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Review Article

Systematic Review and Network Meta-Analysis of Anodal tDCS Effects on Verbal Episodic Memory

Modeling Heterogeneity of Stimulation Locations

Published Online:https://doi.org/10.1027/2151-2604/a000396

Abstract. There is growing interest in the study of transcranial direct current stimulation (tDCS), a non-invasive brain stimulation technique, as an effective intervention to improve memory. In order to evaluate the relative efficacy of tDCS based on the location of anodal electrode sites, we conducted a systematic review examining the effect of stimulation applied during encoding on subsequent verbal episodic memory in healthy adults. We performed a network meta-analysis of 20 studies (23 experiments) with N = 978 participants. Left ventrolateral prefrontal and temporo-parietal sites appeared most likely to enhance episodic memory, although any significant effects were based on findings from single studies only. We did not find evidence for verbal retrieval enhancement of tDCS versus sham stimulation where the effect was based on more than one experimental paper. More frequent replication efforts and stricter reporting standards may improve the quality of evidence and allow more precise estimation of population-level effects of tDCS.

References

  • Bikson, M., Grossman, P., Thomas, C., Zannou, A. L., Jiang, J., Adnan, T., & Brunoni, A. R. (2016). Safety of transcranial direct current stimulation: Evidence based update 2016. Brain Stimulation, 9, 641–661. https://doi.org/10.1016/j.brs.2016.06.004 First citation in articleCrossrefGoogle Scholar

  • 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, e4959. https://doi.org/10.1371/journal.pone.0004959 First citation in articleCrossrefGoogle Scholar

  • Brunyé, T. T., Smith, A. M., Horner, C. B., & Thomas, A. K. (2018). Verbal long-term memory is enhanced by retrieval practice but impaired by prefrontal direct current stimulation. Brain and Cognition, 128, 80–88. https://doi.org/10.1016/j.bandc.2018.09.008 First citation in articleCrossrefGoogle Scholar

  • Cipriani, A., Furukawa, T. A., Salanti, G., Chaimani, A., Atkinson, L. Z., Ogawa, Y., … Egger, M. (2018). Comparative efficacy and acceptability of 21 antidepressant drugs for the acute treatment of adults with major depressive disorder: A systematic review and network meta-analysis. Lancet, 391, 1357–1366. https://doi.org/10.1016/S0140-6736(17)32802-7 First citation in articleCrossrefGoogle Scholar

  • Chaimani, A., & Salanti, G. (2012). Using network meta-analysis to evaluate the existence of small-study effects in a network of interventions. Research Synthesis Methods, 3, 161–176. https://doi.org/10.1002/jrsm.57 First citation in articleCrossrefGoogle Scholar

  • Datta, A., Bansal, V., Diaz, J., Patel, J., Reato, D., & Bikson, M. (2009). Gyri-precise head model of transcranial direct current stimulation: Improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimulation, 2, 201–207. https://doi.org/10.1016/j.brs.2009.03.005 First citation in articleCrossrefGoogle Scholar

  • Dayan, E., Censor, N., Buch, E. R., Sandrini, M., & Cohen, L. G. (2013). Non-invasive brain stimulation: From physiological mechanisms to network dynamics and back. Nature Neuroscience, 16, 838–844. https://doi.org/10.1038/nn.3422 First citation in articleCrossrefGoogle Scholar

  • Dedoncker, J., Brunoni, A. R., Baeken, C., & Vanderhasselt, M. A. (2016). A systematic review and meta-analysis of the effects of transcranial direct current stimulation (tDCS) over the dorsolateral prefrontal cortex in healthy and neuropsychiatric samples: Influence of stimulation parameters. Brain Stimulation, 9, 501–517. https://doi.org/10.1016/j.brs.2016.04.006 First citation in articleCrossrefGoogle Scholar

