Modulating memory performance in healthy subjects with transcranial direct current stimulation over the right dorsolateral prefrontal cortex

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Smirni, Daniela ^a,b   Turriziani, Patrizia ^a,b   Mangano, Giuseppa Renata ^a,b   Cipolotti, Lisa ^a,b,c   Oliveri, Massimiliano ^a,b,d  

^a UNIVERSITY OF PALERMO   (Italy)

^b NeuroTeam Life and Science   (Italy)

^c NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^d IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CLINICAL ARTICLE; DORSOLATERAL PREFRONTAL CORTEX; FACILITATION; HUMAN; LONG TERM MEMORY; MEMORY; MEMORY TEST; RECOGNITION; TRANSCRANIAL DIRECT CURRENT STIMULATION; ADULT; CONTROLLED STUDY; FEMALE; MALE; PHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES; RANDOMIZED CONTROLLED TRIAL; REACTION TIME; YOUNG ADULT;

ADULT; FEMALE; HUMANS; MALE; MEMORY; PREFRONTAL CORTEX; REACTION TIME; RECOGNITION (PSYCHOLOGY); TRANSCRANIAL DIRECT CURRENT STIMULATION; YOUNG ADULT;

EID: 84956692779     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0144838     Document Type: Article

References (63)

1. Ball K, Berch DB, Helmers KF, Jobe JB, Leveck MD, Marsiske M, et al. Effects of cognitive training interventions with older adults: A randomized controlled trial. JAMA. 2002 Nov 13; 288(18):2271-81. PMID: 12425704
2. Willis SL, Tennstedt SL, Marsiske M, Ball K, Elias J, Koepke KM, et al. Long-term effects of cognitive training on everyday functional outcomes in older adults. JAMA. 2006 Dec 20; 296(23):2805-14. PMID: 17179457
3. Acevedo A, Loewenstein DA. Nonpharmacological cognitive interventions in aging and dementia. J Geriatr Psychiatry Neurol. 2007 Dec; 20(4):239-49. Review PMID: 18004010
4. Boggio PS, Fregni F, Valasek C, Ellwood S, Chi R, Gallate J, et al. Temporal lobe cortical electrical stimulation during the encoding and retrieval phase reduces false memories. PLoS One. 2009; 4(3): E4959. doi: 10.1371/journal.pone.0004959 PMID: 19319182
5. Chi RP, Fregni F, Snyder AW. Visual memory improved by non-invasive brain stimulation. Brain Res. 2010 Sep 24; 1353:168-75 doi: 10.1016/j.brainres.2010.07.062 PMID: 20682299
6. Penolazzi B, Di Domenico A, Marzoli D, Mammarella N, Fairfield B, Franciotti R, Brancucci A, Tommasi L. Effects of Transcranial Direct Current Stimulation on episodic memory related to emotional visual stimuli. PLoS One. 2010 May 13; 5(5):e10623. doi: 10.1371/journal.pone.0010623 PMID: 20498700
7. Javadi AH, Cheng P. Transcranial direct current stimulation (tDCS) enhances reconsolidation of longterm memory. Brain Stimul. 2013 Jul; 6(4):668-74. doi: 10.1016/j.brs.2012.10.007 PMID: 23137702
8. Javadi AH, Walsh V. Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory. Brain Stimul. 2012 Jul; 5(3):231-41. doi: 10.1016/j.brs.2011.06. 007 PMID: 21840287
9. Javadi AH, Cheng P, Walsh V. Short duration transcranial direct current stimulation (tDCS) modulates verbal memory. Brain Stimul. 2012 Oct; 5(4):468-74. doi: 10.1016/j.brs.2011.08.003 PMID: 21962975
10. Jacobson TK, Howe MD, Schmidt B, Hinman JR, Escabí MA, Markus EJ. Hippocampal theta, gamma, and theta-gamma coupling: Effects of aging, environmental change, and cholinergic activation. J Neurophysiol. 2013 Apr; 109(7):1852-65. doi: 10.1152/jn.00409.2012 PMID: 23303862
11. Ferrucci R, Mameli F, Guidi I, Mrakic-Sposta S, Vergari M, Marceglia S et al. Transcranial direct current stimulation improves recognition memory in Alzheimer disease. Neurology. 2008 Aug 12; 71(7):493-8. doi: 10.1212/01.wnl.0000317060.43722.a3 PMID: 18525028
