Skip to main content
Top
Published in: Journal of Neural Transmission 3/2011

01-03-2011 | Dementias - Original Article

Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer’s disease: a proof of concept study

Authors: Jonathan Bentwich, Evgenia Dobronevsky, Sergio Aichenbaum, Ran Shorer, Ruth Peretz, Michael Khaigrekht, Revital Gandelman Marton, Jose M. Rabey

Published in: Journal of Neural Transmission | Issue 3/2011

Login to get access

Abstract

The current drug treatment for Alzheimer’s disease (AD) is only partially and temporary effective. Transcranial magnetic stimulation (TMS) is a non-invasive technique that generates an electric current inducing modulation in cortical excitability. In addition, cognitive training (COG) may improve cognitive functions in AD. Our aim was to treat AD patients combining high-frequency repetitive TMS interlaced with COG (rTMS-COG). Eight patients with probable AD, treated for more than 2 months with cholinesterase inhibitors, were subjected to daily rTMS-COG sessions (5/week) for 6 weeks, followed by maintenance sessions (2/week) for an additional 3 months. Six brain regions, located individually by MRI, were stimulated. COG tasks were developed to fit these regions. Primary objectives were average improvement of Alzheimer Disease Assessment Scale-Cognitive (ADAS-cog) and Clinical Global Impression of Change (CGIC) (after 6 weeks and 4.5 months, compared to baseline). Secondary objectives were average improvement of MMSE, ADAS-ADL, Hamilton Depression Scale (HAMILTON) and Neuropsychiatric Inventory (NPI). One patient abandoned the study after 2 months (severe urinary sepsis). ADAS-cog (average) improved by approximately 4 points after both 6 weeks and 4.5 months of treatment (P < 0.01 and P < 0.05) and CGIC by 1.0 and 1.6 points, respectively. MMSE, ADAS-ADL and HAMILTON improved, but without statistical significance. NPI did not change. No side effects were recorded. In this study, rTMS-COG (provided by Neuronix Ltd., Yokneam, Israel) seems a promising effective and safe modality for AD treatment, possibly as good as cholinesterase inhibitors. A European double blind study is underway.
Literature
go back to reference Beach TG, Kuo YM, Spiegel K, Emmerling MR, Sue LI, Kokjohn K, Roher AE (2000) The cholinergic deficit coincides with Abeta deposition at the earliest histopathologic stages of Alzheimer disease. J Neuropathol Exp Neurol 59(4):308–313PubMed Beach TG, Kuo YM, Spiegel K, Emmerling MR, Sue LI, Kokjohn K, Roher AE (2000) The cholinergic deficit coincides with Abeta deposition at the earliest histopathologic stages of Alzheimer disease. J Neuropathol Exp Neurol 59(4):308–313PubMed
go back to reference Bellgowan PS, Buffalo EA, Bodurka J, Martin A (2009) Lateralized spatial and object memory encoding in entorhinal and perirhinal cortices. Learn Mem 16(7):433–438PubMedCrossRef Bellgowan PS, Buffalo EA, Bodurka J, Martin A (2009) Lateralized spatial and object memory encoding in entorhinal and perirhinal cortices. Learn Mem 16(7):433–438PubMedCrossRef
go back to reference Belmaker RH, Grisaru N (1998) Magnetic stimulation of the brain in animal depression models responsive to ECS. J ECT 14(3):194–205PubMed Belmaker RH, Grisaru N (1998) Magnetic stimulation of the brain in animal depression models responsive to ECS. J ECT 14(3):194–205PubMed
