Not all brains are created equal: The relevance of individual differences in responsiveness to transcranial electrical stimulation

Frontiers in Systems Neuroscience

Volumn 8, Issue FEB, 2014, Pages

  Krause, Beatrix ^a   Kadosh, Roi Cohen ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Efficacy; Excitation; Individual; Inhibition; Responsive; Transcranial electrical stimulation

Indexed keywords

EID: 84899689891     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00025     Document Type: Review

References (112)

1. Alonzo, A., Brassil, J., Taylor, J. L., Martin, D., and Loo, C. K. (2012). Daily transcranial direct current stimulation (tDCS) leads to greater increases in cortical excitability than second daily transcranial direct current stimulation. Brain Stimul. 5, 208-213. doi: 10.1016/j.brs.2011.04.006.
2. Antal, A., Terney, D., Poreisz, C., and Paulus, W. (2007). Towards unravelling task-related modulations of neuroplastic changes induced in the human motor cortex. Eur. J. Neurosci. 26, 2687-2691. doi: 10.1111/j.1460-9568.2007.05896.x
3. Batra, N. A., Seres-Mailo, J., Hanstock, C., Seres, P., Khudabux, J., Bellavance, F., et al. (2008). Proton magnetic resonance spectroscopy measurement of brain glutamate levels in premenstrual dysphoric disorder. Biol. Psychiatry 63, 1178-1184. doi: 10.1016/j.biopsych.2007.10.007.
4. Batsikadze, G., Moliadze, V., Paulus, W., Kuo, M. F., and Nitsche, M. A. (2013). Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. J. Physiol. 591, 1987-2000. doi: 10.1113/jphysiol.2012.249730.
5. Bavelier, D., Levi, D. M., Li, R. W., Dan, Y., and Hensch, T. K. (2010). Removing brakes on adult brain plasticity: from molecular to behavioral interventions. J. Neurosci. 30, 14964-14971. doi: 10.1523/jneurosci.4812-10.2010.
6. Belousov, A. B. (2012). Novel model for the mechanisms of glutamate-dependent excitotoxicity: role of neuronal gap junctions. Brain Res. 1487, 123-130. doi: 10. 1016/j.brainres.2012.05.063.
7. Bikson, M., Inoue, M., Akiyama, H., Deans, J. K., Fox, J. E., Miyakawa, H., et al. (2004). Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices invitro. J. Physiol. 557, 175-190. doi: 10.1113/jphysiol.2003. 055772
8. Bikson, M., Rahman, A., and Datta, A. (2012). Computational models of tran-scranial direct current stimulation. Clin. EEG Neurosci. 43, 176-183. doi: 10. 1177/1550059412445138.
9. Bolognini, N., Fregni, F., Casati, C., Olgiati, E., and Vallar, G. (2010). Brain polarization of parietal cortex augments training-induced improvement of visual exploratory and attentional skills. Brain Res. 1349, 76-89. doi: 10.1016/j. brainres.2010.06.053.
10. Brasil-Neto, J. P. (2012). Learning, memory and transcranial direct current stimulation. Front. Psychiatry 3:80. doi: 10.3389/fpsyt.2012.00080.
11. Brem, A.-K., Fried, P. J., Horvath, J. C., Robertson, E. M., and Pascual-Leone, A. (2014). Is neuroenhancement by noninvasive brain stimulation a net zero-sum proposition? Neuroimage 85(Pt. 3), 1058-1068. doi: 10.1016/j.neuroimage.2013. 07.038
12. Brignani, D., Ruzzoli, M., Mauri, P., and Miniussi, C. (2013). Is transcranial alternating current stimulation effective in modulating brain oscillations? PLoS One 8:e56589. doi: 10.1371/journal.pone.0056589.
13. Brittain, J. S., Probert-Smith, P., Aziz, T. Z., and Brown, P. (2013). Tremor suppression by rhythmic transcranial current stimulation. Curr. Biol. 23, 436-440. doi: 10.1016/j.cub.2013.01.068.
14. Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 17, 85-100. doi: 10.1037//0882-7974. 17.1.85
15. Caporale, N., and Dan, Y. (2008). Spike timing-dependent plasticity: a Hebbian learning rule. Annu. Rev. Neurosci. 31, 25-46. doi: 10.1146/annurev.neuro.31. 060407.125639
16. Cohen Kadosh, R. (2013). Using transcranial electrical stimulation to enhance cognitive functions in the typical and atypical brain. Transl. Neurosci. 4, 20-33. doi: 10.2478/s13380-013-0104-7.
