Top

Published in:

01-09-2019 | Mild Cognitive Impairment | Original Article

Effects on cognition of 20-day anodal transcranial direct current stimulation over the left dorsolateral prefrontal cortex in patients affected by mild cognitive impairment: a case-control study

Authors: Enrico Fileccia, Vitantonio Di Stasi, Roberto Poda, Giovanni Rizzo, Michelangelo Stanzani-Maserati, Federico Oppi, Patrizia Avoni, Sabina Capellari, Rocco Liguori

Published in: Neurological Sciences | Issue 9/2019

Abstract

Background

Mild cognitive impairment (MCI) is a common disorder affecting as much as 15% of the elderly population. Transcranial direct current stimulation (tDCS) is a non-invasive technique of neuromodulation that has proven to influence performance in different cognitive domains.

Objective/hypothesis

We investigated the effects on cognition of 20-day anodal tDCS in 17 MCI patients compared with 17 matched MCI patients.

Methods

Patients underwent neuropsychological evaluation at baseline and then were randomly assigned to the anodal or sham group. The tDCS protocol consisted in 20 min, 5 days per week (up to a total of 20 days), of 2-mA anodal stimulation over the left dorsolateral prefrontal cortex (DLPFC). The location of anodal electrode was chosen in accordance with previous reports which relate anodal stimulation of this site with cognitive enhancement. At the end of the last day of stimulation, a second neuropsychological evaluation was performed. We compared baseline and post-stimulation neuropsychological results in the anodal vs sham group using repeated measures ANOVA as a statistical analysis test.

Results

At follow-up, patients exposed to anodal stimulation showed improvement in episodic verbal memory (p < 0.001) and figure naming test (p < 0.01), in a general index of cognitive function (Brief Mental Deterioration Battery) (p < 0.0001) and in a mood measurement test (Beck Depression Inventory) (p < 0.01).

Conclusion

Anodal tDCS could be a useful tool to improve cognitive symptoms in MCI although more evidence is needed to understand the exact underlying mechanisms. Confirmation of its potential benefits in MCI would be significant.

Alexander M, Perera G, Ford G, Arrighi HM, Foskett N, Debove C, Novak G, Gordon FM (2015) Age-stratified prevalence of mild cognitive impairment and dementia in European populations: a systematic review. J Alzheimers Dis 48:355–359. https://doi.org/10.3233/JAD-150168 IOS Press355CrossRefPubMed

Petersen RC, Lopez O, Armstrong MJ, Getchius TSD, Ganguli M, Gloss D, Gronseth GS, Marson D, Pringsheim T, Day GS, Sager M, Stevens J, Rae-Grant A (2018) Practice guideline update summary: Mild cognitive impairment report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology Neurology® 90:1–10. https://doi.org/10.1212/WNL.0000000000004826

Petersen RC, Roberts RO, Knopman DS, Boeve BF, Geda YE, Ivnik RJ, Smith GE, Jack CR Jr (2009) Mild cognitive impairment: ten years later. Arch Neurol 66(12):1447–1455CrossRefPubMedPubMedCentral

Ritchie C, Smailagic N, Noel-Storr AH, Ukoumunne O, Ladds EC, Martin S (2017) CSF tau and the CSF tau/ABeta ratio for the diagnosis of Alzheimer’s disease dementia and other dementias in people with mild cognitive impairment (MCI). Cochrane Database Syst Rev (3):CD010803. https://doi.org/10.1002/14651858.CD010803.pub2

Mitchell AJ, Shiri-Feshki M (2008) Temporal trends in the long term risk of progression of mild cognitive impairment: a pooled analysis. J Neurol Neurosurg Psychiatry 79:1386–1391. https://doi.org/10.1136/jnnp.2007.142679 CrossRefPubMed

Gallassi R, Oppi F, Poda R, Scortichini S, Stanzani Maserati M, Marano G, Sambati L (2010) Are subjective cognitive complaints a risk factor for dementia? NeurolSci 31:327–336. https://doi.org/10.1007/s10072-010-0224-6 CrossRef

