Enhancing verbal episodic memory in older and young subjects after non-invasive brain stimulation

Frontiers in Aging Neuroscience

Volumn 5, Issue SEP, 2013, Pages

  Manenti, Rosa ^a   Brambilla, Michela ^a,b   Petesi, Michela ^a   Ferrari, Clarissa ^a   Cotelli, Maria ^a  

^a IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Aging; Dorsolateral prefrontal cortex; Parietal cortex; TDCS; Verbal retrieval

Indexed keywords

ADULT; ARTICLE; ATTENTION; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTRODE; EPISODIC MEMORY; EXECUTIVE FUNCTION; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; NERVE STIMULATOR; NEUROPSYCHOLOGICAL TEST; NON INVASIVE PROCEDURE; NORMAL HUMAN; PARIETAL CORTEX; PREFRONTAL CORTEX; RANDOMIZED CONTROLLED TRIAL; SENSATION; TASK PERFORMANCE; TRANSCRANIAL DIRECT CURRENT STIMULATION; VERBAL MEMORY; YOUNG ADULT;

EID: 84895789074     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2013.00049     Document Type: Article

References (77)

1. Balota, D. A., Dolan, P. O., and Duchek, J. M. (2000). "Memory changes in healthy young and older adults," in Handbook of Memory, eds E. Tulving and F. I. M. Craik (New York: Oxford University Press), 395-410.
2. Berryhill, M. E. (2012). Insights from neuropsychology: pinpointing the role of the posterior parietal cortex in episodic and working memory. Front. Integr. Neurosci. 6:31. doi: 10.3389/fnint.2012.00031.
3. Berryhill, M. E., and Jones, K. T. (2012). tDCS selectively improves working memory in older adults with more education. Neurosci. Lett. 521, 148-151. doi: 10.1016/j.neulet.2012.05.074.
4. Bertinetto, P. M., Burani, C., Laudanna, A., Marconi, L., Ratti, D., Rolando, C., et al. (2005). Corpus e Lessico di Frequenza dell'Italiano Scritto (CoLFIS). Available at: http://linguistica.sns.it/CoLFIS/Home.htm.
5. Binder, J. R., Westbury, C. F., McKiernan, K. A., Possing, E. T., and Medler, D. A. (2005). Distinct brain systems for processing concrete and abstract concepts. J. Cogn. Neurosci. 17, 905-917. doi: 10.1162/0898929054021102.
6. Boggio, P. S., Ferrucci, R., Mameli, F., Martins, D., Martins, O., Vergari, M., et al. (2012). Prolonged visual memory enhancement after direct current stimulation in Alzheimer's disease. Brain Stimul. 5, 223-230. doi: 10.1016/j.brs.2011.06.006.
7. Boggio, P. S., Fregni, F., Valasek, C., Ellwood, S., Chi, R., Gallate, J., et al. (2009a). Temporal lobe cortical electrical stimulation during the encoding and retrieval phase reduces false memories. PLoS ONE 4:e4959. doi: 10.1371/journal.pone.0004959.
8. Boggio, P. S., Khoury, L. P., Martins, D. C., Martins, O. E., de Macedo, E. C., and Fregni, F. (2009b). Temporal cortex direct current stimulation enhances performance on a visual recognition memory task in Alzheimer disease. J. Neurol. Neurosurg. Psychiatry 80, 444-447. doi: 10.1136/jnnp.2007.141853.
9. Boggio, P. S., Valasek, C. A., Campanha, C., Giglio, A. C., Baptista, N. I., Lapenta, O. M., et al. (2011). Non-invasive brain stimulation to assess and modulate neuroplasticity in Alzheimer's disease. Neuropsychol. Rehabil. 21, 703-716. doi: 10.1080/09602011.2011.617943.
10. Buckner, R. L., Wheeler, M. E., and Sheridan, M. A. (2001). Encoding processes during retrieval tasks. J. Cogn. Neurosci. 13, 406-415. doi: 10.1162/08989290151137430.
