Advertisement

Journal of Neural Transmission

, Volume 118, Issue 4, pp 587–598 | Cite as

Transcranial magnetic stimulation in Alzheimer’s disease: a neurophysiological marker of cortical hyperexcitability

  • Giovanni Pennisi
  • Raffaele Ferri
  • Giuseppe Lanza
  • Mariagiovanna Cantone
  • Manuela Pennisi
  • Valentina Puglisi
  • Giulia Malaguarnera
  • Rita Bella
Dementias - Review Article

Abstract

Recently, neuropathological studies have shown an important motor cortex involvement in Alzheimer’s disease (AD), even in its early stages, despite the lack of clinically evident motor deficit. Transcranial magnetic stimulation (TMS) studies have demonstrated that cortical excitability is enhanced in AD patients. This cortical hyperexcitability is believed to be a compensatory mechanism to execute voluntary movements, despite the progressive impairment of associative cortical areas. At present, it is not clear if these motor cortex excitability changes might be the expression of an involvement of intracortical excitatory glutamatergic circuits or an impairment of inhibitory cholinergic and, to a lesser extent, gabaergic activity. Although the main hypothesis for the pathogenesis of AD remains the degeneration of the basal forebrain cholinergic neurons, the development of specific TMS protocols, such as the paired-pulse TMS and the study of the short-latency afferent inhibition, points out the role of other neurotransmitters, such as gamma-amino-butyric acid, glutamate and dopamine. The potential therapeutic effect of repetitive TMS in restoring or compensating damaged cognitive functions, might become a possible rehabilitation tool in AD patients. Based on different patterns of cortical excitability, TMS may be useful in discriminating between physiological brain aging, mild cognitive impairment, AD and other dementing disorders. The present review provides a perspective of these TMS techniques by further understanding the role of different neurotransmission pathways and plastic remodelling of neuronal networks in the pathogenesis of AD.

Keywords

Transcranial magnetic stimulation Cortical excitability Aging Alzheimer’s disease Neurotransmission Neuroplasticity 

References

  1. Abbruzzese G, Trompetto C (2002) Clinical and research methods for evaluating cortical excitability. J Clin Neurophysiol 19(4):307–321PubMedGoogle Scholar
  2. Alagona G, Bella R, Ferri R, Carnemolla A, Pappalardo A, Costanzo E, Pennisi G (2001) Transcranial magnetic stimulation in Alzheimer disease: motor cortex excitability and cognitive severity. Neurosci Lett 314(1–2):57–60PubMedGoogle Scholar
  3. Alagona G, Ferri R, Pennisi G, Carnemolla A, Maci T, Domina E, Maertens de Noordhout A, Bella R (2004) Motor cortex excitability in Alzheimer’s disease and in subcortical ischemic vascular dementia. Neurosci Lett 362(2):95–98PubMedGoogle Scholar
  4. Alberici A, Bonato C, Calabria M, Agosti C, Zanetti O, Miniussi C, Padovani A, Rossini PM, Borroni B (2008) The contribution of TMS to frontotemporal dementia variants. Acta Neurol Scand 118:275–280PubMedGoogle Scholar
  5. Amassian VE, Cracco RQ, Maccabee PJ, Cracco JB (1992) Cerebello-frontal cortical projections in humans studied with the magnetic coil. Electroencephalogr Clin Neurophysiol 85(4):265–272PubMedGoogle Scholar
  6. Arendt T, Bruckner MK, Bigl V, Marcova L (1995) Dendritic reorganisation in the basal forebrain under degenerative conditions and its defects in Alzheimer’s disease. III. The basal forebrain compared with other subcortical areas. J Comp Neurol 351(2):223–246PubMedGoogle Scholar