12. Boggio PS, Valasek CA, Campanhã C, Giglio AC, Baptista NI, Lapenta OM et al. Non-invasive brain stimulation to assess and modulate neuroplasticity in Alzheimer's disease. Neuropsychol Rehabil. 2011 Oct; 21(5):703-16. Review. doi: 10.1080/09602011.2011.617943 PMID: 21942868
13. Boggio PS, Ferrucci R, Mameli F, Martins D, Martins O, Vergari M, et al. Prolonged visual memory enhancement after direct current stimulation in Alzheimer's disease. Brain Stimul. 2012 Jul; 5(3):223-30. doi: 10.1016/j.brs.2011.06.006 PMID: 21840288
14. Hammer A, Mohammadi B, Schmicker M, Saliger S, Münte TF. Errorless and errorful learning modulated by transcranial direct current stimulation. BMC Neurosci. 2011 Jul 22; 12:72. doi: 10.1186/1471-2202-12-72 PMID: 21781298
15. Manenti R, Brambilla M, Petesi M, Ferrari C, Cotelli M.Enhancing verbal episodic memory in older and young subjects after non-invasive brain stimulation.Front Aging Neurosci. 2013 Sep 11; 5:49. doi: 10. 3389/fnagi.2013.00049 PMID: 24062685
16. Zwissler B, Sperber C, Aigeldinger S, Schindler S, Kissler J, Plewnia C. Shaping memory accuracy by left prefrontal transcranial direct current stimulation. J Neurosci. 2014 Mar 12; 34(11):4022-6. doi: 10. 1523/JNEUROSCI.5407-13.2014 PMID: 24623779
17. Simons JS, Spiers HJ. Prefrontal and medial temporal lobe interactions in long-term memory. Nat Rev Neurosci. 2003 Aug; 4(8):637-48. PMID: 12894239
18. Squire LR. Memory systems of the brain: A brief history and current perspective. Neurobiol Learn Mem. 2004 Nov; 82(3):171-7. Review. PMID: 15464402
19. Milner B, Corsi P, Leonard G. Frontal-lobe contribution to recency judgements. Neuropsychologia. 1991; 29(6):601-18. PMID: 1944864
20. Wagner AD, Desmond JE, Glover GH, Gabrieli JD. Prefrontal cortex and recognition memory. Functional-MRI evidence for context-dependent retrieval processes. Brain. 1998 Oct; 121(Pt 10):1985-2002. PMID: 9798751
21. McDermott KB, Buckner RL, Petersen SE, Kelley WM, Sanders AL. Set-and code-specific activation in frontal cortex: An fMRI study of encoding and retrieval of faces and words. J Cogn Neurosci. 1999 Nov; 11(6):631-40. PMID: 10601744
22. Turriziani P., Oliveri M., Salerno S., Costanzo F., Koch G., Caltagirone C. et al. Recognition memory and prefrontal cortex: Dissociating recollection and familiarity processes using rTMS. Behav. Neurol. 2008. 19, 23-27. PMID: 18413912
23. Turriziani P, Smirni D, Oliveri M, Semenza C, Cipolotti L. The role of the prefrontal cortex in familiarity and recollection processes during verbal and non-verbal recognition memory: An rTMS study. Neuroimage. 2010 Aug 1; 52(1):348-57. doi: 10.1016/j.neuroimage.2010.04.007 PMID: 20399276
24. Turriziani P, Smirni D, Zappalà G, Mangano GR, Oliveri M, Cipolotti L. Enhancing memory performance with rTMS in healthy subjects and individuals with Mild Cognitive Impairment: The role of the right dorsolateral prefrontal cortex. Front Hum Neurosci. 2012 Apr 10; 6:62. doi: 10.3389/fnhum.2012.00062 PMID: 22514525
25. Kirchhoff BA, Wagner AD, Maril A, Stern CE. Prefrontal-temporal circuitry for episodic encoding and subsequent memory. J Neurosci. 2000 Aug 15; 20(16):6173-80. PMID: 10934267
26. Buckner RL, Wheeler ME. The cognitive neuroscience of remembering. Nat Rev Neurosci. 2001 Sep; 2 (9):624-34. Review. PMID: 11533730
27. Fletcher PC, Henson RN. Frontal lobes and human memory: Insights from functional neuroimaging. Brain. 2001 May; 124(Pt 5):849-81. Review PMID: 11335690
28. Rossi S, Cappa SF, Babiloni C, Pasqualetti P, Miniussi C, Carducci F, Babiloni F, Rossini PM. Prefrontal cortex in long-term memory: An "interference" approach using magnetic stimulation. Nat Neurosci. 2001 Sep; 4(9):948-52.
29. Erratum in: Nat Neurosci 2002 Oct;5(10):1017. PMID: 11528428