11. Burke, S. N., and Barnes, C. A. (2006). Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 7, 30-40. doi: 10.1038/nrn1809.
12. Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 17, 85-100. doi: 10.1037/0882-7974.17.1.85.
13. Cabeza, R., Ciaramelli, E., Olson, I. R., and Moscovitch, M. (2008). The parietal cortex and episodic memory: an attentional account. Nat. Rev. Neurosci. 9, 613-625. doi: 10.1038/nrn2459.
14. Cabeza, R., Grady, C. L., Nyberg, L., McIntosh, A. R., Tulving, E., Kapur, S., et al. (1997). Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. J. Neurosci. 17, 391-400.
15. Cabeza, R., Locantore, J. K., and Anderson, N. D. (2003). Lateralization of prefrontal activity during episodic memory retrieval: evidence for the production-monitoring hypothesis. J. Cogn. Neurosci. 15, 249-259. doi: 10.1162/089892903321208187.
16. Cabeza, R., and Nyberg, L. (2003). Functional neuroimaging of memory. Neuropsychologia 41, 241-244. doi: 10.1016/S0028-3932(02)00156-2.
17. Chi, R. P., Fregni, F., and Snyder, A. W. (2010). Visual memory improved by non-invasive brain stimulation. Brain Res. 1353, 168-175. doi: 10.1016/j.brainres.2010.07.062.
18. Cooke, S. F., and Bliss, T. V. (2006). Plasticity in the human central nervous system. Brain 129, 1659-1673. doi: 10.1093/brain/awl082.
19. Cotelli, M., Manenti, R., Brambilla, M., Zanetti, O., and Miniussi, C. (2012). Naming ability changes in physiological and pathological aging. Front. Neurosci. 6:120. doi: 10.3389/fnins.2012.00120.
20. Cotelli, M., Manenti, R., Rosini, S., Calabria, M., Brambilla, M., Bisiacchi, P. S., et al. (2010). Action and object naming in physiological aging: an rTMS study. Front. Aging Neurosci. 2:151. doi: 10.3389/fnagi.2010.00151.
21. Creasey, H., and Rapoport, S. I. (1985). The aging human brain. Ann. Neurol. 17, 2-10. doi: 10.1002/ana.410170103.
22. Dayan, E., Censor, N., Buch, E. R., Sandrini, M., and Cohen, L. G. (2013). Noninvasive brain stimulation: from physiology to network dynamics and back. Nat. Neurosci. 16, 838-844. doi: 10.1038/nn.3422.
23. De Renzi, E., Motti, F., and Nichelli, P. (1980). Imitating gestures. A quantitative approach to ideomotor apraxia. Arch. Neurol. 37, 6-10. doi: 10.1001/archneur.1980.00500500036003.
24. Dror, I. E., and Kosslyn, S. M. (1994). Mental imagery and aging. Psychol. Aging 9, 90-102. doi: 10.1037/0882-7974.9.1.90.
25. Ferrucci, R., Mameli, F., Guidi, I., Mrakic-Sposta, S., Vergari, M., Marceglia, S., et al. (2008). Transcranial direct current stimulation improves recognition memory in Alzheimer disease. Neurology 71, 493-498. doi: 10.1212/01.wnl.0000317060.43722.a3.
26. Fertonani, A., Rosini, S., Cotelli, M., Rossini, P. M., and Miniussi, C. (2010). Naming facilitation induced by transcranial direct current stimulation. Behav. Brain Res. 208, 311-318. doi: 10.1016/j.bbr.2009.10.030.
27. Fiebach, C. J., and Friederici, A. D. (2004). Processing concrete words: fMRI evidence against a specific right-hemisphere involvement. Neuropsychologia 42, 62-70. doi: 10.1016/S0028-3932(03)00145-3.
28. Fletcher, P. C., and Henson, R. N. (2001). Frontal lobes and human memory: insights from functional neuroimaging. Brain 124, 849-881. doi: 10.1093/brain/124.5.849.