  7. Arendt T, Schindler C, Brückner MK, Eschrich K, Bigl V, Zedlick D, Marcova L (1997) Plastic neuronal remodeling is impaired in patients with Alzheimer’s disease carrying apolipoproteins epsilon 4 allele. J Neurosci 17(2):516–529PubMedGoogle Scholar
  8. Arnold SE, Hyman BT, Flory J, Damasio AR, Van Hoesen GW (1991) The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patient with Alzheimer’s disease. Cereb Cortex 1(1):103–116PubMedGoogle Scholar
  9. Babiloni C, Babiloni F, Carducci F, Cincotti F, Del Percio C, De Pino G, Maestrini S, Priori A, Tisei P, Zanetti O, Rossini PM (2000) Movement-related electroencephalographic reactivity in Alzheimer disease. Neuroimage 12(2):139–146PubMedGoogle Scholar
  10. Bartus RT, Dean RL, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217(4558):408–414PubMedGoogle Scholar
  11. Battaglia F, Wang HY, Ghilardi MF, Gashi E, Quartarone A, Friedman E, Nixon RA (2007) Cortical plasticity in Alzheimer’s disease in humans and rodents. Biol Psychiatry 62(12):1405–1412PubMedGoogle Scholar
  12. Becker JT, Boller F, Lopez OL, Saxton J, McGonigle KL (1994) The natural history of Alzheimer’s disease. Arch Neurol 51(6):585–594PubMedGoogle Scholar
  13. Berardelli A, Inghilleri M, Gilio F, Romeo S, Pedace F, Curra A, Manfredi M (1999) Effects of repetitive cortical stimulation on the silent period evoked by magnetic stimulation. Exp Brain Res 125(1):82–86PubMedGoogle Scholar
  14. Berlanga ML, Simpson TK, Alcantara AA (2005) Dopamine D5 receptor localization on cholinergic neurons of the rat forebrain and diencephalon: a potential neuroanatomical substrate involved in mediating dopaminergic influences on acetylcholine release. J Comp Neurol 492(1):34–49PubMedGoogle Scholar
  15. Berretta N, Cherubini E (1998) A novel form of long-term depression in the CA1 area of the adult rat hippocampus independent of glutamate receptors activation. Eur J Neurosci 10(9):2957–2963PubMedGoogle Scholar
  16. Blessed G, Tomlinson BE, Roth M (1968) The association between quantitative measures of dementia and of senile change in the cerebral grey matter of elderly subjects. Br J Psychiatry 114(512):797–811PubMedGoogle Scholar
  17. Borson S, Raskind MA (1997) Clinical features and pharmacological treatment of behavioural symptoms of Alzheimer’s disease. Neurology 48(5 suppl 6):S17–S24PubMedGoogle Scholar
  18. Bracco L, Giovannelli F, Bessi V, Borgheresi A, Di Tullio A, Sorbi S, Zaccara G, Cincotta M (2009) Mild cognitive impairment: loss of linguistic task-induced changes in motor cortex excitability. Neurology 72(10):928–934PubMedGoogle Scholar
  19. Brignani D, Manganotti P, Rossini PM, Miniussi C (2008) Modulation of cortical oscillatory activity during transcranial magnetic stimulation. Hum Brain Mapp 29(5):603–612PubMedGoogle Scholar
  20. Calabresi P, Picconi B, Parnetti L, Di Filippo M (2006) A convergent model for cognitive dysfunctions in Parkinson’s disease: the critical dopamine–acetylcholine synaptic balance. Lancet Neurol 5(11):974–983PubMedGoogle Scholar
  21. Cantello R, Gianelli M, Civardi C, Mutani R (1992) Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology 42(10):1951–1959PubMedGoogle Scholar
  22. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48(5):1398–1403PubMedGoogle Scholar
  23. Chetelat G, Desgranges B, De la Sayette V, Viader F, Berkouk K, Landeau B, Lalevée C, Le Doze F, Dupuy B, Hannequin D, Baron JC, Eustache F (2003) Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain 126(Pt 9):1955–1967PubMedGoogle Scholar
  24. Chibbaro G, Daniele M, Alagona G, Di Pasquale C, Cannavò M, Rapisarda V, Bella R, Pennisi G (2005) Repetitive transcranial magnetic stimulation in schizophrenic patients reporting auditory hallucinations. Neurosci Lett 383(1–2):54–57PubMedGoogle Scholar