  • Dias, S., Welton, N. J., Caldwell, D. M., & Ades, A. E. (2010). Checking consistency in mixed treatment comparison meta‐analysis. Statistics in Medicine, 29, 932–944. https://doi.org/10.1002/sim.3767 First citation in articleCrossrefGoogle Scholar

  • Diez, E., Gomez-Ariza, C. J., Diez-Alamo, A. M., Alonso, M. A., & Fernandez, A. (2017). The processing of semantic relatedness in the brain: Evidence from associative and categorical false recognition effects following transcranial direct current stimulation of the left anterior temporal lobe. Cortex, 93, 133–145. https://doi.org/10.1016/j.cortex.2017.05.004 First citation in articleCrossrefGoogle Scholar

  • Dickerson, B. C., & Eichenbaum, H. (2010). The episodic memory system: Neurocircuitry and disorders. Neuropsychopharmacology, 35, 86–104. https://doi.org/10.1038/npp.2009.126 First citation in articleCrossrefGoogle Scholar

  • Elsner, B., Kwakkel, G., Kugler, J., & Mehrholz, J. (2017). Transcranial direct current stimulation (tDCS) for improving capacity in activities and arm function after stroke: A network meta-analysis of randomised controlled trials. Journal of Neuroengineering and Rehabilitation, 14, 95. https://doi.org/10.1186/s12984-017-0301-7 First citation in articleCrossrefGoogle Scholar

  • Galli, G., Vadillo, M. A., Sirota, M., Feurra, M., & Medvedeva, A. (2018). A systematic review and meta-analysis of the effects of transcranial direct current stimulation (tDCS) on episodic memory. Brain Stimulation, 12, 231–241. https://doi.org/10.1016/j.brs.2018.11.008 First citation in articleCrossrefGoogle Scholar

  • Gaynor, A. M., & Chua, E. F. (2017). tDCS over the prefrontal cortex alters objective but not subjective encoding. Cognitive Neuroscience, 8, 156–161. https://doi.org/10.1080/17588928.2016.1213713 First citation in articleCrossrefGoogle Scholar

  • 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. https://doi.org/10.3389/fnhum.2017.00542 First citation in articleCrossrefGoogle Scholar

  • Higgins, J. P., Altman, D. G., Gøtzsche, P. C., Jüni, P., Moher, D., Oxman, A. D., … Sterne, J. A. (2011). The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. British Medical Journal, 343, d5928. https://doi.org/10.1136/bmj.d5928 First citation in articleCrossrefGoogle Scholar

  • Higgins, J. P., & Welton, N. J. (2015). Network meta-analysis: A norm for comparative effectiveness? The Lancet, 386, 628–630. https://doi.org/10.1016/S0140-6736(15)61478-7 First citation in articleCrossrefGoogle Scholar

  • 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, 535–550. https://doi.org/10.1016/j.brs.2015.01.400 First citation in articleCrossrefGoogle Scholar

  • Hutton, B., Salanti, G., Caldwell, D. M., Chaimani, A., Schmid, C. H., Cameron, C., … Mulrow, C. (2015). The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: Checklist and explanations. Annals of Internal Medicine, 162, 777–784. https://doi.org/10.7326/M14-2385 First citation in articleCrossrefGoogle Scholar

  • Hsu, W. Y., Ku, Y., Zanto, T. P., & Gazzaley, A. (2015). Effects of noninvasive brain stimulation on cognitive function in healthy aging and Alzheimer’s disease: A systematic review and meta-analysis. Neurobiology of Aging, 36, 2348–2359. https://doi.org/10.1016/j.neurobiolaging.2015.04.016 First citation in articleCrossrefGoogle Scholar

  • 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. https://doi.org/10.1016/j.brainres.2011.12.036 First citation in articleCrossrefGoogle Scholar

  • Javadi, A. H., & Walsh, V. (2012). Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory. Brain Stimulation, 5, 231–241. https://doi.org/10.1016/j.brs.2011.06.007 First citation in articleCrossrefGoogle Scholar