29. Fletcher, P. C., Shallice, T., Frith, C. D., Frackowiak, R. S., and Dolan, R. J. (1998). The functional roles of prefrontal cortex in episodic memory. II. Retrieval. Brain 121(Pt 7), 1249-1256. doi: 10.1093/brain/121.7.1249.
30. Floel, A., Suttorp, W., Kohl, O., Kurten, J., Lohmann, H., Breitenstein, C., et al. (2012). Non-invasive brain stimulation improves object-location learning in the elderly. Neurobiol. Aging 33, 1682-1689. doi: 10.1016/j.neurobiolaging.2011.05.007.
31. Folstein, M. F., Folstein, S. E., and McHugh, P. R. (1975). "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189-198. doi: 10.1016/0022-3956(75)90026-6.
32. Goh, J. O., Suzuki, A., and Park, D. C. (2010). Reduced neural selectivity increases fMRI adaptation with age during face discrimination. Neuroimage 51, 336-344. doi: 10.1016/j.neuroimage.2010.01.107.
33. Golby, A. J., Poldrack, R. A., Brewer, J. B., Spencer, D., Desmond, J. E., Aron, A. P., et al. (2001). Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain 124, 1841-1854. doi: 10.1093/brain/124.9.1841.
34. Grady, C. L., McIntosh, A. R., Horwitz, B., Maisog, J. M., Ungerleider, L. G., Mentis, M. J., et al. (1995). Age-related reductions in human recognition memory due to impaired encoding. Science 269, 218-221. doi: 10.1126/science.7618082.
35. Greenwood, P. M. (2007). Functional plasticity in cognitive aging: review and hypothesis. Neuropsychology 21, 657-673. doi: 10.1037/0894-4105.21.6.657.
36. Hardin, J., and Hilbe, J. (2003). Generalized Estimating Equation. London: CRC Press.
37. Jacobson, L., Goren, N., Lavidor, M., and Levy, D. A. (2013). Oppositional transcranial direct current stimulation (tDCS) of parietal substrates of attention during encoding modulates episodic memory. Brain Res. 1439, 66-72. doi: 10.1016/j.brainres.2011.12.036.
38. Jancke, L. (2009). The plastic human brain. Restor. Neurol. Neurosci. 27, 521-538. doi: 10.3233/RNN-2009-0519.
39. Javadi, A. H., and Cheng, P. (2012). Transcranial direct current stimulation (tDCS) enhances reconsolidation of long-term memory. Brain Stimul. 6, 667-674. doi: 10.1016/j.brs.2012.10.007.
40. Javadi, A. H., Cheng, P., and Walsh, V. (2012). Short duration transcranial direct current stimulation (tDCS) modulates verbal memory. Brain Stimul. 5, 468-474. doi: 10.1016/j.brs.2011.08.003.
41. Javadi, A. H., and Walsh, V. (2012). Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory. Brain Stimul. 5, 231-241. doi: 10.1016/j.brs.2011.06.007.
42. Johnson, S. H., and Rybash, J. M. (1993). "A cognitive neuroscience perspective on age-related slowing: developmental changes in the functional architecture," in Adult Information Processing: Limits and Loss, eds J. Cerella, J. Rybash, W. Hoyer, and M. L. Commons (New York: Academic Press), 143-173.
43. Kapur, S., Tulving, E., Cabeza, R., McIntosh, A. R., Houle, S., and Craik, F. I. (1996). The neural correlates of intentional learning of verbal materials: a PET study in humans. Brain Res. Cogn. Brain Res. 4, 243-249. doi: 10.1016/S0926-6410(96)00058-4.
44. Kiefer, M., and Pulvermuller, F. (2012). Conceptual representations in mind and brain: theoretical developments, current evidence and future directions. Cortex 48, 805-825. doi: 10.1016/j.cortex.2011.04.006.
