Effect of transcranial direct current stimulation on prospective memory in healthy individuals: A double-blind randomized sham-controlled trial

Year 2024, Volume: 10 Issue: 1, 24 - 34, 23.04.2024

Serkan Aksu , Eda Özsayın , Aslı Esin Aslan , Yusuf Kaya , Sacit Karamursel

https://doi.org/10.30569/adiyamansaglik.1425915

Abstract

Aim: Prospective memory (PM) has an immense role in the activities of daily living and deficits of PM are common in various neuropsychiatric disorders. Transcranial direct current stimulation (tDCS) is a neuromodulatory technique that yields favorable outcomes yet only a few studies concerning PM with hindering results exist. The present double-blind cross-over randomized sham-controlled study aimed to assess the effect of a single-session of left-righr/sham tDCS over the prefrontal cortex on event-related PM in healthy individuals.
Materials and Methods: 24 participants were administered a single session of 2 mA 20-minute left/right anodal or sham tDCS segregated by 7 days. An event-based PM task was utilized before and after tDCS every week to evaluate PM.
Results: No effects of tDCS on PM were found.
Conclusion: The present results argue against the effect of a single-session of tDCS over the prefrontal cortices on event-related PM. TDCS studies adopting divergent parameters are required.

Keywords

Brain stimulation, Cognition, Memory, Prospective memory, Transcranial direct current stimulation

Ethical Statement

Ethical approval was obtained from the institutional Ethical Committee (decision number 112 dated: 29.01.2019). All procedures were utilized in accordance with the Declaration of Helsinki

Supporting Institution

The authors declare no potential conflicts of interest. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Thanks

We thank all participants for their participation.

Sağlıklı bireylerde transkraniyal doğru akım uyarımının prospektif bellek üzerine etkisi: Çift-kör randomize kontrollü çalışma

Abstract

Amaç: Prospektif bellek (PB), günlük yaşam aktivitelerinde çok büyük bir role sahiptir ve eksiklikleri çeşitli nöropsikiyatrik bozukluklarda yaygındır. Transkraniyal Doğru Akım Uyarımı (tDAU), olumlu sonuçlar sağlayan bir nöromodülasyon tekniğidir ve PB üzerine etkisiyle ilgili sınırlı sonuçları olan yalnızca birkaç çalışma mevcuttur. Mevcut çift-kör, çapraz, randomize sham kontrollü çalışma, sağlıklı bireylerde tek seanslık sol/sağ/sham prefrontal tDAU’nun olaya dayalı PB işlevine etkisini değerlendirmeyi amaçlamıştır.
Gereç ve Yöntem: 24 katılımcıya 7 gün arayla tek bir 2 mA 20 dakikalık sol/sağ anodal veya sham tDAU seansı uygulandı. Olaya dayalı PB testi, PB’yi değerlendirmek için her hafta tDAU’dan önce ve sonra uygulandı.
Bulgular: tDAU’nun PB üzerine etkisi saptanmadı.
Sonuç: Mevcut sonuçlar, prefrontal korteksler üzerine uygulanan tek bir tDAU oturumunun olaya dayalı PB üzerindeki etkisini göstermemiştir. Farklı parametrelerle yürütülen tDAU çalışmalarına ihtiyaç bulunmaktadır.

Keywords

Beyin uyarımı, Bellek, Biliş, Prospektif bellek, Transkraniyal doğru akım uyarımı

Ethical Statement

Ethical approval was obtained from the institutional Ethical Committee (decision number 112 dated: 29.01.2019). All procedures were utilized in accordance with the Declaration of Helsinki.

Supporting Institution

The authors declare no potential conflicts of interest. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Thanks

We thank all participants for their participation.

