Keep calm and carry on: improved frustration tolerance and processing speed by transcranial direct current stimulation (tDCS)

Christian Plewnia, Philipp A Schroeder, Roland Kunze, Florian Faehling, Larissa Wolkenstein, Christian Plewnia, Philipp A Schroeder, Roland Kunze, Florian Faehling, Larissa Wolkenstein

Abstract

Cognitive control (CC) of attention is a major prerequisite for effective information processing. Emotional distractors can bias and impair goal-directed deployment of attentional resources. Frustration-induced negative affect and cognition can act as internal distractors with negative impact on task performance. Consolidation of CC may thus support task-oriented behavior under challenging conditions. Recently, transcranial direct current stimulation (tDCS) has been put forward as an effective tool to modulate CC. Particularly, anodal, activity enhancing tDCS to the left dorsolateral prefrontal cortex (dlPFC) can increase insufficient CC in depression as indicated by a reduction of attentional biases induced by emotionally salient stimuli. With this study, we provide first evidence that, compared to sham stimulation, tDCS to the left dlPFC enhances processing speed measured by an adaptive version of the Paced Auditory Serial Addition Task (PASAT) that is typically thwarted by frustration. Notably, despite an even larger amount of error-related negative feedback, the task-induced upset was suppressed in the group receiving anodal tDCS. Moreover, inhibition of task-related negative affect was correlated with performance gains, suggesting a close link between enhanced processing speed and consolidation of CC by tDCS. Together, these data provide first evidence that activity enhancing anodal tDCS to the left dlPFC can support focused cognitive processing particularly when challenged by frustration-induced negative affect.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Experimental procedure.
Fig 1. Experimental procedure.
All participants completed the ‘Positive and Negative Affect Schedule’ (PANAS) and then performed a baseline measurement of the adaptive Paced Auditory Serial Addition Task (PASAT) without tDCS. Then either sham or anodal tDCS was initiated. For the first 5 minutes of stimulation, participants were instructed to relax. Next, a second and third measurement of PASAT performance were conducted for 5 minutes each, with a break of 5 minutes in between. Afterwards, stimulation was terminated and participants completed the PANAS post questionnaire.
Fig 2. Changes in processing speed as…
Fig 2. Changes in processing speed as a function of stimulation.
Anodal stimulation led to a significant stimulation main effect in the corresponding block x stimulation ANCOVA, driven by shorter ISIs in the stimulation group. Error bars reflect standard errors of the mean.
Fig 3. Feeling ‘upset’ and processing speed.
Fig 3. Feeling ‘upset’ and processing speed.
Whereas participants in the sham stimulation group felt more upset after the experiment, this increase was alleviated in the anodal stimulation group (Panel A). Increase in feeling upset was correlated with less processing speed improvements as measured by the PASAT inter-stimulus interval (ISI; Panel B). Error bars represent standard errors of the mean.

