Transcranial Direct Current Stimulation (tDCS): Modulation of Executive Function in Health and Disease

Current Behavioral Neuroscience Reports

Volumn 1, Issue 2, 2014, Pages 74-85

  Sarkis, Rani A ^a   Kaur, Navneet ^a   Camprodon, Joan A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Brain stimulation; Cognitive enhancement; DLPFC; Dysexecutive syndrome; Executive function; Neuromodulation; Neurotherapeutics; Prefrontal cortex; tDCS; Transcranial direct current stimulation

Indexed keywords

EID: 84922183843     PISSN: None     EISSN: 21962979     Source Type: Journal    
DOI: 10.1007/s40473-014-0009-y     Document Type: Article

References (94)

1. Leh SE, Petrides M, Strafella AP. The neural circuitry of executive functions in healthy subjects and parkinson's disease. Neuropsychopharmacology. 2010;35:70–85. DOI: 10.1038/npp.2009.88
2. Diamond A. Executive functions. Annu Rev Psychol. 2013;64:135–68. Provides a comprehensive overview of executive functions, their development, and their functional impact in health and disease. DOI: 10.1146/annurev-psych-113011-143750
3. Farah MJ, Illes J, Cook-Deegan R, et al. Neurocognitive enhancement: What can we do and what should we do? Nat Rev Neurosci. 2004;5:421–5. A discussion of the bioethical problems raised by cognitive enhancers. DOI: 10.1038/nrn1390
4. Hyman SE. Cognitive enhancement: Promises and perils. Neuron. 2011;69:595–8. DOI: 10.1016/j.neuron.2011.02.012
5. Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;527(Pt 3):633–9. DOI: 10.1111/j.1469-7793.2000.t01-1-00633.x
6. Pena-Gomez C, Sala-Lonch R, Junque C, et al. Modulation of large-scale brain networks by transcranial direct current stimulation evidenced by resting-state functional MRI. Brain Stimu. 2012;5:252–63. One of the first papers to investigate the effects of tDCS and the systems level using neuroimaging measures of connectivity. DOI: 10.1016/j.brs.2011.08.006
7. Pellicciari MC, Brignani D, Miniussi C. Excitability modulation of the motor system induced by transcranial direct current stimulation: A multimodal approach. Neuroimage. 2013;83:569–80. DOI: 10.1016/j.neuroimage.2013.06.076
8. Kuo MF, Paulus W, Nitsche MA. Therapeutic effects of non-invasive brain stimulation with direct currents (tDCS) in neuropsychiatric diseases. Neuroimage. 2014;85(Pt 3):948–60. Provides an updated comprehensive review for the treatment of neuropsychiatric diseases with tDCS. DOI: 10.1016/j.neuroimage.2013.05.117
9. Nitsche MA, Cohen LG, Wassermann EM, et al. Transcranial direct current stimulation: State of the art 2008. Brain Stimul. 2008;1:206–23. A classic paper by some of the leading authors in the field that summarizes our knowledge of tDCS in 2008. DOI: 10.1016/j.brs.2008.06.004
10. Wagner T, Valero-Cabre A, Pascual-Leone A. Noninvasive human brain stimulation. Annu Rev Biomed Eng. 2007;9:527–65. DOI: 10.1146/annurev.bioeng.9.061206.133100
11. Datta A, Bansal V, Diaz J, Patel J, Reato D, Bikson M. Gyri-precise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimul. 2009;2:201–7. DOI: 10.1016/j.brs.2009.03.005
12. de Berker AO, Bikson M, Bestmann S. Predicting the behavioral impact of transcranial direct current stimulation: Issues and limitations. Front Hum Neurosci. 2013;7:613. The authors provide arguments for shying away from simplistic explanations of mechanisms of action in tDCS, and focus on individualized current modeling. DOI: 10.3389/fnhum.2013.00613
13. Gandiga PC, Hummel FC, Cohen LG. Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol. 2006;117:845–50. DOI: 10.1016/j.clinph.2005.12.003