  25. Cicinelli P, Traversa R, Bassi A, Scivoletto G, Rossini PM (1997) Interhemispheric differences of hand muscle representation in human motor cortex. Muscle Nerve 20(5):535–542PubMedGoogle Scholar
  26. Conti F, Weinberg RJ (1999) Shaping excitation at glutamatergic synapses. Trends Neurosci 22(10):451–458PubMedGoogle Scholar
  27. 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):1602–1604PubMedGoogle Scholar
  28. Cotelli M, Manenti R, Cappa SF, Zanetti O, Miniussi C (2008) Transcranial magnetic stimulation improves naming in Alzheimer disease patients at different stages of cognitive decline. Eur J Neurol 15(12):1286–1292PubMedGoogle Scholar
  29. Cotelli M, Calabria M, Manenti R, Rosini S, Zanetti O, Cappa SF, Miniussi C (2010) Improved language performance in Alzheimer disease following brain stimulation. J Neurol Neurosurg Psychiatry [Epub ahead of print]Google Scholar
  30. Cracco RQ, Amassian VE, Maccabee PJ, Cracco JB (1989) Comparison of human transcallosal responses evoked by magnetic coil and electrical stimulation. Electroencephalogr Clin Neurophysiol 74(6):417–424PubMedGoogle Scholar
  31. Dannhauser TM, Walker Z, Stevens T, Lee L, Seal M, Shergill SS (2005) The functional anatomy of divided attention in amnestic mild cognitive impairment. Brain 128(Pt 6):1418–1427PubMedGoogle Scholar
  32. Davies P, Maloney AJ (1976) Selective loss of central cholinergic neurons in Alzheimer’s disease. Lancet 2(8000):1403PubMedGoogle Scholar
  33. de Carvalho M, de Mendonça A, Miranda PC, Garcia C, Luís ML (1997) Magnetic stimulation in Alzheimer’s disease. J Neurol 244(5):304–307PubMedGoogle Scholar
  34. de Mendonça A, Almeida T, Bashir ZI, Ribeiro JA (1997) Endogenous adenosine attenuates long-term depression and depotentiation in the CA1 region of the rat hippocampus. Neuropharmacology 36(2):161–167PubMedGoogle Scholar
  35. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13(7):281–285PubMedGoogle Scholar
  36. Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Di Giovanni S, Zito G, Tonali P, Rothwell JC (2000) Muscarinic receptor blockade has different effects on the excitability of intracortical circuits in human motor cortex. Exp Brain Res 135(4):455–461PubMedGoogle Scholar
  37. Di Lazzaro V, Oliviero A, Profice P, Meglio M, Cioni B, Tonali P, Rothwell JC (2001) Descending spinal cord volleys evoked by transcranial magnetic stimulation of the motor cortex leg area in conscious humans. J Physiol 537(Pt 3):1047–1058PubMedGoogle Scholar
  38. Di Lazzaro V, Oliviero A, Tonali PA, Marra C, Daniele A, Profice P, Saturno E, Pilato F, Masullo C, Rothwell JC (2002) Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation. Neurology 59(3):392–397PubMedGoogle Scholar
  39. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Tonali PA (2003) Motor cortex hyperexcitability to transcranial magnetic stimulation in Alzheimer’s disease: evidence of impaired glutamatergic neurotransmission? Ann Neurol 53(1):824PubMedGoogle Scholar
  40. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Marra C, Daniele A, Ghirlanda S, Gainotti G, Tonali PA (2004) Motor cortex hyperexcitability to transcranial magnetic stimulation in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 75(4):555–559PubMedGoogle Scholar
  41. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Marra C, Ghirlanda S, Ranieri F, Gainotti G, Tonali P (2005) Neurophysiological predictors of long term response to AChE inhibitors in AD patients. J Neurol Neurosurg Psychiatry 76(8):1064–1069PubMedGoogle Scholar
  42. Di Lazzaro V, Pilato F, Dileone M, Saturno E, Oliviero A, Marra C, Daniele A, Ranieri F, Gainotti G, Tonali PA (2006) In vivo cholinergic circuit evaluation in frontotemporal and Alzheimer dementias. Neurology 66(7):1111–1113PubMedGoogle Scholar
