Cellular and molecular mechanisms of action of transcranial direct current stimulation: Evidence from in vitro and in vivo models

International Journal of Neuropsychopharmacology

Volumn 18, Issue 2, 2015, Pages 1-13

  Pelletier, Simon J ^a,b   Cicchetti, Francesca ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Infammation; Long term potentiation; Neurogenesis

Indexed keywords

ANGIOGENESIS; APOPTOSIS; BRAIN ISCHEMIA; CHRONIC STRESS; EPILEPSY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MOLECULAR MECHANICS; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE POTENTIAL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SPREADING CORTICAL DEPRESSION; TRANSCRANIAL DIRECT CURRENT STIMULATION; ANIMAL; BRAIN; CELL MEMBRANE; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROCEDURES;

ANIMALS; BRAIN; CELL MEMBRANE; HUMANS; NEURONAL PLASTICITY; TRANSCRANIAL DIRECT CURRENT STIMULATION;

EID: 84931265498     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyu047     Document Type: Review

References (114)

1. Alexander JK, Fuss B, Colello RJ (2006) Electric feld-induced astrocyte alignment directs neurite outgrowth. Neuron Glia Biol 2:93-103..
2. Anastassiou CA, Perin R, Markram H, Koch C (2011) Ephaptic coupling of cortical neurons. Nat Neurosci 14:217-223..
3. Andrade C (2013) Once- to twice-daily, 3-year domiciliary maintenance transcranial direct current stimulation for severe, disabling, clozapine-refractory continuous auditory hallucinations in schizophrenia. J ECT 29:239-242..
4. Ariza CA, Fleury AT, Tormos CJ, Petruk V, Chawla S, Oh J, Saka-guchi DS, Mallapragada SK (2010) The infuence of electric felds on hippocampal neural progenitor cells. Stem Cell Rev 6:585-600..
5. Arlotti M, Rahman A, Minhas P, Bikson M (2012) Axon terminal polarization induced by weak uniform DC electric felds: a modeling study. Conf Proc IEEE Eng Med Biol Soc 2012:4575-4578..
6. Auvichayapat N, Rotenberg A, Gersner R, Ngodklang S, Tiamkao S, Tassaneeyakul W, Auvichayapat P (2013) Transcranial direct current stimulation for treatment of refractory childhood focal epilepsy. Brain Stimul 6:696-700..
7. Au-Yeung SS, Wang J, Chen Y, Chua E (2014) Transcranial direct current stimulation to primary motor area improves hand dexterity and selective attention in chronic stroke. Am J Phys Med Rehabil doi: 10.1097/PHM.0000000000000127..
8. Babona-Pilipos R, Droujinine IA, Popovic MR, Morshead CM (2011) Adult subependymal neural precursors, but not differentiated cells, undergo rapid cathodal migration in the presence of direct current electric felds. PLoS One 6:e23808..
9. Bai H, Forrester JV, Zhao M (2011) DC electric stimulation upregu-lates angiogenic factors in endothelial cells through activation of VEGF receptors. Cytokine 55:110-115..
10. Batsikadze G, Moliadze V, Paulus W, Kuo MF, Nitsche MA (2013) Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. J Physiol 591:1987-2000..
11. Bedlack RS, Jr, Wei M, Loew LM (1992) Localized membrane depolarizations and localized calcium infux during electric feld-guided neurite growth. Neuron 9:393-403..
12. Ben Taib NO, Manto M (2009) Trains of transcranial direct current stimulation antagonize motor cortex hypoexcitability induced by acute hemicerebellectomy. J Neurosurg 111:796-806..
13. Benninger DH, Lomarev M, Lopez G, Wassermann EM, Li X, Con-sidine E, Hallett M (2010) Transcranial direct current stimulation for the treatment of Parkinson's disease. J Neurol Neurosurg Psychiatry 81:1105-1111..
14. Bikson M, Inoue M, Akiyama H, Deans JK, Fox JE, Miyakawa H, Jefferys JG (2004) Effects of uniform extracellular DC electric felds on excitability in rat hippocampal slices in vitro. J Phys-iol 557:175-190..
15. Bikson M, Reato D, Rahman A (2012) Cellular and network effects of transcranial direct current stimulation: insights from animal models and brain slices. In: Frontiers in neuroscience, pp 55-91. Boca Raton, FL: CRC Press..
