Exploring the impact of intensified multiple session tDCS over the left DLPFC on brain function in MCI: a randomized control trial
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu randomizované kontrolované studie, časopisecké články
Grantová podpora
NV18-04-00256
Ministerstvo Zdravotnictví Ceské Republiky
NV18-04-00256
Ministerstvo Zdravotnictví Ceské Republiky
NV18-04-00256
Ministerstvo Zdravotnictví Ceské Republiky
NV18-04-00256
Ministerstvo Zdravotnictví Ceské Republiky
NV18-04-00256
Ministerstvo Zdravotnictví Ceské Republiky
21-13462L
Czech Science Foundation grant
21-13462L
Czech Science Foundation grant
21-13462L
Czech Science Foundation grant
21-13462L
Czech Science Foundation grant
LX22NPO5107
European Union - Next Generation EU
PubMed
38233437
PubMed Central
PMC10794210
DOI
10.1038/s41598-024-51690-8
PII: 10.1038/s41598-024-51690-8
Knihovny.cz E-zdroje
- MeSH
- dorsolaterální prefrontální kortex MeSH
- dvojitá slepá metoda MeSH
- kognitivní dysfunkce * terapie MeSH
- krátkodobá paměť fyziologie MeSH
- lidé MeSH
- mozek diagnostické zobrazování MeSH
- prefrontální mozková kůra fyziologie MeSH
- přímá transkraniální stimulace mozku * metody MeSH
- senioři MeSH
- Check Tag
- lidé MeSH
- senioři MeSH
- Publikační typ
- časopisecké články MeSH
- randomizované kontrolované studie MeSH
Transcranial direct current stimulation combined with cognitive training (tDCS-cog) represents a promising approach to combat cognitive decline among healthy older adults and patients with mild cognitive impairment (MCI). In this 5-day-long double-blinded randomized trial, we investigated the impact of intensified tDCS-cog protocol involving two trains of stimulation per day on working memory (WM) enhancement in 35 amnestic and multidomain amnestic MCI patients. Specifically, we focused to improve WM tasks relying on top-down attentional control and hypothesized that intensified tDCS would enhance performance of visual object matching task (VOMT) immediately after the stimulation regimen and at a 1-month follow-up. Secondarily, we explored whether the stimulation would augment online visual working memory training. Using fMRI, we aimed to elucidate the neural mechanisms underlying the intervention effects by analyzing BOLD activations during VOMT. Our main finding revealed no superior after-effects of tDCS-cog over the sham on VOMT among individuals with MCI as indicated by insignificant immediate and long-lasting after-effects. Additionally, the tDCS-cog did not enhance online training as predicted. The fMRI analysis revealed brain activity alterations in right insula that may be linked to tDCS-cog intervention. In the study we discuss the insignificant behavioral results in the context of the current evidence in tDCS parameter space and opening the discussion of possible interference between trained cognitive tasks.
Faculty of Medicine Masaryk University Brno Czech Republic
Surgeon General Office of the Slovak Armed Forces Ružomberok Slovak Republic
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Roberts R, Knopman DS. Classification and epidemiology of MCI. Clin. Geriatr. Med. 2013;29:753–772. doi: 10.1016/j.cger.2013.07.003. PubMed DOI PMC
Sperling RA, et al. Toward defining the preclinical stages of Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s Dement. 2011;7(3):280–292. doi: 10.1016/j.jalz.2011.03.003. PubMed DOI PMC
Harper LC. Alzheimer’s disease facts and figures. Alzheimers Dement. 2022;18:700–789. PubMed
Petersen RC. Mild cognitive impairment as a diagnostic entity. J. Intern. Med. 2004;256:183–194. doi: 10.1111/j.1365-2796.2004.01388.x. PubMed DOI
Petersen RC. Mild cognitive impairment. CONTINUUM Lifelong Learn. Neurol. 2016;22:404. doi: 10.1212/CON.0000000000000313. PubMed DOI PMC
Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82:239–259. doi: 10.1007/BF00308809. PubMed DOI
McEvoy LK, Pellouchoud E, Smith ME, Gevins A. Neurophysiological signals of working memory in normal aging. Brain Res. Cogn. Brain Res. 2001;11:363–376. doi: 10.1016/S0926-6410(01)00009-X. PubMed DOI
