Evaluating the Effects of Online tDCS with Emotional n-back Training on Working Memory and Associated Cognitive Abilities

Authors

  • Gregory Samuel Berlin University of Wisconsin-Milwaukee
  • Abel Steven Mathew University of Wisconsin-Milwaukee
  • Salahadin Lotfi University of Wisconsin-Milwaukee
  • Ashleigh Marie Harvey University of Wisconsin-Milwaukee
  • Han-Joo Lee University of Wisconsin-Milwaukee

DOI:

https://doi.org/10.15540/nr.7.3.129

Keywords:

tDCS, working memory training, n-back, dlPFC

Abstract

Working memory (WM) is a core cognitive ability important for everyday functioning. A burgeoning area of research suggests that WM can be improved via working memory training (WMT) paradigms. Additionally, recent research has shown that WM may be enhanced through noninvasive neuromodulation such as transcranial direct current stimulation (tDCS). In this study, we evaluated how a single-session, brief-but-concentrated combination of tDCS over the left dorsolateral prefrontal cortex (dlPFC; F3 region), paired with a WMT paradigm utilizing emotional stimuli (emotional n-back) could produce gains in WM and associated, untrained cognitive abilities. Healthy undergraduate participants were randomized to receive either active tDCS and WMT, or sham-tDCS and WMT. Cognitive abilities (WM, attention control, and cognitive inhibition) were measured before and after the intervention. No significant differences were found in WM performance or associated abilities between those who received active or sham tDCS. Individuals in both groups evidenced a faster reaction time on an Operation Span task, and an Emotional Stroop Task, following the WMT session. These findings add to the mixed picture of the effectiveness of single-session WMT protocols and highlight the importance of the dose-response relationship in training core cognitive processes such as WM.

References

Alonzo, A., Brassil, J., Taylor, J. L., Martin, D., & 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 Stimulation, 5(3), 208–213. https://doi.org/10.1016/j.brs.2011.04.006

Au, J., Buschkuehl, M., Duncan, G. J., & Jaeggi, S. M. (2016). There is no convincing evidence that working memory training is NOT effective: A reply to Melby-Lervåg and Hulme (2015). Psychonomic Bulletin & Review, 23(1), 331–337. https://doi.org/10.3758/s13423-015-0967-4

Baddeley, A. (1992). Working memory. Science, 255(5044), 556–559. https://doi.org/10.1126/science.1736359

Barbey, A. K., Koenigs, M., & Grafman, J. (2013). Dorsolateral prefrontal contributions to human working memory. Cortex, 49(5), 1195–1205. https://doi.org/10.1016/j.cortex.2012.05.022

Beam, W., Borckardt, J. J., Reeves, S. T., & George, M. S. (2009). An efficient and accurate new method for locating the F3 position for prefrontal TMS applications. Brain Stimulation, 2(1), 50–54. https://doi.org/10.1016/j.brs.2008.09.006

Beilock, S. L., & Carr, T. H. (2005). When high-powered people fail: Working memory and “choking under pressure” in math. Psychological Science, 16(2), 101–105. https://doi.org/10.1111/j.0956-7976.2005.00789.x

Bikson, M., Grossman, P., Thomas, C., Zannou, A. L., Jiang, J., Adnan, T., … Woods, A. J. (2016). Safety of transcranial direct current stimulation: Evidence based update 2016. Brain Stimulation, 9(5), 641–661. https://doi.org/10.1016/j.brs.2016.06.004

Bo, J., Jennett, S., & Seidler, R. D. (2011). Working memory capacity correlates with implicit serial reaction time task performance. Experimental Brain Research, 214(1), 73. https://doi.org/10.1007/s00221-011-2807-8

Brunoni, A. R., & Vanderhasselt, M.-A. (2014). Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: A systematic review and meta-analysis. Brain and Cognition, 86, 1–9. https://doi.org/10.1016/j.bandc.2014.01.008

Clarke, P. J. F., Browning, M., Hammond, G., Notebaert, L., & MacLeod, C. (2014). The causal role of the dorsolateral prefrontal cortex in the modification of attentional bias: Evidence from transcranial direct current stimulation. Biological Psychiatry, 76(12), 946–952. https://doi.org/10.1016/j.biopsych.2014.03.003

D’Esposito, M., & Postle, B. R. (2015). The cognitive neuroscience of working memory. Annual Review of Psychology, 66, 115–142. https://doi.org/10.1146/annurev-psych-010814-015031

Dolcos, F., LaBar, K. S., & Cabeza, R. (2004). Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron, 42(5), 855–863. https://doi.org/10.1016/S0896-6273(04)00289-2

