Transcranial direct current stimulation (tDCS). An effective tool for improving episodic memory in young people?
Abstract
The main aim of the present study was to determine the effects of anodal vs sham tDCS administered over the dlPFC during the encoding phase of an episodic memory task, on the accuracy rate (AR) and reaction time (RT) measured in the immediate and delayed recall phases of the task, in a group of 23 healthy young participants.
A randomized double-blind sham-controlled study of tDCS was carried out. The results evidenced significant main effects for factors Block, Session, and Delay on the AR and on RT, but not for the Group factor. Robust intra-session and inter-session learning effects but no Group (anodal vs sham tDCS) effect in episodic memory performance or in pre-post intervention neuropsychological tests were found. However, participants who received anodal tDCS showed shorter RT in the 24 hours delay interval and maintained it one week later, while those who received sham tDCS did not show the 24 hours RT shortening and even showed a RT increase one week later. These results could indicate a subtle modulatory effect of anodal tDCS on memory decay along delay intervals.
The experimental protocol showed its potential utility to be used in samples of healthy elderly or mild cognitive impairment participants
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Andrews, S. C., Hoy, K. E., Enticott, P. G., Daskalakis, Z. J., & Fitzgerald, P. B. (2011). Improving working memory: the effect of combining cognitive activity and anodal transcranial direct current stimulation to the left dorsolateral prefrontal cortex. Brain Stimulation, 4(2), 84-89. doi:10.1016/j.brs.2010.06.004
Balzarotti, S., & Colombo, B. (2016). Effects of Unilateral Transcranial Direct Current Stimulation of Left Prefrontal Cortex on Processing and Memory of Emotional Visual Stimuli. PLoS ONE, 11(7), e0159555. doi:10.1371/journal.pone.0159555
Bartrés-Faz, D., & Vidal-Piñeiro, D. (2016). Noninvasive Brain Stimulation for the Study of Memory Enhancement in Aging. European Psychologist 21(1), 41-54. doi:10.1027/1016-9040/a000241
Berryhill, M. E., & Jones, K. T. (2012). tDCS selectively improves working memory in older adults with more education. Neuroscience Letters, 521(2), 148-151. doi:10.1016/j.neulet.2012.05.074
Berryhill, M. E., Peterson, D. J., Jones, K. T., & Stephens, J. A. (2014). Hits and misses: leveraging tDCS to advance cognitive research. Frontiers in Psychology, 5, 800. doi:10.3389/fpsyg.2014.00800
Breedlove, S. M., Watson, N. V., & Rosenzweig, M. R. (2010). Biological psychology: An introduction to behavioral, cognitive, and clinical neuroscience. Sunderland, MA, US: Sinauer Associates.
Boggio, P. S., Fregni, F., Valasek, C., Ellwood, S., Chi, R., Gallate, J., . . . Snyder, A. (2009). Temporal Lobe Cortical Electrical Stimulation during the Encoding and Retrieval Phase Reduces False Memories. PLoS ONE, 4(3), e4959. doi:10.1371/journal.pone.0004959
Bortoletto, M., Veniero, D., Thut, G., & Miniussi, C. (2015). The contribution of TMS-EEG coregistration in the exploration of the human cortical connectome. Neuroscience & Biobehavioral Reviews, 49, 114-124. doi:10.1016/j.neubiorev.2014.12.014
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. doi:10.1016/j.bandc.2014.01.008
Cespón, J., Rodella, C., Rossini, P. M., Miniussi, C., & Pellicciari, M. C. (2017). Anodal Transcranial Direct Current Stimulation Promotes Frontal Compensatory Mechanisms in Healthy Elderly Subjects. Frontiers in Aging Neuroscience, 9(420). doi:10.3389/fnagi.2017.00420
De Lara, G. A., Knechtges, P. N., Paulus, W., & Antal, A. (2017). Anodal tDCS Over the Left DLPFC Did Not Affect the Encoding and Retrieval of Verbal Declarative Information. . Frontiers in Neuroscience, 11(452). doi:10.3389/fnins.2017.00452
Elmer, S., Burkard, M., Renz, B., Meyer, M., & Jancke, L. (2009). Direct current induced short-term modulation of the left dorsolateral prefrontal cortex while learning auditory presented nouns. Behavioral and Brain Functions, 5, 29. doi:10.1186/1744-9081-5-29
Fertonani, A., & Miniussi, C. (2017). Transcranial Electrical Stimulation: What We Know and Do Not Know About Mechanisms. Neuroscientist, 23(2), 109-123. doi:10.1177/1073858416631966
Floel, A., Rosser, N., Michka, O., Knecht, S., & Breitenstein, C. (2008). Noninvasive brain stimulation improves language learning. Journal of Cognitive Neuroscience, 20(8), 1415-1422. doi:10.1162/jocn.2008.20098
Fregni, F., Boggio, P. S., Mansur, C. G., Wagner, T., Ferreira, M. J., Lima, M. C., . . . Pascual-Leone, A. (2005). Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport, 16(14), 1551-1555.