References

    1. Miller EK. The prefrontal cortex and cognitive control. Nat Rev Neurosci. 2000;1: 59–65.
    1. Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD. Conflict monitoring and cognitive control. Psychol Rev. 2001;108: 624–52.
    1. Vuilleumier P. How brains beware: neural mechanisms of emotional attention. Trends Cogn Sci. 2005;9: 585–94.
    1. Goschke T. Dysfunctions of decision-making and cognitive control as transdiagnostic mechanisms of mental disorders: advances, gaps, and needs in current research. Int J Methods Psychiatr Res. 2014;23 Suppl 1: 41–57. 10.1002/mpr.1410
    1. Disner SG, Beevers CG, Haigh EA, Beck AT. Neural mechanisms of the cognitive model of depression. Nat Rev Neurosci. 2011;12: 467–77. 10.1038/nrn3027
    1. Gotlib IH, Joormann J. Cognition and depression: current status and future directions. Annu Rev Clin Psychol. 2010;6: 285–312. 10.1146/annurev.clinpsy.121208.131305
    1. Mathews A, MacLeod C. Cognitive vulnerability to emotional disorders. Annu Rev Clin Psychol. 2005;1: 167–95.
    1. Clark DA, Beck AT. Cognitive theory and therapy of anxiety and depression: convergence with neurobiological findings. Trends Cogn Sci. Elsevier Ltd; 2010;14: 418–24. 10.1016/j.tics.2010.06.007
    1. Roiser JP, Elliott R, Sahakian BJ. Cognitive mechanisms of treatment in depression. Neuropsychopharmacology. Nature Publishing Group; 2012;37: 117–36. 10.1038/npp.2011.183
    1. Siegle GJ, Ghinassi F, Thase ME. Neurobehavioral Therapies in the 21st Century: Summary of an Emerging Field and an Extended Example of Cognitive Control Training for Depression. Cognit Ther Res. 2007;31: 235–262.
    1. Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24: 167–202.
    1. Koechlin E, Ody C, Kouneiher F. The architecture of cognitive control in the human prefrontal cortex. Science. 2003;302: 1181–5.
    1. Kouneiher F, Charron S, Koechlin E. Motivation and cognitive control in the human prefrontal cortex. Nat Neurosci. 2009;12: 939–45. 10.1038/nn.2321
    1. Anticevic A, Repovs G, Barch DM. Resisting emotional interference: brain regions facilitating working memory performance during negative distraction. Cogn Affect Behav Neurosci. 2010;10: 159–73. 10.3758/CABN.10.2.159
    1. Dolcos F, McCarthy G. Brain systems mediating cognitive interference by emotional distraction. J Neurosci. 2006;26: 2072–9.
    1. Wessa M, Heissler J, Schönfelder S, Kanske P. Goal-directed behavior under emotional distraction is preserved by enhanced task-specific activation. Soc Cogn Affect Neurosci. 2013;8: 305–12. 10.1093/scan/nsr098
    1. Dayan E, Censor N, Buch ER, Sandrini M, Cohen LG. Noninvasive brain stimulation: from physiology to network dynamics and back. Nat Neurosci. Nature Publishing Group; 2013;16: 838–44. 10.1038/nn.3422
    1. 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.
    1. Priori A. Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability. Clin Neurophysiol. 2003;114: 589–595.
    1. Filmer HL, Dux PE, Mattingley JB. Applications of transcranial direct current stimulation for understanding brain function. Trends Neurosci. 2014;37: 742–753. 10.1016/j.tins.2014.08.003
    1. Dockery CA, Hueckel-Weng R, Birbaumer N, Plewnia C. Enhancement of planning ability by transcranial direct current stimulation. J Neurosci. 2009;29: 7271–7. 10.1523/JNEUROSCI.0065-09.2009
    1. Zwissler B, Sperber C, Aigeldinger S, Schindler S, Kissler J, Plewnia C. Shaping Memory Accuracy by Left Prefrontal Transcranial Direct Current Stimulation. J Neurosci. 2014;34: 4022–4026. 10.1523/JNEUROSCI.5407-13.2014
    1. Kuo M-F, Nitsche MA. Effects of transcranial electrical stimulation on cognition. Clin EEG Neurosci. 2012;43: 192–9. 10.1177/1550059412444975
    1. Wolkenstein L, Plewnia C. Amelioration of cognitive control in depression by transcranial direct current stimulation. Biol Psychiatry. 2013;73: 646–51. 10.1016/j.biopsych.2012.10.010
    1. Wolkenstein L, Zeiller M, Kanske P, Plewnia C. Induction of a depression-like negativity bias by cathodal transcranial direct current stimulation. Cortex. 2014;59: 103–112. 10.1016/j.cortex.2014.07.011
    1. Ingram RE, Kendall PC, Smith TW, Donnell C, Ronan K. Cognitive specificity in emotional distress. J Pers Soc Psychol. 1987;53: 734