17. Cohen Kadosh, R., Muggleton, N., Silvanto, J., and Walsh, V. (2010a). Double dissociation of format-dependent and number-specific neurons in human parietal cortex. Cereb. Cortex 20,2166-2171. doi: 10.1093/cercor/bhp273.
18. Cohen Kadosh, R., Soskic, S., Iuculano, T., Kanai, R., and Walsh, V. (2010b). Modulating neuronal activity produces specific and long-lasting changes in numerical competence. Curr. Biol. 20, 2016-2020. doi: 10.1016/j.cub.2010. 10.007
19. Cramer, S. C., Nelles, G., Benson, R. R., Kaplan, J. D., Parker, R. A., Kwong, K. K., et al. (1997). A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28, 2518-2527. doi: 10.1161/01.str.28.12.2518.
20. Cramer, S. C., Sur, M., Dobkin, B. H., O'brien, C., Sanger, T. D., Trojanowski, J. Q., et al. (2011). Harnessing neuroplasticity for clinical applications. Brain 134, 1591-1609. doi: 10.1093/brain/awr039.
21. Datta, A., Truong, D., Minhas, P., Parra, L. C., and Bikson, M. (2012). Interindividual variation during transcranial direct current stimulation and normalization of dose using MRI-derived computational models. Front. Psychiatry 3:91. doi: 10.3389/fpsyt.2012.00091.
22. Dockery, C. A., Hueckel-Weng, R., Birbaumer, N., and Plewnia, C. (2009). Enhancement of planning ability by transcranial direct current stimulation. J. Neurosci. 29, 7271-7277. doi: 10.1523/jneurosci.0065-09.2009.
23. Dorrn, A. L., Yuan, K., Barker, A. J., Schreiner, C. E., and Froemke, R. C. (2010). Developmental sensory experience balances cortical excitation and inhibition. Nature 465, 932-936. doi: 10.1038/nature09119.
24. Edwards, D., Cortes, M., Datta, A., Minhas, P., Wassermann, E. M., and 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. doi: 10.1016/j.neuroimage.2013.01.042.
25. Eichler, S. A., and Meier, J. C. (2008). E-I balance and human diseases-from molecules to networking. Front. Mol. Neurosci. 1:2. doi: 10.3389/neuro.02.002. 2008
26. Epperson, C. N., Haga, K., Mason, G. F., Sellers, E., Gueorguieva, R., Zhang, W., et al. (2002). Cortical gamma-aminobutyric acid levels across the menstrual cycle in healthy women and those with premenstrual dysphoric disorder: a proton magnetic resonance spectroscopy study. Arch. Gen. Psychiatry 59, 851-858. doi: 10.1001/archpsyc.59.9.851.
27. Epperson, C. N., O'malley, S., Czarkowski, K. A., Gueorguieva, R., Jatlow, P., Sanacora, G., et al. (2005). Sex, GABA and nicotine: the impact of smoking on cortical GABA levels across the menstrual cycle as measured with proton magnetic resonance spectroscopy. Biol. Psychiatry 57, 44-48. doi: 10.1016/j. biopsych.2004.09.021.
28. Faden, A. I., Demediuk, P., Panter, S. S., and Vink, R. (1989). The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244, 798-800. doi: 10.1126/science.2567056.
29. Falkenberg, L. E., Westerhausen, R., Specht, K., and Hugdahl, K. (2012). Resting-state glutamate level in the anterior cingulate predicts blood-oxygen level-dependent response to cognitive control. Proc. Natl. Acad. Sci. U S A 109, 5069-5073. doi: 10.1073/pnas.1115628109.
30. Feurra, M., Pasqualetti, P., Bianco, G., Santarnecchi, E., Rossi, A., and Rossi, S. (2013). State-dependent effects of transcranial oscillatory currents on the motor system: what you think matters. J. Neurosci. 33, 17483-17489. doi: 10. 1523/jneurosci.1414-13.2013.
31. Finocchi, C., and Ferrari, M. (2011). Female reproductive steroids and neuronal excitability. Neurol. Sci. 32(Suppl. 1), S31-S35. doi: 10.1007/s10072-011-0532-5
32. Floyer-Lea, A., Wylezinska, M., Kincses, T., and Matthews, P. M. (2006). Rapid modulation of GABA concentration in human sensorimotor cortex during motor learning. J. Neurophysiol. 95, 1639-1644. doi: 10.1152/jn.00346.2005.
