long-term plasticity interaction in human primary motor cortex. European Journal of Neuroscience, 33(10), 1908–1915.PubMedCrossRefGoogle Scholar
  45. Impey, D., de la Salle, S., & Knott, V. (2016). Assessment of anodal and cathodal transcranial direct current stimulation (tDCS) on MMN-indexed auditory sensory processing. Brain and Cognition, 105, 46–54. PMID: 27054908.PubMedCrossRefGoogle Scholar
  46. Impey, D., & Knott, V. (2015). Effect of transcranial direct current stimulation (tDCS) on MMN-indexed auditory discrimination: A pilot study. Journal of Neural Transmission, 122(8), 1175–1185.PubMedCrossRefGoogle Scholar
  47. Jang, S. H., Ahn, S. H., Byun, W. M., Kim, C. S., Lee, M. Y., & Kwon, Y. H. (2009). The effect of transcranial direct current stimulation on the cortical activation by motor task in the human brain: An fMRI study. Neuroscience Letters, 460(2), 117–120.PubMedCrossRefGoogle Scholar
  48. Jefferson, S., Mistry, S., Singh, S., Rothwell, J., & Hamdy, S. (2009). Characterizing the application of transcranial direct current stimulation in human pharyngeal motor cortex. American Journal of Physiology. Gastrointestinal and Liver Physiology, 297(6), G1035–G1040.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Jeffery, D. T., Norton, J. A., Roy, F. D., & Gorassini, M. A. (2007). Effects of transcranial direct current stimulation on the excitability of the leg motor cortex. Experimental Brain Research, 182(2), 281–287.PubMedCrossRefGoogle Scholar
  50. Kasashima, Y., Fujiwara, T., Matsushika, Y., Tsuji, T., Hase, K., Ushiyama, J., … Liu, M. (2012). Modulation of event-related desynchronization during motor imagery with transcranial direct current stimulation (tDCS) in patients with chronic hemiparetic stroke. Experimental Brain Research, 221(3), 263–268.PubMedCrossRefPubMedCentralGoogle Scholar
  51. Kasuga, S., Matsushika, Y., Kasashima-Shindo, Y., Kamatani, D., Fujiwara, T., Liu, M., & Ushiba, J. (2015). Transcranial direct current stimulation enhances mu rhythm desynchronization during motor imagery that depends on handedness. Laterality: Asymmetries of Body, Brain and Cognition, 20(4), 453–468.CrossRefGoogle Scholar
  52. Kawamura, T., Nakasato, N., Seki, K., Kanno, A., Fujita, S., Fujiwara, S., & Yoshimoto, T. (1996). Neuromagnetic evidence of pre-and post-central cortical sources of somatosensory evoked responses. Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section, 100(1), 44–50.CrossRefGoogle Scholar
  53. Keeser, D., Meindl, T., Bor, J., Palm, U., Pogarell, O., Mulert, C., … Padberg, F. (2011). Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI. The Journal of Neuroscience, 31, 15284–15293.PubMedCrossRefPubMedCentralGoogle Scholar
  54. Kessler, S. K., Minhas, P., Woods, A. J., Rosen, A., Gorman, C., & Bikson, M. (2013). Dosage considerations for transcranial direct current stimulation in children: A computational modeling study. PLoS One, 8(9), e76112.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Kim, C. R., Kim, D. Y., Kim, L. S., Chun, M. H., Kim, S. J., & Park, C. H. (2012). Modulation of cortical activity after anodal transcranial direct current stimulation of the lower limb motor cortex: A functional MRI study. Brain Stimulation, 5(4), 462–467.PubMedCrossRefGoogle Scholar
  56. Kirimoto, H., Ogata, K., Onishi, H., Oyama, M., Goto, Y., & Tobimatsu, S. (2011). Transcranial direct current stimulation over the motor association cortex induces plastic changes in ipsilateral primary motor and somatosensory cortices. Clinical Neurophysiology, 122(4), 777–783.PubMedCrossRefGoogle Scholar
  57. Kojima, S., Onishi, H., Miyaguchi, S., Kotan, S., Sugawara, K., Kirimoto, H., & Tamaki, H. (2015). Effects of cathodal transcranial direct current stimulation to primary somatosensory cortex on short-latency afferent inhibition. Neuroreport, 26(11), 634–637.PubMedCrossRefPubMedCentralGoogle Scholar
