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International Journal of Alzheimer’s Disease
Volume 2011, Article ID 263817, 9 pages
http://dx.doi.org/10.4061/2011/263817
Review Article

Transcranial Magnetic Stimulation Studies in Alzheimer's Disease

1Department of Neurology, University Campus Bio-Medico of Rome, 00128 Rome, Italy
2Department of Rehabilitation, University Campus Bio-Medico of Rome, 00128 Rome, Italy
3Department of Neuroscience, University of Pisa, 56126 Pisa, Italy
4Department of Clinical Neurophysiology, University of Eastern Finland, 70210 Kuopio, Finland

Received 30 December 2010; Revised 11 April 2011; Accepted 5 May 2011

Academic Editor: Giuseppe Curcio

Copyright © 2011 Andrea Guerra et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Borson and M. A. Raskind, “Clinical features and pharmacological treatment of behavioural symptoms of Alzheimer’s disease,” Neurology, vol. 48, no. 5, supplement 6, pp. S17–S24, 1997. View at Google Scholar
  2. H. W. Querfurth and F. M. LaFerla, “Alzheimer's disease,” New England Journal of Medicine, vol. 362, no. 4, pp. 329–344, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Kobayashi and A. Pascual-Leone, “Transcranial magnetic stimulation in neurology,” Lancet Neurology, vol. 2, no. 3, pp. 145–156, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. P. M. Rossini and S. Rossi, “Transcranial magnetic stimulation: diagnostic, therapeutic, and research potential,” Neurology, vol. 68, no. 7, pp. 484–488, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. F. Ferreri, F. Pauri, P. Pasqualetti, R. Fini, G. Dal Forno, and P. M. Rossini, “Motor cortex excitability in Alzheimer's disease: a transcranial magnetic stimulation study,” Annals of Neurology, vol. 53, no. 1, pp. 102–108, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. A. T. Barker, R. Jalinous, and I. L. Freeston, “Non-invasive magnetic stimulation of human motor cortex,” Lancet, vol. 1, no. 8437, pp. 1106–1107, 1985. View at Google Scholar · View at Scopus
  7. P. T. Fox, S. Narayana, N. Tandon et al., “Column-based model of electric field excitation of cerebral cortex,” Human Brain Mapping, vol. 22, no. 1, pp. 1–14, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. V. Di Lazzaro, A. Oliviero, P. Profice et al., “Descending spinal cord volleys evoked by transcranial magnetic and electrical stimulation of the motor cortex leg area in conscious humans,” Journal of Physiology, vol. 537, no. 3, pp. 1047–1058, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. P. M. Rossini, G. Martino, L. Narici et al., “Short-term brain “plasticity” in humans: transient finger representation changes in sensory cortex somatotopy following ischemic anesthesia,” Brain Research, vol. 642, no. 1-2, pp. 169–177, 1994. View at Google Scholar · View at Scopus
  10. P. M. Rossini, A. T. Barker, A. Berardelli et al., “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,” Electroencephalography and Clinical Neurophysiology, vol. 91, no. 2, pp. 79–92, 1994. View at Publisher · View at Google Scholar
  11. P. M. Rossini, A. Berardelli, G. Deuschl et al., “Applications of magnetic cortical stimulation. The International Federation of Clinical Neurophysiology,” Electroencephalography and Clinical Neurophysiology, vol. 52, supplement, pp. 171–185, 1999. View at Google Scholar · View at Scopus
  12. U. Ziemann, “TMS and drugs,” Clinical Neurophysiology, vol. 115, no. 8, pp. 1717–1729, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. P. M. Rossini, S. Rossi, C. Babiloni, and J. Polich, “Clinical neurophysiology of aging brain: from normal aging to neurodegeneration,” Progress in Neurobiology, vol. 83, no. 6, pp. 375–400, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Ferreri, P. Pasqualetti, S. Määttä et al., “Motor cortex excitability in Alzheimer's disease: a transcranial magnetic stimulation follow-up study,” Neuroscience Letters, vol. 492, no. 2, pp. 94–98, 2011. View at Publisher · View at Google Scholar
  15. T. Kujirai, M. D. Caramia, J. C. Rothwell et al., “Corticocortical inhibition in human motor cortex,” Journal of Physiology, vol. 471, pp. 501–519, 1993. View at Google Scholar · View at Scopus
  16. T. Shimizu, M. Oliveri, M. M. Filippi, M. G. Palmieri, P. Pasqualetti, and P. M. Rossini, “Effect of paired transcranial magnetic stimulation on the cortical silent period,” Brain Research, vol. 834, no. 1-2, pp. 74–82, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Orth, A. H. Snijders, and J. C. Rothwell, “The variability of intracortical inhibition and facilitation,” Clinical Neurophysiology, vol. 114, no. 12, pp. 2362–2369, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. V. Di Lazzaro, A. Oliviero, P. A. Tonali et al., “Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation,” Neurology, vol. 59, no. 3, pp. 392–397, 2002. View at Google Scholar