33. Fujiyama, H., Hinder, M. R., Schmidt, M. W., Tandonnet, C., Garry, M. I., and Summers, J. J. (2012). Age-related differences in corticomotor excitability and inhibitory processes during a visuomotor RT task. J. Cogn. Neurosci. 24, 1253-1263. doi: 10.1162/jocn_a_00201.
34. Gao, F., Edden, R. A., Li, M., Puts, N. A., Wang, G., Liu, C., et al. (2013). Edited magnetic resonance spectroscopy detects an age-related decline in brain GABA levels. Neuroimage 78, 75-82. doi: 10.1016/j.neuroimage.2013.04.012.
35. Ge, S., and Dani, J. A. (2005). Nicotinic acetylcholine receptors at glutamate synapses facilitate long-term depression or potentiation. J. Neurosci. 25, 6084-6091. doi: 10.1523/jneurosci.0542-05.2005.
36. Goto, N., Yoshimura, R., Moriya, J., Kakeda, S., Ueda, N., Ikenouchi-Sugita, A., et al. (2009). Reduction of brain gamma-aminobutyric acid (GABA) concentrations in early-stage schizophrenia patients: 3T Proton MRS study. Schizophr. Res. 112, 192-193. doi: 10.1016/j.schres.2009.04.026.
37. Guleyupoglu, B., Schestatsky, P., Edwards, D., Fregni, F., and Bikson, M. (2013). Classification of methods in transcranial Electrical Stimulation (tES) and evolving strategy from historical approaches to contemporary innovations. J. Neurosci. Methods 219, 297-311. doi: 10.1016/j.jneumeth.2013.07.016.
38. Hamada, M., Murase, N., Hasan, A., Balaratnam, M., and Rothwell, J. C. (2013). The role of interneuron networks in driving human motor cortical plasticity. Cereb. Cortex 23, 1593-1605. doi: 10.1093/cercor/bhs147.
39. Hamada, M., Ugawa, Y., and Tsuji, S. (2008). High-frequency rTMS over the supplementary motor area for treatment of Parkinson's disease. Mov. Disord. 23, 1524-1531. doi: 10.1002/mds.22168.
40. Harada, M., Kubo, H., Nose, A., Nishitani, H., and Matsuda, T. (2011). Measurement of variation in the human cerebral GABA level by in vivo MEGA-editing proton MR spectroscopy using a clinical 3. T instrument and its dependence on brain region and the female menstrual cycle. Hum. Brain Mapp. 32, 828-833. doi: 10.1002/hbm.21086.
41. Hensch, T. K., and Bilimoria, P. M. (2012). Re-opening windows: manipulating critical periods for brain development. Cerebrum 2012:11.
42. Hensch, T. K., Fagiolini, M., Mataga, N., Stryker, M. P., Baekkeskov, S., and Kash, S. F. (1998). Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282,1504-1508. doi: 10.1126/science.282.5393.1504
43. Hess, G., andDonoghue, J. P. (1994). Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J. Neurophysiol. 71,2543-2547.
44. Hess, G., and Donoghue, J. P. (1996). Long-term potentiation and long-term depression of horizontal connections in rat motor cortex. Acta Neurobiol. Exp. (Wars) 56,397-405.
45. Huang, Y., Su, Y., Rorden, C., Dmochowski, J., Datta, A., and Parra, L. C. (2012). An automated method for high-definition transcranial direct current stimulation modeling. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2012, 5376-5379. doi: 10. 1109/EMBC.2012.6347209.
46. Huber, R., Maki, H., Rosanova, M., Casarotto, S., Canali, P., Casali, A. G., et al. (2013).Human cortical excitability increases with time awake. Cereb. Cortex 23, 332-338. doi: 10.1093/cercor/bhs014
47. Huganir, R. L., and Nicoll, R. A. (2013). AMPARs and synaptic plasticity: the last 25 years. Neuron 80, 704-717. doi: 10.1016/j.neuron.2013.10.025.
48. Iuculano, T., and Cohen Kadosh, R. (2013). The mental cost of cognitive enhancement. J. Neurosci. 33, 4482-4486. doi: 10.1523/jneurosci.4927-12.2013.