  • Jog, M. V., Smith, R. X., Jann, K., Dunn, W., Lafon, B., Truong, D., & Wang, D. J. (2016). In-vivo imaging of magnetic fields induced by transcranial direct current stimulation (tDCS) in human brain using MRI. Scientific Reports, 6, 34385. https://doi.org/10.1038/srep34385 First citation in articleCrossrefGoogle Scholar

  • Jones, K. T., Gözenman, F., & Berryhill, M. E. (2014). Enhanced long-term memory encoding after parietal neurostimulation. Experimental Brain Research, 232, 4043–4054. https://doi.org/10.1007/s00221-014-4090-y First citation in articleCrossrefGoogle Scholar

  • Klem, G. H., Lüders, H. O., Jasper, H. H., & Elger, C. (1999). The ten-twenty electrode system of the International Federation. Electroencephalography and Clinical Neurophysiology, 52, 3–6. First citation in articleGoogle Scholar

  • Lara, G. A. D., 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. https://doi.org/10.3389/fnins.2017.00452 First citation in articleCrossrefGoogle Scholar

  • Leach, R. C., McCurdy, M. P., Trumbo, M. C., Matzen, L. E., & Leshikar, E. D. (2016). Transcranial stimulation over the left inferior frontal gyrus increases false alarms in an associative memory task in older adults. Healthy Aging Research, 5, 1–6. https://doi.org/10.1097/01.HXR.0000511878.91386.f8 First citation in articleCrossrefGoogle Scholar

  • 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, 74(7), 1163–1173. https://doi.org/10.1093/geronb/gby003 First citation in articleCrossrefGoogle Scholar

  • 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. https://doi.org/10.1016/j.neuropsychologia.2017.10.022 First citation in articleCrossrefGoogle Scholar

  • Lu, G., & Ades, A. E. (2006). Assessing evidence inconsistency in mixed treatment comparisons. Journal of the American Statistical Association, 101, 447–459. https://doi.org/10.1198/016214505000001302 First citation in articleCrossrefGoogle Scholar

  • Lumley, T. (2002). Network meta‐analysis for indirect treatment comparisons. Statistics in Medicine, 21, 2313–2324. https://doi.org/10.1002/sim.1201 First citation in articleCrossrefGoogle Scholar

  • Manenti, R., Cotelli, M., Robertson, I. H., & Miniussi, C. (2012). Transcranial brain stimulation studies of episodic memory in young adults, elderly adults and individuals with memory dysfunction: A review. Brain Stimulation, 5, 103–109. https://doi.org/10.1016/j.brs.2012.03.004 First citation in articleCrossrefGoogle Scholar

  • 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, 2592–2598. https://doi.org/10.1016/j.clinph.2016.04.015 First citation in articleCrossrefGoogle Scholar

  • Martin, D. M., Liu, R., Alonzo, A., Green, M., & Loo, C. K. (2014). Use of transcranial direct current stimulation (tDCS) to enhance cognitive training: Effect of timing of stimulation. Experimental Brain Research, 232, 3345–3351. https://doi.org/10.1007/s00221-014-4022-x First citation in articleCrossrefGoogle Scholar

  • Matzen, L. E., Trumbo, M. C., Leach, R. C., & Leshikar, E. D. (2015). Effects of non-invasive brain stimulation on associative memory. Brain Research, 1624, 286–296. https://doi.org/10.1016/j.brainres.2015.07.036 First citation in articleCrossrefGoogle Scholar

  • Medvedeva, A., Materassi, M., Neacsu, V., Beresford-Webb, J., Hussin, A., Khan, N., … Galli, G. (2018). Effects of anodal transcranial direct current stimulation over the ventrolateral prefrontal cortex on episodic memory formation and retrieval. Cerebral Cortex, 29, 657–665. https://doi.org/10.1093/cercor/bhx347 First citation in articleCrossrefGoogle Scholar