American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, Fifth Edition (DSM-5). American Psychiatric Association, Arlington

Petersen RC, Caracciolo B, Brayne C, Gauthier S, Jelic V, Fratiglioni L (2014) Mild cognitive impairment: a concept in evolution. J Intern Med 275(3):214–228. https://doi.org/10.1111/joim.12190 CrossRefPubMedPubMedCentral

Cooper C, Li R, Lyketsos C, Livingston G (2013) Treatment for mild cognitive impairment: systematic review. Br J Psychiatry 203(3):255–264. https://doi.org/10.1192/bjp.bp.113.127811 CrossRefPubMedPubMedCentral

10.

Doody RS, Ferris SH, Salloway S, Sun Y, Goldman R, Watkins WE, Xu Y, Murthy AK (2009) Donepezil treatment of patients with MCI: a 48-week randomized, placebo-controlled trial. Neurology 72(18):1555Y1561. https://doi.org/10.1212/01.wnl.0000344650.95823.03 CrossRef

11.

Feldman HH, Ferris S, Winblad B, Sfikas N, Mancione L, He Y, Tekin S, Burns A, Cummings J, del Ser T, Inzitari D, Orgogozo JM, Sauer H, Scheltens P, Scarpini E, Herrmann N, Farlow M, Potkin S, Charles HC, Fox NC, Lane R (2007) Effect of rivastigmine on delay to diagnosis of Alzheimer’s disease from mild cognitive impairment: the InDDEx study. Lancet Neurol 6(6):501Y512. https://doi.org/10.1016/S1474-4422(07)70109-6 CrossRef

12.

Lautenschlager NT, Cox KL, Flicker L, Foster JK, van Bockxmeer FM, Xiao J, Greenop KR, Almeida OP (2008) Effect of physical activity on cognitive function in older adults at risk for Alzheimer disease: a randomized trial. JAMA 300(9):1027Y1037. https://doi.org/10.1001/jama.300.9.1027 CrossRef

13.

Petersen RC, Thomas RG, Grundman M, Bennett D, Doody R, Ferris S, Galasko D, Jin S, Kaye J, Levey A, Pfeiffer E, Sano M, van Dyck CH, Thal LJ, Alzheimer’s Disease Cooperative Study Group (2005) Vitamin E and donepezil for the treatment of mild cognitive impairment. N Engl J Med 352(23):2379Y2388. https://doi.org/10.1056/NEJMoa050151 CrossRef

14.

Thal LJ, Ferris SH, Kirby L et al (2005) A randomized,double-blind, study of rofecoxib in patients with mild cognitive impairment. Neuropsychopharmacology 30(6):1204Y1215. https://doi.org/10.1038/sj.npp.1300690 CrossRef

15.

Bikson M, Grossman P, Thomas C, Zannou AL, Jiang J, Adnan T, Mourdoukoutas AP, Kronberg G, Truong D, Boggio P, Brunoni AR, Charvet L, Fregni F, Fritsch B, Gillick B, Hamilton RH, Hampstead BM, Jankord R, Kirton A, Knotkova H, Liebetanz D, Liu A, Loo C, Nitsche MA, Reis J, Richardson JD, Rotenberg A, Turkeltaub PE, Woods AJ (2016) Safety of transcranial direct current stimulation: evidence based update 2016. Brain Stimul 9(5):641–661. https://doi.org/10.1016/j.brs.2016.06.004 CrossRefPubMedPubMedCentral

16.

Woods AJ, Antal A, Bikson M, Boggio PS, Brunoni AR, Celnik P, Cohen LG, Fregni F, Herrmann CS, Kappenman ES, Knotkova H, Liebetanz D, Miniussi C, Miranda PC, Paulus W, Priori A, Reato D, Stagg C, Wenderoth N, Nitsche MA (2016) A technical guide to tDCS, and related non-invasive brain stimulation tools. ClinNeurophysiol. 127(2):1031–1048. https://doi.org/10.1016/j.clinph.2015.11.012 CrossRef

17.

Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527(Pt 3):633–639. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00633.x CrossRefPubMedPubMedCentral

18.

Jamil A, Batsikadze G, Kuo HI, Labruna L, Hasan A, Paulus W, Nitsche MA (2017) Systematic evaluation of the impact of stimulation intensity on neuroplastic after-effects induced by transcranial direct current stimulation. J Physiol 595(4):1273–1288. Published online 2016 Nov 8. https://doi.org/10.1113/JP272738 CrossRefPubMed

19.

Antal A, Nitsche MA, Kruse W, Kincses TZ, Hoffmann K-P, Paulus W (2004) Direct current stimulation over V5 enhances visuomotor coordination by improving motion perception in humans. J Cogn Neurosci 16:521–527CrossRefPubMed

20.

Fertonani A, Rosini S, Cotelli M, Rossini MP, Miniussi C (2010) Naming facilitation induced by transcranial direct current stimulation. Behav Brain Res 208:311–318CrossRefPubMed

21.

Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E, Celnik PA, Krakauer JW (2009) Non invasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci U S A 106:1590–1595CrossRefPubMedPubMedCentral

22.

Zaehle T, Sandmann P, Thorne J, Jäncke L, Herrmann C (2011) Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: combined behavioural and electrophysiological evidence. BMC Neurosci 12:2CrossRefPubMedPubMedCentral

23.

Ferrucci R, Mameli F, Guidi I, Mrakic-Sposta S, Vergari M, Marceglia S, Cogiamanian F, Barbieri S, Scarpini E, Priori A (2008) Transcranial direct current stimulation improves recognition memory in Alzheimer disease. Neurology. 71(7):493–498. https://doi.org/10.1212/01.wnl.0000317060.43722.a3 CrossRefPubMed

24.

Loo CK, Alonzo A, Martin D, Mitchell PB, Galvez V, Sachdev P (2012) Transcranial direct current stimulation for depression: 3-week, randomised,sham-controlled trial. Br J Psychiatry 200:52–59CrossRefPubMed

25.

Meinzer M, Lindenberg R, Phan MT, Ulm L, Volk C, Floel A (2014) Transcranial direct current stimulation in mild cognitive impairment: Behavioral effects and neural mechanisms. Alzheimers Dement 1–9. https://doi.org/10.1016/j.jalz.2014.07.159

26.

Liu CS, Rau A, Gallagher D, Rajji TK, Krista L, Lancto T, Herrmann N Using transcranial direct current stimulation to treat symptoms in mild cognitive impairment and Alzheimer’s disease. Neurodegener Dis Manag. Published online: 18 October 2017. https://doi.org/10.2217/nmt-2017-0021

27.

Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, Snyder PJ, Carrillo MC, Thies B, Phelps CH et al (2011) Alzheimers Dement 7(3):270Y279. https://doi.org/10.1016/j.jalz.2011.03.008 CrossRef

28.

Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198. https://doi.org/10.1016/0022-3956(75)90026-6 CrossRefPubMed

29.

Measso G, Cavarzeran F, Zappalà G et al (1993) The Mini-Mental State Examination: normative study of an Italian random sample. Dev Neuropsychol 9:77–85CrossRef

30.

Gallassi R, Lenzi P, Stracciari A, Lorusso S, Ciardulli C, Morreale A, Mussuto V (1986) Neuropsychological assessment of mental deterioration: purpose of a brief battery and a probabilistic definition of ‘normality’ and ‘non normality’. Acta Psychiatr Scand 75:62–67CrossRef

31.

Carlesimo GA, Caltagirone C, Gainotti G (1996) The Mental Deterioration Battery: normative data, diagnostic reliabilityand qualitative analyses of cognitive impairment. The Group for the Standardization of the Mental Deterioration Battery. Eur Neurol 36(6):378–384CrossRefPubMed

32.

Gallassi R, Morreale A, Di Sarro R, Lorusso S (2002) Value of clinical data and neuropsychological measures in probable Alzheimer’s disease. Arch Gerontol Geriatr 34(2):123–134CrossRefPubMed

33.

Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A (2002) Una versione abbreviata del test di Stroop: Dati normativi nella popolazione Italiana. Nuova Riv Neurol 12(4):111–115

34.

Novelli G, Papagno C, Capitani E et al (1986) Tre test clinici di ricerca e produzione lessicale. Taratura su soggetti normali. Arch Psicol Neurol Psichiatr 47:279–296

35.

Cavalli M, De Renzi E, Faglioni P, Vitale A (1981) Impairment of right brain-damaged patients on a linguistic cognitive task. Cortex 17(4):545–555

36.

Laiacona M, Barbarotto R, Trivelli C, Capitani E (1993) Dissociazioni semantiche intercategoriali: descrizione di una batteria standardizzata e dati normativi [category specific semantic defects: a standardised test with normative data]. Arch Psicol Neurol Psichiatr 54(2):209–248

37.

Snodgrass JG, Vanderwart M (1980) A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. J Exp Psychol Hum Learn 6(2):174–215CrossRefPubMed

38.

Spielberger CD, Vagg PR, Barker LR et al (1980) The factor structure of the State-Trait Anxiety Inventory. In: Sarason IG, Spielberger CD (eds) Stress and anxiety. Hemisphere/Wiley, New York, pp 95–109

39.

Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 45:561–571CrossRef

40.

Yun K, Songand I-U, Chung Y-A (2016) Changes in cerebral glucose metabolism after 3 weeks of noninvasive electrical stimulation of mild cognitive impairmentpatients. Alzheimers Res Ther 8:49. https://doi.org/10.1186/s13195-016-0218-6 CrossRefPubMedPubMedCentral

41.

Tatti E, Rossi S, Innocenti I, Rossi A, Santarnecchi E (2016) Non-invasive brain stimulation of the aging brain: state of the art and future perspectives. Ageing Res Rev 29:66–89. https://doi.org/10.1016/j.arr.2016.05.006 CrossRefPubMed

42.

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. Front Aging Neurosci 5:1–9. https://doi.org/10.3389/fnagi.2013.00049 CrossRef

43.

Sandrini M, Brambilla M, Manenti R, Rosini S, Cohen LG, Cotelli M (2014) Noninvasive stimulation of prefrontal cortex strengthens existing episodic memories and reduces forgetting in the elderly. Front Aging Neurosci 6:289. https://doi.org/10.3389/fnagi.2014.00289 CrossRefPubMedPubMedCentral

44.

Manor B, Zhou J, Jor’dan A, Zhang J, Fang J, Pascual-Leone A (2016) Reduction of dual-task costs by noninvasive modulation of prefrontal activity in healthy elders. J Cogn Neurosci 28:275–281. https://doi.org/10.1162/jocn_a_00897 CrossRefPubMed

45.

Kim SH, Han HJ, Ahn HM, Kim SA, Kim SE (2012) Effects of five daily high frequency rTMS on Stroop task performance in aging individuals. Neurosci Res 74:256–260. https://doi.org/10.1016/j.neures.2012.08.008 CrossRefPubMed

46.

Fisk JE, Sharp CA (2004) Age-related impairment in executive functioning: updating, inhibition, shifting, and access. J Clin Exp Neuropsychol 26(7):874Y890. https://doi.org/10.1080/13803390490510680 CrossRef

47.

Rabinovici GD, Stephens ML, Possin KL (2015) Executive dysfunction. Continuum (Minneap Minn) 21(3):646–659

48.

Gallassi R, Sambati L, Stanzani Maserati M, Poda R, Oppi F, De Matteis M, Marano G (2014) Simple verbal analogies test: normative data on a short task exploring abstract thinking. Aging Clin Exp Res 26:67–71. https://doi.org/10.1007/s40520-013-0180-0 CrossRefPubMed

49.