49. Jackson, J. D., Balota, D. A., Duchek, J. M., and Head, D. (2012). White matter integrity and reaction time intraindividual variability in healthy aging and early-stage Alzheimer disease. Neuropsychologia 50, 357-366. doi: 10.1016/j. neuropsychologia.2011.11.024.
50. Johnston, M. V. (2009). Plasticity in the developing brain: implications for rehabilitation. Dev. Disabil. Res. Rev. 15, 94-101. doi: 10.1002/ddrr.64.
51. Kabakov, A. Y., Muller, P. A., Pascual-Leone, A., Jensen, F. E., and Rotenberg, A. (2012). Contribution of axonal orientation to pathway-dependent modulation of excitatory transmission by direct current stimulation in isolated rat hippocampus. J. Neurophysiol. 107, 1881-1889. doi: 10.1152/jn.00715. 2011
52. Kanai, R., Chaieb, L., Antal, A., Walsh, V., and Paulus, W. (2008). Frequency-dependent electrical stimulation of the visual cortex. Curr. Biol. 18, 1839-1843. doi: 10.1016/j.cub.2008.10.027.
53. Keeser, D., Meindl, T., Bor, J., Palm, U., Pogarell, O., Mulert, C., et al. (2011). Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI. J. Neurosci. 31, 15284-15293. doi: 10. 1523/jneurosci.0542-11.2011.
54. Knudsen, E. I. (2004). Sensitive periods in the development of the brain and behavior. J. Cogn.Neurosci. 16, 1412-1425. doi: 10.1162/0898929042304796.
55. Krause, B., and Cohen Kadosh, R. (2013). Can transcranial electrical stimulation improve learning difficulties in atypical brain development? A future possibility for cognitive training. Dev. Cogn. Neurosci. 6, 176-194. doi: 10.1016/j.dcn.2013. 04.001
56. Krause, B., Marquez-Ruiz, J., and Cohen Kadosh, R. (2013). The effect of transcra-nial direct current stimulation: a role for cortical excitation/inhibition balance? Front. Hum. Neurosci. 7:602. doi: 10.3389/fnhum.2013.00602.
57. Kubas, B., Kulak, W., Sobaniec, W., Tarasow, E., Lebkowska, U., and Walecki, J. (2012). Metabolite alterations in autistic children: a 1H MR spectroscopy study. Adv. Med. Sci. 57, 152-156. doi: 10.2478/v10039-012-0014-x
58. Lang, N., Rothkegel, H., Reiber, H., Hasan, A., Sueske, E., Tergau, F., et al. (2011). Circadian modulation of GABA-mediated cortical inhibition. Cereb. Cortex 21, 2299-2306. doi: 10.1093/cercor/bhr003.
59. Lang, N., Siebner, H. R., Ernst, D., Nitsche, M. A., Paulus, W., Lemon, R. N., et al. (2004). Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction ofafter-effects. Biol. Psychiatry56, 634-639. doi: 10.1016/ j.biopsych.2004.07.017.
60. Lasarge, C. L., Banuelos, C., Mayse, J. D., and Bizon, J. L. (2009). Blockade of GABA(B) receptors completely reverses age-related learning impairment. Neuroscience 164, 941-947. doi: 10.1016/j.neuroscience.2009.08.055.
61. Lopez Alonso, V., Cheeran, B., Rio-Rodriguez, D., and Fernandez-Del-Olmo, M. (2014).Inter-individual variability in response to non-invasive brain stimulation paradigms. Brain Stimul. (in press).
62. McConnell, G. C., So, R. Q., Hilliard, J. D., Lopomo, P., and Grill, W. M. (2012). Effective deep brain stimulation suppresses low-frequency network oscillations in the basal ganglia by regularizing neural firing patterns. J. Neurosci. 32, 15657-15668. doi: 10.1523/jneurosci.2824-12.2012.
63. Mcdonnell, M. N., Orekhov, Y., and Ziemann, U. (2007). Suppression of LTP-like plasticity in human motor cortex by the GABAB receptor agonist baclofen. Exp. Brain Res. 180, 181-186. doi: 10.1007/s00221-006-0849-0.
64. Mcentee, W. J., and Crook, T. H. (1993). Glutamate: its role in learning, memory and the aging brain. Psychopharmacology (Berl) 111, 391-401. doi: 10. 1007/bf02253527.
