Advertisement

Neuroscience Bulletin

, Volume 31, Issue 2, pp 198–206 | Cite as

Exploring prefrontal cortex functions in healthy humans by transcranial electrical stimulation

  • Min-Fang Kuo
  • Michael A. Nitsche
Review

Abstract

The prefrontal cortex is involved in a multitude of cognitive, emotional, motivational, and social processes, so exploring its specific functions is crucial for understanding human experience and behavior. Functional imaging approaches have largely contributed to the enhancement of our understanding, but might have limitations in establishing causal relationships between physiology and the related psychological and behavioral processes. Non-invasive electrical stimulation with direct or alternating currents can help to enhance our understanding with regard to specific processes, and might provide future protocols able to improve them in case of malfunctions. We review the current state of the field, and provide an outlook for future developments.

Keywords

affective disorders brain stimulation frontal lobe 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. [1]
    Briand LA, Gritton H, Howe WM, Young DA, Sarter M. Modulators in concert for cognition: modulator interactions in the prefrontal cortex. Prog Neurobiol 2007, 83: 69–91.CrossRefPubMedCentralPubMedGoogle Scholar
  2. [2]
    Courtin J, Bienvenu TC, Einarsson EÖ, Herry C. Medial prefrontal cortex neuronal circuits in fear behavior. Neuroscience 2013, 240: 219–242.CrossRefPubMedGoogle Scholar
  3. [3]
    Diamond A. Biological and social influences on cognitive control processes dependent on prefrontal cortex. Prog Brain Res 2011, 189: 319–339.CrossRefPubMedCentralPubMedGoogle Scholar
  4. [4]
    Goto Y, Yang CR, Otani S. Functional and dysfunctional synaptic plasticity in prefrontal cortex: roles in psychiatric disorders. Biol Psychiatry 2010, 67: 199–207.CrossRefPubMedGoogle Scholar
  5. [5]
    Langner R, Eickhoff SB. Sustaining attention to simple tasks: a meta-analytic review of the neural mechanisms of vigilant attention. Psychol Bull 2013, 139: 870–900.CrossRefPubMedCentralPubMedGoogle Scholar
  6. [6]
    Ray RD, Zald DH. Anatomical insights into the interaction of emotion and cognition in the prefrontal cortex. Neurosci Biobehav Rev 2012, 36: 479–501.CrossRefPubMedCentralPubMedGoogle Scholar
  7. [7]
    Lett TA, Voineskos AN, Kennedy JL, Levine B, Daskalakis ZJ. treating working memory deficits in schizophrenia: a review of the neurobiology. Biol Psychiatry 2014, 75: 361–370CrossRefPubMedGoogle Scholar
  8. [8]
    Luijten M, Machielsen MW, Veltman DJ, Hester R, de Haan L, Franken IH. Systematic review of ERP and fMRI studies investigating inhibitory control and error processing in people with substance dependence and behavioural addictions. J Psychiatry Neurosci 2013, 38: 130052.Google Scholar
  9. [9]
    Maillet D, Rajah MN. Association between prefrontal activity and volume change in prefrontal and medial temporal lobes in aging and dementia: a review. Ageing Res Rev 2013, 12: 479–489.CrossRefPubMedGoogle Scholar
  10. [10]
    Narayanan NS, Rodnitzky RL, Uc EY. Prefrontal dopamine signaling and cognitive symptoms of Parkinson’s disease. J Psychiatry Neurosci 2013, 38: 130052Google Scholar
  11. [11]
    Trivedi MH, Greer TL. Cognitive dysfunction in unipolar depression: implications for treatment. J Affect Disord 2014, 152–154: 19–27.CrossRefPubMedGoogle Scholar
  12. [12]
    Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, et al. Transcranial direct current stimulation: State of the art 2008. Brain Stimul 2008, 1: 206–223.CrossRefPubMedGoogle Scholar
  13. [13]