  58. Krajbich, I., & Dean, M. (2015). How can neuroscience inform economics? Current Opinion Behavioral Science, 5, 51–57.CrossRefGoogle Scholar
  59. 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 Stimulation, 7(3), 443–450.PubMedCrossRefPubMedCentralGoogle Scholar
  60. Kuo, H. I., Bikson, M., Datta, A., Minhas, P., Paulus, W., Kuo, M. F., & Nitsche, M. A. (2013). Comparing cortical plasticity induced by conventional and high-definition 4× 1 ring tDCS: A neurophysiological study. Brain Stimulation, 6(4), 644–648.PubMedCrossRefGoogle Scholar
  61. Kuo, H. I., Paulus, W., Batsikadze, G., Jamil, A., Kuo, M. F., & Nitsche, M. A. (2016). Chronic enhancement of serotonin facilitates excitatory transcranial direct current stimulation-induced neuroplasticity. Neuropsychopharmacology, 41(5), 1223.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kuo, M. F., Paulus, W., & Nitsche, M. A. (2008). Boosting focally-induced brain plasticity by dopamine. Cerebral Cortex, 18(3), 648–651.PubMedCrossRefGoogle Scholar
  63. Kwon, Y. H., & Jang, S. H. (2011). The enhanced cortical activation induced by transcranial direct current stimulation during hand movements. Neuroscience Letters, 492(2), 105–108.PubMedCrossRefPubMedCentralGoogle Scholar
  64. Kwon, Y. H., Kang, K. W., Son, S. M., & Lee, N. K. (2015). Is effect of transcranial direct current stimulation on visuomotor coordination dependent on task difficulty? Neural Regeneration Research, 10(3), 463–466.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kwon, Y. H., Ko, M. H., Ahn, S. H., Kim, Y. H., Song, J. C., Lee, C. H., … Jang, S. H. (2008). Primary motor cortex activation by transcranial direct current stimulation in the human brain. Neuroscience Letters, 435(1), 56–59.PubMedCrossRefPubMedCentralGoogle Scholar
  66. Labruna, L., Jamil, A., Fresnoza, S., Batsikadze, G., Kuo, M. F., Vanderschelden, B., … Nitsche, M. A. (2016). Efficacy of anodal transcranial direct current stimulation is related to sensitivity to transcranial magnetic stimulation. Brain Stimulation, 9(1), 8–15.PubMedCrossRefGoogle Scholar
  67. 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? European Journal of Neuroscience, 22(2), 495–504.PubMedCrossRefPubMedCentralGoogle Scholar
  68. Lapenta, O. M., Di Sierve, K., de Macedo, E. C., Fregni, F., & Boggio, P. S. (2014). Transcranial direct current stimulation modulates ERP-indexed inhibitory control and reduces food consumption. Appetite, 83, 42–48.PubMedCrossRefGoogle Scholar
  69. Lapenta, O. M., Minati, L., Fregni, F., & Boggio, P. S. (2013). Je pense donc je fais: transcranial direct current stimulation modulates brain oscillations associated with motor imagery and movement observation. Frontiers in human neuroscience, 7, 256.Google Scholar
  70. 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(10), 2238–2247.PubMedCrossRefGoogle Scholar
  71. Lisman, J. E. (2001). Three Ca2+ levels affect plasticity differently: The LTP zone, the LTD zone and no man’s land. The Journal of Physiology, 532(2), 285–285.PubMedPubMedCentralCrossRefGoogle Scholar
  72. López-Alonso, V., Fernández-Del-Olmo, M., Costantini, A., Gonzalez-Henriquez, J. J., & Cheeran, B. (2015). Intra-individual variability in the response to anodal transcranial direct current stimulation. Clinical Neurophysiology, 126(12), 2342–2347.PubMedCrossRefGoogle Scholar
  73. Malenka, R. C., & Bear, M. F. (2004). LTP and LTD: An embarrassment of riches. Neuron, 44(1), 5–21.CrossRefGoogle Scholar
  74. Mathys, C., Loui, P., Zheng, X., & Schlaug, G. (2010). Non-invasive brain stimulation applied to Heschl’s gyrus modulates pitch discrimination. Frontiers in Psychology, 1, 193.PubMedPubMedCentralCrossRefGoogle Scholar