  • Meier, B., & Sauter, P. (2018). Boosting memory by tDCS to frontal or parietal brain regions? A study of the enactment effect shows no effects for immediate and delayed recognition. Frontiers in Psychology, 9, 867. https://doi.org/10.3389/fpsyg.2018.00867 First citation in articleCrossrefGoogle Scholar

  • Munafò, M. R., Nosek, B. A., Bishop, D. V., Button, K. S., Chambers, C. D., Du Sert, N. P., … Ioannidis, J. P. (2017). A manifesto for reproducible science. Nature Human Behaviour, 1, 21. https://doi.org/10.1038/s41562-016-0021 First citation in articleCrossrefGoogle Scholar

  • 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, 633–639. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00633.x First citation in articleCrossrefGoogle Scholar

  • 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. https://doi.org/10.1016/j.neuroimage.2015.05.019 First citation in articleCrossrefGoogle Scholar

  • Perceval, G., Martin, A. K., Copland, D. A., Laine, M., & Meinzer, M. (2017). High-definition tDCS of the temporo-parietal cortex enhances access to newly learned words. Scientific Reports, 7, 17023. https://doi.org/10.1038/s41598-017-17279-0 First citation in articleCrossrefGoogle Scholar

  • Riley, R. D., Jackson, D., Salanti, G., Burke, D. L., Price, M., Kirkham, J., & White, I. R. (2017). Multivariate and network meta-analysis of multiple outcomes and multiple treatments: rationale, concepts, and examples. British Medical Journal, 358, j3932. https://doi.org/10.1136/bmj.j3932 First citation in articleCrossrefGoogle Scholar

  • Rivera-Urbina, G. N., Mendez Joya, M. F., Nitsche, M. A., & Molero-Chamizo, A. (2019). Anodal tDCS over Wernicke’s area improves verbal memory and prevents the interference effect during words learning. Neuropsychology, 33, 263. https://doi.org/10.1037/neu0000514 First citation in articleCrossrefGoogle Scholar

  • Ronnlund, M., Nyberg, L., Backman, L., & Nilsson, L. G. (2005). Stability, growth, and decline in adult life span development of declarative memory: Cross-sectional and longitudinal data from a population-based study. Psychological Aging, 20, 3–18. https://doi.org/10.1037/0882-7974.20.1.3 First citation in articleCrossrefGoogle Scholar

  • Rücker, G., & Schwarzer, G. (2015). Ranking treatments in frequentist network meta-analysis works without resampling methods. BMC Medical Research Methodology, 15, 58. https://doi.org/10.1186/s12874-015-0060-8 First citation in articleCrossrefGoogle Scholar

  • Rugg, M. D., & King, D. R. (2018). Ventral lateral parietal cortex and episodic memory retrieval. Cortex, 107, 238–250. https://doi.org/10.1016/j.cortex.2017.07.012 First citation in articleCrossrefGoogle Scholar

  • Sandrini, M., & Cohen, L. G. (2013). Noninvasive brain stimulation in neurorehabilitation. Handbook of Clinical Neurology, 116, 499–524. https://doi.org/10.3389/fnhum.2014.00378 First citation in articleCrossrefGoogle Scholar

  • Sandrini, M., & Cohen, L. G. (2014). Effects of brain stimulation on declarative and procedural memories. In R. Cohen KadoshEd., The stimulated brain (pp. 237–263). London, UK: Academic Press. First citation in articleGoogle Scholar

  • 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. https://doi.org/10.1016/j.neurobiolaging.2015.12.010 First citation in articleCrossrefGoogle Scholar

  • Schulz, K. F., Altman, D. G., & Moher, D. (2010). CONSORT 2010 statement: Updated guidelines for reporting parallel group randomised trials. BMC Medicine, 8, 18. https://doi.org/10.1186/1741-7015-8-18 First citation in articleCrossrefGoogle Scholar