Saunders NLJ, Summers MJ. Attention and working memory deficits in mild cognitive impairment. J. Clin. Exp. Neuropsychol. 2010;32:350–357. doi: 10.1080/13803390903042379. PubMed DOI
Petersen RC, et al. Neuropathologic features of amnestic mild cognitive impairment. Arch. Neurol. 2006;63:665–672. doi: 10.1001/archneur.63.5.665. PubMed DOI
Saunders NLJ, Summers MJ. Longitudinal deficits to attention, executive, and working memory in subtypes of mild cognitive impairment. Neuropsychology. 2011;25:237–248. doi: 10.1037/a0021134. PubMed DOI
Summers MJ, Saunders NLJ. Neuropsychological measures predict decline to Alzheimer’s dementia from mild cognitive impairment. Neuropsychology. 2012;26:498–508. doi: 10.1037/a0028576. PubMed DOI
Huntley JD, Howard RJ. Working memory in early Alzheimer’s disease: A neuropsychological review. Int. J. Geriatr. Psychiatry. 2010;25:121–132. doi: 10.1002/gps.2314. PubMed DOI
Garcia-Alvarez L, Gomar JJ, Sousa A, Garcia-Portilla MP, Goldberg TE. Breadth and depth of working memory and executive function compromises in mild cognitive impairment and their relationships to frontal lobe morphometry and functional competence. Alzheimers Dement. 2019;11:170–179. PubMed PMC
Albert M, Blacker D, Moss MB, Tanzi R, McArdle JJ. Longitudinal change in cognitive performance among individuals with mild cognitive impairment. Neuropsychology. 2007;21:158–169. doi: 10.1037/0894-4105.21.2.158. PubMed DOI
Tabert MH, et al. Neuropsychological prediction of conversion to Alzheimer disease in patients with mild cognitive impairment. Arch. Gen. Psychiatry. 2006;63:916–924. doi: 10.1001/archpsyc.63.8.916. PubMed DOI
Baddeley AD, Hitch G. Working memory. In: Bower GH, editor. Psychology of Learning and Motivation. Academic Press; 1974. pp. 47–89.
Baddeley A. Working memory. Science. 1992;255:556–559. doi: 10.1126/science.1736359. PubMed DOI
Baddeley A. Working memory: Looking back and looking forward. Nat. Rev. Neurosci. 2003;4:829–839. doi: 10.1038/nrn1201. PubMed DOI
Gazzaley A, Nobre AC. Top-down modulation: Bridging selective attention and working memory. Trends Cogn. Sci. 2012;16:129–135. doi: 10.1016/j.tics.2011.11.014. PubMed DOI PMC
Gazzaley A, et al. Functional interactions between prefrontal and visual association cortex contribute to top-down modulation of visual processing. Cereb. Cortex. 2007;17:125–135. doi: 10.1093/cercor/bhm113. PubMed DOI PMC
Nemcova Elfmarkova N, Gajdos M, Rektorova I, Marecek R, Rapcsak SZ. Neural evidence for defective top-down control of visual processing in Parkinson’s and Alzheimer’s disease. Neuropsychologia. 2017;106:236–244. doi: 10.1016/j.neuropsychologia.2017.09.034. PubMed DOI
He H, et al. Decline in the integration of top-down and bottom-up attentional control in older adults with mild cognitive impairment. Neuropsychologia. 2021;161:108014. doi: 10.1016/j.neuropsychologia.2021.108014. PubMed DOI
Zanto TP, Rubens MT, Thangavel A, Gazzaley A. Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory. Nat. Neurosci. 2011;14:656–661. doi: 10.1038/nn.2773. PubMed DOI PMC
Šimko P, Kent JA, Rektorova I. Is non-invasive brain stimulation effective for cognitive enhancement in Alzheimer’s disease? An updated meta-analysis. Clin. Neurophysiol. 2022;144:23–40. doi: 10.1016/j.clinph.2022.09.010. PubMed DOI
Chou Y. Effects of repetitive TMS on cognitive function in Alzheimer’s disease and mild cognitive impairment: A systematic review and meta-analysis. Brain Stimul. 2019;12:528–529. doi: 10.1016/j.brs.2018.12.740. DOI
Cheng CPW, et al. Effects of repetitive transcranial magnetic stimulation on improvement of cognition in elderly patients with cognitive impairment: A systematic review and meta-analysis. Int. J. Geriatr. Psychiatry. 2018;33:e1–e13. doi: 10.1002/gps.4726. PubMed DOI