16. Bolzoni F, Pettersson LG, Jankowska E (2013a) Evidence for long-lasting subcortical facilitation by transcranial direct current stimulation in the cat. J Physiol 591:3381-3399..
17. Bolzoni F, Baczyk M, Jankowska E (2013b) Subcortical effects of transcranial direct current stimulation (tDCS) in the rat. J Physiol 15; 591:4027-4042..
18. Borgens RB, Blight AR, McGinnis ME (1987) Behavioral recovery induced by applied electric felds after spinal cord hemisec-tion in guinea pig. Science 238:366-369..
19. Borgens RB, Blight AR, McGinnis ME (1990) Functional recovery after spinal cord hemisection in guinea pigs: the effects of applied electric felds. J Comp Neurol 296:634-653..
20. Borgens RB, Toombs JP, Blight AR, McGinnis ME, Bauer MS, Wid-mer WR, Cook JR Jr. (1993) Effects of applied electric felds on clinical cases of complete paraplegia in dogs. Restor Neurol Neurosci 5:305-322..
21. Borgens RB, Shi R, Mohr TJ, Jaeger CB (1994) Mammalian cortical astrocytes align themselves in a physiological voltage gradient. Exp Neurol 128:41-49..
22. Brunoni AR, Nitsche MA, Bolognini N, Bikson M, Wagner T, Mer-abet L, Edwards DJ, Valero-Cabre A, Rotenberg A, Pascual-Leone A, Ferrucci R, Priori A, Boggio PS, Fregni F (2012) Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul 5:175-195..
23. Cambiaghi M, Velikova S, Gonzalez-Rosa JJ, Cursi M, Comi G, Leocani L (2010) Brain transcranial direct current stimulation modulates motor excitability in mice. Eur J Neurosci 31:704-709..
24. Cambiaghi M, Teneud L, Velikova S, Gonzalez-Rosa JJ, Cursi M, Comi G, Leocani L (2011) Flash visual evoked potentials in mice can be modulated by transcranial direct current stimulation. Neuroscience 185:161-165..
25. Cooper MS, Keller RE (1984) Perpendicular orientation and directional migration of amphibian neural crest cells in dc electrical felds. Proc Natl Acad Sci U S A 81:160-164..
26. Cork RJ, McGinnis ME, Tsai J, Robinson KR (1994) The growth of PC12 neurites is biased towards the anode of an applied electrical feld. J Neurobiol 25:1509-1516..
27. Cormie P, Robinson KR (2007) Embryonic zebrafsh neuronal growth is not affected by an applied electric feld in vitro. Neurosci Lett 411:128-132..
28. Dell'Osso B, Zanoni S, Ferrucci R, Vergari M, Castellano F, D'Urso N, Dobrea C, Benatti B, Arici C, Priori A, Altamura AC (2012) Transcranial direct current stimulation for the outpatient treatment of poor-responder depressed patients. Eur Psychiatry 27:513-517..
29. Derkach VA, Oh MC, Guire ES, Soderling TR (2007) Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 8:101-113..
30. Dockery CA, Liebetanz D, Birbaumer N, Malinowska M, Wesi-erska MJ (2011) Cumulative benefts of frontal transcranial direct current stimulation on visuospatial working memory training and skill learning in rats. Neurobiol Learn Mem 96:452-460..
31. Erskine L, Stewart R, McCaig CD (1995) Electric feld-directed growth and branching of cultured frog nerves: effects of ami-noglycosides and polycations. J Neurobiol 26:523-536..
32. Fecteau S, Agosta S, Hone-Blanchet A, Fregni F, Boggio P, Ciraulo D, Pascual-Leone A (2014) Modulation of smoking and decision-making behaviors with transcranial direct current stimulation in tobacco smokers: a preliminary study. Drug Alcohol Depend 140:78-84..
33. Feng JF, Liu J, Zhang XZ, Zhang L, Jiang JY, Nolta J, Zhao M (2012) Guided migration of neural stem cells derived from human embryonic stem cells by an electric feld. Stem Cells 30:349-355..
34. Ferrucci R, Vergari M, Cogiamanian F, Bocci T, Ciocca M, Tomasini E, De Riz M, Scarpini E, Priori A (2014) Transcranial direct current stimulation (tDCS) for fatigue in multiple sclerosis. Neu-roRehabilitation 34:121-127..