30. Sandrini M, Cappa SF, Rossi S, Rossini PM, Miniussi C. The role of prefrontal cortex in verbal episodic memory: RTMS evidence. J Cogn Neurosci. 2003 Aug 15; 15(6):855-61. PMID: 14511538
31. Floel A, Poeppel D, Buffalo EA, Braun A, Wu CW, Seo HJ, Stefan K, Knecht S, Cohen LG. Prefrontal cortex asymmetry for memory encoding of words and abstract shapes. Cereb Cortex. 2004 Apr; 14 (4):404-9. PMID: 15028644
32. Tulving E, Kapur S, Craik FI, Moscovitch M, Houle S. Hemispheric encoding/retrieval asymmetry in episodic memory: Positron emission tomography findings. Proc Natl Acad Sci U S A. 1994 Mar 15; 91 (6):2016-20. Review. PMID: 8134342
33. Habib R, Nyberg L, Tulving E. Hemispheric asymmetries of memory: The HERA model revisited. Trends Cogn Sci. 2003 Jun; 7(6):241-245. PMID: 12804689
34. Spaniol J, Davidson PS, Kim AS, Han H, Moscovitch M, Grady CL. Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation. Neuropsychologia. 2009 Jul; 47(8-9):1765-79. doi: 10.1016/j.neuropsychologia.2009.02.028 PMID: 19428409
35. Aron AR, Robbins TW, Poldrack RA. Inhibition and the right inferior frontal cortex. Trends Cogn Sci. 2004 Apr; 8(4):170-7. Review. PMID: 15050513
36. Tomita H, Ohbayashi M, Nakahara K, Hasegawa I, Miyashita Y. Top-down signal from prefrontal cortex in executive control of memory retrieval. Nature. 1999 Oct 14; 401(6754):699-703. PMID: 10537108
37. Juan CH, Muggleton NG. Brain stimulation and inhibitory control. Brain Stimul. 2012 Apr; 5(2):63-9. doi: 10.1016/j.brs.2012.03.012 Epub 2012 Apr 3. PMID: 22494830
38. Smirni D, Turriziani P, Oliveri M, Smirni P, Cipolotti L. Standardizzazione di tre nuovi test di memoria di riconoscimento verbale e non verbale: Uno studio preliminare. G. I. P. 2010. 1, 227-245.
39. Warrington EK. Recognition Memory Test. 1984. Windsor, Berks: NFER-Nelson.
40. Warrington EK. The Camden Memory Tests. 1996. Hove, UK: Psychology Press.
41. Cipolotti L, Bird C, Good T, Macmanus D, Rudge P, Shallice T. Recollection and familiarity in dense hippocampal amnesia: A case study. Neuropsychologia 2006. 39, 151-172.
42. Cipolotti L, Husain M, Crinion J, Bird CM, Khan SS, Losseff N. et al. The role of the thalamus in amnesia: A tractography, high-resolution MRI and neuropsychological study. Neuropsychologia 2008. 46, 2745-2758. doi: 10.1016/j.neuropsychologia.2008.05.009 PMID: 18597798
43. Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001 Nov 27; 57(10):1899-901. PMID: 11723286
44. Gandiga PC, Hummel FC, Cohen LG. Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol. 2006 Apr; 117(4):845-50. PMID: 16427357
45. Kincses TZ, Antal A, Nitsche MA, Bartfai O, Paulus W. Facilitation of probabilistic classification learning by transcranial direct current stimulation of the prefrontal cortex in the human. Neuropsychologia. 2004; 42(1):113-117. PMID: 14615081
46. Manenti R, Cotelli M, Robertson IH, Miniussi C. Transcranial brain stimulation studies of episodic memory in young adults, elderly adults and individuals with memory dysfunction: A review. Brain Stimul. 2012 Apr; 5(2):103-9. Review doi: 10.1016/j.brs.2012.03.004 PMID: 22503472
47. Cotelli M, Manenti R, Brambilla M, Petesi M, Rosini S, Ferrari C et al. Anodal tDCS during face-name associations memory training in Alzheimer's patients. Front Aging Neurosci. 2014 Mar 19; 6:38. doi: 10. 3389/fnagi.2014.00038 PMID: 24678298
48. Kamida T, Kong S, Eshima N, Abe T, Fujiki M, Kobayashi H. Transcranial direct current stimulation decreases convulsions and spatial memory deficits following pilocarpine-induced status epilepticus in immature rats. Behav Brain Res. 2011 Feb 2; 217(1):99-103 doi: 10.1016/j.bbr.2010.08.050 PMID: 20826186
