Older adults with lower working memory capacity benefit from transcranial direct current stimulation when combined with working memory training: A preliminary study

Sara Assecondi, Rong Hu, Jacob Kroeker, Gail Eskes, Kim Shapiro, Sara Assecondi, Rong Hu, Jacob Kroeker, Gail Eskes, Kim Shapiro

Abstract

Aging is a very diverse process: successful agers retain most cognitive functioning, while others experience mild to severe cognitive decline. This decline may eventually negatively impact one's everyday activities. Therefore, scientists must develop approaches to counteract or, at least, slow down the negative change in cognitive performance of aging individuals. Combining cognitive training and transcranial direct current stimulation (tDCS) is a promising approach that capitalizes on the plasticity of brain networks. However, the efficacy of combined methods depends on individual characteristics, such as the cognitive and emotional state of the individual entering the training program. In this report, we explored the effectiveness of working memory training, combined with tDCS to the right dorsolateral prefrontal cortex (DLPFC), to manipulate working memory performance in older individuals. We hypothesized that individuals with lower working memory capacity would benefit the most from the combined regimen. Thirty older adults took part in a 5-day combined regimen. Before and after the training, we evaluated participants' working memory performance with five working memory tasks. We found that individual characteristics influenced the outcome of combined cognitive training and tDCS regimens, with the intervention selectively benefiting old-old adults with lower working memory capacity. Future work should consider developing individualized treatments by considering individual differences in cognitive profiles.

Keywords: individual differences; non-invasive brain stimulation (NIBS); older adults; plasticity; tDCS—transcranial direct current stimulation; working memory training (WMT).

Conflict of interest statement

A patent application has been submitted by the University of Birmingham and Dalhousie University with SA, KS, and GE named as inventors. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2022 Assecondi, Hu, Kroeker, Eskes and Shapiro.

Figures

FIGURE 1
FIGURE 1
Diagram of the procedure to calculate composite working memory capacity (WMC) scores. Dependent variables measuring working memory performance were extracted from each task, standardized, and averaged, obtaining a composite score for each participant. The obtained distribution of composite scores is shown for each age and stimulation group.
FIGURE 2
FIGURE 2
Flowchart of the procedure. CT, cognitive training.
FIGURE 3
FIGURE 3
Training performance (n¯) for each training day, for the SHAM and ACTIVE groups, within each AGE level. Error bars represent the standard error of the mean.