References

• Ellis J, Kvavilashvili L, Milne A. Experimental tests of prospective remembering: the influence of cue-event frequency on performance. Br J Psychol. 1999;90(1):9-23.
• Burgess PW, Gonen-Yaacovi G, Volle E. Functional neuroimaging studies of prospective memory: what have we learnt so far? Neuropsychologia. 2011;49(8):2246-2257.
• Blondelle G, Hainselin M, Gounden Y, Quaglino V. Instruments Measuring Prospective Memory: A Systematic and Meta-Analytic Review. Arch Clin Neuropsychol. 2020;35(5):576-596.
• Blondelle G, Sugden N, Hainselin M. Prospective memory assessment: Scientific advances and future directions. Front Psychol. 2022;13:4637.
• Smith RE, Bayen UJ. A multinomial model of event-based prospective memory. J Exp Psychol Learn Mem Cogn. 2004;30(4):756-777.
• McDaniel MA, Einstein GO. Strategic and automatic processes in prospective memory retrieval: a multiprocess framework. Appl Cogn Psychol. 2000;14(7):S127-S144.
• Palermo L, Cinelli MC, Piccardi L, et al. Cognitive functions underlying prospective memory deficits: A study on traumatic brain injury. Appl Neuropsychol Adult. 2020;27(2):158-172.
• Fuermaier ABM, Tucha L, Koerts J, et al. Complex Prospective Memory in Adults with Attention Deficit Hyperactivity Disorder. PLoS One. 2013;8(3):e58338.
• Martin M, Kliegel M, McDaniel MA. The involvement of executive functions in prospective memory performance of adults. Int J Psychol. 2003;38(4):195-206.
• Tam JW, Schmitter-Edgecombe M. Event-based Prospective Memory and Everyday Forgetting in Healthy Older Adults and Individuals with Mild Cognitive Impairment. J Clin Exp Neuropsychol. 2013;35(3):279-290.
• Basso D, Ferrari M, Palladino P. Prospective memory and working memory: Asymmetrical effects during frontal lobe TMS stimulation. Neuropsychologia. 2010;48(11):3282-3290.
• Ball BH, Brewer GA. Proactive control processes in event-based prospective memory: Evidence from intraindividual variability and ex-Gaussian analyses. J Exp Psychol Learn Mem Cogn. 2018;44(5):793-811.
• McDaniel MA, Umanath S, Einstein GO, Waldum ER. Dual pathways to prospective remembering. Front Hum Neurosci. 2015;9(JULY):392.
• Cona G, Scarpazza C, Sartori G, Moscovitch M, Bisiacchi PS. Neural bases of prospective memory: a meta-analysis and the “Attention to Delayed Intention” (AtoDI) model. Neurosci Biobehav Rev. 2015;52:21-37.
• Henry JD, MacLeod MS, Phillips LH, Crawford JR. A meta-analytic review of prospective memory and aging. Psychol Aging. 2004;19(1):27-39.
• Ihle A, Hering A, Mahy CEV, Bisiacchi PS, Kliegel M. Adult age differences, response management, and cue focality in event-based prospective memory: a meta-analysis on the role of task order specificity. Psychol Aging. 2013;28(3):714-720.
• Sullivan KL, Neighbors C, Bucks RS, Weinborn M, Gavett BE, Woods SP. Longitudinal declines in event-based, but not time-based, prospective memory among community-dwelling older adults. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. 2020;29(1):70-86.
• Gonneaud J, Kalpouzos GG, Bon L, Viader F, Eustache F, Desgranges BA. Distinct and shared cognitive functions mediate event- and time-based prospective memory impairment in normal ageing. Memory. 2011;19(4):360-377.
• Woods SP, Weinborn M, Velnoweth A, Rooney A, Bucks RS. Memory for intentions is uniquely associated with instrumental activities of daily living in healthy older adults. J Int Neuropsychol Soc. 2012;18(1):134-138.
• Tierney SM, Bucks RS, Weinborn M, Hodgson E, Woods SP. Retrieval cue and delay interval influence the relationship between prospective memory and activities of daily living in older adults. J Clin Exp Neuropsychol. 2016;38(5):572-584.