  43. Di Lazzaro V, Pilato F, Dileone M, Saturno E, Profice P, Marra C, Daniele A, Ranieri F, Quaranta D, Gainotti G, Tonali PA (2007) Functional evaluation of cerebral cortex in dementia with Lewy bodies. Neuroimage 37(2):422–429PubMedGoogle Scholar
  44. Disterhoft JF, Oh MM (2007) Alterations in intrinsic neuronal excitability during normal aging. Aging Cell 6(3):327–336PubMedGoogle Scholar
  45. Ferreri F, Pauri F, Pasqualetti P, Fini R, Dal Forno G, Rossini PM (2003) Motor cortex excitability in Alzheimer’s disease: a transcranial magnetic stimulation study. Ann Neurol 53:102–108PubMedGoogle Scholar
  46. Fitzgerald PB, Brown TL, Marston NA, Daskalakis ZJ, De Castella A, Kulkarni J (2003) Transcranial magnetic stimulation in the treatment of depression: a double-blind, placebo-controlled trial. Arch Gen Psychiatry 60(10):1002–1008PubMedGoogle Scholar
  47. 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):189–198PubMedGoogle Scholar
  48. Francis PT, Sims NR, Procter AW, Bowen DM (1993) Cortical pyramidal neurone loss may cause glutamatergic hypoactivity and cognitive impairment in Alzheimer’s disease: investigative and therapeutic perspectives. J Neurochem 60(5):1589–1604PubMedGoogle Scholar
  49. Francis PT, Palmer AM, Snape M, Wilcock GK (1999) The cholinergic hypothesis of Alzheimer’s disease: a review of progress. J Neurol Neurosurg Psychiatry 66(2):137–147PubMedGoogle Scholar
  50. Friedland RP, Budinger TF, Koss E, Ober BA (1985) Alzheimer disease: anterior–posterior and lateral hemispheric alteration in cortical glucose utilization. Neurosci Lett 53(3):235–240PubMedGoogle Scholar
  51. Funkenstein HH, Albert MS, Cook NR, West CG, Scherr PA, Chown MJ, Pilgrim D, Evans DA (1993) Extrapyramidal signs and other neurological findings in clinically diagnosed Alzheimer’s disease. Arch Neurol 50(1):51–56PubMedGoogle Scholar
  52. Geula C (1998) Abnormalities of neural circuitry in Alzheimer’s disease: hippocampus and cortical cholinergic innervation. Neurology 51(1 Suppl 1):S18–S29PubMedGoogle Scholar
  53. Gladding CM, Fitzjohn SM, Molnár E (2009) Metabotropic glutamate receptor-mediated long-term depression: molecular mechanisms. Pharmacol Rev 61(4):395–412PubMedGoogle Scholar
  54. Gray CW, Patel AJ (1995) Neurodegeneration mediated by glutamate and beta-amyloid peptide: a comparison and possible interaction. Brain Res 691(1–2):169–179PubMedGoogle Scholar
  55. Hardy JA, Mann DM, Wester P, Winblad B (1986) An integrative hypothesis concerning the pathogenesis and progression of Alzheimer’s disease. Neurobiol Aging 7(6):489–502PubMedGoogle Scholar
  56. Herholz K, Weisenbach S, Zundorf G, Lenz O, Schroder H, Bauer B, Kalbe E, Heiss WD (2004) In vivo study of acetylcholine esterase in basal forebrain, amygdala, and cortex in mild to moderate Alzheimer disease. Neuroimage 21(1):136–143PubMedGoogle Scholar
  57. Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL (1982) A new clinical scale for the staging of dementia. Br J Psychiatry 140:566–572PubMedGoogle Scholar
  58. Hyman BT, Van Hoesen GW, Damasio AR (1987) Alzheimer’s disease: glutamate depletion in the hippocampal perforant pathway zone. Ann Neurol 22(1):37–40PubMedGoogle Scholar
  59. Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Näätänen R, Katila T (1997) Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8(16):3537–3540PubMedGoogle Scholar
  60. Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 466:521–534PubMedGoogle Scholar
  61. Inghilleri M, Conte A, Frasca V, Scaldaferri N, Gilio F, Santini M, Fabbrini G, Prencipe M, Berardelli A (2006) Altered response to rTMS in patients with Alzheimer’s disease. Clin Neurophysiol 117(1):103–109PubMedGoogle Scholar