14. Palm U, Reisinger E, Keeser D, et al. Evaluation of sham transcranial direct current stimulation for randomized, placebo-controlled clinical trials. Brain Stimul. 2013;6:690–5. DOI: 10.1016/j.brs.2013.01.005
15. Zaehle T, Rach S, Herrmann CS. Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS One. 2010;5:e13766. DOI: 10.1371/journal.pone.0013766
16. Antal A, Paulus W. Transcranial alternating current stimulation (tACS). Front Hum Neurosci. 2013;7:317. DOI: 10.3389/fnhum.2013.00317
17. Terney D, Chaieb L, Moliadze V, Antal A, Paulus W. Increasing human brain excitability by transcranial high-frequency random noise stimulation. J Neurosci. 2008;28:14147–55. DOI: 10.1523/JNEUROSCI.4248-08.2008
18. Borckardt JJ, Bikson M, Frohman H, et al. A pilot study of the tolerability and effects of high-definition transcranial direct current stimulation (HD-tDCS) on pain perception. J Pain. 2012;13:112–20. DOI: 10.1016/j.jpain.2011.07.001
19. Edwards D, Cortes M, Datta A, Minhas P, Wassermann EM, Bikson M. Physiological and modeling evidence for focal transcranial electrical brain stimulation in humans: A basis for high-definition tDCS. Neuroimage. 2013;74:266–75. DOI: 10.1016/j.neuroimage.2013.01.042
20. Minhas P, Bansal V, Patel J, et al. Electrodes for high-definition transcutaneous DC stimulation for applications in drug delivery and electrotherapy, including tDCS. J Neurosci Methods. 2010;190:188–97. DOI: 10.1016/j.jneumeth.2010.05.007
21. Villamar MF, Volz MS, Bikson M, Datta A, Dasilva AF, Fregni F. Technique and considerations in the use of 4x1 ring high-definition transcranial direct current stimulation (HD-tDCS). J Vis Exp. 2013;77:50309.
22. Kuo HI, Bikson M, Datta A, et al. Comparing cortical plasticity induced by conventional and high-definition 4 x 1 ring tDCS: A neurophysiological study. Brain Stimul. 2013;6:644–8. DOI: 10.1016/j.brs.2012.09.010
23. Caparelli-Daquer EM, Zimmermann TJ, Mooshagian E, et al. A pilot study on effects of 4x1 high-definition tDCS on motor cortex excitability. Conf Proc IEEE Eng Med Biol Soc. 2012;2012:735–8.
24. Poreisz C, Boros K, Antal A, Paulus W. Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res Bull. 2007;72:208–14. DOI: 10.1016/j.brainresbull.2007.01.004
25. Islam N, Aftabuddin M, Moriwaki A, Hattori Y, Hori Y. Increase in the calcium level following anodal polarization in the rat brain. Brain Res. 1995;684:206–8. DOI: 10.1016/0006-8993(95)00434-R
26. Nitsche MA, Fricke K, Henschke U, et al. Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol. 2003;553:293–301. DOI: 10.1113/jphysiol.2003.049916
27. Nitsche MA, Liebetanz D, Schlitterlau A, et al. GABAergic modulation of DC stimulation-induced motor cortex excitability shifts in humans. Eur J Neurosci. 2004;19:2720–6. DOI: 10.1111/j.0953-816X.2004.03398.x
28. Monte-Silva K, Kuo MF, Thirugnanasambandam N, Liebetanz D, Paulus W, Nitsche MA. Dose-dependent inverted U-shaped effect of dopamine (D2-like) receptor activation on focal and nonfocal plasticity in humans. J Neurosci. 2009;29:6124–31. DOI: 10.1523/JNEUROSCI.0728-09.2009
29. Nitsche MA, Kuo MF, Karrasch R, Wachter B, Liebetanz D, Paulus W. Serotonin affects transcranial direct current-induced neuroplasticity in humans. Biol Psychiatry. 2009;66:503–8. DOI: 10.1016/j.biopsych.2009.03.022
30. Kuo MF, Grosch J, Fregni F, Paulus W, Nitsche MA. Focusing effect of acetylcholine on neuroplasticity in the human motor cortex. J Neurosci. 2007;27:14442–7. DOI: 10.1523/JNEUROSCI.4104-07.2007