Ebbinghaus, H. (2013). Memory: A contribution to experimental psychology. Annals of Neurosciences, 20(4), 155. https://doi.org/10.5214/ans.0972.7531.200408

Eriksson, J., Vogel, E. K., Lansner, A., Bergström, F., & Nyberg, L. (2015). Neurocognitive architecture of working memory. Neuron, 88(1), 33–46. https://doi.org/10.1016/j.neuron.2015.09.020

Fan, J., McCandliss, B. D., Sommer, T., Raz, A., & Posner, M. I. (2002). Testing the efficiency and independence of attentional networks. Journal of Cognitive Neuroscience, 14(3), 340–347. https://doi.org/10.1162/089892902317361886

Figueira, J. S. B., Oliveira, L., Pereira, M. G., Pacheco, L. B., Lobo, I., Motta-Ribeiro, G. C., & David, I. A. (2017). An unpleasant emotional state reduces working memory capacity: Electrophysiological evidence. Social Cognitive and Affective Neuroscience, 12(6), 984–992. https://doi.org/10.1093/scan/nsx030

Filmer, H. L., Lyons, M., Mattingley, J. B., & Dux, P. E. (2017). Anodal tDCS applied during multitasking training leads to transferable performance gains. Scientific Reports, 7(1), 12988. https://doi.org/10.1038/s41598-017-13075-y

Fregni, F., Boggio, P. S., Nitsche, M., Bermpohl, F., Antal, A., Feredoes, E., … Pascual-Leone, A. (2005). Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Experimental Brain Research, 166(1), 23–30. https://doi.org/10.1007/s00221-005-2334-6

Gögler, N., Willacker, L., Funk, J., Strube, W., Langgartner, S., Napiórkowski, N., … Finke, K. (2017). Single-session transcranial direct current stimulation induces enduring enhancement of visual processing speed in patients with major depression. European Archives of Psychiatry and Clinical Neuroscience, 267(7), 671–686. https://doi.org/10.1007/s00406-016-0761-y

Hill, A. T., Fitzgerald, P. B., & Hoy, K. E. (2016). Effects of anodal transcranial direct current stimulation on working memory: A systematic review and meta-analysis of findings from healthy and neuropsychiatric populations. Brain Stimulation, 9(2), 197–208. https://doi.org/10.1016/j.brs.2015.10.006

Holmes, J., Gathercole, S. E., & Dunning, D. L. (2009). Adaptive training leads to sustained enhancement of poor working memory in children. Developmental Science, 12(4), F9–F15. https://doi.org/10.1111/j.1467-7687.2009.00848.x

Horvath, J. C., Forte, J. D., & Carter, O. (2015). Quantitative review finds no evidence of cognitive effects in healthy populations from single-session transcranial direct current stimulation (tDCS). Brain Stimulation, 8(3), 535–550. https://doi.org/10.1016/j.brs.2015.01.400

Hoy, K. E., Emonson, M. R. L., Arnold, S. L., Thomson, R. H., Daskalakis, Z. J., & Fitzgerald, P. B. (2013). Testing the limits: Investigating the effect of tDCS dose on working memory enhancement in healthy controls. Neuropsychologia, 51(9), 1777–1784. https://doi.org/10.1016/j.neuropsychologia.2013.05.018

Hur, J., Iordan, A. D., Dolcos, F., & Berenbaum, H. (2017). Emotional influences on perception and working memory. Cognition and Emotion, 31(6), 1294–1302. https://doi.org/10.1080/02699931.2016.1213703

Jaeggi, S. M., & Buschkuehl, M. (2014). Working memory training and transfer: Theoretical and practical considerations. In B. Toni (Ed.), New Frontiers of Multidisciplinary Research in STEAM-H (Science, Technology, Engineering, Agriculture, Mathematics, and Health) (Vol 90, pp. 19–43). https://doi.org/10.1007/978-3-319-07755-0_2

Jaeggi, S. M., Buschkuehl, M., Jonides, J., & Perrig, W. J. (2008). Improving fluid intelligence with training on working memory. Proceedings of the National Academy of Sciences of the United States of America, 105(19), 6829–6833. https://doi.org/10.1073/pnas.0801268105

Jaeggi, S. M., Buschkuehl, M., Jonides, J., & Shah, P. (2011). Short- and long-term benefits of cognitive training. Proceedings of the National Academy of Sciences, 108(25), 10081–10086. https://doi.org/10.1073/pnas.1103228108

Jaeggi, S. M., Buschkuehl, M., Shah, P., & Jonides, J. (2014). The role of individual differences in cognitive training and transfer. Memory & Cognition, 42(3), 464–480. https://doi.org/10.3758/s13421-013-0364-z