35. Franke K, Gruler H (1990) Galvanotaxis of human granulocytes: electric feld jump studies. Eur Biophys J 18:335-346..
36. Fregni F, Pascual-Leone A (2007) Technology insight: noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol 3:383-393..
37. Frey U, Frey S, Schollmeier F, Krug M (1996) Infuence of actino-mycin D, a RNA synthesis inhibitor, on long-term potentia-tion in rat hippocampal neurons in vivo and in vitro. J Physiol 490(Pt 3):703-711..
38. Fritsch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG, Lu B (2010) Direct current stimulation promotes BDNF-depend-ent synaptic plasticity: potential implications for motor learning. Neuron 66:198-204..
39. Gersner R, Kravetz E, Feil J, Pell G, Zangen A (2011) Long-term effects of repetitive transcranial magnetic stimulation on markers for neuroplasticity: differential outcomes in anesthetized and awake animals. J Neurosci 31:7521-7526..
40. Huang R, Peng L, Hertz L (1997) Effects of a low-voltage static electric feld on energy metabolism in astrocytes. Bioelectro-magnetics 18:77-80..
41. Hubbard JI, Willis WD (1962) Hyperpolarization of mammalian motor nerve terminals. J Physiol 163:115-137..
42. Hunter MA, Coffman BA, Trumbo MC, Clark VP (2013) Tracking the neuroplastic changes associated with transcranial direct current stimulation: a push for multimodal imaging. Front Hum Neurosci 7:495..
43. Im CH, Park JH, Shim M, Chang WH, Kim YH (2012) Evaluation of local electric fields generated by transcranial direct current stimulation with an extracephalic reference electrode based on realistic 3D body modeling. Phys Med Biol 57:2137-2150..
44. Ingvar S (1920) Reaction of cells to the galvanic current in tissue cultures. Exp Biol Med 17:198-199..
45. Jennings J, Chen D, Feldman D (2008) Transcriptional response of dermal fbroblasts in direct current electric felds. Bioelectro-magnetics 29:394-405..
46. Jiang T, Xu RX, Zhang AW, Di W, Xiao ZJ, Miao JY, Luo N, Fang YN (2012) Effects of transcranial direct current stimulation on hemichannel pannexin-1 and neural plasticity in rat model of cerebral infarction. Neuroscience 226:421-426..
47. Kabakov AY, Muller PA, Pascual-Leone A, Jensen FE, Rotenberg A (2012) Contribution of axonal orientation to pathway-dependent modulation of excitatory transmission by direct current stimulation in isolated rat hippocampus. J Neuro-physiol 107:1881-1889..
48. Kamida T, Kong S, Eshima N, Abe T, Fujiki M, Kobayashi H (2011) Transcranial direct current stimulation decreases convulsions and spatial memory deficits following pilocarpine-induced status epilepticus in immature rats. Behav Brain Res 217:99-103..
49. Kampa BM, Clements J, Jonas P, Stuart GJ (2004) Kinetics of Mg2+ unblock of NMDA receptors: implications for spike-timing dependent synaptic plasticity. J Physiol 556:337-345..
50. Kim SJ, Kim BK, Ko YJ, Bang MS, Kim MH, Han TR (2010) Functional and histologic changes after repeated transcranial direct current stimulation in rat stroke model. J Korean Med Sci 25:1499-1505..
51. Koppes AN, Seggio AM, Thompson DM (2011) Neurite outgrowth is significantly increased by the simultaneous presentation of Schwann cells and moderate exogenous electric felds. J Neural Eng 8:046023..
52. Lamy JC, Boakye M (2013) BDNF Val66Met polymorphism alters spinal DC stimulation-induced plasticity in humans. J Neuro-physiol 110:109-116..
53. Lang N, Siebner HR, Ward NS, Lee L, Nitsche MA, Paulus W, Rothwell JC, Lemon RN, Frackowiak RS (2005) How does tran-scranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur J Neurosci 22:495-504.
54. Laste G, Caumo W, Adachi LN, Rozisky JR, De Macedo IC, Filho PR, Partata WA, Fregni F, Torres IL (2012) After-effects of consecutive sessions of transcranial direct current stimulation (tDCS) in a rat model of chronic infammation. Exp Brain Res 221:75-83..