45. Kiehl, K. A., Liddle, P. F., Smith, A. M., Mendrek, A., Forster, B. B., and Hare, R. D. (1999). Neural pathways involved in the processing of concrete and abstract words. Hum. Brain Mapp. 7, 225-233. doi: 10.1002/(SICI)1097-0193(1999)7:4.
46. Klostermann, E. C., Kane, A. J., and Shimamura, A. P. (2008). Parietal activation during retrieval of abstract and concrete auditory information. Neuroimage 40, 896-901. doi: 10.1016/j.neuroimage.2007.10.068.
47. Laudanna, A., Thornton, A. M., Brown, G., Burani, C., and Marconi, L. (1995). "Un corpus dell'italiano scritto contemporaneo dalla parte del ricevente," in III Giornate Internazionali di Analisi Statistica dei Dati Testuali, Vol. I, eds S. Bolasco, L. Lebart, and A. Salem (Roma: Cisu), 103-109.
48. Lezak, M., Howieson, D., and Loring, D. W. (2004). Neuropsychological Assessment, 4th Edn. New York: Oxford University Press.
49. Macmillan, N. A., and Creelman, C. D. (2005). Detection Theory: A User's Guide. Mahwah, NJ: Lawrence Erlbaum Associates.
50. Manenti, R., Cotelli, M., and Miniussi, C. (2011). Successful physiological aging and episodic memory: a brain stimulation study. Behav. Brain Res. 216, 153-158. doi: 10.1016/j.bbr.2010.07.027.
51. Manenti, R., Tettamanti, M., Cotelli, M., Miniussi, C., and Cappa, S. F. (2010). The neural bases of word encoding and retrieval: a fMRI-guided transcranial magnetic stimulation study. Brain Topogr. 22, 318-332. doi: 10.1007/s10548-009-0126-1.
52. 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. doi: 10.1016/j.brs.2008.06.004.
53. Nitsche, M. A., Liebetanz, D., Lang, N., Antal, A., Tergau, F., and Paulus, W. (2003a). Safety criteria for transcranial direct current stimulation (tDCS) in humans. Clin. Neurophysiol. 114, 2220-2222; author reply 2222-2223. doi: 10.1016/S1388-2457(03)00235-9.
54. Nitsche, M. A., Schauenburg, A., Lang, N., Liebetanz, D., Exner, C., Paulus, W., et al. (2003b). Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J. Cogn. Neurosci. 15, 619-626. doi: 10.1162/089892903321662994.
55. Nitsche, M. A., and Paulus, W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 527(Pt 3), 633-639. doi: 10.1111/j.1469-7793.2000.t01-1-00633.x.
56. Nitsche, M. A., and Paulus, W. (2001). Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57, 1899-1901. doi: 10.1212/WNL.57.10.1899.
57. Nyberg, L., Persson, J., Habib, R., Tulving, E., McIntosh, A. R., Cabeza, R., et al. (2000). Large scale neurocognitive networks underlying episodic memory. J. Cogn. Neurosci. 12, 163-173. doi: 10.1162/089892900561805.
58. Park, D. C., Polk, T. A., Park, R., Minear, M., Savage, A., and Smith, M. R. (2004). Aging reduces neural specialization in ventral visual cortex. Proc. Natl. Acad. Sci. U.S.A. 101, 13091-13095. doi: 10.1073/pnas.0405148101.
59. Park, D. C., and Reuter-Lorenz, P. (2009). The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 60, 173-196. doi: 10.1146/annurev.psych.59.103006.093656.
60. Penolazzi, B., Di Domenico, A., Marzoli, D., Mammarella, N., Fairfield, B., Franciotti, R., et al. (2010). Effects of transcranial direct current stimulation on episodic memory related to emotional visual stimuli. PLoS ONE 5:e10623. doi: 10.1371/journal.pone.0010623.