  75. Matsumoto, J., Fujiwara, T., Takahashi, O., Liu, M., Kimura, A., & Ushiba, J. (2010). Modulation of mu rhythm desynchronization during motor imagery by transcranial direct current stimulation. Journal of Neuroengineering and Rehabilitation, 7(1), 1.CrossRefGoogle Scholar
  76. Matsunaga, K., Nitsche, M. A., Tsuji, S., & Rothwell, J. C. (2004). Effect of transcranial DC sensorimotor cortex stimulation on somatosensory evoked potentials in humans. Clinical Neurophysiology, 115(2), 456–460.PubMedCrossRefPubMedCentralGoogle Scholar
  77. Mauguiere, F. (1999). Somatosensory evoked potentials: Normal responses, abnormal waveforms and clinical applications in neurological diseases. In E. Niedermeyer & F. Lopes Da Silva (Eds.), Electrocephalography: Basic principles,clinical applications and related fields (pp. 1014–1058). Baltimore: Williams and Wilkins.Google Scholar
  78. Mayberg, H. S., Lozano, A. M., Voon, V., Mcneely, H. E., Seminowicz, D., Hamani, C., … Kennedy, S. H. (2005). Deep brain stimulation for treatment-resistant depression. Neuron, 45, 651–660.PubMedCrossRefPubMedCentralGoogle Scholar
  79. Merritt, K., McGuire, P., & Egerton, A. (2013). Relationship between glutamate dysfunction and symptoms and cognitive function in psychosis. Frontiers in Psychiatry, 4, 151.Google Scholar
  80. Mccambridge, A. B., Stinear, J. W., & Byblow, W. D. (2015). ‘I-wave’ recruitment determines response to tDCS in the upper limb, but only so far. Brain Stimulation, 8(6), 1124–1129.PubMedCrossRefPubMedCentralGoogle Scholar
  81. Miyamoto, S., Miyake, N., Jarskog, L. F., Fleischhacker, W. W., & Lieberman, J. A. (2012). Pharmacological treatment of schizophrenia: A critical review of the pharmacology and clinical effects of current and future therapeutic agents. Molecular Psychiatry, 17, 1206–1227.PubMedCrossRefPubMedCentralGoogle Scholar
  82. Monte-Silva, K., Kuo, M. F., Hessenthaler, S., Fresnoza, S., Liebetanz, D., Paulus, W., & Nitsche, M. A. (2013). Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimulation, 6(3), 424–432.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Monte-Silva, K., Kuo, M. F., Liebetanz, D., Paulus, W., & Nitsche, M. A. (2010). Shaping the optimal repetition interval for cathodal transcranial direct current stimulation (tDCS). Journal of Neurophysiology, 103(4), 1735–1740.PubMedPubMedCentralCrossRefGoogle Scholar
  84. Nitsche, M. A., Doemkes, S., Karakoese, 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(4), 3109–3117.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Nitsche, M. A., Fricke, K., Henschke, U., Schlitterlau, A., Liebetanz, D., Lang, N., … Paulus, W. (2003a). Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. The Journal of Physiology, 553(1), 293–301.PubMedPubMedCentralCrossRefGoogle Scholar
  86. Nitsche, M. A., Jaussi, W., Liebetanz, D., Lang, N., Tergau, F., & Paulus, W. (2004a). Consolidation of human motor cortical neuroplasticity by D-cycloserine. Neuropsychopharmacology, 29(8), 1573–1578.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Nitsche, M. A., Kuo, M. F., Karrasch, R., Wächter, B., Liebetanz, D., & Paulus, W. (2009). Serotonin affects transcranial direct current–induced neuroplasticity in humans. Biological Psychiatry, 66(5), 503–508.PubMedPubMedCentralCrossRefGoogle Scholar
  88. Nitsche, M. A., Lampe, C., Antal, A., Liebetanz, D., Lang, N., Tergau, F., & Paulus, W. (2006). Dopaminergic modulation of long-lasting direct current-induced cortical excitability changes in the human motor cortex. European Journal of Neuroscience, 23(6), 1651–1657.PubMedCrossRefPubMedCentralGoogle Scholar