References

    1. Antal A., Alekseichuk I., Bikson M., Brockmöller J., Brunoni A. R., Chen R., et al. (2017). Low intensity transcranial electric stimulation: Safety, ethical, legal regulatory and application guidelines. Clin. Neurophysiol. 128 1774–1809. 10.1016/j.clinph.2017.06.001
    1. Antonenko D., Grittner U., Saturnino G., Nierhaus T., Thielscher A., Flöel A. (2020). Inter-individual and age-dependent variability in simulated electric fields induced by conventional transcranial electrical stimulation. NeuroImage 224:117413. 10.1016/j.neuroimage.2020.117413
    1. Antonenko D., Külzow N., Sousa A., Prehn K., Grittner U., Flöel A. (2018). Neuronal and behavioral effects of multi-day brain stimulation and memory training. Neurobiol. Aging 61 245–254. 10.1016/j.neurobiolaging.2017.09.017
    1. Assecondi S. (2021). Impact of tDCS on working memory training is enhanced by strategy instructions in individuals with low working memory capacity. Sci. Rep. 11:5531. 10.1038/s41598-021-84298-3
    1. Assecondi S., Hu R., Eskes G., Pan X., Zhou J., Shapiro K. (2021). Impact of tDCS on working memory training is enhanced by strategy instructions in individuals with low working memory capacity. Sci. Rep. 11:5531.
    1. Au J., Karsten C., Buschkuehl M., Jaeggi S. M. (2017). Optimizing transcranial direct current stimulation protocols to promote long-term learning. J. Cogn. Enhanc. 1 65–72. 10.1007/s41465-017-0007-6
    1. Au J., Katz B., Buschkuehl M., Bunarjo K., Senger T., Zabel C., et al. (2016). Enhancing working memory training with transcranial direct current stimulation. J. Cogn. Neurosci. 28 1–14. 10.1162/jocn_a_00979
    1. Au J., Smith-Peirce R. N., Carbone E., Moon A., Evans M., Jonides J., et al. (2022). Effects of multisession prefrontal transcranial direct current stimulation on long-term memory and working memory in older adults. J. Cogn. Neurosci. 34 1015–1037. 10.1162/jocn_a_01839
    1. Barrett L. F., Tugade M. M., Engle R. W. (2004). Individual differences in working memory capacity and dual-process theories of the mind. Psychol. Bull. 130:553. 10.1037/0033-2909.130.4.553
    1. Benwell C. S. Y., Learmonth G., Miniussi C., Harvey M., Thut G. (2015). Non-linear effects of transcranial direct current stimulation as a function of individual baseline performance: Evidence from biparietal tDCS influence on lateralized attention bias. Cortex 69 152–165. 10.1016/j.cortex.2015.05.007
    1. Berryhill M. E. (2017). Longitudinal tDCS: Consistency across working memory training studies. AIMS Neurosci. 4:71. 10.3934/Neuroscience.2017.2.71
    1. Berryhill M. E., Jones K. T. (2012). tDCS selectively improves working memory in older adults with more education. Neurosci. Lett. 521 148–151. 10.1016/j.neulet.2012.05.074
    1. Bikson M., Rahman A. (2013). Origins of specificity during tDCS: Anatomical, activity-selective, and input-bias mechanisms. Front. Hum. Neurosci. 7:688. 10.3389/fnhum.2013.00688
    1. Button K. S., Ioannidis J. P. A., Mokrysz C., Nosek B. A., Flint J., Robinson E. S. J., et al. (2013). Power failure: Why small sample size undermines the reliability of neuroscience. Nat. Rev. Neurosci. 14 365–376. 10.1038/nrn3475
    1. Cespón J., Miniussi C., Pellicciari M. C. (2018). Interventional programmes to improve cognition during healthy and pathological ageing: Cortical modulations and evidence for brain plasticity. Ageing Res. Rev. 43 81–98. 10.1016/j.arr.2018.03.001
    1. Cespón J., Rodella C., Miniussi C., Pellicciari M. C. (2019). Behavioural and electrophysiological modulations induced by transcranial direct current stimulation in healthy elderly and Alzheimer’s disease patients: A pilot study. Clin. Neurophysiol. 130 2038–2052. 10.1016/j.clinph.2019.08.016
    1. 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. Front. Aging Neurosci. 9:420. 10.3389/fnagi.2017.00420
    1. Cohen R. A., Marsiske M. M., Smith G. E. (2019). Neuropsychology of aging. Handb. Clin. Neurol. 167 149–180. 10.1016/b978-0-12-804766-8.00010-8
    1. Dahlin E., Neely A. S., Larsson A., Bäckman L., Nyberg L. (2008). Transfer of learning after updating training mediated by the striatum. Science 320 1510–1512. 10.1126/science.1155466
    1. Engle R. W., Kane M. J. (2003). Executive attention, working memory capacity, and a two-factor theory of cognitive control. Psychol. Learn. Motiv. 44 145–199. 10.1016/S0079-7421(03)44005-X