    1. Davidson RJ, Irwin W, Anderle MJ, Kalin NH. The neural substrates of affective processing in depressed patients treated with venlafaxine. Am J Psychiatry. 2003;160: 64–75.
    1. Siegle GJ, Thompson W, Carter CS, Steinhauer SR, Thase ME. Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol Psychiatry. 2007;61: 198–209.
    1. Oei NY, Veer IM, Wolf OT, Spinhoven P, Rombouts SA, Elzinga BM. Stress shifts brain activation towards ventral “affective” areas during emotional distraction. Soc Cogn Affect Neurosci. 2012;7: 403–12. 10.1093/scan/nsr024
    1. Moriya J, Sugiura Y. High visual working memory capacity in trait social anxiety. PLoS One. 2012;7: e34244 10.1371/journal.pone.0034244
    1. Hester R, Garavan H. Working memory and executive function: the influence of content and load on the control of attention. Mem Cognit. 2005;33: 221–33.
    1. Holdwick D Jr. The Subjective Experience of PASAT Testing Does the PASAT Induce Negative Mood? Arch Clin Neuropsychol. 1999;14: 273–284.
    1. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9: 97–113.
    1. Gronwall DM, Sampson H. The psychological effects of concussion Oxford, England: Auckland U Press; 1974.
    1. Lejuez CW, Kahler CW, Brown RA. A modified computer version of the Paced Auditory Serial Addition Task (PASAT) as a laboratory-based stressor. Behav Ther. 2003;26: 290–293.
    1. Lazeron RHC, Rombouts SARB, de Sonneville L, Barkhof F, Scheltens P. A paced visual serial addition test for fMRI. J Neurol Sci. 2003;213: 29–34.
    1. Jasper HH. The ten twenty electrode system of the international federation. Electroencephalogr Clin Neurophysiol. 1958;10: 371–375.
    1. Priori A, Mameli F, Cogiamanian F, Marceglia S, Tiriticco M, Mrakic-Sposta S, et al. Lie-specific involvement of dorsolateral prefrontal cortex in deception. Cereb Cortex. 2008;18: 451–5.
    1. 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.
    1. Watson D, Clark LA, Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol. 1988;54: 1063–1070.
    1. Crawford JR, Henry JD. The positive and negative affect schedule (PANAS): construct validity, measurement properties and normative data in a large non-clinical sample. Br J Clin Psychol. 2004;43: 245–265.
    1. Krohne HW, Egloff B, Kohlmann C-W, Tausch A. Untersuchungen mit einer deutschen Version der “Positive and Negative Affect Schedule” (PANAS). / Investigations with a German version of the Positive and Negative Affect Schedule (PANAS). Diagnostica. 1996;42: 139–156.
    1. Brunoni AR, Boggio PS, De Raedt R, Benseñor IM, Lotufo PA, Namur V, et al. Cognitive control therapy and transcranial direct current stimulation for depression: a randomized, double-blinded, controlled trial. J Affect Disord. 2014;162: 43–9. 10.1016/j.jad.2014.03.026
    1. Vanderhasselt M-A, Brunoni AR, Loeys T, Boggio PS, De Raedt R. Nosce te ipsum—Socrates revisited? Controlling momentary ruminative self-referent thoughts by neuromodulation of emotional working memory. Neuropsychologia. 2013;51: 2581–9. 10.1016/j.neuropsychologia.2013.08.011
    1. Segrave RA, Arnold S, Hoy K, Fitzgerald PB. Concurrent cognitive control training augments the antidepressant efficacy of tDCS: A pilot study. Brain Stimul. 2014;7: 325–331. 10.1016/j.brs.2013.12.008
    1. Kanske P, Heissler J, Schönfelder S, Bongers A, Wessa M. How to regulate emotion? Neural networks for reappraisal and distraction. Cereb Cortex. 2011;21: 1379–88. 10.1093/cercor/bhq216
    1. Schweizer S, Grahn J, Hampshire A, Mobbs D, Dalgleish T. Training the emotional brain: improving affective control through emotional working memory training. J Neurosci. 2013;33: 5301–11. 10.1523/JNEUROSCI.2593-12.2013
    1. Clarke PJF, Browning M, Hammond G, Notebaert L, MacLeod C. The Causal Role of the Dorsolateral Prefrontal Cortex in the Modification of Attentional Bias: Evidence from Transcranial Direct Current Stimulation. Biol Psychiatry. 2014;76: 1–7.
    1. Calkins AW, McMorran KE, Siegle GJ, Otto MW. The Effects of Computerized Cognitive Control Training on Community Adults with Depressed Mood. Behav Cogn Psychother. 2014; 1–12.
    1. Fregni F, Boggio PS, Nitsche MA, 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.
    1. 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. 10.1016/j.brs.2010.06.004