  89. Nitsche, M. A., Liebetanz, D., Schlitterlau, A., Henschke, U., Fricke, K., Frommann, K., … Tergau, F. (2004b). GABAergic modulation of DC stimulation-induced motor cortex excitability shifts in humans. European Journal of Neuroscience, 19(10), 2720–2726.PubMedCrossRefPubMedCentralGoogle Scholar
  90. Nitsche, M. A., Nitsche, M. S., Klein, C. C., Tergau, F., Rothwell, J. C., & Paulus, W. (2003b). Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clinical Neurophysiology, 114(4), 600–604.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Nitsche, M. A., & Paulus, W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. The Journal of Physiology, 527(3), 633–639.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Nitsche, M. A., & Paulus, W. (2001). Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology, 57(10), 1899–1901.PubMedPubMedCentralCrossRefGoogle Scholar
  93. Nitsche, M. A., Schauenburg, A., Lang, N., Liebetanz, D., Exner, C., Paulus, W., & Tergau, F. (2003c). Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. Journal of Cognitive Neuroscience, 15(4), 619–626.PubMedCrossRefPubMedCentralGoogle Scholar
  94. Nitsche, M. A., Seeber, A., Frommann, K., Klein, C. C., Rochford, C., Nitsche, M. S., … Paulus, W. (2005). Modulating parameters of excitability during and after transcranial direct current stimulation of the human motor cortex. The Journal of Physiology, 568(1), 291–303.PubMedPubMedCentralCrossRefGoogle Scholar
  95. Okun, M., & Lampl, I. (2008). Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nature Neuroscience, 11, 535–537.PubMedCrossRefPubMedCentralGoogle Scholar
  96. Pellicciari, M. C., Brignani, D., & Miniussi, C. (2013). Excitability modulation of the motor system induced by transcranial direct current stimulation: A multimodal approach. NeuroImage, 83, 569–580.PubMedCrossRefPubMedCentralGoogle Scholar
  97. Peña-Gómez, C., Sala-Lonch, R., Junqué, C., Clemente, I. C., Vidal, D., Bargalló, N., … Bartrés-Faz, D. (2012). Modulation of large-scale brain networks by transcranial direct current stimulation evidenced by resting-state functional MRI. Brain Stimulation, 5, 252–263.PubMedCrossRefPubMedCentralGoogle Scholar
  98. Pfefferbaum, A., Ford, J. M., Weller, B. J., & Kopell, B. S. (1985). ERPs to response production and inhibition. Electroencephalography and Clinical Neurophysiology, 60(5), 423–434.PubMedCrossRefPubMedCentralGoogle Scholar
  99. Polanía, R., Krajbich, I., Grueschow, M., & Ruff, C. C. (2014). Neural oscillations and synchronization differentially support evidence accumulation in perceptual and value-based decision making. Neuron, 82(3), 709–720.PubMedCrossRefPubMedCentralGoogle Scholar
  100. Polanía, R., Moisa, M., Opitz, A., Grueschow, M., & Ruff, C. C. (2015). The precision of value-based choices depends causally on fronto-parietal phase coupling. Nature Communications, 6, 8090.PubMedPubMedCentralCrossRefGoogle Scholar
  101. Polanía, R., Nitsche, M. A., Korman, C., Batsikadze, G., & Paulus, W. (2012a). The importance of timing in segregated theta phase-coupling for cognitive performance. Current Biology, 22(14), 1314–1318.PubMedCrossRefPubMedCentralGoogle Scholar
  102. Polanía, R., Nitsche, M. A., & Paulus, W. (2011a). Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation. Human Brain Mapping, 32(8), 1236–1249.PubMedCrossRefPubMedCentralGoogle Scholar
  103. Polanía, R., Paulus, W., Antal, A., & Nitsche, M. A. (2011b). Introducing graph theory to track for neuroplastic alterations in the resting human brain: A transcranial direct current stimulation study. NeuroImage, 54(3), 2287–2296.PubMedCrossRefPubMedCentralGoogle Scholar
  104. Polanía, R., Paulus, W., & Nitsche, M. A. (2012b). Noninvasively decoding the contents of visual working memory in the human prefrontal cortex within high-gamma oscillatory patterns. Journal of Cognitive Neuroscience, 24(2), 304–314.PubMedCrossRefGoogle Scholar