  62. Jalinous R (1991) Technical and practical aspects of magnetic nerve stimulation. J Clin Neurophysiol 8(1):10–25PubMedGoogle Scholar
  63. Jansen KL, Faull RL, Dragunow M, Synek BL (1990) Alzheimer’s disease: changes in hippocampal N-methyl-d-aspartate, quisqualate, neurotensin, adenosine, benzodiazepine, serotonin and opioid receptors–an autoradiographic study. Neuroscience 39(3):613–627PubMedGoogle Scholar
  64. 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):270–276PubMedGoogle Scholar
  65. Kähkönen S, Kesäniemi M, Nikouline VV, Karhu J, Ollikainen M, Holi M, Ilmoniemi RJ (2001) Ethanol modulates cortical activity: direct evidence with combined TMS and EEG. Neuroimage 14(2):322–328PubMedGoogle Scholar
  66. Kasa P, Rakonczay Z, Gulya K (1997) The cholinergic system in Alzheimer’s disease. Prog Neurobiol 52(6):511–535PubMedGoogle Scholar
  67. Kemp N, Bashir ZI (1999) Induction of LTD in the adult hippocampus by the synaptic activation of AMPA/kainate and metabotropic glutamate receptors. Neuropharmacology 38(4):495–504PubMedGoogle Scholar
  68. Kemppainen N, Laine M, Laakso MP, Kaasinen V, Någren K, Vahlberg T, Kurki T, Rinne JO (2003) Hippocampal dopamine D2 receptors correlate with memory functions in Alzheimer’s disease. Eur J Neurosci 18(1):149–154PubMedGoogle Scholar
  69. Kim M, Thompson CK (2000) Patterns of comprehension and production of nouns and verbs in agrammatism: implications for lexical organization. Brain Lang 74(1):1–25PubMedGoogle Scholar
  70. Kimiskidis VK, Papagiannopoulos S, Sotirakoglou K, Kazis DA, Kazis A, Mills KR (2005) Silent period to transcranial magnetic stimulation: construction and properties of stimulus-response curves in healthy volunteers. Exp Brain Res 163(1):21–31PubMedGoogle Scholar
  71. Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF (1999) Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 19(5):1599–1609PubMedGoogle Scholar
  72. Kobayashi M, Pascual-Leone A (2003) Transcranial magnetic stimulation in neurology. Lancet Neurol 2(3):145–156PubMedGoogle Scholar
  73. Koenig T, Prichep L, Dierks T, Hubl D, Wahlund LO, John ER, Jelic V (2005) Decreased EEG synchronization in Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging 26(2):165–171PubMedGoogle Scholar
  74. Korchounov A, Ilic TV, Ziemann U (2007) TMS-assisted neurophysiological profiling of the dopamine receptor agonist cabergoline in human motor cortex. J Neural Transm 114(2):223–229PubMedGoogle Scholar
  75. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519PubMedGoogle Scholar
  76. Lakmache Y, Lassonde M, Gauthier S, Frigon JY, Lepore F (1998) Interhemispheric disconnection syndrome in Alzheimer’s disease. Proc Natl Acad Sci USA 95(15):9042–9046PubMedGoogle Scholar
  77. Lidow MS, Gallager DW, Rakic P, Goldman-Rakic PS (1989) Regional differences in the distribution of muscarinic cholinergic receptors in the macaque cerebral cortex. J Comp Neurol 289(2):247–259PubMedGoogle Scholar
  78. Liepert J, Wessel K, Schwenkreis P, Trillenberg P, Otto V, Vorgerd M, Malin JP, Tegenthoff M (1998) Reduced intracortical facilitation in the motor cortex of patients with cerebellar degeneration. Acta Neurol Scand 98(5):318–323PubMedGoogle Scholar
  79. Liepert J, Bär KJ, Meskea U, Weiller C (2001) Motor cortex disinhibition in Alzheimer’s disease. Clin Neurophysiol 112(8):1436–1441PubMedGoogle Scholar
  80. Lowe SL, Francis PT, Procter AW, Palmer AM, Davison AN, Bowen DM (1988) Gamma-aminobutyric acid concentration in brain tissue at two stages of Alzheimer’s disease. Brain 111(Pt 4):785–799PubMedGoogle Scholar