• Zogg JB, Woods SP, Sauceda JA, Wiebe JS, Simoni JM. The Role of Prospective Memory in Medication Adherence: A Review of an Emerging Literature. J Behav Med. 2012;35(1):47-62.
• Woods SP, Weinborn M, Maxwell BR, et al. Event-based prospective memory is independently associated with self-report of medication management in older adults. Aging Ment Health. 2014;18(6):745-753.
• Hering A, Kliegel M, Rendell PG, Craik FIM, Rose NS. Prospective Memory Is a Key Predictor of Functional Independence in Older Adults. J Int Neuropsychol Soc. 2018;24(6):640-645.
• Sheppard DP, Matchanova A, Sullivan KL, Kazimi SI, Woods SP. Prospective memory partially mediates the association between aging and everyday functioning. Clin Neuropsychol. 2020;34(4):755-774.
• Kinsella GJ, Pike KE, Cavuoto MG, Lee SD. Mild cognitive impairment and prospective memory: translating the evidence into neuropsychological practice. Clin Neuropsychol. 2018;32(5):960-980.
• Smith G, Della Sala S, Logie RH, Maylor EA. Prospective and retrospective memory in normal ageing and dementia: a questionnaire study. Memory. 2000;8(5):311-321.
• Raskin SA. Prospective memory in clinical populations. Clin Neuropsychol. 2018;32(5):741-747.
• Mathias JL, Mansfield KM. Prospective and declarative memory problems following moderate and severe traumatic brain injury. Brain Inj. 2005;19(4):271-282.
• Ramanan S, Kumar D. Prospective memory in Parkinson’s disease: a meta-analysis. J Int Neuropsychol Soc. 2013;19(10):1109-1118.
• Van Den Berg E, Kant N, Postma A. Remember to buy milk on the way home! A meta-analytic review of prospective memory in mild cognitive impairment and dementia. J Int Neuropsychol Soc. 2012;18(4):706-716.
• Wang Y, Cui J, Chan RCK, et al. Meta-analysis of prospective memory in schizophrenia: Nature, extent, and correlates. Schizophr Res. 2009;114(1-3):64-70.
• Landsiedel J, Williams DM, Abbot-Smith K. A Meta-Analysis and Critical Review of Prospective Memory in Autism Spectrum Disorder. J Autism Dev Disord. 2017;47(3):646-666.
• Zhou FC, Wang YY, Zheng W, et al. Prospective memory deficits in patients with depression: A meta-analysis. J Affect Disord. 2017;220:79-85.
• Woods SP, Iudicello JE, Moran LM, et al. HIV-associated prospective memory impairment increases risk of dependence in everyday functioning. Neuropsychology. 2008;22(1):110-117.
• Weber E, Chiaravalloti ND, Deluca J, Goverover Y. Time-Based Prospective Memory Is Associated with Functional Performance in Persons with MS. J Int Neuropsychol Soc. 2019;25(10):1035-1043.
• Twamley EW, Woods SP, Zurhellen CH, et al. Neuropsychological substrates and everyday functioning implications of prospective memory impairment in schizophrenia. Schizophr Res. 2008;106(1):42-49.
• Tsang APL, Au A, Lo HHM. Prospective Memory Training for Healthy Older Adults: A Systematic Review. Clin Gerontol. 2022;45(3):486-502.
• Tse ZCK, Cao Y, Ogilvie JM, Chau BKH, Ng DHC, Shum DHK. Prospective Memory Training in Older Adults: A Systematic Review and Meta-Analysis. Neuropsychol Rev. 2022;1:1-26.
• Scullin MK, Jones WE, Phenis R, et al. Using smartphone technology to improve prospective memory functioning: A randomized controlled trial. J Am Geriatr Soc. 2022;70(2):459-469.
• Raskin SA, Williams J, Aiken EM. A review of prospective memory in individuals with acquired brain injury. Clin Neuropsychol. 2018;32(5):891-921.
• Rose NS, Rendell PG, Hering A, Kliegel M, Bidelman GM, Craik FIM. Cognitive and neural plasticity in older adults’ prospective memory following training with the Virtual Week computer game. Front Hum Neurosci. 2015;9(OCTOBER):592.
• Woods AJ, Antal A, Bikson M, et al. A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol. 2016;127(2):1031-1048.