31. Paulus W. Transcranial electrical stimulation (tES - tDCS; tRNS, tACS) methods. Neuropsychol Rehabil. 2011;21:602–17. A good review of the newer methodological variants of cortical electrical stimulation. DOI: 10.1080/09602011.2011.557292
32. Liebetanz D, Nitsche MA, Tergau F, Paulus W. Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain. 2002;125:2238–47. DOI: 10.1093/brain/awf238
33. Nitsche MA, Lampe C, Antal A, et al. Dopaminergic modulation of long-lasting direct current-induced cortical excitability changes in the human motor cortex. Eur J Neurosci. 2006;23:1651–7. DOI: 10.1111/j.1460-9568.2006.04676.x
34. Bai S, Loo C, Dokos S. A review of computational models of transcranial electrical stimulation. Crit Rev Biomed Eng. 2013;41:21–35. DOI: 10.1615/CritRevBiomedEng.2013007163
35. Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24:167–202. An important paper that proposes a classic model of prefrontal cortex function. DOI: 10.1146/annurev.neuro.24.1.167
36. Petrides M. Lateral prefrontal cortex: Architectonic and functional organization. Philos Trans R Soc Lond B Biol Sci. 2005;360:781–95. DOI: 10.1098/rstb.2005.1631
37. Burzynska AZ, Nagel IE, Preuschhof C, et al. Microstructure of frontoparietal connections predicts cortical responsivity and working memory performance. Cereb Cortex. 2011;21:2261–71. DOI: 10.1093/cercor/bhq293
38. D’Esposito M. From cognitive to neural models of working memory. Philos Trans R Soc Lond B Biol Sci. 2007;362:761–72. DOI: 10.1098/rstb.2007.2086
39. Blackburn HL, Benton AL. Revised administration and scoring of the digit span test. J Consult Psychol. 1957;21:139–43. DOI: 10.1037/h0047235
40. Weschler D. Wechsler adult intelligence scale-fourth edition. San Antonio: Pearson; 2008.
41. Gaudino EA, Geisler MW, Squires NK. Construct validity in the trail making test: What makes part B harder? J Clin Exp Neuropsychol. 1995;17:529–35. DOI: 10.1080/01688639508405143
42. Benton A. Differential behavioral effects in frontal lobe disease. Neuropsychologia. 1968;6:53–60. DOI: 10.1016/0028-3932(68)90038-9
43. Shallice T. Specific impairments of planning. Philos Trans R Soc Lond B Biol Sci. 1982;298:199–209. DOI: 10.1098/rstb.1982.0082
44. MacLeod CM. Half a century of research on the stroop effect: An integrative review. Psychol Bull. 1991;109:163–203. DOI: 10.1037/0033-2909.109.2.163
45. Kirchner WK. Age differences in short-term retention of rapidly changing information. J Exp Psychol. 1958;55:352–8. DOI: 10.1037/h0043688
46. Verbruggen F, Logan GD, Stevens MA. STOP-IT: Windows executable software for the stop-signal paradigm. Behav Res Methods. 2008;40:479–83. DOI: 10.3758/BRM.40.2.479
47. Langenecker SA, Zubieta JK, Young EA, Akil H, Nielson KA. A task to manipulate attentional load, set-shifting, and inhibitory control: Convergent validity and test-retest reliability of the parametric go/no-go test. J Clin Exp Neuropsychol. 2007;29:842–53. DOI: 10.1080/13803390601147611
48. Hoy KE, Emonson MR, Arnold SL, Thomson RH, Daskalakis ZJ, Fitzgerald PB. Testing the limits: Investigating the effect of tDCS dose on working memory enhancement in healthy controls. Neuropsychologia. 2013;51:1777–84. DOI: 10.1016/j.neuropsychologia.2013.05.018
49. Leite J, Carvalho S, Fregni F, Boggio PS, Goncalves OF. The effects of cross-hemispheric dorsolateral prefrontal cortex transcranial direct current stimulation (tDCS) on task switching. Brain Stimul. 2013;6:660–7. DOI: 10.1016/j.brs.2012.10.006