go back to reference Berlingeri M, Crepaldi D, Roberti R, Scialfa G, Luzzatti C, Paulesu E (2008) Nouns and verbs in the brain: grammatical class and task specific effects as revealed by fMRI. Cogn Neuropsychol 25(4):528–558PubMedCrossRef Berlingeri M, Crepaldi D, Roberti R, Scialfa G, Luzzatti C, Paulesu E (2008) Nouns and verbs in the brain: grammatical class and task specific effects as revealed by fMRI. Cogn Neuropsychol 25(4):528–558PubMedCrossRef
go back to reference Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39PubMedCrossRef Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39PubMedCrossRef
go back to reference Bohning DE, Shastri A, McConnell KA, Nahas Z, Lorberbaum JP, Roberts DR, Teneback C, Vincent DJ, George MS (1999) A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatr 45(4):385–394CrossRef Bohning DE, Shastri A, McConnell KA, Nahas Z, Lorberbaum JP, Roberts DR, Teneback C, Vincent DJ, George MS (1999) A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatr 45(4):385–394CrossRef
go back to reference Bohning DE, Shastri A, Wassermann EM, Ziemann U, Lorberbaum JP, Nahas Z, Lomarev MP, George MS (2000) BOLD-f MRI response to single-pulse transcranial magnetic stimulation (TMS). J Magn Resonance Imaging 11(6):569–574CrossRef Bohning DE, Shastri A, Wassermann EM, Ziemann U, Lorberbaum JP, Nahas Z, Lomarev MP, George MS (2000) BOLD-f MRI response to single-pulse transcranial magnetic stimulation (TMS). J Magn Resonance Imaging 11(6):569–574CrossRef
go back to reference Boroojerdi B, Phipps M, Kopylev L, Wharton CM, Cohen LG, Grafman J (2001) Enhancing analogic reasoning with rTMS over the left prefrontal cortex. Neurology 56(4):526–528PubMed Boroojerdi B, Phipps M, Kopylev L, Wharton CM, Cohen LG, Grafman J (2001) Enhancing analogic reasoning with rTMS over the left prefrontal cortex. Neurology 56(4):526–528PubMed
go back to reference Braun M, Finke C, Ostendorf F, Lehmann TN, Hoffmann KT, Ploner CJ (2008) Reorganization of associative memory in humans with long-standing hippocampal damage. Brain 131(Pt 10):2742–2750PubMedCrossRef Braun M, Finke C, Ostendorf F, Lehmann TN, Hoffmann KT, Ploner CJ (2008) Reorganization of associative memory in humans with long-standing hippocampal damage. Brain 131(Pt 10):2742–2750PubMedCrossRef
go back to reference Brookmeyer R, Johnson E, Ziegler-Graham K, Arrighi HM (2007) Forecasting the global burden of Alzheimer’s disease. Alzheimers Dement 3(3):186–191PubMedCrossRef Brookmeyer R, Johnson E, Ziegler-Graham K, Arrighi HM (2007) Forecasting the global burden of Alzheimer’s disease. Alzheimers Dement 3(3):186–191PubMedCrossRef
go back to reference Buck BH, Black SE, Behrmann M, Caldwell C, Bronskill MJ (1997) Spatial- and object-based attentional deficits in Alzheimer’s disease. Relationship to HMPAO-SPECT measures of parietal perfusion. Brain 120(Pt 7):1229–1244PubMedCrossRef Buck BH, Black SE, Behrmann M, Caldwell C, Bronskill MJ (1997) Spatial- and object-based attentional deficits in Alzheimer’s disease. Relationship to HMPAO-SPECT measures of parietal perfusion. Brain 120(Pt 7):1229–1244PubMedCrossRef
go back to reference Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 239(Pt 7):1659–1673CrossRef Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 239(Pt 7):1659–1673CrossRef
go back to reference Cotelli M, Manenti R, Cappa SF, Geroldi C, Zanetti O, Rossini PM, Miniussi C (2006) Effect of transcranial magnetic stimulation on action naming in patients with Alzheimer disease. Arch Neurol 63(11):1602–1604PubMedCrossRef Cotelli M, Manenti R, Cappa SF, Geroldi C, Zanetti O, Rossini PM, Miniussi C (2006) Effect of transcranial magnetic stimulation on action naming in patients with Alzheimer disease. Arch Neurol 63(11):1602–1604PubMedCrossRef