• Aparício LVM, Guarienti F, Razza LB, Carvalho AF, Fregni F, Brunoni AR. A Systematic Review on the Acceptability and Tolerability of Transcranial Direct Current Stimulation Treatment in Neuropsychiatry Trials. Brain Stimul. 2016;9(5):671-681.
• Thair H, Holloway AL, Newport R, Smith AD. Transcranial Direct Current Stimulation (tDCS): A Beginner’s Guide for Design and Implementation. Front Neurosci. 2017;11(NOV):641.
• Gomes-Osman J, Indahlastari A, Fried PJ, et al. Non-invasive Brain Stimulation: Probing Intracortical Circuits and Improving Cognition in the Aging Brain. Front Aging Neurosci. 2018;10(JUN):177.
• Goldthorpe RA, Rapley JM, Violante IR. A Systematic Review of Non-invasive Brain Stimulation Applications to Memory in Healthy Aging. Front Neurol. 2020;11:575075.
• Hill AT, Fitzgerald PB, Hoy KE. Effects of Anodal Transcranial Direct Current Stimulation on Working Memory: A Systematic Review and Meta-Analysis of Findings From Healthy and Neuropsychiatric Populations. Brain Stimul. 2016;9(2):197-208.
• Brunoni AR, Vanderhasselt MA. Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: a systematic review and meta-analysis. Brain Cogn. 2014;86(1):1-9.
• Farhat LC, Carvalho AF, Solmi M, Brunoni AR. Evidence-based umbrella review of cognitive effects of prefrontal tDCS. Soc Cogn Affect Neurosci. 2022;17(1):43.
• Dedoncker J, Brunoni AR, Baeken C, Vanderhasselt MA. The effect of the interval-between-sessions on prefrontal transcranial direct current stimulation (tDCS) on cognitive outcomes: a systematic review and meta-analysis. J Neural Transm (Vienna). 2016;123(10):1159-1172.
• Imburgio MJ, Orr JM. Effects of prefrontal tDCS on executive function: Methodological considerations revealed by meta-analysis. Neuropsychologia. 2018;117:156-166.
• Rose NS, Thomson H, Kliegel M. No Effect of Transcranial Direct-Current Stimulation to Dorsolateral Prefrontal Cortex on Naturalistic Prospective Memory in Healthy Young and Older Adults. Journal of Cognitive Enhancement 2019 4:2. 2019;4(2):211-218.
• Ellis DM, Veloria GKG, Arnett CR, Vogel AE, Pitães M, Brewer GA. No Evidence for Enhancing Prospective Memory with Anodal Transcranial Direct Current Stimulation Across Dorsolateral Prefrontal Cortex. Journal of Cognitive Enhancement 2019 4:3. 2019;4(3):333-339.
• Bisiacchi PS, Cona G, Schiff S, Basso D. Modulation of a fronto-parietal network in event-based prospective memory: an rTMS study. Neuropsychologia. 2011;49(8):2225-2232.
• Okuda J, Fujii T, Yamadori A, et al. Participation of the prefrontal cortices in prospective memory: evidence from a PET study in humans. Neurosci Lett. 1998;253(2):127-130.
• Cheng HD, Wang K, Xi CH, Niu CS, Fu XM. Prefrontal cortex involvement in the event-based prospective memory: evidence from patients with lesions in the prefrontal cortex. Brain Inj. 2008;22(9):697-704.
• Smith RE, Bayen UJ. The source of adult age differences in event-based prospective memory: a multinomial modeling approach. J Exp Psychol Learn Mem Cogn. 2006;32(3):623-635.
• Haatveit BC, Sundet K, Hugdahl K, Ueland T, Melle I, Andreassen OA. The validity of d prime as a working memory index: results from the “Bergen n-back task.” J Clin Exp Neuropsychol. 2010;32(8):871-880.
• Basu A, Mukherjee T. Prospective Memory as A Function of Reward Responsiveness and Ongoing Task Difficulty. International Journal of Indian Psychology. 2022;10(4):1641-1662.
• McDaniel MA, LaMontagne P, Beck SM, Scullin MK, Braver TS. Dissociable neural routes to successful prospective memory. Psychol Sci. 2013;24(9):1791-1800.
• Volle E, Gonen-Yaacovi G, de Lacy Costello A, Gilbert SJ, Burgess PW. The role of rostral prefrontal cortex in prospective memory: a voxel-based lesion study. Neuropsychologia. 2011;49(8):2185-2198.