55. Li L, El-Hayek YH, Liu B, Chen Y, Gomez E, Wu X, Ning K, Li L, Chang N, Zhang L, Wang Z, Hu X, Wan Q (2008) Direct-current electrical feld guides neuronal stem/progenitor cell migration. Stem Cells 26:2193-2200..
56. Li J, Nandagopal S, Wu D, Romanuik SF, Paul K, Thomson DJ, Lin F (2011a) Activated T lymphocytes migrate toward the cathode of DC electric felds in microfuidic devices. Lab Chip 11:1298-1304..
57. Li Y, Tian X, Qian L, Yu X, Jiang W (2011b) Anodal transcranial direct current stimulation relieves the unilateral bias of a rat model of Parkinson's disease. Conf Proc IEEE Eng Med Biol Soc 2011:765-768..
58. Liebetanz D, Nitsche MA, Tergau F, Paulus W (2002) Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain 125:2238-2247..
59. Liebetanz D, Fregni F, Monte-Silva KK, Oliveira MB, Amancio-dos-Santos A, Nitsche MA, Guedes RC (2006a) After-effects of transcranial direct current stimulation (tDCS) on cortical spreading depression. Neurosci Lett 398:85-90..
60. Liebetanz D, Klinker F, Hering D, Koch R, Nitsche MA, Potschka H, Loscher W, Paulus W, Tergau F (2006b) Anticonvulsant effects of transcranial direct-current stimulation (tDCS) in the rat cortical ramp model of focal epilepsy. Epilepsia 47:1216-1224..
61. Liebetanz D, Koch R, Mayenfels S, Konig F, Paulus W, Nitsche MA (2009) Safety limits of cathodal transcranial direct current stimulation in rats. Clin Neurophysiol 120:1161-1167..
62. Lin SL, Li Y, Woolley AT, Lee ML, Tolley HD, Warnick KF (2008) Programmed elution and peak profles in electric feld gradient focusing. Electrophoresis 29:1058-1066..
63. Long H, Yang G, Wang Z (2011) Galvanotactic migration of EA. Hy926 endothelial cells in a novel designed electric feld bioreactor. Cell Biochem Biophys 61:481-491..
64. Marquez-Ruiz J, Leal-Campanario R, Sanchez-Campusano R, Molaee-Ardekani B, Wendling F, Miranda PC, Ruffni G, Gru-art A, Delgado-Garcia JM (2012) Transcranial direct-current stimulation modulates synaptic mechanisms involved in associative learning in behaving rabbits. Proc Natl Acad Sci U S A 109:6710-6715..
65. McCaig CD, Sangster L, Stewart R (2000) Neurotrophins enhance electric feld-directed growth cone guidance and directed nerve branching. Dev Dyn 217:299-308..
66. McCaig CD, Rajnicek AM, Song B, Zhao M (2005) Controlling cell behavior electrically: current views and future potential. Physiol Rev 85:943-978..
67. McLaughlin S, Poo MM (1981) The role of electro-osmosis in the electric-feld-induced movement of charged macromolecules on the surfaces of cells. Biophys J 34:85-93..
68. Meng X, Arocena M, Penninger J, Gage FH, Zhao M, Song B (2011) PI3K mediated electrotaxis of embryonic and adult neural progenitor cells in the presence of growth factors. Exp Neurol 227:210-217..
69. Minichiello L (2009) TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 10:850-860..
70. Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, Nitsche MA (2013) Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul 6:424-432..
71. Mycielska ME, Djamgoz MB (2004) Cellular mechanisms of direct-current electric feld effects: galvanotaxis and meta-static disease. J Cell Sci 117:1631-1639..
72. Neal AP, Guilarte TR (2010) Molecular neurobiology of lead (Pb (2+)): effects on synaptic function. Mol Neurobiol 42:151-160..
73. Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57:1899-1901..
74. Nitsche MA, 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. Eur J Neurosci 23:1651-1657..
75. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: State of the art 2008. Brain Stimul 1:206-223..
76. Nitsche MA, Kuo MF, Karrasch R, Wachter B, Liebetanz D, Paulus W (2009) Serotonin affects transcranial direct current-induced neuroplasticity in humans. Biol Psychiatry 66:503-508..