go back to reference Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J (1994) The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 44(12):2308–2314PubMed Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J (1994) The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 44(12):2308–2314PubMed
go back to reference Fleischmann A, Hirschmann S, Dolberg OT, Dannon PN, Grunhaus L (1999) Chronic treatment with repetitive transcranial magnetic stimulation inhibits seizure induction by electroconvulsive shock in rats. Biol Psychiatry 45(6):759–763PubMedCrossRef Fleischmann A, Hirschmann S, Dolberg OT, Dannon PN, Grunhaus L (1999) Chronic treatment with repetitive transcranial magnetic stimulation inhibits seizure induction by electroconvulsive shock in rats. Biol Psychiatry 45(6):759–763PubMedCrossRef
go back to reference Foerster S, Buschert VC, Buchholz HG, Teipel SJ, Zach C, Bartenstein P, Buerger K (2009) Positive effects of a 6-month stage-specific cognitive intervention program on brain metabolism in subjects with amnestic mild cognitive impairment (aMCI) and mild Alzheimer’s Disease (AD). Alzheimers Dementia 5(4 Suppl 1):38CrossRef Foerster S, Buschert VC, Buchholz HG, Teipel SJ, Zach C, Bartenstein P, Buerger K (2009) Positive effects of a 6-month stage-specific cognitive intervention program on brain metabolism in subjects with amnestic mild cognitive impairment (aMCI) and mild Alzheimer’s Disease (AD). Alzheimers Dementia 5(4 Suppl 1):38CrossRef
go back to reference 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):189–198PubMedCrossRef 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):189–198PubMedCrossRef
go back to reference Fratiglioni L, Launer LJ, Andersen K, Breteler MM, Copeland JR, Lobo A, Martinez-Lage J, Soininen H, Hofman A (2000) Incidence of dementia and major subtypes in Europe: A collaborative study of population-based cohorts. Neurol Dis Elderly Res Group 54(11 Suppl 5):S10–15 Fratiglioni L, Launer LJ, Andersen K, Breteler MM, Copeland JR, Lobo A, Martinez-Lage J, Soininen H, Hofman A (2000) Incidence of dementia and major subtypes in Europe: A collaborative study of population-based cohorts. Neurol Dis Elderly Res Group 54(11 Suppl 5):S10–15
go back to reference George MS, Lisanby SH, Avery D, McDonald WM, Durkalski V, Pavlicova M, Anderson B, Nahas Z, Bulow P, Zarkowski P, Holtzheimer PE 3rd, Schwartz T, Sackeim HA (2010) Daily left prefrontal transcranial magnetic stimulation therapy for major depressive disorder: a sham-controlled randomized trial. Arch General Psychiatr 67(5):507–516CrossRef George MS, Lisanby SH, Avery D, McDonald WM, Durkalski V, Pavlicova M, Anderson B, Nahas Z, Bulow P, Zarkowski P, Holtzheimer PE 3rd, Schwartz T, Sackeim HA (2010) Daily left prefrontal transcranial magnetic stimulation therapy for major depressive disorder: a sham-controlled randomized trial. Arch General Psychiatr 67(5):507–516CrossRef
go back to reference Grafman J, Pascual-Leone A, Alway D, Nichelli P, Gomez-Tortosa E, Hallett M (1994) Induction of a recall deficit by rapid-rate transcranial magnetic stimulation. Neuroreport 5(9):1157–1160PubMedCrossRef Grafman J, Pascual-Leone A, Alway D, Nichelli P, Gomez-Tortosa E, Hallett M (1994) Induction of a recall deficit by rapid-rate transcranial magnetic stimulation. Neuroreport 5(9):1157–1160PubMedCrossRef
go back to reference Grossman M, Rhee J (2001) Cognitive resources during sentence processing in Alzheimer’s disease. Neuropsychologia 39(13):1419–1431PubMedCrossRef Grossman M, Rhee J (2001) Cognitive resources during sentence processing in Alzheimer’s disease. Neuropsychologia 39(13):1419–1431PubMedCrossRef