Jaeggi, S. M., Studer-Luethi, B., Buschkuehl, M., Su, Y.-F., Jonides, J., & Perrig, W. J. (2010). The relationship between n-back performance and matrix reasoning—implications for training and transfer. Intelligence, 38(6), 625–635. https://doi.org/10.1016/j.intell.2010.09.001

Karbach, J., & Verhaeghen, P. (2014). Making working memory work: A meta-analysis of executive-control and working memory training in older adults. Psychological Science, 25(11), 2027–2037. https://doi.org/10.1177/0956797614548725

Larsen, S. E., Lotfi, S., Bennett, K. P., Larson, C. L., Dean-Bernhoft, C., & Lee, H.-J. (2019). A pilot randomized trial of a dual n-back emotional working memory training program for veterans with elevated PTSD symptoms. Psychiatry Research, 275, 261–268. https://doi.org/10.1016/j.psychres.2019.02.015

Lovibond, P. F., & Lovibond, S. H. (1995). The structure of negative emotional states: Comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behaviour Research and Therapy, 33(3), 335–343. https://doi.org/10.1016/0005-7967(94)00075-U

Lukasik, K. M., Waris, O., Soveri, A., Lehtonen, M., & Laine, M. (2019). The relationship of anxiety and stress with working memory performance in a large non-depressed sample. Frontiers in Psychology, 10, 4. https://doi.org/10.3389/fpsyg.2019.00004

Mancuso, L. E., Ilieva, I. P., Hamilton, R. H., & Farah, M. J. (2016). Does transcranial direct current stimulation improve healthy working memory?: A meta-analytic review. Journal of Cognitive Neuroscience, 28(8), 1063–1089. https://doi.org/10.1162/jocn_a_00956

Martin, D. M., Teng, J. Z., Lo, T. Y., Alonzo, A., Goh, T., Iacoviello, B. M., … Loo, C. K. (2018). Clinical pilot study of transcranial direct current stimulation combined with Cognitive Emotional Training for medication resistant depression. Journal of Affective Disorders, 232, 89–95. https://doi.org/10.1016/j.jad.2018.02.021

Matsuo, K., Glahn, D. C., Peluso, M. A. M., Hatch, J. P., Monkul, E. S., Najt, P., … Soares, J. C. (2007). Prefrontal hyperactivation during working memory task in untreated individuals with major depressive disorder. Molecular Psychiatry, 12(2), 158–166. https://doi.org/10.1038/sj.mp.4001894

Meinzer, M., Jähnigen, S., Copland, D. A., Darkow, R., Grittner, U., Avirame, K., … Flöel, A. (2014). Transcranial direct current stimulation over multiple days improves learning and maintenance of a novel vocabulary. Cortex, 50, 137–147. https://doi.org/10.1016/j.cortex.2013.07.013

Melby-Lervåg, M., & Hulme, C. (2013). Is working memory training effective? A meta-analytic review. Developmental Psychology, 49(2), 270–291. https://doi.org/10.1037/a0028228

Melby-Lervåg, M., & Hulme, C. (2016). There is no convincing evidence that working memory training is effective: A reply to Au et al. (2014) and Karbach and Verhaeghen (2014). Psychonomic Bulletin & Review, 23(1), 324–330. https://doi.org/10.3758/s13423-015-0862-z

Moon, C.-M., & Jeong, G.-W. (2015). Functional neuroanatomy on the working memory under emotional distraction in patients with generalized anxiety disorder. Psychiatry and Clinical Neurosciences, 69(10), 609–619. https://doi.org/10.1111/pcn.12295

Moran, T. P. (2016). Anxiety and working memory capacity: A meta-analysis and narrative review. Psychological Bulletin, 142(8), 831–864. https://doi.org/10.1037/bul0000051

Nitsche, M. A., Fricke, K., Henschke, U., Schlitterlau, A., Liebetanz, D., Lang, N., … Paulus, W. (2003). Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. The Journal of Physiology, 553(1), 293–301. https://doi.org/10.1113/jphysiol.2003.049916

Oswald, F. L., McAbee, S. T., Redick, T. S., & Hambrick, D. Z. (2015). The development of a short domain-general measure of working memory capacity. Behavior Research Methods, 47(4), 1343–1355. https://doi.org/10.3758/s13428-014-0543-2

Owens, M., Koster, E. H. W., & Derakshan, N. (2013). Improving attention control in dysphoria through cognitive training: Transfer effects on working memory capacity and filtering efficiency. Psychophysiology, 50(3), 297–307. https://doi.org/10.1111/psyp.12010

Plewnia, C., Schroeder, P. A., Kunze, R., Faehling, F., & Wolkenstein, L. (2015). Keep calm and carry on: Improved frustration tolerance and processing speed by transcranial direct current stimulation (tDCS). PLoS ONE, 10(4). https://doi.org/10.1371/journal.pone.0122578