50. Jeon SY, Han SJ. Improvement of the working memory and naming by transcranial direct current stimulation. Ann Rehabil Med. 2012;36:585–95. DOI: 10.5535/arm.2012.36.5.585
51. Ohn SH, Park CI, Yoo WK, et al. Time-dependent effect of transcranial direct current stimulation on the enhancement of working memory. Neuroreport. 2008;19:43–7. DOI: 10.1097/WNR.0b013e3282f2adfd
52. Fregni F, Boggio PS, Nitsche M, et al. Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp Brain Res. 2005;166:23–30. DOI: 10.1007/s00221-005-2334-6
53. Iyer MB, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann EM. Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology. 2005;64:872–5. DOI: 10.1212/01.WNL.0000152986.07469.E9
54. Coffman BA, Trumbo MC, Clark VP. Enhancement of object detection with transcranial direct current stimulation is associated with increased attention. BMC Neurosci. 2012;13:108–2202. DOI: 10.1186/1471-2202-13-108
55. Nelson JT, McKinley RA, Golob EJ, Warm JS, Parasuraman R. Enhancing vigilance in operators with prefrontal cortex transcranial direct current stimulation (tDCS). Neuroimage. 2014;85(Pt 3):909–17. DOI: 10.1016/j.neuroimage.2012.11.061
56. Gladwin TE, den Uyl TE, Fregni FF, Wiers RW. Enhancement of selective attention by tDCS: Interaction with interference in a sternberg task. Neurosci Lett. 2012;512:33–7. DOI: 10.1016/j.neulet.2012.01.056
57. Berryhill ME, Jones KT. tDCS selectively improves working memory in older adults with more education. Neurosci Lett. 2012;521:148–51. DOI: 10.1016/j.neulet.2012.05.074
58. Andrews SC, Hoy KE, Enticott PG, Daskalakis ZJ, Fitzgerald PB. Improving working memory: The effect of combining cognitive activity and anodal transcranial direct current stimulation to the left dorsolateral prefrontal cortex. Brain Stimul. 2011;4:84–9. DOI: 10.1016/j.brs.2010.06.004
59. Martin DM, Liu R, Alonzo A, et al. Can transcranial direct current stimulation enhance outcomes from cognitive training? A randomized controlled trial in healthy participants. Int J Neuropsychopharmacol. 2013;16:1927–36. DOI: 10.1017/S1461145713000539
60. Park SH, Seo JH, Kim YH, Ko MH. Long-term effects of transcranial direct current stimulation combined with computer-assisted cognitive training in healthy older adults. Neuroreport. 2014;25:122–6. DOI: 10.1097/WNR.0000000000000080
61. Filmer HL, Mattingley JB, Dux PE. Improved multitasking following prefrontal tDCS. Cortex. 2013;49:2845–52. DOI: 10.1016/j.cortex.2013.08.015
62. Motohashi N, Yamaguchi M, Fujii T, Kitahara Y. Mood and cognitive function following repeated transcranial direct current stimulation in healthy volunteers: A preliminary report. Neurosci Res. 2013;77:64–9. DOI: 10.1016/j.neures.2013.06.001
63. Plewnia C, Zwissler B, Langst I, Maurer B, Giel K, Kruger R. Effects of transcranial direct current stimulation (tDCS) on executive functions: Influence of COMT val/met polymorphism. Cortex. 2013;49:1801–7. In this trial, 46 healthy individuals had their COMT genetic status phenotyped. They then received sham or anodal tDCS stimulation over F3 and were tested on a parametric GoNoGo task. The results showed that in the subgroup of patients with COMT Met/Met status, tDCS actually had a detrimental effect on their performance. DOI: 10.1016/j.cortex.2012.11.002
64. Hsu TY, Tseng LY, Yu JX, et al. Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex. Neuroimage. 2011;56:2249–57. DOI: 10.1016/j.neuroimage.2011.03.059
65. Kwon YH, Kwon JW. Is transcranial direct current stimulation a potential method for improving response inhibition? Neural Regen Res. 2013;8:1048–54.