• Horvath JC, Forte JD, Carter O. Quantitative Review Finds No Evidence of Cognitive Effects in Healthy Populations From Single-session Transcranial Direct Current Stimulation (tDCS). Brain Stimul. 2015;8(3):535-550.
• Mancuso LE, Ilieva IP, Hamilton RH, Farah MJ. Does Transcranial Direct Current Stimulation Improve Healthy Working Memory?: A Meta-analytic Review. J Cogn Neurosci. 2016;28(8):1063-1089.
• Luque-Casado A, Rodríguez-Freiría R, Fogelson N, Iglesias-Soler E, Fernández-del-Olmo M. An Integrative Clustering Approach to tDCS Individual Response Variability in Cognitive Performance: Beyond a Null Effect on Working Memory. Neuroscience. 2020;443:120-130.
• Begemann MJ, Brand BA, C¨určić-Blake B, Aleman A, Sommer IE. Efficacy of non-invasive brain stimulation on cognitive functioning in brain disorders: a meta-analysis. Psychol Med. 2020;50(15):2465-2486.
• Berryhill ME, Martin D. Cognitive Effects of Transcranial Direct Current Stimulation in Healthy and Clinical Populations: An Overview. J ECT. 2018;34(3):e25-e35.
• Kalpouzos G, Eriksson J, Sjölie D, Molin J, Nyberg L. Neurocognitive systems related to real-world prospective memory. PLoS One. 2010;5(10):13304.
• Costa A, Oliveri M, Barban F, et al. The Right Frontopolar Cortex Is Involved in Visual-Spatial Prospective Memory. PLoS One. 2013;8(2):56039.
• Debarnot U, Crépon B, Orriols E, et al. Intermittent theta burst stimulation over left BA10 enhances virtual reality-based prospective memory in healthy aged subjects. Neurobiol Aging. 2015;36(8):2360-2369.
• Ball H, Peper P, Alakbarova D, Brewer G, Gilbert SJ. Individual differences in working memory capacity predict benefits to memory from intention offloading. Memory. 2022;30(2):77-91.
• Levén A, Lyxell B, Danielsson H, Rönnberg J, Andersson J. Prospective Memory, Working Memory, Retrospective Memory and Self-Rated Memory Performance in Persons with Intellectual Disability. Scandinavian Journal of Disability Research. 2008;10(3):147-165.
• Dedoncker J, Brunoni AR, Baeken C, Vanderhasselt MA. 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 Stimul. 2016;9(4):501-517.
• Habich A, Fehér KD, Antonenko D, et al. Stimulating aged brains with transcranial direct current stimulation: Opportunities and challenges. Psychiatry Res Neuroimaging. 2020;306:111179.
• Learmonth G, Thut G, Benwell CSY, Harvey M. The implications of state-dependent tDCS effects in aging: Behavioural response is determined by baseline performance. Neuropsychologia. 2015;74:108-119.
• Krebs C, Peter J, Wyss P, Brem AK, Klöppel S. Transcranial electrical stimulation improves cognitive training effects in healthy elderly adults with low cognitive performance. Clin Neurophysiol. 2021;132(6):1254-1263.
• Perceval G, Martin AK, Copland DA, Laine M, Meinzer M. Multisession transcranial direct current stimulation facilitates verbal learning and memory consolidation in young and older adults. Brain Lang. 2020;205:104788.
• Habich A, Klöppel S, Abdulkadir A, Scheller E, Nissen C, Peter J. Anodal tDCS Enhances Verbal Episodic Memory in Initially Low Performers. Front Hum Neurosci. 2017;11:542.
• Katz B, Au J, Buschkuehl M, et al. Individual Differences and Long-term Consequences of tDCS-augmented Cognitive Training. J Cogn Neurosci. 2017;29(9):1498-1508.
• Arciniega H, Gözenman F, Jones KT, Stephens JA, Berryhill ME. Frontoparietal tDCS benefits visual working memory in older adults with Low working memory capacity. Front Aging Neurosci. 2018;10(FEB):57.
• Matysiak O, Kroemeke A, Brzezicka A. Working Memory Capacity as a Predictor of Cognitive Training Efficacy in the Elderly Population. Front Aging Neurosci. 2019;11(MAY):126.