go back to reference Grossman M, Koenig P, DeVita C, Glosser G, Alsop D, Detre J, Gee J (2002) The neural basis for category-specific knowledge: an fMRI study. Neuroimage 15(4):936–948PubMedCrossRef Grossman M, Koenig P, DeVita C, Glosser G, Alsop D, Detre J, Gee J (2002) The neural basis for category-specific knowledge: an fMRI study. Neuroimage 15(4):936–948PubMedCrossRef
go back to reference Guse B, Falkai P, Wobrock T (2010) Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: a systematic review. J Neural Transm 117(1):105–122PubMedCrossRef Guse B, Falkai P, Wobrock T (2010) Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: a systematic review. J Neural Transm 117(1):105–122PubMedCrossRef
go back to reference Guy W (1976) Clinical global impressions. In: ECDEU assessment manual for psychopharmacology, revised (DHEW Publ No ADM 76–338). National Institute of Mental Health, Rockville, pp 218–222 Guy W (1976) Clinical global impressions. In: ECDEU assessment manual for psychopharmacology, revised (DHEW Publ No ADM 76–338). National Institute of Mental Health, Rockville, pp 218–222
go back to reference Hamidi M, Tononi G, Postle BR (2008) Evaluating the role of prefrontal and parietal cortices in memory-guided response with repetitive transcranial magnetic stimulation. Neuropsychologia 47(2):295–302PubMedCrossRef Hamidi M, Tononi G, Postle BR (2008) Evaluating the role of prefrontal and parietal cortices in memory-guided response with repetitive transcranial magnetic stimulation. Neuropsychologia 47(2):295–302PubMedCrossRef
go back to reference Hamilton M (1980) Rating depressive patients. J Clin Psychiatr 41(12 Pt 2):21–24 Hamilton M (1980) Rating depressive patients. J Clin Psychiatr 41(12 Pt 2):21–24
go back to reference Hao J, Li K, Li K, Zhang D, Wang W, Yang Y, Yan B, Shan B, Zhou X (2005) Visual attention deficits in Alzheimer’s disease: an fMRI study. Neurosci Lett 385(1):18–23PubMedCrossRef Hao J, Li K, Li K, Zhang D, Wang W, Yang Y, Yan B, Shan B, Zhou X (2005) Visual attention deficits in Alzheimer’s disease: an fMRI study. Neurosci Lett 385(1):18–23PubMedCrossRef
go back to reference Harpaz Y, Levkovitz Y, Lavidor M (2009) Lexical ambiguity resolution in Wernicke’s area and its right homologue. Cortex 45(9):1097–1103PubMedCrossRef Harpaz Y, Levkovitz Y, Lavidor M (2009) Lexical ambiguity resolution in Wernicke’s area and its right homologue. Cortex 45(9):1097–1103PubMedCrossRef
go back to reference Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch Neurol 60(8):1119–1122PubMedCrossRef Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch Neurol 60(8):1119–1122PubMedCrossRef
go back to reference Hyman BT, Damasio H, Damasio AR, Van Hoesen GW (1989) Alzheimer’s disease. Annu Rev Public Health 10:115–140PubMedCrossRef Hyman BT, Damasio H, Damasio AR, Van Hoesen GW (1989) Alzheimer’s disease. Annu Rev Public Health 10:115–140PubMedCrossRef
go back to reference Julkunen P, Jauhiainen AM, Westerén-Punnonen S, Pirinen E, Soininen H, Könönen M, Pääkkönen A, Määttä S, Karhu J (2008) Navigated TMS combined with EEG in mild cognitive impairment and Alzheimer’s disease: a pilot study. J Neurosci Methods 172(2):270–276PubMedCrossRef Julkunen P, Jauhiainen AM, Westerén-Punnonen S, Pirinen E, Soininen H, Könönen M, Pääkkönen A, Määttä S, Karhu J (2008) Navigated TMS combined with EEG in mild cognitive impairment and Alzheimer’s disease: a pilot study. J Neurosci Methods 172(2):270–276PubMedCrossRef