    1. Esposito M., Ferrari C., Fracassi C., Miniussi C., Brignani D. (2022). Responsiveness to left-prefrontal tDCS varies according to arousal levels. Eur. J. Neurosci. 55 762–777. 10.1111/ejn.15584
    1. Esposito M., Mauri P., Panizza L., Mazza V., Miniussi C., Brignani D. (2021). Baseline levels of alertness influence tES effects along different age-related directions. Neuropsychologia 160:107966. 10.1016/j.neuropsychologia.2021.107966
    1. Farnsworth D. (1943). The Farnsworth-Munsell 100-hue and dichotomous tests for color vision*. J. Opt. Soc. Am. 33 568–578. 10.1364/JOSA.33.000568
    1. Ferreri F., Guerra A., Vollero L., Ponzo D., Maatta S., Mervaala E., et al. (2017). Age-related changes of cortical excitability and connectivity in healthy humans: Non-invasive evaluation of sensorimotor network by means of TMS-EEG. Neuroscience 357 255–263. 10.1016/j.neuroscience.2017.06.014
    1. Filmer H. L., Dux P. E., Mattingley J. B. (2014). Applications of transcranial direct current stimulation for understanding brain function. Trends Neurosci. 37 742–753. 10.1016/j.tins.2014.08.003
    1. Flegal K. E., Ragland J. D., Ranganath C. (2019). Adaptive task difficulty influences neural plasticity and transfer of training. NeuroImage 188 111–121. 10.1016/j.neuroimage.2018.12.003
    1. Foster J. L., Harrison T. L., Hicks K. L., Draheim C., Redick T. S., Engle R. W. (2017). Do the effects of working memory training depend on baseline ability level? J. Exp. Psychol. Learn. Mem. Cogn. 43 1677–1689. 10.1037/xlm0000426
    1. Gözenman F., Berryhill M. E. (2016). Working memory capacity differentially influences responses to tDCS and HD-tDCS in a retro-cue task. Neurosci. Lett. 629 105–109. 10.1016/j.neulet.2016.06.056
    1. Grady C. (2012). The cognitive neuroscience of ageing. Nat. Rev. Neurosci. 13 491–505. 10.1038/nrn3256
    1. Green S. C., Bavelier D., Kramer A. F., Vinogradov S., Ansorge U., Ball K. K., et al. (2019). Improving methodological standards in behavioral interventions for cognitive enhancement. J. Cogn. Enhanc. 3 2–29. 10.1007/s41465-018-0115-y
    1. Harvey P. D., McGurk S. R., Mahncke H., Wykes T. (2018). Controversies in computerized cognitive training. Biol. Psychiatry Cogn. Neurosci. Neuroimaging 3 907–915. 10.1016/j.bpsc.2018.06.008
    1. Hedges L. V. (1981). Distribution theory for Glass’s estimator of effect size and related estimators. J. Educ. Stat. 6 107–128. 10.2307/1164588
    1. Hill R. D., Backman L., Stigsdotter-Neely A. (2000). Cognitive Rehabilitation in Old Age. Oxford: Oxford University Press.
    1. Horne K. S., Filmer H. L., Nott Z. E., Hawi Z., Pugsley K., Mattingley J. B., et al. (2021). Evidence against benefits from cognitive training and transcranial direct current stimulation in healthy older adults. Nat. Hum. Behav. 5 146–158. 10.1038/s41562-020-00979-5
    1. Hsu T.-Y., Tseng P., Liang W.-K., Cheng S.-K., Juan C.-H. (2014). Transcranial direct current stimulation over right posterior parietal cortex changes prestimulus alpha oscillation in visual short-term memory task. NeuroImage 98 306–313. 10.1016/j.neuroimage.2014.04.069
    1. Hurley R., Machado L. (2018). Using transcranial direct current stimulation to improve verbal working memory: A detailed review of the methodology. J. Clin. Exp. Neuropsychol. 40 790–804. 10.1080/13803395.2018.1434133
    1. JASP Team (2020). JASP (Version 0.14.1)[Computer software]. New York, NY: JASP team.
    1. Johns M. W. (1991). A new method for measuring daytime sleepiness: The epworth sleepiness scale. Sleep 14 540–545. 10.1093/sleep/14.6.540
    1. Jones K. T., Gözenman F., Berryhill M. E. (2015a). The strategy and motivational influences on the beneficial effect of neurostimulation: A tDCS and fNIRS study. NeuroImage 105 238–247. 10.1016/j.neuroimage.2014.11.012
    1. Jones K. T., Stephens J. A., Alam M., Bikson M., Berryhill M. E. (2015b). Longitudinal neurostimulation in older adults improves working memory. PLoS One 10:e0121904. 10.1371/journal.pone.0121904
    1. Jones S., Nyberg L., Sandblom J., Stigsdotter Neely A., Ingvar M., Magnus Petersson K., et al. (2006). Cognitive and neural plasticity in aging: General and task-specific limitations. Neurosci. Biobehav. Rev. 30 864–871. 10.1016/j.neubiorev.2006.06.012
    1. Katz B., Au J., Buschkuehl M., Abagis T., Zabel C., Jaeggi S. M., et al. (2017). Individual differences and long-term consequences of tDCS-augmented cognitive training. J. Cogn. Neurosci. 29 1498–1508. 10.1162/jocn_a_01115