  81. Lowe SL, Bowen DM, Francis PT, Neary D (1990) Ante mortem cerebral amino acid concentrations indicate selective degeneration of glutamate-enriched neurons in Alzheimer’s disease. Neuroscience 38(3):571–577PubMedGoogle Scholar
  82. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 133(4):425–430PubMedGoogle Scholar
  83. Mariorenzi R, Zarola F, Caramia MD, Paradiso C, Rossini PM (1991) Non-invasive evaluation of central motor tract excitability changes following peripheral nerve stimulation in humans. Electroencephalogr Clin Neurophysiol 81(2):90–101PubMedGoogle Scholar
  84. Martorana A, Stefani A, Calmieri MG, Esposito Z, Bernardi G, Sancesario G, Pierantozzi M (2008) L-dopa modulates motor cortex excitability in Alzheimer’s disease patients. J Neural Transm 115(9):1313–1319PubMedGoogle Scholar
  85. Martorana A, Mori F, Esposito Z, Kusayanagi H, Monteleone F, Codecà C, Sancesario G, Bernardi G, Koch G (2009) Dopamine modulates cholinergic cortical excitability in Alzheimer’s disease patients. Neuropsychopharmacology 34(10):2323–2328PubMedGoogle Scholar
  86. Masliah E, Alford M, DeTeresa R, Mallory M, Hansen L (1996) Deficient glutamate transport is associated with neurodegeneration in Alzheimer’s disease. Ann Neurol 40(5):759–766PubMedGoogle Scholar
  87. Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1983) Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214(2):170–197PubMedGoogle Scholar
  88. Mesulam M, Shaw P, Mash D, Weintraub S (2004) Cholinergic nucleus basalis tauopathy emerges early in the aging-MCI-AD continuum. Ann Neurol 55(6):815–828PubMedGoogle Scholar
  89. Moghaddam B, Adams B, Verma A, Daly D (1997) Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 17:2921–2927PubMedGoogle Scholar
  90. Morris JC, Storandt M, Miller JP, McKeel DW, Price JL, Rubin EH (2001) Mild cognitive impairment represents early-stage Alzheimer disease. Arch Neurol 58(3):397–405PubMedGoogle Scholar
  91. Nägga K, Bogdanovic N, Marcusson J (1999) GABA transporters (GAT-1) in Alzheimer’s disease. J Neural Transm 106(11–12):1141–1149PubMedGoogle Scholar
  92. Nardone R, Bratti A, Tezzon F (2006) Motor cortex inhibitory circuits in dementia with Lewy bodies and in Alzheimer’s disease. J Neural Transm 113(11):1679–1684PubMedGoogle Scholar
  93. Nardone R, Bergmann J, Kronbichler M, Kunz A, Klein S, Caleri F, Tezzon F, Ladurner G, Golaszewski S (2008) Abnormal short latency afferent inhibition in early Alzheimer’s disease: a transcranial magnetic demonstration. J Neural Transm 115(11):1557–1562PubMedGoogle Scholar
  94. Nordberg A (1992) Neuroreceptor changes in Alzheimer disease. Cerebrovasc Brain Metab Rev 4(4):303–328PubMedGoogle Scholar
  95. Ohyama M, Senda M, Ishiwata K, Kitamura S, Mishina M, Ishii K, Toyama H, Oda K, Katayama Y (1999) Preserved benzodiazepine receptors in Alzheimer’s disease measured with C-11 flumazenil PET and I-123 iomazenil STECT in comparison with CBF. Ann Nucl Med 13(5):309–315PubMedGoogle Scholar
  96. Olazarán J, Prieto J, Cruz I, Esteban A (2010) Cortical excitability in very mild Alzheimer’s disease: a long-term follow-up study. J Neurol 257(12):2078–2085Google Scholar
  97. Oliviero A, Profice P, Tonali PA, Pilato F, Saturno E, Dileone M, Ranieri F, Di Lazzaro V (2006) Effects of aging on motor cortex excitability. Neurosci Res 55(1):74–77PubMedGoogle Scholar
  98. Pascual-Leone A, Valls-Sole′ J, Wassermann E, Hallett M (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117(Pt 4):847–858PubMedGoogle Scholar
  99. Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC (1997) Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J Neurosci 17(9):3178–3184PubMedGoogle Scholar