66. Jacobson L, Javitt DC, Lavidor M. Activation of inhibition: Diminishing impulsive behavior by direct current stimulation over the inferior frontal gyrus. J Cogn Neurosci. 2011;23:3380–7. DOI: 10.1162/jocn_a_00020
67. Beeli G, Casutt G, Baumgartner T, Jancke L. Modulating presence and impulsiveness by external stimulation of the brain. Behav Brain Funct. 2008;4:33–4. DOI: 10.1186/1744-9081-4-33
68. Sandrini M, Fertonani A, Cohen LG, Miniussi C. Double dissociation of working memory load effects induced by bilateral parietal modulation. Neuropsychologia. 2012;50:396–402. DOI: 10.1016/j.neuropsychologia.2011.12.011
69. Oliveira JF, Zanao TA, Valiengo L, et al. Acute working memory improvement after tDCS in antidepressant-free patients with major depressive disorder. Neurosci Lett. 2013;537:60–4. DOI: 10.1016/j.neulet.2013.01.023
70. Loo CK, Sachdev P, Martin D, et al. A double-blind, sham-controlled trial of transcranial direct current stimulation for the treatment of depression. Int J Neuropsychopharmacol. 2010;13:61–9. DOI: 10.1017/S1461145709990411
71. Fregni F, Boggio PS, Nitsche MA, Rigonatti SP, Pascual-Leone A. Cognitive effects of repeated sessions of transcranial direct current stimulation in patients with depression. Depress Anxiety. 2006;23:482–4. DOI: 10.1002/da.20201
72. Ferrucci R, Bortolomasi M, Vergari M, et al. Transcranial direct current stimulation in severe, drug-resistant major depression. J Affect Disord. 2009;118:215–9. DOI: 10.1016/j.jad.2009.02.015
73. Loo CK, Alonzo A, Martin D, Mitchell PB, Galvez V, Sachdev P. Transcranial direct current stimulation for depression: 3-week, randomised, sham-controlled trial. Br J Psychiatry. 2012;200:52–9. A randomized, sham-controlled trial of 64 patients with major depressive disorder receiving tDCS either over 30 sessions, or starting with 15 sham then 15 active sessions. tDCS was found to improve mood at last follow up, but did not have an apparent effect on neuropsychological measures. DOI: 10.1192/bjp.bp.111.097634
74. Boggio PS, Ferrucci R, Rigonatti SP, et al. Effects of transcranial direct current stimulation on working memory in patients with parkinson's disease. J Neurol Sci. 2006;249:31–8. DOI: 10.1016/j.jns.2006.05.062
75. Pereira JB, Junque C, Bartres-Faz D, et al. Modulation of verbal fluency networks by transcranial direct current stimulation (tDCS) in parkinson's disease. Brain Stimul. 2013;6:16–24. DOI: 10.1016/j.brs.2012.01.006
76. Jo JM, Kim YH, Ko MH, Ohn SH, Joen B, Lee KH. Enhancing the working memory of stroke patients using tDCS. Am J Phys Med Rehabil. 2009;88:404–9. DOI: 10.1097/PHM.0b013e3181a0e4cb
77. Kang EK, Baek MJ, Kim S, Paik NJ. Non-invasive cortical stimulation improves post-stroke attention decline. Restor Neurol Neurosci. 2009;27:645–50.