61. Poldrack, R. A., Wagner, A. D., Prull, M. W., Desmond, J. E., Glover, G. H., and Gabrieli, J. D. (1999). Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex. Neuroimage 10, 15-35. doi: 10.1006/nimg.1999.0441.
62. Poreisz, C., Boros, K., Antal, A., and Paulus, W. (2007). Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res. Bull. 72, 208-214. doi: 10.1016/j.brainresbull.2007.01.004.
63. Priori, A. (2003). Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability. Clin. Neurophysiol. 114, 589-595. doi: 10.1016/S1388-2457(02)00437-6.
64. Rodriguez-Ferreiro, J., Gennari, S. P., Davies, R., and Cuetos, F. (2011). Neural correlates of abstract verb processing. J. Cogn. Neurosci. 23, 106-118. doi: 10.1162/jocn.2010.21414.
65. Rugg, M. D., and Wilding, E. L. (2000). Retrieval processing and episodic memory. Trends Cogn. Sci. 4, 108-115. doi: 10.1016/S1364-6613(00)01445-5.
66. Sabsevitz, D. S., Medler, D. A., Seidenberg, M., and Binder, J. R. (2005). Modulation of the semantic system by word imageability. Neuroimage 27, 188-200. doi: 10.1016/j.neuroimage.2005.04.012.
67. Schacter, D. L., Savage, C. R., Alpert, N. M., Rauch, S. L., and Albert, M. S. (1996). The role of hippocampus and frontal cortex in age-related memory changes: a PET study. Neuroreport 7, 1165-1169. doi: 10.1097/00001756-199604260-00014.
68. Simons, J. S., and Spiers, H. J. (2003). Prefrontal and medial temporal lobe interactions in long-term memory. Nat. Rev. Neurosci. 4, 637-648. doi: 10.1038/nrn1178.
69. Spaniol, J., Davidson, P. S., Kim, A. S., Han, H., Moscovitch, M., and Grady, C. L. (2009). Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia 47, 1765-1779. doi: 10.1016/j.neuropsychologia.2009.02.028.
70. Spencer, W. D., and Raz, N. (1995). Differential effects of aging on memory for content and context: a meta-analysis. Psychol. Aging 10, 527-539. doi: 10.1037/0882-7974.10.4.527.
71. Thickbroom, G. W. (2007). Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp. Brain Res. 180, 583-593. doi: 10.1007/s00221-007-0991-3.
72. Tulving, E. (1983). Elements of Episodic Memory. London: Oxford University Press.
73. Tulving, E., Kapur, S., Craik, F. I., Moscovitch, M., and Houle, S. (1994). Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc. Natl. Acad. Sci. U.S.A. 91, 1989-1991. doi: 10.1073/pnas.91.6.2016.
74. Wagner, A. D., Poldrack, R. A., Eldridge, L. L., Desmond, J. E., Glover, G. H., and Gabrieli, J. D. (1998). Material-specific lateralization of prefrontal activation during episodic encoding and retrieval. Neuroreport 9, 3711-3717. doi: 10.1097/00001756-199811160-00026.
75. Ziemann, U., and Siebner, H. R. (2008). Modifying motor learning through gating and homeostatic metaplasticity. Brain Stimul. 1, 60-66. doi: 10.1016/j.brs.2007.08.003.
76. Zimerman, M., Nitsch, M., Giraux, P., Gerloff, C., Cohen, L. G., and Hummel, F. C. (2013). Neuroenhancement of the aging brain: restoring skill acquisition in old subjects. Ann. Neurol. 73, 10-15. doi: 10.1002/ana.23761.
77. Zollig, J., and Eschen, A. (2009). Measuring compensation and its plasticity across the lifespan. Restor. Neurol. Neurosci. 27, 421-433. doi: 10.3233/RNN-2009-0513.