    1. Kim G.-W., Ko M.-H. (2013). Facilitation of corticospinal tract excitability by transcranial direct current stimulation combined with voluntary grip exercise. Neurosci. Lett. 548 181–184. 10.1016/j.neulet.2013.05.037
    1. Kirchner W. K. (1958). Age differences in short-term retention of rapidly changing information. J. Exp. Psychol. 55 352–358. 10.1037/h0043688
    1. Krause B., Cohen Kadosh R. (2014). Not all brains are created equal: The relevance of individual differences in responsiveness to transcranial electrical stimulation. Front. Syst. Neurosci. 8:25. 10.3389/fnsys.2014.00025
    1. Krause B., Márquez-Ruiz J., Cohen Kadosh R. (2013). The effect of transcranial direct current stimulation: A role for cortical excitation/inhibition balance? Front. Hum. Neurosci. 7:602. 10.3389/fnhum.2013.00602
    1. Krebs C., Peter J., Wyss P., Brem A.-K., Klöppel S. (2021). Transcranial electrical stimulation improves cognitive training effects in healthy elderly adults with low cognitive performance. Clin. Neurophysiol. 132 1254–1263. 10.1016/j.clinph.2021.01.034
    1. Kronberg G., Rahman A., Sharma M., Bikson M., Parra L. C. (2020). Direct current stimulation boosts hebbian plasticity in vitro. Brain Stimul. 13 287–301. 10.1016/j.brs.2019.10.014
    1. Lapenta O. M., Minati L., Fregni F., Boggio P. S. (2013). Je pense donc je fais: Transcranial direct current stimulation modulates brain oscillations associated with motor imagery and movement observation. Front. Hum. Neurosci. 7:256. 10.3389/fnhum.2013.00256
    1. Matysiak O., Kroemeke A., Brzezicka A. (2019). Working memory capacity as a predictor of cognitive training efficacy in the elderly population. Front. Aging Neurosci. 11:126. 10.3389/fnagi.2019.00126
    1. Mohammed S., Flores L., Deveau J., Hoffing R. C., Phung C., Parlett C. M., et al. (2017). The benefits and challenges of implementing motivational features to boost cognitive training outcome. J. Cogn. Enhanc. Integr. Theory Pract. 1 491–507. 10.1007/s41465-017-0047-y
    1. Morais R. M., Pera M. V., Ladera V., Oliveira J., García R. (2018). Individual differences in working memory abilities in healthy adults. J. Adult Dev. 25 222–228. 10.1007/s10804-018-9287-z
    1. Nasreddine Z., Phillips N., Bédirian V., Charbonneau S., Whitehead V., Collin I., et al. (2005). The montreal cognitive assessment, MoCA: A brief screening tool for mild cognitive impairment. J. Am. Geriatr. Soc. 53 695–699. 10.1111/j.1532-5415.2005.53221.x
    1. Nguyen L., Murphy K., Andrews G. (2019). Cognitive and neural plasticity in old age: A systematic review of evidence from executive functions cognitive training. Ageing Res. Rev. 53:100912. 10.1016/j.arr.2019.100912
    1. Nissim N. R., O’Shea A., Indahlastari A., Kraft J. N., von Mering O., Aksu S., et al. (2019). Effects of transcranial direct current stimulation paired with cognitive training on functional connectivity of the working memory network in older adults. Front. Aging Neurosci. 11:340. 10.3389/fnagi.2019.00340
    1. Nitsche M. A., Cohen L. G., Wassermann E. M., Priori A., Lang N., Antal A., et al. (2008). Transcranial direct current stimulation: State of the art 2008. Brain Stimul. 1 206–223. 10.1016/j.brs.2008.06.004
    1. Oliviero A., Profice P., Tonali P. A., Pilato F., Saturno E., Dileone M., et al. (2006). Effects of aging on motor cortex excitability. Neurosci. Res. 55 74–77. 10.1016/j.neures.2006.02.002
    1. Opitz A., Paulus W., Will S., Antunes A., Thielscher A. (2015). Determinants of the electric field during transcranial direct current stimulation. NeuroImage 109 140–150. 10.1016/j.neuroimage.2015.01.033
    1. Park S.-H., Seo J.-H., Kim Y.-H., Ko M.-H. (2014). Long-term effects of transcranial direct current stimulation combined with computer-assisted cognitive training in healthy older adults. Neuroreport 25:122. 10.1097/WNR.0000000000000080
    1. Pauwels L., Chalavi S., Swinnen S. P. (2018b). Aging and brain plasticity. Aging 10 1789–1790. 10.18632/aging.101514
    1. Pauwels L., Chalavi S., Gooijers J., Maes C., Albouy G., Sunaert S., et al. (2018a). Challenge to promote change: The neural basis of the contextual interference effect in young and older adults. J. Neurosci. 38 3333–3345. 10.1523/JNEUROSCI.2640-17.2018
    1. Pearson-Fuhrhop K. M., Kleim J. A., Cramer S. C. (2009). Brain plasticity and genetic factors. Top. Stroke Rehabil. 16 282–299. 10.1310/tsr1604-282