Galli, G., Vadillo, M. A., Sirota, M., Feurra, M., & Medvedeva, A. (2019). A systematic review and meta-analysis of the effects of transcranial direct current stimulation (tDCS) on episodic memory. Brain Stimulation, 12(2), 231-241. doi:10.1016/j.brs.2018.11.008
Gaynor, A. M., & Chua, E. F. (2017). tDCS over the prefrontal cortex alters objective but not subjective encoding. Cognitive Neuroscience, 8(3), 156-161. doi:10.1080/17588928.2016.1213713
Gazzaniga, M. S., Ivry, R. B., & Mangun, G. R. (2009). Cognitive neuroscience : the biology of the mind. New York: W.W. Norton.
Gray, S. J., Brookshire, G., Casasanto, D., & Gallo, D. A. (2015). Electrically stimulating prefrontal cortex at retrieval improves recollection accuracy. Cortex, 73, 188-194. doi:https://doi.org/10.1016/j.cortex.2015.09.003
Habib, R., Nyberg, L., & Tulving, E. (2003). Hemispheric asymmetries of memory: the HERA model revisited. Trends in Cognitive Sciences, 7(6), 241-245.
Habich, A., Klöppel, S., Abdulkadir, A., Scheller, E., Nissen, C., & Peter, J. (2017). Anodal tDCS Enhances Verbal Episodic Memory in Initially Low Performers. Frontiers in Human Neuroscience, 11, 542-542. doi:10.3389/fnhum.2017.00542
Hammer, A., Mohammadi, B., Schmicker, M., Saliger, S., & Münte, T. F. (2011). Errorless and errorful learning modulated by transcranial direct current stimulation. Bmc Neuroscience, 12, 72-72. doi:10.1186/1471-2202-12-72
Hoy, K. E., Emonson, M. R., 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. doi:10.1016/j.neuropsychologia.2013.05.018
Jacobson, L., Goren, N., Lavidor, M., & Levy, D. A. (2012). Oppositional transcranial direct current stimulation (tDCS) of parietal substrates of attention during encoding modulates episodic memory. Brain Research, 1439, 66-72. doi:10.1016/j.brainres.2011.12.036
Javadi, A. H., & Cheng, P. (2013). Transcranial direct current stimulation (tDCS) enhances reconsolidation of long-term memory. Brain Stimulation, 6(4), 668-674. doi:10.1016/j.brs.2012.10.007
Javadi, A. H., Cheng, P., & Walsh, V. (2012). Short duration transcranial direct current stimulation (tDCS) modulates verbal memory. Brain Stimulation, 5(4), 468-474. doi:10.1016/j.brs.2011.08.003
Javadi, A. H., & Walsh, V. (2012). Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation, 5(3), 231-241. doi:10.1016/j.brs.2011.06.007
Lafontaine, M. P., Théoret, H., Gosselin, F., & Lippé, S. (2013). Transcranial Direct Current Stimulation of the Dorsolateral Prefrontal Cortex Modulates Repetition Suppression to Unfamiliar Faces: An ERP Study. PLoS ONE, 8(12), e81721. doi:10.1371/journal.pone.0081721
Leach, R. C., McCurdy, M. P., Trumbo, M. C., Matzen, L. E., & Leshikar, E. D. (2018). Differential Age Effects of Transcranial Direct Current Stimulation on Associative Memory. The Journals of Gerontology: Series B , gby003. doi:10.1093/geronb/gby003