  100. Peinemann A, Lehner C, Conrad B, Siebner HR (2001) Age-related decrease in paired-pulse intracortical inhibition in the human primary motor cortex. Neurosci Lett 313(1–2):33–36PubMedGoogle Scholar
  101. Pennisi G, Alagona G, Ferri R, Greco S, Santonocito D, Pappalardo A, Bella R (2002) Motor cortex excitability in Alzheimer disease: one year follow-up study. Neurosci Lett 329(3):293–296PubMedGoogle Scholar
  102. Pepin JL, Bogacz D, de Pasqua V, Delwaide PJ (1999) Motor cortex inhibition is not impaired in patients with Alzheimer’s disease: evidence from paired transcranial magnetic stimulation. J Neurol Sci 170(2):119–123PubMedGoogle Scholar
  103. Perretti A, Grossi D, Fragassi N, Lanzillo B, Nolano M, Pisacreta AI, Caruso G, Santoro L (1996) Evaluation of the motor cortex by magnetic stimulation in patients with Alzheimer disease. J Neurol Sci 135(1):31–37PubMedGoogle Scholar
  104. Perry EK, Tomlinson BE, Blessed G, Bergmann K, Gibson PH, Perry RH (1978) Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. BMJ 2(6150):1457–1459PubMedGoogle Scholar
  105. Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256(3):183–194PubMedGoogle Scholar
  106. Pierantozzi M, Panella M, Calmieri MG, Koch G, Giordano A, Marciani MG, Bernardi G, Stanzione P, Stefani A (2004) Different TMS patterns of intracortical inhibition in early onset Alzheimer dementia and frontotemporal dementia. Clin Neurophysiol 115(10):2410–2418PubMedGoogle Scholar
  107. Pitcher JB, Ogston KM, Miles TS (2003) Age and sex differences in human motor cortex input–output characteristics. J Physiol 546(Pt 2):605–613PubMedGoogle Scholar
  108. Reisberg B, Ferris SH (1982) Diagnosis and assessment of the older patients. Hosp Community Psychiatry 32:104–110Google Scholar
  109. Robinson KM, Grossman M, White-Devine T, D’Esposito M (1996) Category-specific difficulty naming with verbs in Alzheimer’s disease. Neurology 47(1):178–182PubMedGoogle Scholar
  110. Rogers J, Morrison JH (1985) Quantitative morphology and regional and laminar distribution of senile plaques in Alzheimer’s disease. J Neurosci 5(10):2801–2808PubMedGoogle Scholar
  111. Romeo S, Gilio F, Pedace F, Ozkaynak S, Inghilleri M, Manfredi M, Berardelli A (2000) Changes in the cortical silent period after repetitive magnetic stimulation of cortical motor areas. Exp Brain Res 135(4):504–510PubMedGoogle Scholar
  112. Rossi S, Miniussi C, Pasqualetti P, Babiloni C, Rossini PM, Cappa SF (2004) Age-related functional changes of prefrontal cortex in long-term memory: a repetitive transcranial magnetic stimulation study. J Neurosci 24(36):7939–7944PubMedGoogle Scholar
  113. Rossini PM, Desiato MT, Caramia MD (1992) Age-related changes of motor evoked potentials in healthy humans: non-invasive evaluation of central and peripheral motor tracts excitability and conductivity. Brain Res 593(1):14–19PubMedGoogle Scholar
  114. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijević MR, Hallett M, Katayama Y, Lücking CH, et al (1994a) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr. Clin. Neurophysiol 91(2):79–92Google Scholar
  115. Rossini PM, Martino G, Narici L, Pasquarelli A, Peresson M, Pizzella V, Tecchio F, Torrioli G, Romani GL (1994b) Short-term brain ‘plasticity’ in humans: transient finger representation changes in sensory cortex somatotopy following ischemic anesthesia. Brain Res 642(1–2):169–177PubMedGoogle Scholar
  116. Rossini PM, Del Percio C, Pasqualetti P, Cassetta E, Binetti G, Dal Forno G, Ferreri F, Frisoni G, Chiovenda P, Miniussi C, Parisi L, Tombini M, Vecchio F, Babiloni C (2006) Conversion from mild cognitive impairment to Alzheimer’s disease is predicted by sources and coherence of brain electroencephalography rhythms. Neuroscience 143(3):793–803PubMedGoogle Scholar