go back to reference Kimbrell TA, Little JT, Dunn RT, Frye MA, Greenberg BD, Wassermann EM, Repella JD, Danielson AL, Willis MW, Benson BE, Speer AM, Osuch E, George MS, Post RM (1999) Frequency dependence of antidepressant response to left prefrontal repetitive transcranial magnetic stimulation (rTMS) as a function of baseline cerebral glucose metabolism. Biol Psychiatr 46(12):1603–1613CrossRef Kimbrell TA, Little JT, Dunn RT, Frye MA, Greenberg BD, Wassermann EM, Repella JD, Danielson AL, Willis MW, Benson BE, Speer AM, Osuch E, George MS, Post RM (1999) Frequency dependence of antidepressant response to left prefrontal repetitive transcranial magnetic stimulation (rTMS) as a function of baseline cerebral glucose metabolism. Biol Psychiatr 46(12):1603–1613CrossRef
go back to reference Lisanby SH, Luber B, Perera T, Sackeim HA (2000) Transcranial magnetic stimulation: applications in basic neuroscience and neuropsychopharmacology. Int J Neuropsychopharmacol 3(3):259–273PubMedCrossRef Lisanby SH, Luber B, Perera T, Sackeim HA (2000) Transcranial magnetic stimulation: applications in basic neuroscience and neuropsychopharmacology. Int J Neuropsychopharmacol 3(3):259–273PubMedCrossRef
go back to reference Mantovani A, Lisanby SH (2004) Applications of transcranial magnetic stimulation to therapy in psychiatry. Psychiatr Times 21(9) Mantovani A, Lisanby SH (2004) Applications of transcranial magnetic stimulation to therapy in psychiatry. Psychiatr Times 21(9)
go back to reference Mecocci P, Bladstrom A, Stender K (2009) Effects of memantine on cognition in patients with moderate to severe Alzheimer’s disease: post-hoc analyses of ADAS-cog and SIB total and single-item scores from six randomized, double-blind, placebo-controlled studies. Int J Geriatr Psychiatr 24(5):532–538CrossRef Mecocci P, Bladstrom A, Stender K (2009) Effects of memantine on cognition in patients with moderate to severe Alzheimer’s disease: post-hoc analyses of ADAS-cog and SIB total and single-item scores from six randomized, double-blind, placebo-controlled studies. Int J Geriatr Psychiatr 24(5):532–538CrossRef
go back to reference Nakamura H, Kitagawa H, Kawaguchi Y, Tsuji H (1997) Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol 498(Pt 3):817–823PubMed Nakamura H, Kitagawa H, Kawaguchi Y, Tsuji H (1997) Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol 498(Pt 3):817–823PubMed
go back to reference Nixon P, Lazarova J, Hodinott-Hill I, Gough P, Passingham R (2004) The inferior frontal gyrus and phonological processing: an investigation using rTMS. J Cogn Neurosci 16(2):289–300PubMedCrossRef Nixon P, Lazarova J, Hodinott-Hill I, Gough P, Passingham R (2004) The inferior frontal gyrus and phonological processing: an investigation using rTMS. J Cogn Neurosci 16(2):289–300PubMedCrossRef
go back to reference Onder G, Zanetti O, Giacobini E, Frisoni GB, Bartorelli L, Carbone G, Lambertucci P, Silveri MC, Bernabei R (2005) Reality orientation therapy combined with cholinesterase inhibitors in Alzheimer’s disease: randomised controlled trial. Br J Psychiatry 187:450–455PubMedCrossRef Onder G, Zanetti O, Giacobini E, Frisoni GB, Bartorelli L, Carbone G, Lambertucci P, Silveri MC, Bernabei R (2005) Reality orientation therapy combined with cholinesterase inhibitors in Alzheimer’s disease: randomised controlled trial. Br J Psychiatry 187:450–455PubMedCrossRef