Leshikar, E. D., Leach, R. C., McCurdy, M. P., Trumbo, M. C., Sklenar, A. M., Frankenstein, A. N., & Matzen, L. E. (2017). Transcranial direct current stimulation of dorsolateral prefrontal cortex during encoding improves recall but not recognition memory. Neuropsychologia, 106, 390-397. doi:10.1016/j.neuropsychologia.2017.10.022
Liebetanz, D., Nitsche, M. A., Tergau, F., & Paulus, W. (2002). Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain, 125(Pt 10), 2238-2247.
Lu, Y., Wang, C., Chen, C., & Xue, G. (2015). Spatiotemporal Neural Pattern Similarity Supports Episodic Memory. Current Biology, 25(6), 780-785. doi:https://doi.org/10.1016/j.cub.2015.01.055
Manenti, R., Brambilla, M., Petesi, M., Ferrari, C., & Cotelli, M. (2013). Enhancing verbal episodic memory in older and young subjects after non-invasive brain stimulation. Frontiers in Aging Neuroscience 5(49). doi:10.3389/fnagi.2013.00049
Manuel, A. L., & Schnider, A. (2016). Effect of prefrontal and parietal tDCS on learning and recognition of verbal and non-verbal material. Clinical Neurophysiology, 127(7), 2592-2598. doi:10.1016/j.clinph.2016.04.015
Marian, M., Szollosi, A., & Racsmany, M. (2018). Anodal transcranial direct current stimulation of the right dorsolateral prefrontal cortex impairs long-term retention of reencountered memories. Cortex, 108, 80-91. doi:10.1016/j.cortex.2018.07.012
Marshall, L., Molle, M., Hallschmid, M., & Born, J. (2004). Transcranial direct current stimulation during sleep improves declarative memory. Journal of Neuroscience, 24(44), 9985-9992. doi:10.1523/jneurosci.2725-04.2004
Miniussi, C., Harris, J. A., & Ruzzoli, M. (2013). Modelling non-invasive brain stimulation in cognitive neuroscience. Neuroscience & Biobehavioral Reviews, 37(8), 1702-1712. doi:10.1016/j.neubiorev.2013.06.014
Morgan, H. M., Davis, N. J., & Bracewell, R. M. (2014). Does Transcranial Direct Current Stimulation to Prefrontal Cortex Affect Mood and Emotional Memory Retrieval in Healthy Individuals? PLoS ONE, 9(3), e92162. doi:10.1371/journal.pone.0092162
Mulquiney, P. G., Hoy, K. E., Daskalakis, Z. J., & Fitzgerald, P. B. (2011). Improving working memory: exploring the effect of transcranial random noise stimulation and transcranial direct current stimulation on the dorsolateral prefrontal cortex. Clinical Neurophysiology, 122(12), 2384-2389. doi:10.1016/j.clinph.2011.05.009
Nikolin, S., Loo, C. K., Bai, S., Dokos, S., & Martin, D. M. (2015). Focalised stimulation using high definition transcranial direct current stimulation (HD-tDCS) to investigate declarative verbal learning and memory functioning. NeuroImage, 117, 11-19. doi:10.1016/j.neuroimage.2015.05.019
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(Pt 1), 293-301. doi:10.1113/jphysiol.2003.049916
Nitsche, M. A., Jaussi, W., Liebetanz, D., Lang, N., Tergau, F., & Paulus, W. (2004). Consolidation of human motor cortical neuroplasticity by D-cycloserine. Neuropsychopharmacology, 29(8), 1573-1578. doi:10.1038/sj.npp.1300517
Nitsche, M. A., & Paulus, W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. The Journal of Physiology, 527 Pt 3(Pt 3), 633-639. doi:10.1111/j.1469-7793.2000.t01-1-00633.x