Milev RV, Giacobbe P, Kennedy SH, Blumberger DM, Daskalakis ZJ, Downar J, Modirrousta M, Patry S, Vila-Rodriguez F, Lam RW, MacQueen GM, Parikh SV, Ravindran AV, CANMAT Depression Work Group (2016) Canadian Network for Mood and Anxiety Treatments (CANMAT) 2016 clinical guidelines for the management of adults with major depressive disorder: section 4. Neurostimulation treatments. Can J Psychiatr 61(9):561–575. https://doi.org/10.1177/0706743716660033 CrossRef

50.

Matthews BR (2015) Memory dysfunction. Continuum (Minneap Minn) 21(3):613–626

51.

Mariano TY, Van’t Wout M, Garnaat SL, Rasmussen SA, Greenberg BD (2016) Transcranial direct current stimulation (tDCS) targeting left dorsolateral prefrontal cortex modulates task-induced acute pain in healthy volunteers. Pain Med 17(4):737–745. https://doi.org/10.1093/pm/pnv042 CrossRefPubMed

52.

Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, Henning S, Tergau F, Paulus W (2003) Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 553:293–301CrossRefPubMedPubMedCentral

53.

Stagg CJ, Nitsche MA (2011) Physiological basis of transcranial direct current stimulation. Neuroscientist 17:37–53CrossRefPubMed

54.

Liebetanz D, Nitsche MA, Tergau F, Paulus W (2002) Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain J Neurol 125:2238–2247CrossRef

55.

Stafford J, Brownlow ML, Qualley A, Jankord R (2018) AMPA receptor translocation and phosphorylation are induced by transcranial direct current stimulation in rats. Neurobiology of Learning and Memory. Available online 11 November 2017 In Press, Accepted Manuscript https://doi.org/10.1016/j.nlm.2017.11.002,

56.

Mull BR, Seyal M (2001) Transcranial magnetic stimulation of left prefrontal cortex impairs working memory. Clin Neurophysiol 112:1672–1675CrossRefPubMed

57.

Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science. 313(5790):1093–1097CrossRefPubMed

58.

de Aguiar V, Paolazzi C, Miceli G (2015) tDCS in post-stroke aphasia: the role of stimulation parameters, behavioral treatment and patient characteristics. Cortex. 63:296–316. https://doi.org/10.1016/j.cortex.2014.08.015 CrossRefPubMed

59.

Elsner B, Kugler J, Pohl M, Mehrholz J (2015) Transcranial direct current stimulation (tDCS) for improving aphasia in patients with aphasia after stroke. Cochrane Database Syst Rev 5:CD009760. https://doi.org/10.1002/14651858.CD009760.pub3 CrossRef

Title: Effects on cognition of 20-day anodal transcranial direct current stimulation over the left dorsolateral prefrontal cortex in patients affected by mild cognitive impairment: a case-control study
Authors: Enrico Fileccia
Vitantonio Di Stasi
Roberto Poda
Giovanni Rizzo
Michelangelo Stanzani-Maserati
Federico Oppi
Patrizia Avoni
Sabina Capellari
Rocco Liguori
Publication date: 01-09-2019
Publisher: Springer International Publishing
Keyword: Mild Cognitive Impairment
Published in: Neurological Sciences / Issue 9/2019
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-019-03903-6

At a glance: The STEP trials

Springer Medicine

Effects on cognition of 20-day anodal transcranial direct current stimulation over the left dorsolateral prefrontal cortex in patients affected by mild cognitive impairment: a case-control study

Abstract

Background

Objective/hypothesis

Methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Objective/hypothesis

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 9/2019

Highlights of the issue 9, 2019

Hypertension, seizures, and epilepsy: a review on pathophysiology and management

BDNF Val66Met polymorphism and cognitive impairment in Parkinson’s disease—a meta-analysis

Cerebral lipiodol embolism after transarterial hepatic chemoembolization studied with susceptibility-weighted imaging

Continuous subcutaneous apomorphine infusion in Parkinson’s disease: causes of discontinuation and subsequent treatment strategies

Gender and thrombolysis therapy in acute ischemic stroke patients with incidence of obesity