  105. Polanía, R., Paulus, W., & Nitsche, M. A. (2012c). Reorganizing the intrinsic functional architecture of the human primary motor cortex during rest with non-invasive cortical stimulation. PLoS One, 7(1), e30971.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Polanía, R., Paulus, W., & Nitsche, M. A. (2012d). Modulating cortico-striatal and thalamo-cortical functional connectivity with transcranial direct current stimulation. Human Brain Mapping, 33(10), 2499–2508.PubMedPubMedCentralCrossRefGoogle Scholar
  107. Ragert, P., Becker, M., Tegenthoff, M., Pleger, B., & Dinse, H. R. (2004a). Sustained increase of somatosensory cortex excitability by 5 Hz repetitive transcranial magnetic stimulation studied by paired median nerve stimulation in humans. Neuroscience Letters, 356(2), 91–94.PubMedCrossRefPubMedCentralGoogle Scholar
  108. Ragert, P., Franzkowiak, S., Schwenkreis, P., Tegenthoff, M., & Dinse, H. R. (2008a). Improvement of tactile perception and enhancement of cortical excitability through intermittent theta burst rTMS over human primary somatosensory cortex. Experimental Brain Research, 184(1), 1–11.PubMedCrossRefPubMedCentralGoogle Scholar
  109. Ragert, P., Schmidt, A., Altenmuèller, E., & Dinse, H. R. (2004b). Superior tactile performance and learning in professional pianists: Evidence for meta-plasticity in musicians. European Journal of Neuroscience, 19(2), 473–478.PubMedCrossRefPubMedCentralGoogle Scholar
  110. Ragert, P., Vandermeeren, Y., Camus, M., & Cohen, L. G. (2008b). Improvement of spatial tactile acuity by transcranial direct current stimulation. Clinical Neurophysiology, 119(4), 805–811.PubMedPubMedCentralCrossRefGoogle Scholar
  111. Raja, B. A., Polanía, R., Hare, T. A., & Ruff, C. C. (2015). Transcranial stimulation over Frontopolar cortex elucidates the choice attributes and neural mechanisms used to resolve exploration–exploitation trade-offs. The Journal of Neuroscience, 35(43), 14544–14556.CrossRefGoogle Scholar
  112. Rangel, A., Camerer, C., & Montague, P. R. (2008). A framework for studying the neurobiology of value-based decision making. Nature Reviews Neuroscience, 9(7), 545–556.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Rangel, A., & Hare, T. (2010). Neural computations associated with goal-directed choice. Current Opinion in Neurobiology, 20(2), 262–270.PubMedCrossRefPubMedCentralGoogle Scholar
  114. Ray Li, C.-S., Huang, C., Constable, R. T., & Sinha, R. (2006). Imaging response inhibition in a stop-signal task: Neural correlates independent of signal monitoring and post-response processing. The Journal of Neuroscience, 26, 186–192.CrossRefGoogle Scholar
  115. Rehmann, R., Sczesny-Kaiser, M., Lenz, M., Gucia, T., Schliesing, A., Schwenkreis, P., … Höffken, O. (2016). Polarity-specific cortical effects of transcranial direct current stimulation in primary somatosensory cortex of healthy humans. Frontiers in Human Neuroscience, 10, 208.Google Scholar
  116. Reis, J., Schambra, H. M., Cohen, L. G., Buch, E. R., Fritsch, B., Zarahn, E., … Krakauer, J. W. (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proceedings of the National Academy of Sciences, 106(5), 1590–1595.CrossRefGoogle Scholar
  117. Rivera-Urbina, G. N., Batsikadze, G., Molero-Chamizo, A., Paulus, W., Kuo, M. F., & Nitsche, M. A. (2015). Parietal transcranial direct current stimulation modulates primary motor cortex excitability. European Journal of Neuroscience, 41(6), 845–855.PubMedCrossRefPubMedCentralGoogle Scholar
  118. Rogalewski, A., Breitenstein, C., Nitsche, M. A., Paulus, W., & Knecht, S. (2004). Transcranial direct current stimulation disrupts tactile perception. European Journal of Neuroscience, 20(1), 313–316.PubMedCrossRefPubMedCentralGoogle Scholar