Chou YH, Ton That V, Sundman M. A systematic review and meta-analysis of rTMS effects on cognitive enhancement in mild cognitive impairment and Alzheimer’s disease. Neurobiol. Aging. 2020;86:1–10. doi: 10.1016/j.neurobiolaging.2019.08.020. PubMed DOI PMC
Goldsworthy MR, Hordacre B. Dose dependency of transcranial direct current stimulation: Implications for neuroplasticity induction in health and disease. J. Physiol. 2017;595:3265–3266. doi: 10.1113/JP274089. PubMed DOI PMC
Agboada D, Mosayebi Samani M, Jamil A, Kuo M-F, Nitsche MA. Expanding the parameter space of anodal transcranial direct current stimulation of the primary motor cortex. Sci. Rep. 2019;9:18185. doi: 10.1038/s41598-019-54621-0. PubMed DOI PMC
Batsikadze G, Moliadze V, Paulus W, Kuo M-F, Nitsche MA. Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. J. Physiol. 2013;591:1987–2000. doi: 10.1113/jphysiol.2012.249730. PubMed DOI PMC
Monte-Silva K, et al. Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul. 2013;6:424–432. doi: 10.1016/j.brs.2012.04.011. PubMed DOI
Agboada D, Mosayebi-Samani M, Kuo M-F, Nitsche MA. Induction of long-term potentiation-like plasticity in the primary motor cortex with repeated anodal transcranial direct current stimulation - Better effects with intensified protocols? Brain Stimul. 2020;13:987–997. doi: 10.1016/j.brs.2020.04.009. PubMed DOI
Bradley C, Nydam AS, Dux PE, Mattingley JB. State-dependent effects of neural stimulation on brain function and cognition. Nat. Rev. Neurosci. 2022;23(8):459–475. doi: 10.1038/s41583-022-00598-1. PubMed DOI
Pupíková M, Rektorová I. Non-pharmacological management of cognitive impairment in Parkinson’s disease. J. Neural Transm. 2020;127:799–820. doi: 10.1007/s00702-019-02113-w. PubMed DOI
Chu CS, et al. Cognitive effects and acceptability of non-invasive brain stimulation on Alzheimer’s disease and mild cognitive impairment: A component network meta-analysis. J. Neurol. Neurosurg. Psychiatry. 2021;92:195–203. doi: 10.1136/jnnp-2020-323870. PubMed DOI PMC
Antonenko D, et al. Randomized trial of cognitive training and brain stimulation in non-demented older adults. Alzheimers Dement. 2022;8:e12262. doi: 10.1002/trc2.12262. PubMed DOI PMC
Horne KS, et al. Evidence against benefits from cognitive training and transcranial direct current stimulation in healthy older adults. Nat. Hum. Behav. 2021;5:146–158. doi: 10.1038/s41562-020-00979-5. PubMed DOI
Šimko P, Pupíková M, Gajdo M, Rektorová I. Cognitive aftereffects of acute tDCS coupled with cognitive training: An fMRI study in healthy seniors. Neural Plast. 2021;2021:6664479. doi: 10.1155/2021/6664479. PubMed DOI PMC
Das N, et al. Cognitive training and transcranial direct current stimulation in mild cognitive impairment: A randomized pilot trial. Front. Neurosci. 2018;13:307. doi: 10.3389/fnins.2019.00307. PubMed DOI PMC
Mosayebi-Samani M, et al. The impact of individual electrical fields and anatomical factors on the neurophysiological outcomes of tDCS: A TMS-MEP and MRI study. Brain Stimul. 2021;14:316–326. doi: 10.1016/j.brs.2021.01.016. PubMed DOI
Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC, Wager TD. Large-scale automated synthesis of human functional neuroimaging data. Nat. Methods. 2011;8:665–670. doi: 10.1038/nmeth.1635. PubMed DOI PMC
Das N, et al. Cognitive training and transcranial direct current stimulation in mild cognitive impairment: A randomized pilot trial. Front. Neurosci. 2019;13:307. doi: 10.3389/fnins.2019.00307. PubMed DOI PMC
Bagattini C, et al. Enhancing cognitive training effects in Alzheimer’s disease: rTMS as an add-on treatment. Brain Stimul. 2020;13:1655–1664. doi: 10.1016/j.brs.2020.09.010. PubMed DOI
Antonenko D, et al. Neuronal and behavioral effects of multi-day brain stimulation and memory training. Neurobiol. Aging. 2018;61:245–254. doi: 10.1016/j.neurobiolaging.2017.09.017. PubMed DOI
Jones KT, Stephens JA, Alam M, Bikson M, Berryhill ME. Longitudinal neurostimulation in older adults improves working memory. PLoS One. 2015;10:e0121904. doi: 10.1371/journal.pone.0121904. PubMed DOI PMC