65. Mekle, R., Mlynarik, V., Gambarota, G., Hergt, M., Krueger, G., and Gruetter, R. (2009). MR spectroscopy of the human brain with enhanced signal intensity at ultrashort echo times on a clinical platform at 3T and 7T. Magn. Reson. Med. 61, 1279-1285. doi: 10.1002/mrm.21961.
66. Miniussi, C., Cappa, S. F., Cohen, L. G., Floel, A., Fregni, F., Nitsche, M. A., et al. (2008).Efficacy of repetitive transcranial magnetic stimulation/transcranial direct current stimulation in cognitive neurorehabilitation. Brain Stimul. 1, 326-336. doi: 10.1016/j.brs.2008.07.002
67. Moliadze, V., Antal, A., and Paulus, W. (2010). Electrode-distance dependent aftereffects of transcranial direct and random noise stimulation with extracephalic reference electrodes. Clin. Neurophysiol. 121, 2165-2171. doi: 10.1016/j.clinph. 2010.04.033
68. Moliadze, V., Atalay, D., Antal, A., and Paulus, W. (2012). Close to threshold transcranial electrical stimulation preferentially activates inhibitory networks before switching to excitation with higher intensities. Brain Stimul. 5, 505-511. doi: 10.1016/j.brs.2011.11.004.
69. Murphy, K. M., Beston, B. R., Boley, P. M., and Jones, D. G. (2005). Development of human visual cortex: a balance between excitatory and inhibitory plasticity mechanisms. Dev. Psychobiol. 46, 209-221. doi: 10.1002/dev.20053.
70. Muthukumaraswamy, S. D., Edden, R. A., Jones, D. K., Swettenham, J. B., and Singh, K. D. (2009). Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proc. Natl. Acad. Sci. USA 106, 8356-8361. doi: 10.1073/pnas.0900728106.
71. Muthukumaraswamy, S. D., Evans, C. J., Edden, R. A., Wise, R. G., and Singh, K. D. (2012).Individual variability in the shape and amplitude of the BOLD-HRF correlates with endogenous GABAergic inhibition. Hum. Brain Mapp. 33, 455-465. doi: 10.1002/hbm.21223
72. Neuling, T., Rach, S., and Herrmann, C. S. (2013). Orchestrating neuronal networks: sustained after-effects of transcranial alternating current stimulation depend upon brain states. Front. Hum. Neurosci. 7:161. doi: 10.3389/fnhum. 2013.00161
73. Neuling, T., Wagner, S., Wolters, C. H., Zaehle, T., and Herrmann, C. S. (2012). Finite-element model predicts current density distribution for clinical applications of tDCS and tACS. Front. Psychiatry 3:83. doi: 10.3389/fpsyt.2012.00083.
74. Nitsche, M.A., Kuo, M.F., Karrasch, R., Wachter, B., Liebetanz, D., and Paulus, W. (2009).Serotonin affects transcranial direct current-induced neuroplasticity in humans. Biol. Psychiatry 66, 503-508. doi: 10.1016/j.biopsych.2009.03.022
75. Nitsche, M. A., Nitsche, M. S., Klein, C. C., Tergau, F., Rothwell, J. C., and Paulus, W. (2003). Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin. Neurophysiol. 114, 600-604. doi: 10.1016/s1388-2457(02)00412-1
76. Nitsche, M. A., and Paulus, W. (2001). Sustained excitabilityelevations induced by transcranial DC motor cortexstimulation in humans. Neurology 57, 1899-1901. doi: 10.1212/wnl.57.10.1899.
77. Park, C. H., Chang, W. H., Park, J. Y., Shin, Y. I., Kim, S. T., and Kim, Y. H. (2013). Transcranial direct current stimulation increases resting state interhemispheric connectivity. Neurosci. Lett. 539,7-10. doi: 10.1016/j.neulet.2013.01.047.
78. Peterchev, A. V., Wagner, T. A., Miranda, P. C., Nitsche, M. A., Paulus, W., Lisanby, S.H., et al. (2012). Fundamentals of transcranial electric and magnetic stimulation dose: definition, selection and reporting practices. Brain Stimul. 5, 435-453. doi: 10.1016/j.brs.2011.10.001.
79. Pinto, J. G., Hornby, K. R., Jones, D. G., and Murphy, K. M. (2010). Developmental changes in GABAergic mechanisms in human visual cortex across the lifespan. Front. Cell. Neurosci. 4:16. doi: 10.3389/fncel.2010.00016.