  • Schwarzer, G. (2007). meta: An R package for meta-analysis. R News, 7, 40–45. https://doi.org/10.1136/bmj.c332 First citation in articleGoogle Scholar

  • Shin, Y. I., Foerster, A., & Nitsche, M. A. (2015). Transcranial direct current stimulation (tDCS) – application in neuropsychology. Neuropsychologia, 69, 154–175. https://doi.org/10.1016/j.neuropsychologia.2015.02.002 First citation in articleCrossrefGoogle Scholar

  • Spaniol, J., Davidson, P. S., Kim, A. S., Han, H., Moscovitch, M., & Grady, C. L. (2009). Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation. Neuropsychologia, 47, 1765–1779. https://doi.org/10.1016/j.neuropsychologia.2009.02.028 First citation in articleCrossrefGoogle Scholar

  • Summers, J. J., Kang, N., & Cauraugh, J. H. (2016). Does transcranial direct current stimulation enhance cognitive and motor functions in the ageing brain? A systematic review and meta-analysis. Ageing Research Reviews, 25, 42–54. https://doi.org/10.1016/j.arr.2015.11.004 First citation in articleCrossrefGoogle Scholar

  • Szczepanski, S. M., & Knight, R. T. (2014). Insights into human behavior from lesions to the prefrontal cortex. Neuron, 83, 1002–1018. https://doi.org/10.1016/j.neuron.2014.08.011 First citation in articleCrossrefGoogle Scholar

  • Szucs, D., & Ioannidis, J. P. (2017). Empirical assessment of published effect sizes and power in the recent cognitive neuroscience and psychology literature. PLoS Biology, 15, e2000797. https://doi.org/10.1371/journal.pbio.2000797 First citation in articleCrossrefGoogle Scholar

  • Tremblay, S., Lepage, J. F., Latulipe-Loiselle, A., Fregni, F., Pascual-Leone, A., & Théoret, H. (2014). The uncertain outcome of prefrontal tDCS. Brain Stimulation, 7, 773–783. https://doi.org/10.1016/j.brs.2014.10.003 First citation in articleCrossrefGoogle Scholar

  • Tulving, E. (1983). Elements of episodic memory. London, UK: Oxford University Press. First citation in articleGoogle Scholar

  • Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36, 1–48. https://doi.org/10.18637/jss.v036.i03 First citation in articleCrossrefGoogle Scholar

  • Villamar, M. F., Volz, M. S., Bikson, M., Datta, A., DaSilva, A. F., & Fregni, F. (2013). Technique and considerations in the use of 4×1 ring high-definition transcranial direct current stimulation (HD-tDCS). Journal of Visualized Experiments, 77, e50309. https://doi.org/10.3791/50309 First citation in articleGoogle Scholar

  • Vöröslakos, M., Takeuchi, Y., Brinyiczki, K., Zombori, T., Oliva, A., Fernández-Ruiz, A., … Berényi, A. (2018). Direct effects of transcranial electric stimulation on brain circuits in rats and humans. Nature Communications, 9, 483. https://doi.org/10.1038/s41467-018-02928-3 First citation in articleCrossrefGoogle Scholar

  • Woods, A. J., Antal, A., Bikson, M., Boggio, P. S., Brunoni, A. R., Celnik, P., … Knotkova, H. (2016). A technical guide to tDCS, and related non-invasive brain stimulation tools. Clinical Neurophysiology, 127, 1031–1048. https://doi.org/10.1016/j.clinph.2015.11.012 First citation in articleCrossrefGoogle Scholar

  • Zhang, J., Liu, J., Li, J., Zhang, C., & Qu, M. (2018). Non‐invasive brain stimulation for improving cognitive function in people with dementia and mild cognitive impairment. Cochrane Database of Systematic Reviews, (7). https://doi.org/10.1002/14651858.CD013065 First citation in articleGoogle Scholar