49. Pisoni A, Turi Z, Raithel A, Ambrus GG, Alekseichuk I, Schacht A, Paulus W, Antal A. Separating recognition processes of declarative memory via anodal tDCS: Boosting old item recognition by temporal and new item detection by parietal stimulation. PLoS One. 2015 Mar 27; 10(3).
50. Sandrini M, Censor N, Mishoe J, Cohen LG. Causal role of prefrontal cortex in strengthening of episodic memories through reconsolidation. Curr Biol. 2013 Nov 4; 23(21):2181-4 doi: 10.1016/j.cub.2013.08. 045 PMID: 24206845
51. Knoch D, Gianotti LR, Pascual-Leone A, Treyer V, Regard M, Hohmann M, Brugger P. Disruption of right prefrontal cortex by low-frequency repetitive transcranial magnetic stimulation induces risk-taking behavior. J Neurosci. 2006 Jun 14; 26(24):6469-72. PMID: 16775134
52. De Neys W, Vartanian O, Goel V.Smarter than we think: When our brains detect that we are biased. Psychol Sci. 2008 May; 19(5):483-9. doi: 10.1111/j.1467-9280.2008.02113.x PMID: 18466410
53. Penolazzi B, Stramaccia DF, Braga M, Mondini S, Galfano G.Human memory retrieval and inhibitory control in the brain: Beyond correlational evidence. J Neurosci. 2014 May 7; 34(19):6606-10. doi: 10. 1523/JNEUROSCI.0349-14.2014 PMID: 24806685
54. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J. Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS. Neuroimage. 2003 Nov; 20(3):1685-96. PMID: 14642478
55. Rounis E, Stephan KE, Lee L, Siebner HR, Pesenti A, Friston KJ et al. Acute changes in frontoparietal activity after repetitive transcranial magnetic stimulation over the dorsolateral prefrontal cortex in a cued reaction time task. J Neurosci. 2006 Sep 20; 26(38):9629-38. PMID: 16988033
56. Bilek E, Schäfer A, Ochs E, Esslinger C, Zangl M, Plichta MM, et al. Application of high-frequency repetitive transcranial magnetic stimulation to the DLPFC alters human prefrontal-hippocampal functional interaction. J Neurosci. 2013 Apr 17; 33(16):7050-6. doi: 10.1523/JNEUROSCI.3081-12.2013 PMID: 23595762
57. Kelly A, Uddin LQ, Biswal BB, Castellanos FX, and Milham M. Competition between functional brain networks mediates behavioral variability. Neuroimage 2008; 39: 527-537. PMID: 17919929
58. Wermke M, Sorg C, Wohlschläger AM, Drzezga A. A new integrative model of cerebral activation, deactivation and default mode function in Alzheimer's disease. Eur J Nucl Med Mol Imaging. 2008 Mar; 35 Suppl 1:S12 doi: 10.1007/s00259-007-0698-5 PMID: 18299829
59. Jacobs HI, Dillen KN, Risius O, Göreci Y, Onur OA, Fink GR, Kukolja J. Consolidation in older adults depends upon competion between resting-state networks. Front Aging Neurosci. 2015 Jan 9; 6:344. doi: 10.3389/fnagi.2014.00344 PMID: 25620930
60. Van Kesteren MT, Fernández G, Norris DG, Hermans EJ. Persistent schema-dependent hippocampalneocortical connectivity during memory encoding and postencoding rest in humans. Proc Natl Acad Sci U S A. 2010 Apr 20; 107(16):7550-5. doi: 10.1073/pnas.0914892107 PMID: 20363957
61. Williams JA, Pascual-Leone A, Fregni F. Interhemispheric modulation induced by cortical stimulation and motor training. Phys Ther. 2010 Mar; 90(3):398-410. doi: 10.2522/ptj.20090075 PMID: 20110339
62. Oliveri M, Rossini PM, Traversa R, Cicinelli P, Filippi MM, Pasqualetti P, et al. Left frontal transcranial magnetic stimulation reduces contralesional extinction in patients with unilateral right brain damage. Brain. 1999 Sep; 122(Pt 9):1731-9. PMID: 10468512
63. Boggio PS, Ferrucci R, Rigonatti SP, Covre P, Nitsche M, Pascual-Leone A, et al. Effects of transcranial direct current stimulation on working memory in patients with Parkinson's disease. J Neurol Sci. 2006 Nov 1; 249(1):31-8. PMID: 16843494