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97-113. doi:https://doi.org/10.1016/0028-3932(71)90067-4
Passow, S., Thurm, F., & Li, S. C. (2017). Activating Developmental Reserve Capacity Via Cognitive Training or Non-invasive Brain Stimulation: Potentials for Promoting Fronto-Parietal and Hippocampal-Striatal Network Functions in Old Age. Frontiers in Aging Neuroscience, 9, 33. doi:10.3389/fnagi.2017.00033
Paulus, W. (2011). Transcranial electrical stimulation (tES - tDCS; tRNS, tACS) methods. Neuropsychological Rehabilitation, 21(5), 602-617. doi:10.1080/09602011.2011.557292
Purpura, D. P., & McMurtry, J. G. (1965). Intracellular activities and evoked potential changes during polarization of motor cortex. Journal of Neurophysiology, 28, 166-185. doi:10.1152/jn.1965.28.1.166
Reynolds, J. R., McDermott, K. B., & Braver, T. S. (2006). A direct comparison of anterior prefrontal cortex involvement in episodic retrieval and integration. Cerebral Cortex, 16(4), 519-528. doi:10.1093/cercor/bhi131
Rugg, M. D., & Wilding, E. L. (2000). Retrieval processing and episodic memory. Trends in Cognitive Sciences, 4(3), 108-115.
Sandrini, M., Manenti, R., Brambilla, M., Cobelli, C., Cohen, L. G., & Cotelli, M. (2016). Older adults get episodic memory boosting from noninvasive stimulation of prefrontal cortex during learning. Neurobiology of Aging, 39, 210-216. doi:10.1016/j.neurobiolaging.2015.12.010
Smirni, D., Turriziani, P., Mangano, G. R., Cipolotti, L., & Oliveri, M. (2015). Modulating Memory Performance in Healthy Subjects with Transcranial Direct Current Stimulation Over the Right Dorsolateral Prefrontal Cortex. PLoS ONE, 10(12), e0144838. doi:10.1371/journal.pone.0144838
Smith, E. E., & Kosslyn, S. M. (2008). Procesos cognitivos : modelos y bases neurales (Vol. xvi): Harlow : Pearson. Prentice Hall.
Tromp, D., Dufour, A., Lithfous, S., Pebayle, T., & Despres, O. (2015). Episodic memory in normal aging and Alzheimer disease: Insights from imaging and behavioral studies. Ageing Research Reviews, 24(Pt B), 232-262. doi:10.1016/j.arr.2015.08.006
Tulving, E. (1972). Episodic and semantic memory. In Tulving, E., & Donaldson, W. (Eds.) (1972). Organization of Memory. New York: Academic Press.
Tulving, E. (1983). Elements of episodic memory. New York: Oxford University Press.
Utz, K. S., Dimova, V., Oppenlander, K., & Kerkhoff, G. (2010). Electrified minds: transcranial direct current stimulation (tDCS) and galvanic vestibular stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology--a review of current data and future implications. Neuropsychologia, 48(10), 2789-2810. doi:10.1016/j.neuropsychologia.2010.06.002
Zwissler, B., Sperber, C., Aigeldinger, S., Schindler, S., Kissler, J., & Plewnia, C. (2014). Shaping memory accuracy by left prefrontal transcranial direct current stimulation. Journal of Neuroscience, 34(11), 4022-4026. doi:10.1523/jneurosci.5407-13.2014
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