  19. U. Ziemann, F. Tergau, E. M. Wassermann, S. Wischer, J. Hildebrandt, and W. Paulus, “Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation,” Journal of Physiology, vol. 511, no. 1, pp. 181–190, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. U. Ziemann, M. Hallett, and L. G. Cohen, “Mechanisms of deafferentation-induced plasticity in human motor cortex,” Journal of Neuroscience, vol. 18, no. 17, pp. 7000–7007, 1998. View at Google Scholar · View at Scopus
  21. R. Hanajima, Y. Ugawa, Y. Terao et al., “Paired-pulse magnetic stimulation of the human motor cortex: differences among I waves,” Journal of Physiology, vol. 509, no. 2, pp. 607–618, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. T. D. Sanger, R. R. Garg, and R. Chen, “Interactions between two different inhibitory systems in the human motor cortex,” Journal of Physiology, vol. 530, no. 2, pp. 307–317, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. F. Ferreri, G. Curcio, P. Pasqualetti, L. De Gennaro, R. Fini, and P. M. Rossini, “Mobile phone emissions and human brain excitability,” Annals of Neurology, vol. 60, no. 2, pp. 188–196, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Mariorenzi, F. Zarola, M. D. Caramia, C. Paradiso, and P. M. Rossini, “Non-invasive evaluation of central motor tract excitability changes following peripheral nerve stimulation in healthy humans,” Electroencephalography and Clinical Neurophysiology, vol. 81, no. 2, pp. 90–101, 1991. View at Google Scholar · View at Scopus
  25. K. Stefan, E. Kunesch, L. G. Cohen, R. Benecke, and J. Classen, “Induction of plasticity in the human motor cortex by paired associative stimulation,” Brain, vol. 123, no. 3, pp. 572–584, 2000. View at Google Scholar
  26. H. Tokimura, V. Di Lazzaro, Y. Tokimura et al., “Short latency inhibition of human hand motor cortex by somatosensory input from the hand,” Journal of Physiology, vol. 523, no. 2, pp. 503–513, 2000. View at Google Scholar · View at Scopus
  27. V. Di Lazzaro, A. Oliviero, P. Profice et al., “Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex,” Experimental Brain Research, vol. 135, no. 4, pp. 455–461, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Post and M. E. Keck, “Transcranial magnetic stimulation as a therapeutic tool in psychiatry: what do we know about the neurobiological mechanisms?” Journal of Psychiatric Research, vol. 35, no. 4, pp. 193–215, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. R. E. Hoffman and I. Cavus, “Slow transcranial magnetic stimulation, long-term depotentiation, and brain hyperexcitability disorders,” American Journal of Psychiatry, vol. 159, no. 7, pp. 1093–1102, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. V. Di Lazzaro, A. Oliviero, F. Pilato et al., “Motor cortex hyperexcitability to transcranial magnetic stimulation in Alzheimer's disease,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 75, no. 4, pp. 555–559, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. V. Di Lazzaro, A. Oliviero, F. Pilato et al., “Neurophysiological predictors of long term response to AChE inhibitors in AD patients,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 76, no. 8, pp. 1064–1069, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. V. Di Lazzaro, F. Pilato, M. Dileone et al., “In vivo cholinergic circuit evaluation in frontotemporal and Alzheimer dementias,” Neurology, vol. 66, no. 7, pp. 1111–1113, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Pennisi, R. Ferri, M. Cantone et al., “A review of transcranial magnetic stimulation in vascular dementia,” Dementia and Geriatric Cognitive Disorders, vol. 31, no. 1, pp. 71–80, 2011. View at Publisher · View at Google Scholar
  34. G. Pennisi, R. Ferri, G. Lanza et al., “Transcranial magnetic stimulation in Alzheimer's disease: a neurophysiological marker of cortical hyperexcitability,” Journal of Neural Transmission, vol. 118, no. 4, pp. 587–598, 2011. View at Publisher · View at Google Scholar