    Nitsche MA, Paulus W. Transcranial direct current stimulation—update 2011. Restor Neurol Neurosci 2011, 29: 463–492.PubMedGoogle Scholar
  14. [14]
    Herrmann CS, Rach S, Neuling T, Strüber D. Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes. Front Hum Neurosci 2013, 7: 279.CrossRefPubMedCentralPubMedGoogle Scholar
  15. [15]
    Ziemann U, Paulus W, Nitsche MA, Pascual-Leone A, Byblow WD, Berardelli A, et al. Consensus: Motor cortex plasticity protocols. Brain Stimul 2008, 1: 164–182.CrossRefPubMedGoogle Scholar
  16. [16]
    Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 2000, 527: 633–639.CrossRefPubMedCentralPubMedGoogle Scholar
  17. [17]
    Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 2001, 57: 1899–1901.CrossRefPubMedGoogle Scholar
  18. [18]
    Nitsche MA, Nitsche MS, Klein CC, Tergau F, Rothwell JC, Paulus W. Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin Neurophysiol 2003a, 114: 600–604.CrossRefPubMedGoogle Scholar
  19. [19]
    Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, et al. Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 2003, 553: 293–301.CrossRefPubMedCentralPubMedGoogle Scholar
  20. [20]
    Nitsche MA, Jaussi W, Liebetanz D, Lang N, Tergau F, Paulus W. Consolidation of human motor cortical neuroplasticity by D-cycloserine. Neuropsychopharmacology 2004, 29: 1573–1578.CrossRefPubMedGoogle Scholar
  21. [21]
    Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 2004, 44: 5–21.CrossRefPubMedGoogle Scholar
  22. [22]
    Antal A, Boros K, Poreisz C, Chaieb L, Terney D, Paulus W. Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans. Brain Stimul 2008, 2: 97–105.CrossRefGoogle Scholar
  23. [23]
    Antal A, Paulus W. Transcranial alternating current stimulation (tACS). Front Hum Neurosci 2013, 7: 317.CrossRefPubMedCentralPubMedGoogle Scholar
  24. [24]
    Ali MM, Sellers KK, Fröhlich F. Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J Neurosci 2013, 27: 11262–11275.CrossRefGoogle Scholar
  25. [25]
    Helfrich RF, Schneider TR, Rach S, Trautmann-Lengsfeld SA, Engel AK, Herrmann CS. Entrainment of brain oscillations by transcranial alternating current stimulation. Curr Biol 2014, 24: 333–339.CrossRefPubMedGoogle Scholar
  26. [26]
    Kanai R, Chaieb L, Antal A, Walsh V, Paulus W. Frequency-dependent electrical stimulation of the visual cortex. Curr Biol 2008, 18: 1839–1843.CrossRefPubMedGoogle Scholar
  27. [27]
    Zaehle T, Rach S, Herrmann CS. Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS One 2010, 5: e13766.CrossRefPubMedCentralPubMedGoogle Scholar
  28. [28]
    Mannie ZN, Harmer CJ, Cowen PJ, Norbury R. A functional magnetic resonance imaging study of verbal working memory in young people at increased familial risk of depression. Biol Psychiatry. 2010, 67: 471–477.CrossRefPubMedCentralPubMedGoogle Scholar
  29. [29]
    Fregni F, Boggio PS, Nitsche M, Bermpohl F, Antal A, Feredoes E, et al. Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp Brain Res 2005, 166: 23–30.CrossRefPubMedGoogle Scholar
  30. [30]
    Ohn SH, Park CI, Yoo WK, Ko MH, Choi KP, Kim GM, et al. Time-dependent effect of transcranial direct current stimulation on the enhancement of working memory. Neuroreport 2008, 19: 43–47.CrossRefPubMedGoogle Scholar
  31. [31]
    Zaehle T, Sandmann P, Thorne JD, Jäncke L, Herrmann CS. Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: combined behavioural and electrophysiological evidence. BMC Neurosci 2011, 12: 2.CrossRefPubMedCentralPubMedGoogle Scholar
  32. [32]
    Mulquiney PG, Hoy KE, Daskalakis ZJ, Fitzgerald PB. Improving working memory: exploring the effect of transcranial random noise stimulation and transcranial direct current stimulation on the dorsolateral prefrontal cortex. Clin Neurophysiol. 2011, 122: 2384–2389.CrossRefPubMedGoogle Scholar