  119. Roy, A., Baxter, B., & He, B. (2014). High-definition transcranial direct current stimulation induces both acute and persistent changes in broadband cortical synchronization: A simultaneous tDCS–EEG study. IEEE Transactions on Biomedical Engineering, 61(7), 1967–1978.PubMedCrossRefPubMedCentralGoogle Scholar
  120. Ruff, C. C., Ugazio, G., & Fehr, E. (2013). Changing social norm compliance with noninvasive brain stimulation. Science, 342, 482–484.PubMedCrossRefPubMedCentralGoogle Scholar
  121. Saiote, C., Polanía, R., Rosenberger, K., Paulus, W., & Antal, A. (2013). High-frequency TRNS reduces BOLD activity during visuomotor learning. PLoS One, 8(3), e59669.PubMedPubMedCentralCrossRefGoogle Scholar
  122. Sanes, J. N. (2000). Motor cortex rules for learning and memory. Current Biology, 10, R495–R497.PubMedCrossRefGoogle Scholar
  123. Schade, S., Moliadze, V., Paulus, W., & Antal, A. (2012). Modulating neuronal excitability in the motor cortex with tDCS shows moderate hemispheric asymmetry due to subjects’ handedness: A pilot study. Restorative Neurology and Neuroscience, 30(3), 191–198.PubMedGoogle Scholar
  124. Sczesny-Kaiser, M., Beckhaus, K., Dinse, H. R., Schwenkreis, P., Tegenthoff, M., & Höffken, O. (2016). Repetitive transcranial direct current stimulation induced excitability changes of primary visual cortex and visual learning effects—A pilot study. Frontiers in Behavioral Neuroscience, 10, 116.PubMedPubMedCentralCrossRefGoogle Scholar
  125. Shah, B., Nguyen, T. T., & Madhavan, S. (2013). Polarity independent effects of cerebellar tDCS on short term ankle visuomotor learning. Brain Stimulation, 6(6), 966–968.PubMedCrossRefGoogle Scholar
  126. Siegel, M., Donner, T. H., & Engel, A. K. (2012). Spectral fingerprints of large-scale neuronal interactions. Nature Reviews Neuroscience, 13(2), 121–134.PubMedCrossRefGoogle Scholar
  127. Song, S., Sandrini, M., & Cohen, L. G. (2011). Modifying somatosensory processing with non-invasive brain stimulation. Restorative Neurology and Neuroscience, 29(6), 427–437.PubMedPubMedCentralGoogle Scholar
  128. Spitzer, M., Fischbacher, U., Herrnberger, B., Grön, G., & Fehr, E. (2007). The neural signature of social norm compliance. Neuron, 56, 185–196.PubMedCrossRefGoogle Scholar
  129. Stagg, C. J., Bachtiar, V., Amadi, U., Gudberg, C. A., Ilie, A. S., Sampaio-Baptista, C., … Near, J. (2014). Local GABA concentration is related to network-level resting functional connectivity. eLife, 3, e01465.PubMedPubMedCentralCrossRefGoogle Scholar
  130. Stagg, C. J., Best, J. G., Stephenson, M. C., O’Shea, J., Wylezinska, M., Kincses, Z. T., … Johansen-Berg, H. (2009). Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. The Journal of Neuroscience, 29(16), 5202–5206.PubMedPubMedCentralCrossRefGoogle Scholar
  131. Stam, C. J., Jones, B. F., Nolte, G., Breakspear, M., & Scheltens, P. (2007). Small-world networks and functional connectivity in Alzheimer’s disease. Cerebral Cortex, 17(1), 92–99.PubMedCrossRefGoogle Scholar
  132. Sugawara, K., Onishi, H., Yamashiro, K., Kojima, S., Miyaguchi, S., Kirimoto, H., … Kameyama, S. (2015). The effect of anodal transcranial direct current stimulation over the primary motor or somatosensory cortices on somatosensory evoked magnetic fields. Clinical Neurophysiology, 126(1), 60–67.PubMedCrossRefGoogle Scholar
  133. Tanaka, S., Hanakawa, T., Honda, M., & Watanabe, K. (2009). Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation. Experimental Brain Research, 196(3), 459–465.PubMedPubMedCentralCrossRefGoogle Scholar
  134. Thirugnanasambandam, N., Grundey, J., Adam, K., Drees, A., Skwirba, A. C., Lang, N., … Nitsche, M. A. (2011). Nicotinergic impact on focal and non-focal neuroplasticity induced by non-invasive brain stimulation in non-smoking humans. Neuropsychopharmacology, 36(4), 879–886.PubMedCrossRefGoogle Scholar