Stephens JA, Berryhill ME. Older adults improve on everyday tasks after working memory training and neurostimulation. Brain Stimul. 2016;9:553–559. doi: 10.1016/j.brs.2016.04.001. PubMed DOI PMC
Nilsson J, Lebedev AV, Rydström A, Lövdén M. Direct-current stimulation does little to improve the outcome of working memory training in older adults. Psychol. Sci. 2017;28:907–920. doi: 10.1177/0956797617698139. PubMed DOI PMC
Forstmann BU, et al. The speed-accuracy tradeoff in the elderly brain: a structural model-based approach. J. Neurosci. 2011;31:17242–17249. doi: 10.1523/JNEUROSCI.0309-11.2011. PubMed DOI PMC
Anderkova L, Eliasova I, Marecek R, Janousova E, Rektorova I. Grey matter atrophy in mild Alzheimer’s disease impacts on cognitive effects of noninvasive brain stimulation. Clin. Neurophysiol. 2016;127:e28. doi: 10.1016/j.clinph.2015.11.083. PubMed DOI
Menon V, Uddin LQ. Saliency, switching, attention and control: A network model of insula function. Brain Struct. Funct. 2010;214:655–667. doi: 10.1007/s00429-010-0262-0. PubMed DOI PMC
Namkung H, Kim S-H, Sawa A. The insula: An underestimated brain area in clinical neuroscience, psychiatry, and neurology. Trends Neurosci. 2018;41:551–554. doi: 10.1016/j.tins.2018.05.004. PubMed DOI
Perri RL, Berchicci M, Bianco V, Spinelli D, Di Russo F. Brain waves from an “isolated” cortex: Contribution of the anterior insula to cognitive functions. Brain Struct. Funct. 2018;223:1343–1355. PubMed
Schendan HE, Stern CE. Mental rotation and object categorization share a common network of prefrontal and dorsal and ventral regions of posterior cortex. Hum. Brain Mapp. J. 2007;35:1264–1277. PubMed
Schendan HE, Stern CE. Where vision meets memory: Prefrontal-posterior networks for visual object constancy during categorization and recognition. Cereb. Cortex. 2008;18:1695–1711. doi: 10.1093/cercor/bhm197. PubMed DOI
Trujillo JP, et al. Reduced neural connectivity but increased task-related activity during working memory in de novo Parkinson patients. Hum. Brain Mapp. 2015;36:1554–1566. doi: 10.1002/hbm.22723. PubMed DOI PMC
Yun K, Song I-U, Chung Y-A. Changes in cerebral glucose metabolism after 3 weeks of noninvasive electrical stimulation of mild cognitive impairment patients. Alzheimers Res. Ther. 2016;8:1–9. doi: 10.1186/s13195-016-0218-6. PubMed DOI PMC
Antonenko D, et al. Microstructural and functional plasticity following repeated brain stimulation during cognitive training in older adults. Nat. Commun. 2023;14:3184. doi: 10.1038/s41467-023-38910-x. PubMed DOI PMC
Lu H, et al. Randomized controlled trial of TDCS on cognition in 201 seniors with mild neurocognitive disorder. Ann. Clin. Transl. Neurol. 2019;6:1938–1949. doi: 10.1002/acn3.50823. PubMed DOI PMC
Martin DM, et al. A pilot double-blind randomized controlled trial of cognitive training combined with transcranial direct current stimulation for amnestic mild cognitive impairment. J. Alzheimers Dis. 2019;71:503–512. doi: 10.3233/JAD-190306. PubMed DOI
Cui H, et al. Repetitive transcranial magnetic stimulation induced hypoconnectivity within the default mode network yields cognitive improvements in amnestic mild cognitive impairment: A randomized controlled study. J. Alzheimers Dis. 2019;69:1137–1151. doi: 10.3233/JAD-181296. PubMed DOI
Drumond Marra HL, et al. Transcranial magnetic stimulation to address mild cognitive impairment in the elderly: A randomized controlled study. Behav. Neurol. 2015;2015:287843. doi: 10.1155/2015/287843. PubMed DOI PMC
Solé-Padullés C, et al. Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study. Cereb. Cortex. 2006;16:1487–1493. doi: 10.1093/cercor/bhj083. PubMed DOI
Petersen RC, et al. Current concepts in mild cognitive impairment. Arch. Neurol. 2001;58:1985–1992. doi: 10.1001/archneur.58.12.1985. PubMed DOI
Bartoš A, Martínek P, Bezdíček O, Buček A, Řípová D. Dotazník funkčního stavu FAQ-CZ—Česká verze pro zhodnocení každodenních aktivit pacientů s Alzheimerovou nemocí. Psychiatr. Pro Praxi. 2008;1:31–34.