    1. Perceval G., Flöel A., Meinzer M. (2016). Can transcranial direct current stimulation counteract age-associated functional impairment? Neurosci. Biobehav. Rev. 65 157–172. 10.1016/j.neubiorev.2016.03.028
    1. Pirulli C., Fertonani A., Miniussi C. (2013). The role of timing in the induction of neuromodulation in perceptual learning by transcranial electric stimulation. Brain Stimul. 6 683–689. 10.1016/j.brs.2012.12.005
    1. Pitcher J. B., Ogston K. M., Miles T. S. (2003). Age and sex differences in human motor cortex input–output characteristics. J. Physiol. 546 605–613. 10.1113/jphysiol.2002.029454
    1. Ploughman M., Eskes G. A., Kelly L. P., Kirkland M. C., Devasahayam A. J., Wallack E. M., et al. (2019). Synergistic benefits of combined aerobic and cognitive training on fluid intelligence and the role of IGF-1 in chronic stroke. Neurorehabil. Neural Repair 33 199–212. 10.1177/1545968319832605
    1. R Core Team. (2020). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
    1. Reato D., Bikson M., Parra L. C. (2015). Lasting modulation of in vitro oscillatory activity with weak direct current stimulation. J. Neurophysiol. 113 1334–1341. 10.1152/jn.00208.2014
    1. Reato D., Rahman A., Bikson M., Parra L. C. (2010). Low-intensity electrical stimulation affects network dynamics by modulating population rate and spike timing. J. Neurosci. 30 15067–15079. 10.1523/JNEUROSCI.2059-10.2010
    1. Rossini P. M., Desiato M. T., Caramia M. D. (1992). Age-related changes of motor evoked potentials in healthy humans: Non-invasive evaluation of central and peripheral motor tracts excitability and conductivity. Brain Res. 593 14–19. 10.1016/0006-8993(92)91256-E
    1. Ruf S., Fallgatter A. J., Plewnia C. (2017). Augmentation of working memory training by transcranial direct current stimulation (tDCS). Sci. Rep. 7:876. 10.1038/s41598-017-01055-1
    1. Shipstead Z., Redick T. S., Engle R. W. (2012). Is working memory training effective? Psychol. Bull. 138:628. 10.1037/a0027473
    1. Soveri A., Antfolk J., Karlsson L., Salo B., Laine M. (2017a). Working memory training revisited: A multi-level meta-analysis of n-back training studies. Psychon. Bull. Rev. 24 1077–1096. 10.3758/s13423-016-1217-0
    1. Soveri A., Karlsson E. P. A., Waris O., Grönholm-Nyman P., Laine M. (2017b). Pattern of near transfer effects following working memory training with a dual n-back task. Exp. Psychol. 64 240–252. 10.1027/1618-3169/a000370
    1. Stagg C. J., Nitsche M. A. (2011). Physiological Basis of Transcranial Direct Current Stimulation. Neuroscientist 17 37–53. 10.1177/1073858410386614
    1. Tseng P., Hsu T.-Y., Chang C.-F., Tzeng O. J. L., Hung D. L., Muggleton N. G., et al. (2012). Unleashing potential: Transcranial direct current stimulation over the right posterior parietal cortex improves change detection in low-performing individuals. J. Neurosci. 32 10554–10561. 10.1523/JNEUROSCI.0362-12.2012
    1. Verhaeghen P., Basak C. (2005). Ageing and switching of the focus of attention in working memory: Results from a modified n-back task. Q. J. Exp. Psychol. Sec. A 58, 134–154. 10.1080/02724980443000241
    1. von Bastian C. C., Oberauer K. (2014). Effects and mechanisms of working memory training: A review. Psychol. Res. 78 803–820. 10.1007/s00426-013-0524-6
    1. Wang S., Itthipuripat S., Ku Y. (2019). Electrical Stimulation Over Human Posterior Parietal Cortex Selectively Enhances the Capacity of Visual Short-Term Memory. J. Neurosci. 39 528–536. 10.1523/JNEUROSCI.1959-18.2018
    1. Waris O., Soveri A., Laine M. (2015). Transfer after Working Memory Updating Training. PLoS One 10:e0138734. 10.1371/journal.pone.0138734
    1. Weller S., Nitsche M. A., Plewnia C. (2020). Enhancing cognitive control training with transcranial direct current stimulation: A systematic parameter study. Brain Stimul. 13 1358–1369. 10.1016/j.brs.2020.07.006
    1. World Health Organization [WHO] (1996). Whoqol-bref introduction, administration, scoring and generic version of the assessment?: Field trial version. Available Online at: (accessed Jul 17, 2021).
    1. World Health Organization [WHO] (2019). Risk Reduction of Cognitive Decline and Dementia: WHO Guidelines. Geneva: World Health Organization.
    1. Zigmond A. S., Snaith R. P. (1983). The hospital anxiety and depression scale. Acta Psychiatr. Scand. 67 361–370. 10.1111/j.1600-0447.1983.tb09716.x

Source: PubMed

スポンサーと協力者

医学的状態

薬物療法

3
購読する