  33. [33]
    Teo F, Hoy KE, Daskalakis ZJ, Fitzgerald PB. Investigating the role of current strength in tdcs modulation of working memory performance in healthy controls. Front Psychiatry 2011, 2: 45CrossRefPubMedCentralPubMedGoogle Scholar
  34. [34]
    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: 1777–1784.CrossRefPubMedGoogle Scholar
  35. [35]
    Berryhill ME, Jones KT. tDCS selectively improves working memory in older adults with more education. Neurosci Lett 2012, 521: 148–151.CrossRefPubMedGoogle Scholar
  36. [36]
    Kim JH, Kim DW, Chang WH, Kim YH, Kim K, Im CH. Inconsistent outcomes of transcranial direct current stimulation may originate from anatomical differences among individuals: Electric field simulation using individual MRI data. Neurosci Lett 2014, 564C: 6–10.CrossRefGoogle Scholar
  37. [37]
    Meiron O, Lavidor M. Unilateral prefrontal direct current stimulation effects are modulated by working memory load and gender. Brain Stimul 2013, 6: 440–447.CrossRefPubMedGoogle Scholar
  38. [38]
    Lally N, Nord CL, Walsh V, Roiser JP. Does excitatory fronto-extracerebral tDCS lead to improved working memory performance? Version 2. F1000Res. 2013, 2: 219.Google Scholar
  39. [39]
    Jeon SY, Han SJ. Improvement of the working memory and naming by transcranial direct current stimulation. Ann Rehabil Med 2012, 36585–36595.Google Scholar
  40. [40]
    Polanía R, Nitsche MA, Korman C, Batsikadze G, Paulus W. The importance of timing in segregated theta phase-coupling for cognitive performance. Curr Biol 2012a, 22: 1314–1318.CrossRefPubMedGoogle Scholar
  41. [41]
    Meiron O, Lavidor M. Prefrontal oscillatory stimulation modulates access to cognitive control references in retrospective metacognitive commentary. Clin Neurophysiol 2014, 125: 77–82.CrossRefPubMedGoogle Scholar
  42. [42]
    Polanía R, Paulus W, Nitsche MA. Noninvasively decoding the contents of visual working memory in the human prefrontal cortex within high-gamma oscillatory patterns. J Cogn Neurosci 2012b, 24: 304–314.CrossRefPubMedGoogle Scholar
  43. [43]
    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: 909–917.CrossRefPubMedGoogle Scholar
  44. [44]
    Plewnia C, Zwissler B, Längst I, Maurer B, Giel K, Krüger R. Effects of transcranial direct current stimulation (tDCS) on executive functions: influence of COMT Val/Met polymorphism. Cortex 2013, 49: 1801–1807.CrossRefPubMedGoogle Scholar
  45. [45]
    Javadi AH, Walsh V. Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory. Brain Stimul 2012, 5: 231–241.CrossRefPubMedGoogle Scholar
  46. [46]
    Javadi AH, Cheng P. Transcranial direct current stimulation (tDCS) enhances reconsolidation of long-term memory. Brain Stimul 2013, 6: 668–674.CrossRefPubMedGoogle Scholar
  47. [47]
    Manenti R, Brambilla M, Petesi M, Ferrari C, Cotelli M. Enhancing verbal episodic memory in older and young subjects after non-invasive brain stimulation. Front Aging Neurosci 2013, 5: 49.CrossRefPubMedCentralPubMedGoogle Scholar
  48. [48]
    Cerruti C, Schlaug G. Anodal transcranial direct current stimulation of the prefrontal cortex enhances complex verbal associative thought. J Cogn Neurosci 2009, 21: 1980–1987.CrossRefPubMedCentralPubMedGoogle Scholar
  49. [49]
    Metuki N, Sela T, Lavidor M. Enhancing cognitive control components of insight problems solving by anodal tDCS of the left dorsolateral prefrontal cortex. Brain Stimul 2012, 5: 110–115.CrossRefPubMedGoogle Scholar
  50. [50]