77. Nitsche MA, Muller-Dahlhaus F, Paulus W, Ziemann U (2012) The pharmacology of neuroplasticity induced by non-invasive brain stimulation: building models for the clinical use of CNS active drugs. J Physiol. 590:4641-4662.
78. Opazo P, Labrecque S, Tigaret CM, Frouin A, Wiseman PW, De Koninck P, Choquet D (2010) CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of star-gazin. Neuron 67:239-252..
79. Orida N, Feldman JD (1982) Directional protrusive pseudopodial activity and motility in macrophages induced by extracellular electric felds. Cell Motil 2:243-255..
80. Palmer AM, Messerli MA, Robinson KR (2000) Neuronal galva-notropism is independent of external Ca (2+) entry or internal Ca (2+) gradients. J Neurobiol 45:30-38..
81. Pan L, Borgens RB (2010) Perpendicular organization of sympathetic neurons within a required physiological voltage. Exp Neurol 222:161-164..
82. Patel N, Poo MM (1982) Orientation of neurite growth by extracellular electric felds. J Neurosci 2:483-496..
83. Pedron S, Monnin J, Haffen E, Sechter D, Van Waes V (2014) Repeated transcranial direct current stimulation prevents abnormal behaviors associated with abstinence from chronic nicotine consumption. Neuropsychopharmacology 39:981-988..
84. Pelletier SJ, Lagace M, St-Amour I, Arsenault D, Cisbani G, Chabrat A, Fecteau S, Levesque M, Cicchetti F (2014) The morphological and molecular changes of brain cells exposed to direct current electric feld stimulation. Int J Neuropsychopharmacol in press..
85. Perret S, Cantereau A, Audin J, Dufy B, Georgescauld D (1999) Interplay between Ca2+ release and Ca2+ infux underlies localized hyperpolarization-induced [Ca2+]i waves in pros-tatic cells. Cell Calcium 25:297-311..
86. Peruzzotti-Jametti L, Cambiaghi M, Bacigaluppi M, Gallizioli M, Gaude E, Mari S, Sandrone S, Cursi M, Teneud L, Comi G, Musco G, Martino G, Leocani L (2013) Safety and efficacy of transcranial direct current stimulation in acute experimental ischemic stroke. Stroke 44:3166-3174..
87. Pozzo-Miller LD, Gottschalk W, Zhang L, McDermott K, Du J, Gopalakrishnan R, Oho C, Sheng ZH, Lu B (1999) Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J Neurosci 19:4972-4983..
88. Purpura DP, McMurtry JG (1965) Intracellular activities and evoked potential changes during polarization of motor cortex. J Neurophysiol 28:166-185..
89. Radman T, Ramos RL, Brumberg JC, Bikson M (2009) Role of cortical cell type and morphology in subthreshold and suprath-reshold uniform electric feld stimulation in vitro. Brain Stimul 2:215-228, 228 e211-213..
90. Rahman A, Reato D, Arlotti M, Gasca F, Datta A, Parra LC, Bikson M (2013) Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects. J Physiol 591:2563-2578..
91. Rajnicek AM, Foubister LE, McCaig CD (2006) Temporally and spatially coordinated roles for Rho, Rac, Cdc42 and their effectors in growth cone guidance by a physiological electric feld. J Cell Sci 119:1723-1735..
92. Ranieri F, Podda MV, Riccardi E, Frisullo G, Dileone M, Profice P, Pilato F, Di Lazzaro V, Grassi C (2012) Modulation of LTP at rat hippocampal CA3-CA1 synapses by direct current stimulation. J Neurophysiol 107:1868-1880..
93. Rueger MA, Keuters MH, Walberer M, Braun R, Klein R, Sparing R, Fink GR, Graf R, Schroeter M (2012) Multi-session transcranial direct current stimulation (tDCS) elicits infammatory and regenerative processes in the rat brain. PLoS One 7:e43776..
94. Schweid L, Rushmore RJ, Valero-Cabre A (2008) Cathodal tran-scranial direct current stimulation on posterior parietal cortex disrupts visuo-spatial processing in the contralateral visual feld. Exp Brain Res 186:409-417..
95. Smolen P (2007) A model of late long-term potentiation simulates aspects of memory maintenance. PLoS One 2:e445..
96. Sohn MK, Jee SJ, Kim YW (2013) Effect of transcranial direct current stimulation on postural stability and lower extremity strength in hemiplegic stroke patients. Ann Rehabil Med 37:759-765..