80. Rahman, A., Reato, D., Arlotti, M., Gasca, F., Datta, A., Parra, L. C., et al. (2013).Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects. J. Physiol. 591, 2563-2578. doi: 10.1113/jphysiol.2012. 247171
81. Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson, A., et al. (2005). Regional brain changes in aging healthyadults: general trends, individual differences and modifiers. Cereb. Cortex 15, 1676-1689. doi: 10. 1093/cercor/bhi044
82. Reato, D., Rahman, A., Bikson, M., and Parra, L. C. (2010). Low-intensityelectrical stimulation affects network dynamics by modulating population rate and spike timing. J. Neurosci. 30, 15067-15079. doi: 10.1523/jneurosci.2059-10.2010.
83. Reis, J., Schambra, H. M., Cohen, L. G., Buch, E. R., Fritsch, B., Zarahn, E., et al. (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl. Acad. Sci. USA 106, 1590-1595. doi: 10.1073/pnas.0805413106.
84. Rivera, S. M., Reiss, A. L., Eckert, M. A., and Menon, V. (2005). Developmental changes in mental arithmetic: evidence for increased functional specialization in the left inferior parietal cortex. Cereb. Cortex 15, 1779-1790. doi: 10. 1093/cercor/bhi055
85. Rojas, D. C., Singel, D., Steinmetz, S., Hepburn, S., and Brown, M. S. (2013). Decreased left perisylvian GABA concentration in children with autism and unaffected siblings. Neuroimage 86, 28-34. doi: 10.1016/j.neuroimage.2013.01.045
86. Romei, V., Rihs, T., Brodbeck, V., and Thut, G. (2008). Resting electroencephalogram alpha-power over posterior sites indexes baseline visual cortex excitability. Neuroreport 19, 203-208. doi: 10.1097/wnr.0b013e3282f454c4.
87. Ross, L. A., Mccoy, D., Wolk, D. A., Coslett, H. B., and Olson, I. R. (2010). Improved proper name recall by electrical stimulation of the anterior temporal lobes. Neuropsychologia 48, 3671-3674. doi: 10.1016/j.neuropsychologia.2010.07.024.
88. Ross, L. A., Mccoy, D., Wolk, D. A., Coslett, H. B., and Olson, I. R. (2011). Improved proper name recall in aging after electrical stimulation of the anterior temporal lobes. Front. Aging Neurosci. 3:16. doi: 10.3389/fnagi.2011.00016.
89. Siebner, H. R., Lang, N., Rizzo, V., Nitsche, M. A., Paulus, W., Lemon, R. N., et al. (2004). Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J. Neurosci. 24, 3379-3385. doi: 10. 1523/jneurosci.5316-03.2004.
90. Silvanto, J., Muggleton, N. G., Cowey, A., and Walsh, V. (2007). Neural adaptation reveals state-dependent effects of transcranial magnetic stimulation. Eur. J. Neurosci. 25, 1874-1881. doi: 10.1111/j.1460-9568.2007.05440.x
91. Silvanto, J., Muggleton, N., and Walsh, V. (2008). State-dependency in brain stimulation studies of perception and cognition. Trends Cogn. Sci. 12, 447-454. doi: 10.1016/j.tics.2008.09.004.
92. Smith, M. J., Adams, L. F., Schmidt, P. J., Rubinow, D. R., and Wassermann, E. M. (2002). Effects of ovarian hormones on human cortical excitability. Ann. Neurol. 51, 599-603. doi: 10.1002/ana.10180.
93. Smith, M. J., Keel, J. C., Greenberg, B. D., Adams, L. F., Schmidt, P. J., Rubinow, D. A., et al. (1999). Menstrual cycle effects on cortical excitability. Neurology53, 2069-2072. doi: 10.1212/wnl.53.9.2069.
94. Smith, A. E., Ridding, M. C., Higgins, R. D., Wittert, G. A., and Pitcher, J. B. (2009). Age-related changes in short-latency motor cortex inhibition. Exp. Brain Res. 198, 489-500. doi: 10.1007/s00221-009-1945-8.