    Dockery CA, Hueckel-Weng R, Birbaumer N, Plewnia C. Enhancement of planning ability by transcranial direct current stimulation. J Neurosci 2009, 29: 7271–7277.CrossRefPubMedGoogle Scholar
  51. [51]
    Santarnecchi E, Polizzotto NR, Godone M, Giovannelli F, Feurra M, Matzen L, et al. Frequency-dependent enhancement of fluid intelligence induced by transcranial oscillatory potentials. Curr Biol 2013, 23: 1449–1453.CrossRefPubMedGoogle Scholar
  52. [52]
    Fecteau S, Pascual-Leone A, Zald DH, Liguori P, Théoret H, Boggio PS, et al. Activation of prefrontal cortex by transcranial direct current stimulation reduces appetite for risk during ambiguous decision making. J Neurosci 2007a, 27: 6212–6218.CrossRefPubMedGoogle Scholar
  53. [53]
    Fecteau S, Knoch D, Fregni F, Sultani N, Boggio P, Pascual-Leone A. Diminishing risk-taking behavior by modulating activity in the prefrontal cortex: a direct current stimulation study. J Neurosci 2007b, 27: 12500–12505.CrossRefPubMedGoogle Scholar
  54. [54]
    Boggio PS, Campanhã C, Valasek CA, Fecteau S, Pascual-Leone A, Fregni F. Modulation of decision-making in a gambling task in older adults with transcranial direct current stimulation. Eur J Neurosci 2010, 31: 593–597.CrossRefPubMedGoogle Scholar
  55. [55]
    Pripfl J, Neumann R, Köhler U, Lamm C. Effects of transcranial direct current stimulation on risky decision making are mediated by ‘hot’ and ‘cold’ decisions, personality, and hemisphere. Eur J Neurosci 2013, 38: 3778–3785.CrossRefPubMedGoogle Scholar
  56. [56]
    Minati L, Campanhã C, Critchley HD, Boggio PS. Effects of transcranial direct-current stimulation (tDCS) of the dorsolateral prefrontal cortex (DLPFC) during a mixedgambling risky decision-making task. Cogn Neurosci 2012, 3: 80–88.CrossRefPubMedGoogle Scholar
  57. [57]
    Knoch D, Nitsche MA, Fischbacher U, Eisenegger C, Pascual-Leone A, Fehr E. Studying the neurobiology of social interaction with transcranial direct current stimulation—the example of punishing unfairness. Cereb Cortex 2008, 18: 1987–1990.CrossRefPubMedGoogle Scholar
  58. [58]
    Ruff CC, Ugazio G, Fehr E. Changing social norm compliance with non-invasive brain stimulation. Science 2013, 342: 482–484.CrossRefPubMedGoogle Scholar
  59. [59]
    Phan KL, Wager T, Taylor SF, Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 2002, 16: 331–348.CrossRefPubMedGoogle Scholar
  60. [60]
    Steele JD, Lawrie SM. Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis. Neuroimage. 2004, 21: 868–875.CrossRefPubMedGoogle Scholar
  61. [61]
    Grimm S, Schmidt CF, Bermpohl F, Heinzel A, Dahlem Y, Wyss M, et al. Segregated neural representation of distinct emotion dimensions in the prefrontal cortex-an fMRI study. Neuroimage 2006, 30: 325–340.CrossRefPubMedGoogle Scholar
  62. [62]
    Sergerie K, Lepage M, Armony JL. A face to remember: emotional expression modulates prefrontal activity during memory formation. Neuroimage. 2005, 24: 580–585.CrossRefPubMedGoogle Scholar
  63. [63]
    Ueda K, Okamoto Y, Okada G, Yamashita H, Hori T, Yamawaki S. Brain activity during expectancy of emotional stimuli: an fMRI study. Neuroreport 2003, 14: 51–55.CrossRefPubMedGoogle Scholar
  64. [64]
    Habel U, Klein M, Kellermann T, Shah NJ, Schneider F. Same or different? Neural correlates of happy and sad mood in healthy males. Neuroimage 2005, 26: 206–214.CrossRefPubMedGoogle Scholar
  65. [65]
    Herrington JD, Mohanty A, Koven NS, Fisher JE, Stewart JL, Banich MT, et al. Emotion-modulated performance and activity in left dorsolateral prefrontal cortex. Emotion 2005, 5: 200–207.CrossRefPubMedGoogle Scholar
  66. [66]
    Belyi BI. Mental impairment in unilateral frontal tumours: role of the laterality of the lesion. Int J Neurosci 1987, 32: 799–810.CrossRefPubMedGoogle Scholar