go back to reference Orrell M, Spector A, Thorgrimsen L, Woods B (2005) A pilot study examining the effectiveness of maintenance Cognitive Stimulation Therapy (MCST) for people with dementia. Int J Geriatr Psychiatr 20:446–451CrossRef Orrell M, Spector A, Thorgrimsen L, Woods B (2005) A pilot study examining the effectiveness of maintenance Cognitive Stimulation Therapy (MCST) for people with dementia. Int J Geriatr Psychiatr 20:446–451CrossRef
go back to reference Perry EK, Perry RH, Blessed G, Tomlinson BE (1977) Necropsy evidence of central cholinergic deficits in senile dementia. Lancet 1(8004):189PubMedCrossRef Perry EK, Perry RH, Blessed G, Tomlinson BE (1977) Necropsy evidence of central cholinergic deficits in senile dementia. Lancet 1(8004):189PubMedCrossRef
go back to reference Plassman BL, Langa KM, Fisher GG, Heeringa SG, Weir DR, Ofstedal MB, Burke JR, Hurd MD, Potter GG, Rodgers WL, Steffens DX, Willis RJ, Wallace RB (2007) Prevalence of dementia in the United States: the aging, demographics, and memory study. Neuroepidemiology 29(1–2):125–132PubMedCrossRef Plassman BL, Langa KM, Fisher GG, Heeringa SG, Weir DR, Ofstedal MB, Burke JR, Hurd MD, Potter GG, Rodgers WL, Steffens DX, Willis RJ, Wallace RB (2007) Prevalence of dementia in the United States: the aging, demographics, and memory study. Neuroepidemiology 29(1–2):125–132PubMedCrossRef
go back to reference Robinson DM, Keating GM (2006) Memantine: a review of its use in Alzheimer’s disease. Drugs 66(11):1515–1534PubMedCrossRef Robinson DM, Keating GM (2006) Memantine: a review of its use in Alzheimer’s disease. Drugs 66(11):1515–1534PubMedCrossRef
go back to reference Rogalsky C, Matchin W, Hickok G (2008) Broca’s area, sentence comprehension, and working memory: an fMRI Study. Front Hum Neurosci 2:14PubMedCrossRef Rogalsky C, Matchin W, Hickok G (2008) Broca’s area, sentence comprehension, and working memory: an fMRI Study. Front Hum Neurosci 2:14PubMedCrossRef
go back to reference Rogers SL, Friedhoff LT (1996) The efficacy and safety of donepezil in patients with Alzheimer’s disease: results of a US Multicentre, Randomized, Double-Blind, Placebo-Controlled Trial. The Donepezil Study Group. Dementia 7(6):293–303PubMed Rogers SL, Friedhoff LT (1996) The efficacy and safety of donepezil in patients with Alzheimer’s disease: results of a US Multicentre, Randomized, Double-Blind, Placebo-Controlled Trial. The Donepezil Study Group. Dementia 7(6):293–303PubMed
go back to reference Rosen WG, Mohs RC, Davis KL (1984) A new rating scale for Alzheimer’s disease. Am J Psychiatr 141(11):1356–1364PubMed Rosen WG, Mohs RC, Davis KL (1984) A new rating scale for Alzheimer’s disease. Am J Psychiatr 141(11):1356–1364PubMed
go back to reference Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120(12):2008–2039PubMedCrossRef Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120(12):2008–2039PubMedCrossRef
go back to reference Siebner HR, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148(1):1–16PubMedCrossRef Siebner HR, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148(1):1–16PubMedCrossRef
go back to reference Sitzer DI, Twamley EW, Jeste DV (2006) Cognitive training in Alzheimer’s disease: a meta-analysis of the literature. Acta Psychiatr Scand 114(2):75–90PubMedCrossRef Sitzer DI, Twamley EW, Jeste DV (2006) Cognitive training in Alzheimer’s disease: a meta-analysis of the literature. Acta Psychiatr Scand 114(2):75–90PubMedCrossRef