78. Huey ED, Probasco JC, Moll J, et al. No effect of DC brain polarization on verbal fluency in patients with advanced frontotemporal dementia. Clin Neurophysiol. 2007;118:1417–8. DOI: 10.1016/j.clinph.2007.02.026
79. Boggio PS, Khoury LP, Martins DC, Martins OE, de Macedo EC, Fregni F. Temporal cortex direct current stimulation enhances performance on a visual recognition memory task in alzheimer disease. J Neurol Neurosurg Psychiatry. 2009;80:444–7. DOI: 10.1136/jnnp.2007.141853
80. Zaehle T, Sandmann P, Thorne JD, Jancke L, Herrmann CS. Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: Combined behavioural and electrophysiological evidence. BMC Neurosci. 2011;12.
81. Stone DB, Tesche CD. Transcranial direct current stimulation modulates shifts in global/local attention. Neuroreport. 2009;20:1115–9.
82. Datta A, Truong D, Minhas P, Parra LC, Bikson M. Inter-individual variation during transcranial direct current stimulation and normalization of dose using MRI-derived computational models. Front Psychiatry. 2012;3:91. DOI: 10.3389/fpsyt.2012.00091
83. Leite J, Carvalho S, Fregni F, Goncalves OF. Task-specific effects of tDCS-induced cortical excitability changes on cognitive and motor sequence set shifting performance. PLoS One. 2011;6:e24140. DOI: 10.1371/journal.pone.0024140
84. Dockery CA, Hueckel-Weng R, Birbaumer N, Plewnia C. Enhancement of planning ability by transcranial direct current stimulation. J Neurosci. 2009;29:7271–7. DOI: 10.1523/JNEUROSCI.0065-09.2009
85. Clark VP, Coffman BA, Trumbo MC, Gasparovic C. Transcranial direct current stimulation (tDCS) produces localized and specific alterations in neurochemistry: A (1)H magnetic resonance spectroscopy study. Neurosci Lett. 2011;500:67–71. DOI: 10.1016/j.neulet.2011.05.244
86. Nord CL, Lally N, Charpentier CJ. Harnessing electric potential: DLPFC tDCS induces widespread brain perfusion changes. Front Syst Neurosci. 2013;7:99. DOI: 10.3389/fnsys.2013.00099
87. Holtzer R, Ozelius L, Xue X, Wang T, Lipton RB, Verghese J. Differential effects of COMT on gait and executive control in aging. Neurobiol Aging. 2010;31:523–31. DOI: 10.1016/j.neurobiolaging.2008.05.011
88. Kim JH, Kim DW, Chang WH, Kim YH, Im CH. Inconsistent outcomes of transcranial direct current stimulation (tDCS) may be originated from the anatomical differences among individuals: A simulation study using individual MRI data. Conf Proc IEEE Eng Med Biol Soc. 2013;2013:823–5.
89. Freitas C, Mondragon-Llorca H, Pascual-Leone A. Noninvasive brain stimulation in alzheimer's disease: Systematic review and perspectives for the future. Exp Gerontol. 2011;46:611–27.
90. Bai S, Dokos S, Ho KA, Loo C. A computational modelling study of transcranial direct current stimulation montages used in depression. Neuroimage. 2014;87:332–44. DOI: 10.1016/j.neuroimage.2013.11.015
91. Keeser D, Meindl T, Bor J, et al. Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI. J Neurosci. 2011;31:15284–93. DOI: 10.1523/JNEUROSCI.0542-11.2011
92. Brem AK, Fried PJ, Horvath JC, Robertson EM, Pascual-Leone A. Is neuroenhancement by noninvasive brain stimulation a net zero-sum proposition? Neuroimage. 2014;85(Pt 3):1058–68. DOI: 10.1016/j.neuroimage.2013.07.038
93. Ditye T, Jacobson L, Walsh V, Lavidor M. Modulating behavioral inhibition by tDCS combined with cognitive training. Exp Brain Res. 2012;219:363–8. DOI: 10.1007/s00221-012-3098-4
94. Marshall L, Molle M, Siebner HR, Born J. Bifrontal transcranial direct current stimulation slows reaction time in a working memory task. BMC Neurosci. 2005;6:23. DOI: 10.1186/1471-2202-6-23