  135. Trepel, C., & Racine, R. J. (2000). GABAergic modulation of neocortical long-term potentiation in the freely moving rat. Synapse, 35(2), 120–128.CrossRefGoogle Scholar
  136. Tsakiris, M., Costantini, M., & Haggard, P. (2008). The role of the right temporo-parietal junction in maintaining a coherent sense of one’s body. Neuropsychologia, 46(12), 3014–3018.PubMedCrossRefGoogle Scholar
  137. Van Den Heuvel, M. P., & Pol, H. E. H. (2010). Exploring the brain network: A review on resting-state fMRI functional connectivity. European Neuropsychopharmacology, 20(8), 519–534.PubMedCrossRefGoogle Scholar
  138. Vines, B. W., Schnider, N. M., & Schlaug, G. (2006). Testing for causality with transcranial direct current stimulation: Pitch memory and the left supramarginal gyrus. Neuroreport, 17(10), 1047–1050.PubMedPubMedCentralCrossRefGoogle Scholar
  139. Wang, L., Yu, C., Chen, H., Qin, W., He, Y., Fan, F., … Woodward, T. S. (2010). Dynamic functional reorganization of the motor execution network after stroke. Brain, 133(4), 1224–1238.PubMedCrossRefGoogle Scholar
  140. Wang, Y., Hao, Y., Zhou, J., Fried, P. J., Wang, X., Zhang, J., … Manor, B. (2015). Direct current stimulation over the human sensorimotor cortex modulates the brain’s hemodynamic response to tactile stimulation. European Journal of Neuroscience, 42(3), 1933–1940.PubMedCrossRefGoogle Scholar
  141. Wiethoff, S., Hamada, M., & Rothwell, J. C. (2014). Variability in response to transcranial direct current stimulation of the motor cortex. Brain Stimulation, 7(3), 468–475.PubMedCrossRefGoogle Scholar
  142. Williams, S. M., & Goldman-Rakic, P. S. (1991). Characterization of the dopaminergic innervation of the primate frontal cortex using a dopamine-specific antibody. Cerebral Cortex, 3, 199–222.CrossRefGoogle Scholar
  143. Yang, B., Yang, S., Zhao, L., Yin, L., Liu, X., & An, S. (2009). Event-related potentials in a go/Nogo task of abnormal response inhibition in heroin addicts. Science in China Series C: Life Sciences, 52(8), 780–788.PubMedGoogle Scholar
  144. Yu, J., Tseng, P., Hung, D. L., Wu, S.-W., & Juan, C.-H. (2015). Brain stimulation improves cognitive control by modulating medial-frontal activity and preSMA-vmPFC functional connectivity. Human Brain Mapping, 36, 4004–4015.PubMedCrossRefGoogle Scholar
  145. Zaehle, T., Beretta, M., Jäncke, L., Herrmann, C. S., & Sandmann, P. (2011). Excitability changes induced in the human auditory cortex by transcranial direct current stimulation: Direct electrophysiological evidence. Experimental Brain Research, 215(2), 135–140.PubMedCrossRefGoogle Scholar
  146. Zheng, X., Alsop, D. C., & Schlaug, G. (2011). Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. NeuroImage, 58(1), 26–33.PubMedPubMedCentralCrossRefGoogle Scholar
  147. Zhou, Y., Liang, M., Jiang, T., Tian, L., Liu, Y., Liu, Z., … Kuang, F. (2007). Functional dysconnectivity of the dorsolateral prefrontal cortex in first-episode schizophrenia using resting-state fMRI. Neuroscience Letters, 417(3), 297–302.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2019

Authors and Affiliations

  • Helena Knotkova
    • 1
    • 2
  • Michael A. Nitsche
    • 3
    • 4
  • Rafael Polania
    • 5
    Email author
  1. 1.MJHS Institute for Innovation in Palliative CareNew YorkUSA
  2. 2.Department of Family and Social MedicineAlbert Einstein College of MedicineBronxUSA
  3. 3.Department of Psychology and NeurosciencesLeibniz Research Centre for Working Environment and Human FactorsDortmundGermany
  4. 4.University Medical Hospital BergmannsheilBochumGermany
  5. 5.ETH ZurichDecision Neuroscience Lab, Department of Health Sciences and TechnologyZurichSwitzerland

Personalised recommendations