go back to reference Spector A, Thorgrimsen L, Woods B, Royan L, Davies S, Butterworth M, Orrell M (2003) Efficacy of an evidence-based cognitive stimulation therapy programme for people with dementia: randomised controlled trial. Br J Psychiatr 183:248–254CrossRef Spector A, Thorgrimsen L, Woods B, Royan L, Davies S, Butterworth M, Orrell M (2003) Efficacy of an evidence-based cognitive stimulation therapy programme for people with dementia: randomised controlled trial. Br J Psychiatr 183:248–254CrossRef
go back to reference Stern Y (2002) What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 8(3):448–460PubMedCrossRef Stern Y (2002) What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 8(3):448–460PubMedCrossRef
go back to reference Tárraga L, Boada M, Modinos G, Espinosa A, Diego S, Morera A, Guitart M, Balcells J, Lopez OL, Becker JT (2006) A randomised pilot study to assess the efficacy of an interactive, multimedia tool of cognitive stimulation in Alzheimer’s disease. J Neurol Neurosurg Psychiatr 77(10):1116–1121PubMedCrossRef Tárraga L, Boada M, Modinos G, Espinosa A, Diego S, Morera A, Guitart M, Balcells J, Lopez OL, Becker JT (2006) A randomised pilot study to assess the efficacy of an interactive, multimedia tool of cognitive stimulation in Alzheimer’s disease. J Neurol Neurosurg Psychiatr 77(10):1116–1121PubMedCrossRef
go back to reference Thickbroom GW (2007) Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp Brain Res 180(4):583–593PubMedCrossRef Thickbroom GW (2007) Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp Brain Res 180(4):583–593PubMedCrossRef
go back to reference van Duijn CM (1996) Epidemiology of the dementias: recent developments and new approaches. J Neurol Neurosurg Psychiatr 60(5):478–488PubMedCrossRef van Duijn CM (1996) Epidemiology of the dementias: recent developments and new approaches. J Neurol Neurosurg Psychiatr 60(5):478–488PubMedCrossRef
go back to reference Wassermann EM, Grafman J, Berry C, Hollnagel C, Wild K, Clark K, Hallett M (1996) Use and safety of a new repetitive transcranial magnetic stimulator. Electroencephalogr Clin Neurophysiol 101(5):412–417PubMed Wassermann EM, Grafman J, Berry C, Hollnagel C, Wild K, Clark K, Hallett M (1996) Use and safety of a new repetitive transcranial magnetic stimulator. Electroencephalogr Clin Neurophysiol 101(5):412–417PubMed
go back to reference Zheng XM (2000) Regional cerebral blood flow changes in drug-resistant depressed patients following treatment with transcranial magnetic stimulation: a statistical parametric mapping analysis. Psychiatr Res 100(2):75–80CrossRef Zheng XM (2000) Regional cerebral blood flow changes in drug-resistant depressed patients following treatment with transcranial magnetic stimulation: a statistical parametric mapping analysis. Psychiatr Res 100(2):75–80CrossRef
Metadata
Title
Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer’s disease: a proof of concept study
Authors
Jonathan Bentwich
Evgenia Dobronevsky
Sergio Aichenbaum
Ran Shorer
Ruth Peretz
Michael Khaigrekht
Revital Gandelman Marton
Jose M. Rabey
Publication date
01-03-2011
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue 3/2011
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-010-0578-1

Other articles of this Issue 3/2011

Journal of Neural Transmission 3/2011 Go to the issue

Basic Neurosciences, Genetics and Immunology - Original Article

Active cortical innervation protects striatal neurons from slow degeneration in culture

Basic Neurosciences, Genetics and Immunology - Review Article

Heme oxygenase-1 in Alzheimer disease: a tribute to Moussa Youdim

Basic Neurosciences, Genetics and Immunology - Review Article

Ultrastructural aspects of iron storage, transport and metabolism