  67. [67]
    Perini GE. Emotions and personality in complex partial seizures. Psychother Psychosom 1986, 45: 141–148.CrossRefPubMedGoogle Scholar
  68. [68]
    Robinson RG, Lipsey JR. Cerebral localization of emotion based on clinical-neuropathological correlations: methodological issues. Psychiatr Dev 1985, 3: 335–347.PubMedGoogle Scholar
  69. [69]
    Schutter DJ van Honk J. A framework for targeting alternative brain regions with repetitive transcranial magnetic stimulation in the treatment of depression. J Psychiatry Neurosci 2005, 30: 91–97.PubMedCentralPubMedGoogle Scholar
  70. [70]
    Nitsche MA, Koschack J, Pohlers H, Hullemann S, Paulus W, Happe S. Effects of frontal transcranial direct current stimulation on emotional state and processing in healthy humans. Front Psychiatry 2012, 3: 58.CrossRefPubMedCentralPubMedGoogle Scholar
  71. [71]
    Plazier M, Joos K, Vanneste S, Ost J, De Ridder D. Bifrontal and bioccipital transcranial direct current stimulation (tDCS) does not induce mood changes in healthy volunteers: a placebo controlled study. Brain Stimul 2012, 5: 454–461.CrossRefPubMedGoogle Scholar
  72. [72]
    Boggio PS, Zaghi S, Fregni F. Modulation of emotions associated with images of human pain using anodal transcranial direct current stimulation (tDCS). Neuropsychologia. 2009, 47: 212–217.CrossRefPubMedGoogle Scholar
  73. [73]
    Maeoka H1, Matsuo A, Hiyamizu M, Morioka S, Ando H. Influence of transcranial direct current stimulation of the dorsolateral prefrontal cortex on pain related emotions: a study using electroencephalographic power spectrum analysis. Neurosci Lett 2012, 512: 12–16.CrossRefPubMedGoogle Scholar
  74. [74]
    Peña-Gómez C, Vidal-Piñeiro D, Clemente IC, Pascual-Leone Á, Bartrés-Faz D. Down-regulation of negative emotional processing by transcranial direct current stimulation: effects of personality characteristics. PLoS One 2011, 6: e22812.CrossRefPubMedCentralPubMedGoogle Scholar
  75. [75]
    Vanderhasselt MA, De Raedt R, Brunoni AR, Campanhã C, Baeken C, Remue J, et al. tDCS over the left prefrontal cortex enhances cognitive control for positive affective stimuli. PLoS One 2013, 8: e62219.CrossRefPubMedCentralPubMedGoogle Scholar
  76. [76]
    Feeser M, Prehn K, Kazzer P, Mungee A, Bajbouj M. Transcranial direct current stimulation enhances cognitive control during emotion regulation. Brain Stimul 2014, 7: 105–112.CrossRefPubMedGoogle Scholar
  77. [77]
    Mungee A, Kazzer P, Feeser M, Nitsche MA, Schiller D, Bajbouj M. Transcranial direct current stimulation of the prefrontal cortex: a means to modulate fear memories. Neuroreport 2014, 25: 480–484.PubMedGoogle Scholar
  78. [78]
    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: 266–275.CrossRefPubMedCentralPubMedGoogle Scholar
  79. [79]
    Bikson M, Rahman A, Datta A. Computational models of transcranial direct current stimulation. Clin EEG Neurosci 2012, 43176–43183.Google Scholar
  80. [80]
    Nitsche MA, Doemkes S, Karaköse T, Antal A, Liebetanz D, Lang N, et al. Shaping the effects of transcranial direct current stimulation of the human motor cortex. J Neurophysiol 2007, 97: 3109–3117.CrossRefPubMedGoogle Scholar
  81. [81]
    Polanía R, Nitsche MA, Paulus W. Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation. Hum Brain Mapp 2011, 32: 1236–1249CrossRefPubMedGoogle Scholar

Copyright information

© Shanghai Institutes for Biological Sciences, CAS and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Clinical Neurophysiology, University Medical CenterGeorg-August-UniversityGoettingenGermany

Personalised recommendations