95. Snowball, A., Tachtsidis, I., Popescu, T., Thompson, J., Delazer, M., Zamarian, L., et al. (2013). Long-term enhancement of brain function and cognition using cognitive training and brain stimulation. Curr. Biol. 23, 987-992. doi: 10.1016/j. cub.2013.04.045
96. Stagg, C. J., Bachtiar, V., and Johansen-Berg, H. (2011). The role of GABA in human motor learning. Curr. Biol. 21, 480-484. doi: 10.1016/j.cub.2011.01.069.
97. Stagg, C. J., Best, J. G., Stephenson, M. C., O'shea, J., Wylezinska, M., Kincses, Z. T., et al. (2009). Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J. Neurosci. 29, 5202-5206. doi: 10.1523/jneurosci. 4432-08.2009
98. Strelau, J. (1997). The contribution of pavlov's typology of CNS properties to personality research. Eur. Psychol. 2, 125-138. doi: 10.1027/1016-9040.2.2.125.
99. Tecchio, F., Cancelli, A., Cottone, C., Tomasevic, L., Devigus, B., Zito, G., et al. (2013). Regional personalized electrodes to select transcranial current stimulation target. Front. Hum. Neurosci. 7:131. doi: 10.3389/fnhum.2013.00131.
100. Teo, F., Hoy, K. E., Daskalakis, Z. J., and Fitzgerald, P. B. (2011). Investigating the role of current strength in tDCS modulation of working memory performance in healthy controls. Front. Psychiatry 2:45. doi: 10.3389/fpsyt.2011.00045.
101. Terney, D., Chaieb, L., Moliadze, V., Antal, A., and Paulus, W. (2008). Increasing human brain excitability by transcranial high-frequency random noise stimulation. J. Neurosci. 28, 14147-14155. doi: 10.1523/JNEUROSCI.4248-08.2008.
102. Trepel, C., and Racine, R. J. (2000). GABAergic modulation of neocortical longterm potentiation in the freely moving rat. Synapse 35, 120-128. doi: 10. 1002/(sici)1098-2396(200002)35:2<120::aid-syn4>3.0.co;2-6.
103. Truong, D. Q., Magerowski, G., Blackburn, G. L., Bikson, M., and Alonso-Alonso, M. (2013). Computational modeling of transcranial direct current stimulation (tDCS) in obesity: impact of head fat and dose guidelines. Neuroimage Clin. 2, 759-766. doi: 10.1016/j.nicl.2013.05.011.
104. Turrigiano, G. G., and Nelson, S. B. (2000). Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 10, 358-364. doi: 10.1016/s0959-4388(00)00091-x
105. Turrigiano, G. G., and Nelson, S. B. (2004). Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5, 97-107. doi: 10.1038/nrn1327.
106. Wassermann, E. M. (2002). Variation in the response to transcranial magnetic brain stimulation in the general population. Clin. Neurophysiol. 113, 1165-1171. doi: 10.1016/s1388-2457(02)00144-x
107. Weiss, M., and Lavidor, M. (2012). When less is more: evidence for a facilitative cathodal tDCS effect in attentional abilities. J. Cogn. Neurosci. 24, 1826-1833. doi: 10.1162/jocn_a_00248.
108. Wenk, G. L., Walker, L. C., Price, D. L., and Cork, L. C. (1991). Loss of NMDA, but not GABA-A, binding in the brains of aged rats and monkeys. Neurobiol. Aging 12, 93-98. doi: 10.1016/0197-4580(91)90047-n
109. Yoon, J. H., Maddock, R. J., Rokem, A., Silver, M. A., Minzenberg, M. J., Ragland, J. D., et al. (2010). GABA concentration is reduced in visual cortex in schizophrenia and correlates with orientation-specific surround suppression. J. Neurosci. 30, 3777-3781. doi: 10.1523/JNEUROSCI.6158-09.2010.
110. Zaghi, S., Acar, M., Hultgren, B., Boggio, P. S., and Fregni, F. (2010). Noninvasive brain stimulation with low-intensity electrical currents: putative mechanisms of action for direct and alternating current stimulation. Neuroscientist16, 285-307. doi: 10.1177/1073858409336227.
111. Zheng, X., Alsop, D. C., and Schlaug, G. (2011). Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. Neuroimage 58, 26-33. doi: 10.1016/j.neuroimage.2011.06.018.
112. Zimmerman, M., and Hummel, F. (in press). "Brain stimulation and its role in neurological diseases," in The Stimulated Brain, ed K. Cohen Kadosh (Amsterdam: Elsevier).