97. Song B, Gu Y, Pu J, Reid B, Zhao Z, Zhao M (2007) Application of direct current electric felds to cells and tissues in vitro and modulation of wound electric feld in vivo. Nat Protoc 2:1479-1489..
98. Spezia Adachi LN, Caumo W, Laste G, Fernandes Medeiros L, Rip-oll Rozisky J, De Souza A, Fregni F, Torres IL (2012) Reversal of chronic stress-induced pain by transcranial direct current stimulation (tDCS) in an animal model. Brain Res 1489:17-26..
99. Stagg CJ, Nitsche MA (2011) Physiological basis of transcranial direct current stimulation. Neuroscientist 17:37-53..
100. Stagg CJ, O'Shea J, Kincses ZT, Woolrich M, Matthews PM, Johansen-Berg H (2009a) Modulation of movement-associated cortical activation by transcranial direct current stimulation. Eur J Neurosci 30:1412-1423..
101. Stagg CJ, Best JG, Stephenson MC, O'Shea J, Wylezinska M, Kinc-ses ZT, Morris PG, Matthews PM, Johansen-Berg H (2009b) Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci 29:5202-5206..
102. Tahtis V, Kaski D, Seemungal BM (2014) The effect of single session bi-cephalic transcranial direct current stimulation on gait performance in sub-acute stroke: a pilot study. Restor Neurol Neurosci, doi: 10.3233/RNN-140393..
103. Takano Y, Yokawa T, Masuda A, Niimi J, Tanaka S, Hironaka N (2011) A rat model for measuring the effectiveness of transcranial direct current stimulation using fMRI. Neurosci Lett 491:40-43..
104. Tanaka T, Takano Y, Tanaka S, Hironaka N, Kobayashi K, Hanakawa T, Watanabe K, Honda M (2013) Transcranial direct-current stimulation increases extracellular dopamine levels in the rat striatum. Front Syst Neurosci 7:6..
105. Viard P, Butcher AJ, Halet G, Davies A, Nurnberg B, Heblich F, Dolphin AC (2004) PI3K promotes voltage-dependent calcium channel trafficking to the plasma membrane. Nat Neurosci 7:939-946..
106. Wachter D, Wrede A, Schulz-Schaeffer W, Taghizadeh-Waghef A, Nitsche MA, Kutschenko A, Rohde V, Liebetanz D (2011) Tran-scranial direct current stimulation induces polarity-specific changes of cortical blood perfusion in the rat. Exp Neurol 227:322-327..
107. Wood MD, Willits RK (2009) Applied electric feld enhances DRG neurite growth: infuence of stimulation media, surface coating and growth supplements. J Neural Eng 6:046003..
108. Yoon KJ, Oh BM, Kim DY (2012) Functional improvement and neuroplastic effects of anodal transcranial direct current stimulation (tDCS) delivered 1 day vs.1 week after cerebral ischemia in rats. Brain Res 1452:61-72..
109. Zhang P, Liu ZT, He GX, Liu JP, Feng J (2011) Low-voltage direct-current stimulation is safe and promotes angiogenesis in rabbits with myocardial infarction. Cell Biochem Biophys 59:19-27..
110. Zhao M (2009) Electrical felds in wound healing: an overriding signal that directs cell migration. Semin Cell Dev Biol 20:674-682..
111. Zhao M, Bai H, Wang E, Forrester JV, McCaig CD (2004) Electrical stimulation directly induces pre-angiogenic responses in vascular endothelial cells by signaling through VEGF receptors. J Cell Sci 117:397-405..
112. Zhao M, Song B, Pu J, Wada T, Reid B, Tai G, Wang F, Guo A, Wal-czysko P, Gu Y, Sasaki T, Suzuki A, Forrester JV, Bourne HR, Devreotes PN, McCaig CD, Penninger JM (2006) Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature 442:457-460..
113. Zhao Z, Qin L, Reid B, Pu J, Hara T, Zhao M (2012) Directing migration of endothelial progenitor cells with applied DC electric felds. Stem Cell Res 8:38-48..
114. Zobeiri M, Van Luijtelaar G (2013) Noninvasive transcranial direct current stimulation in a genetic absence model. Epilepsy Behav 26:42-50.