  117. Rossini PM, Rossi S, Babiloni C, Polich J (2007) Clinical neurophysiology of aging brain: from normal aging to neurodegeneration. Prog Neurobiol 83(6):375–400PubMedGoogle Scholar
  118. Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W (1999) Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 52:97–103PubMedGoogle Scholar
  119. Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R (2003) Short and long latency afferent inhibition in Parkinson’s disease. Brain 126(Pt 8):1883–1894PubMedGoogle Scholar
  120. Sakuma K, Murakami T, Nakashima K (2007) Short latency afferent inhibition is not impaired in mild cognitive impairment. Clin Neurophysiol 118(7):1460–1463PubMedGoogle Scholar
  121. Schönfeldt-Lecuona C, Lefaucheur JP, Cardenas-Morales L, Wolf RC, Kammer T, Herwig U (2010) The value of neuronavigated rTMS for the treatment of depression. Neurophysiol Clin 40(1):37–43PubMedGoogle Scholar
  122. Stefan K, Kunesh E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123(Pt 3):572–584PubMedGoogle Scholar
  123. Stokes MG, Chambers CD, Gould IC, English T, McNaught E, McDonald O, Mattingley JB (2007) Distance-adjusted motor threshold for transcranial magnetic stimulation. Clin Neurophysiol 118(7):1617–1625PubMedGoogle Scholar
  124. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, Raman R, Davies P, Masliah E, Williams DS, Goldstein LS (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer’s disease. Science 307(5713):1282–1288PubMedGoogle Scholar
  125. Strafella AP, Paus T, Barrett J, Dagher A (2001) Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci 21(15):RC157Google Scholar
  126. Suva D, Favre I, Kraftsik R, Esteban M, Lobrinus A, Miklossy J (1999) Primary motor cortex involvement in Alzheimer disease. J Neuropathol Exp Neurol 58(11):1125–1134PubMedGoogle Scholar
  127. Tales A, Muir JL, Bayer A, Snowden RJ (2002) Spatial shifts in visual attention in normal ageing and dementia of the Alzheimer type. Neuropsychologia 40(12):2000–2012PubMedGoogle Scholar
  128. Tokimura H, Di Lazzaro V, Tokimura Y, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (2000) Short latency inhibition of human hand motor cortex by somatosensory inputs from the hand. J Physiol 523(Pt 2):503–553PubMedGoogle Scholar
  129. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J (1999) Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 517(Pt 2):591–597PubMedGoogle Scholar
  130. Whitehouse PJ, Price DL, Clark AW, Coyle JT, DeLong MR (1981) Alzheimer disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann Neurol 10(2):122–126PubMedGoogle Scholar
  131. Ziemann U (2004) TMS and drugs. Clin Neurophysiol 115(8):1717–1722PubMedGoogle Scholar
  132. Ziemann U, Tergau F, Bruns D, Baudewig J, Paulus W (1997) Changes in human motor cortex excitability induced by dopaminergic and anti-dopaminergic drugs. Electroencephalogr Clin Neurophysiol 105(6):430–437PubMedGoogle Scholar
  133. Ziemann U, Hallett M, Cohen LG (1998) Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci 18(17):7000–7007PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Giovanni Pennisi
    • 1
  • Raffaele Ferri
    • 2
  • Giuseppe Lanza
    • 1
  • Mariagiovanna Cantone
    • 1
  • Manuela Pennisi
    • 3
  • Valentina Puglisi
    • 1
  • Giulia Malaguarnera
    • 1
  • Rita Bella
    • 1
  1. 1.Department of NeuroscienceUniversity of CataniaCataniaItaly
  2. 2.Department of Neurology I.C.Oasi Institute for Research on Mental Retardation and Brain Aging (IRCCS)TroinaItaly
  3. 3.Department of ChemistryUniversity of CataniaCataniaItaly

Personalised recommendations