Yesavage JA, et al. Development and validation of a geriatric depression screening scale: A preliminary report. J. Psychiatr. Res. 1982;17:37–49. doi: 10.1016/0022-3956(82)90033-4. PubMed DOI
Lefaucheur JP, et al. Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS) Clin. Neurophysiol. 2016;128:56–92. doi: 10.1016/j.clinph.2016.10.087. PubMed DOI
Bikson M, et al. Brain stimulation safety of transcranial direct current stimulation: Evidence based update 2016. Brain Stimul. 2016;9:641–661. doi: 10.1016/j.brs.2016.06.004. PubMed DOI PMC
Antal A, et al. Low intensity transcranial electric stimulation: Safety, ethical, legal regulatory and application guidelines. Clin. Neurophysiol. 2017;128:1774–1809. doi: 10.1016/j.clinph.2017.06.001. PubMed DOI PMC
DaSilva AF, Volz MS, Bikson M, Fregni F. Electrode positioning and montage in transcranial direct current stimulation. J. Vis. Exp. 2011 doi: 10.3791/2744. PubMed DOI PMC
Thielscher A, Antunes A, Saturnino GB. Field modeling for transcranial magnetic stimulation: A useful tool to understand the physiological effects of TMS? Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. 2015;2015:222–225. PubMed
Pupíková M, Šimko P, Gajdoš M, Rektorová I. Modulation of working memory and resting-state fMRI by tDCS of the right frontoparietal network. Neural Plast. 2021;2021:5594305. doi: 10.1155/2021/5594305. PubMed DOI PMC
Ma DS, Correll J, Wittenbrink B. The Chicago face database: A free stimulus set of faces and norming data. Behav. Res. Methods. 2015;47:1122–1135. doi: 10.3758/s13428-014-0532-5. PubMed DOI
Burton AM, White D, McNeill A. The glasgow face matching test. Behav. Res. Methods. 2010;42:286–291. doi: 10.3758/BRM.42.1.286. PubMed DOI
Villanueva RAM, Chen ZJ. ggplot2: Elegant graphics for data analysis. Measurement (Mahwah NJ) 2019;17:160–167.
Westfall J, Kenny DA, Judd CM. Statistical power and optimal design in experiments in which samples of participants respond to samples of stimuli. J. Exp. Psychol. Gen. 2014;143(5):2020. doi: 10.1037/xge0000014. PubMed DOI
Poser BA, Versluis MJ, Hoogduin JM, Norris DG. BOLD contrast sensitivity enhancement and artifact reduction with multiecho EPI: Parallel-acquired inhomogeneity-desensitized fMRI. Magn. Reson. Med. 2006;55:1227–1235. doi: 10.1002/mrm.20900. PubMed DOI
Gajdoš M, Mikl M, Mareček R. Mask_explorer: A tool for exploring brain masks in fMRI group analysis. Comput. Methods Programs Biomed. 2016;134:155–163. doi: 10.1016/j.cmpb.2016.07.015. PubMed DOI
Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. Steps toward optimizing motion artifact removal in functional connectivity MRI; A reply to Carp. NeuroImage. 2013;76:439–441. doi: 10.1016/j.neuroimage.2012.03.017. PubMed DOI PMC
Gronenschild EHBM, et al. The effects of FreeSurfer version, workstation type, and Macintosh operating system version on anatomical volume and cortical thickness measurements. PLoS One. 2012;7:e38234. doi: 10.1371/journal.pone.0038234. PubMed DOI PMC
Fischl B, et al. Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33:341–355. doi: 10.1016/S0896-6273(02)00569-X. PubMed DOI
Risacher SL, et al. Alzheimer disease brain atrophy subtypes are associated with cognition and rate of decline. Neurology. 2017;89:2176–2186. doi: 10.1212/WNL.0000000000004670. PubMed DOI PMC
Desikan RS, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968–980. doi: 10.1016/j.neuroimage.2006.01.021. PubMed DOI
Hayasaka S, Phan KL, Liberzon I, Worsley KJ, Nichols TE. Nonstationary cluster-size inference with random field and permutation methods. Neuroimage. 2004;22:676–687. doi: 10.1016/j.neuroimage.2004.01.041. PubMed DOI
Worsley KJ, Andermann M, Koulis T, MacDonald D, Evans AC. Detecting changes in nonisotropic images. Hum. Brain Mapp. 1999;8:98–101. doi: 10.1002/(SICI)1097-0193(1999)8:2/3<98::AID-HBM5>3.0.CO;2-F. PubMed DOI PMC
Non-invasive stimulation for treating cognitive impairment in Alzheimer disease