    1. Tombaugh TN. A comprehensive review of the Paced Auditory Serial Addition Test (PASAT). Arch Clin Neuropsychol. 2006;21: 53–76.
    1. Ochsner KN, Silvers JA, Buhle JT. Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Ann N Y Acad Sci. 2012;1251: E1–24. 10.1111/j.1749-6632.2012.06751.x
    1. Ochsner KN, Gross JJ. The cognitive control of emotion. Trends Cogn Sci. 2005;9: 242–249.
    1. Subramaniam K, Vinogradov S. Improving the neural mechanisms of cognition through the pursuit of happiness. Front Hum Neurosci. 2013;7: 452 10.3389/fnhum.2013.00452
    1. Wells A, Matthews G. Attention and Emotion: A Clinical Perspective. Psychology Press; 1995.
    1. Carver C, Scheier M. The experience of emotions during goal pursuit. In: Reinhard Pekrun LL-G, editor. International Handbook of Emotions in Education. 2014.
    1. Oatley K, Johnson-Laird PN. Cognitive approaches to emotions. Trends Cogn Sci. 2014;18: 134–40. 10.1016/j.tics.2013.12.004
    1. Rock PL, Roiser JP, Riedel WJ, Blackwell AD. Cognitive impairment in depression: A systematic review and meta-analysis. Psychol Med. 2013;44: 1–12. 10.1017/S0033291712003030
    1. Foland-Ross LC, Gotlib IH. Cognitive and neural aspects of information processing in major depressive disorder: an integrative perspective. Front Psychol. 2012;3: 489 10.3389/fpsyg.2012.00489
    1. Mayberg HS. Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. Br Med Bull. 2003;65: 193–207.
    1. Elliott R, Baker SC, Rogers RD, O’Leary DA, Paykel ES, Frith CD, et al. Prefrontal dysfunction in depressed patients performing a complex planning task: a study using positron emission tomography. Psychol Med. 1997;27: 931–942.
    1. Okada G, Okamoto Y, Morinobu S, Yamawaki S, Yokota N. Attenuated left prefrontal activation during a verbal fluency task in patients with depression. Neuropsychobiology. 2003;47: 21–26.
    1. Gemar MC, Kapur S, Segal ZV, Brown GM, Houle S. Effects of self-generated sad mood on regional cerebral activity: A PET study in normal subjects. Depression. 1996;4: 81–88.
    1. Eysenck MW, Derakshan N, Santos R, Calvo MG. Anxiety and cognitive performance: attentional control theory. Emotion. 2007; 7:336
    1. Staal MA, Staal MA, Field M, Field M. Stress, Cognition, and Human Performance: A Literature Review and Conceptual Framework. NASA technical memorandum: 212824. 2004.
    1. Jones NP, Siegle GJ, Muelly ER, Haggerty A, Ghinassi F. Poor performance on cognitive tasks in depression: Doing too much or not enough? Cogn Affect Behav Neurosci. 2010;10: 129–40. 10.3758/CABN.10.1.129
    1. Deary IJ, Langan SJ, Hepburn DA, Frier BM. Which abilities does the PASAT test? Pers Individ Dif. 1991;12: 983–987.
    1. Nejad AB, Fossati P, Lemogne C. Self-referential processing, rumination, and cortical midline structures in major depression. Front Hum Neurosci. 2013;7: 666 10.3389/fnhum.2013.00666
    1. Vanderhasselt M-A, De Raedt R, Namur V, Lotufo PA, Bensenor IM, Boggio PS, et al. Transcranial electric stimulation and neurocognitive training in clinically depressed patients: A pilot study of the effects on rumination. Prog Neuro-Psychopharmacology Biol Psychiatry. 2015;57: 93–99. 10.1016/j.pnpbp.2014.09.015
    1. Ambrus GG, Al-Moyed H, Chaieb L, Sarp L, Antal A, Paulus W. The fade-in—short stimulation—fade out approach to sham tDCS—reliable at 1 mA for naïve and experienced subjects, but not investigators. Brain Stimul. 2012;5: 499–504. 10.1016/j.brs.2011.12.001
    1. Herz DM, Christensen MS, Bruggemann N, Hulme OJ, Ridderinkhof KR, Madsen KH, et al. Motivational tuning of fronto-subthalamic connectivity facilitates control of action impulses. J Neurosci. 2014;34: 3210–7. 10.1523/JNEUROSCI.4081-13.2014
    1. Clemens B, Jung S, Mingoia G, Weyer D, Domahs F, Willmes K. Influence of anodal transcranial direct current stimulation (tDCS) over the right angular gyrus on brain activity during rest. PLoS One. 2014;9: e95984 10.1371/journal.pone.0095984
    1. 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: 1801–7. 10.1016/j.cortex.2012.11.002
    1. Vanderhasselt M-A, 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 10.1371/journal.pone.0062219

Source: PubMed

Sponsorit ja yhteistyökumppanit

Sairaudet

Huumeiden interventiot

3
Tilaa