Ruf, S. P., Fallgatter, A. J., & Plewnia, C. (2017). Augmentation of working memory training by transcranial direct current stimulation (tDCS). Scientific Reports, 7(1), 876. https://doi.org/10.1038/s41598-017-01055-1

Salazar-Villanea, M., Liebmann, E., Garnier-Villarreal, M., Montenegro-Montenegro, E., & Johnson, D. K. (2015). Depressive symptoms affect working memory in healthy older adult hispanics. Journal of Depression & Anxiety, 4(4). https://doi.org/10.4172/2167-1044.1000204

Sari, B. A., Koster, E. H. W., Pourtois, G., & Derakshan, N. (2016). Training working memory to improve attentional control in anxiety: A proof-of-principle study using behavioral and electrophysiological measures. Biological Psychology, 121, 203–212. https://doi.org/10.1016/j.biopsycho.2015.09.008

Schmidt, M. E., Wolkenstein, L., & Plewnia, C. (2015). P165. Effects of transcranial direct current stimulation on training cognitive control over emotional distraction. Clinical Neurophysiology, 126(8), e142. https://doi.org/10.1016/j.clinph.2015.04.230

Schulze, L., Grove, M., Tamm, S., Renneberg, B., & Roepke, S. (2019). Effects of transcranial direct current stimulation on the cognitive control of negative stimuli in borderline personality disorder. Scientific Reports, 9(1), 332. https://doi.org/10.1038/s41598-018-37315-x

Schwaighofer, M., Fischer, F., & Bühner, M. (2015). Does working memory training transfer? A meta-analysis including training conditions as moderators. Educational Psychologist, 50(2), 138–166. https://doi.org/10.1080/00461520.2015.1036274

Schweizer, S., Grahn, J., Hampshire, A., Mobbs, D., & Dalgleish, T. (2013). Training the emotional brain: Improving affective control through emotional working memory training. Journal of Neuroscience, 33(12), 5301–5311. https://doi.org/10.1523/JNEUROSCI.2593-12.2013

Schweizer, S., Hampshire, A., & Dalgleish, T. (2011). Extending brain-training to the affective domain: Increasing cognitive and affective executive control through emotional working memory training. PLoS ONE, 6(9), e24372. https://doi.org/10.1371/journal.pone.0024372

Schweizer, S., Samimi, Z., Hasani, J., Moradi, A., Mirdoraghi, F., & Khaleghi, M. (2017). Improving cognitive control in adolescents with post-traumatic stress disorder (PTSD). Behaviour Research and Therapy, 93, 88–94. https://doi.org/10.1016/j.brat.2017.03.017

Smith, P., & Waterman, M. (2003). Processing bias for aggression words in forensic and nonforensic samples. Cognition and Emotion, 17(5), 681–701. https://doi.org/10.1080/02699930302281

Soveri, A., Antfolk, J., Karlsson, L., Salo, B., & Laine, M. (2017). Working memory training revisited: A multi-level meta-analysis of n-back training studies. Psychonomic Bulletin & Review, 24(4), 1077–1096. https://doi.org/10.3758/s13423-016-1217-0

Stout, D. M., Shackman, A. J., Johnson, J. S., & Larson, C. L. (2015). Worry is associated with impaired gating of threat from working memory. Emotion, 15(1), 6–11. https://doi.org/10.1037/emo0000015

Stout, D. M., Shackman, A. J., & Larson, C. L. (2013). Failure to filter: Anxious individuals show inefficient gating of threat from working memory. Frontiers in Human Neuroscience, 7. https://doi.org/10.3389/fnhum.2013.00058

Thompson, T. W., Waskom, M. L., & Gabrieli, J. D. E. (2016). Intensive working memory training produces functional changes in large-scale frontoparietal networks. Journal of Cognitive Neuroscience, 28(4), 575–588. https://doi.org/10.1162/jocn_a_00916

Van der Molen, M. J., Van Luit, J. E. H., Van der Molen, M. W., Klugkist, I., & Jongmans, M. J. (2010). Effectiveness of a computerised working memory training in adolescents with mild to borderline intellectual disabilities. Journal of Intellectual Disability Research: JIDR, 54(5), 433–447. https://doi.org/10.1111/j.1365-2788.2010.01285.x

Westwood, S. J., & Romani, C. (2017). Transcranial direct current stimulation (tDCS) modulation of picture naming and word reading: A meta-analysis of single session tDCS applied to healthy participants. Neuropsychologia, 104, 234–249. https://doi.org/10.1016/j.neuropsychologia.2017.07.031

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Published

2020-09-29

Issue

Vol. 7 No. 3 (2020)

Section

Research Papers

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