  35. A. Perretti, D. Grossi, N. Fragassi et al., “Evaluation of the motor cortex by magnetic stimulation in patients with Alzheimer disease,” Journal of the Neurological Sciences, vol. 135, no. 1, pp. 31–37, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. P. M. Rossini, M. T. Desiato, and M. D. Caramia, “Age-related changes of motor evoked potentials in healthy humans: non-invasive evaluation of central and peripheral motor tracts excitability and conductivity,” Brain Research, vol. 593, no. 1, pp. 14–19, 1992. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Peinemann, C. Lehner, B. Conrad, and H. R. Siebner, “Age-related decrease in paired-pulse intracortical inhibition in the human primary motor cortex,” Neuroscience Letters, vol. 313, no. 1-2, pp. 33–36, 2001. View at Publisher · View at Google Scholar
  38. M. De Carvalho, A. De Mendonça, P. C. Miranda, C. Garcia, and M. De Lourdes Sales Luís, “Magnetic stimulation in Alzheimer's disease,” Journal of Neurology, vol. 244, no. 5, pp. 304–307, 1997. View at Publisher · View at Google Scholar
  39. J. L. Pepin, D. Bogacz, V. De Pasqua, and P. J. Delwaide, “Motor cortex inhibition is not impaired in patients with Alzheimer's disease: evidence from paired transcranial magnetic stimulation,” Journal of the Neurological Sciences, vol. 170, no. 2, pp. 119–123, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Alagona, R. Bella, R. Ferri et al., “Transcranial magnetic stimulation in Alzheimer disease: motor cortex excitability and cognitive severity,” Neuroscience Letters, vol. 314, no. 1-2, pp. 57–60, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Pennisi, G. Alagona, R. Ferri et al., “Motor cortex excitability in Alzheimer disease: one year follow-up study,” Neuroscience Letters, vol. 329, no. 3, pp. 293–296, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Inghilleri, A. Conte, V. Frasca et al., “Altered response to rTMS in patients with Alzheimer's disease,” Clinical Neurophysiology, vol. 117, no. 1, pp. 103–109, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Liepert, K. J. Bär, U. Meske, and C. Weiller, “Motor cortex disinhibition in Alzheimer's disease,” Clinical Neurophysiology, vol. 112, no. 8, pp. 1436–1441, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Pierantozzi, M. Panella, M. G. Palmieri et al., “Different TMS patterns of intracortical inhibition in early onset Alzheimer dementia and frontotemporal dementia,” Clinical Neurophysiology, vol. 115, no. 10, pp. 2410–2418, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Nardone, A. Bratti, and F. Tezzon, “Motor cortex inhibitory circuits in dementia with Lewy bodies and in Alzheimer's disease,” Journal of Neural Transmission, vol. 113, no. 11, pp. 1679–1684, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. V. Di Lazzaro, A. Oliviero, F. Pilato et al., “Motor cortex hyperexcitability to transcranial magnetic stimulation in Alzheimer's disease: evidence of impaired glutamatergic neurotransmission?” Annals of Neurology, vol. 53, no. 6, pp. 824–825, 2003. View at Google Scholar
  47. V. Di Lazzaro, A. Oliviero, P. Profice et al., “Ketamine increases human motor cortex excitability to transcranial magnetic stimulation,” Journal of Physiology, vol. 547, no. 2, pp. 485–496, 2003. View at Publisher · View at Google Scholar
  48. M. R. Farlow, “NMDA receptor antagonists: a new therapeutic approach for Alzheimer's disease,” Geriatrics, vol. 59, no. 6, pp. 22–27, 2004. View at Google Scholar · View at Scopus
  49. M. R. Hynd, H. L. Scott, and P. R. Dodd, “Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer's disease,” Neurochemistry International, vol. 45, no. 5, pp. 583–595, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Voisin, E. Reynish, F. Portet, H. Feldman, and B. Vellas, “What are the treatment options for patients with severe Alzheimer's disease?” CNS Drugs, vol. 18, no. 9, pp. 575–583, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. P. T. Francis, A. M. Palmer, M. Snape, and G. K. Wilcock, “The cholinergic hypothesis of Alzheimer's disease: a review of progress,” Journal of Neurology Neurosurgery and Psychiatry, vol. 66, no. 2, pp. 137–147, 1999. View at Google Scholar · View at Scopus
  52. S. L. Lowe, D. M. Bowen, P. T. Francis, and D. Neary, “Ante mortem cerebral amino acid concentrations indicate selective degeneration of glutamate-enriched neurons in Alzheimer's disease,” Neuroscience, vol. 38, no. 3, pp. 571–577, 1990. View at Publisher · View at Google Scholar
  53. S. L. Lowe, P. T. Francis, A. W. Procter, A. M. Palmer, A. N. Davison, and D. M. Bowen, “Gamma-aminobutyric acid concentration in brain tissue at two stages of Alzheimer's disease,” Brain, vol. 111, no. 4, pp. 785–799, 1988. View at Google Scholar · View at Scopus
  54. K. Stefan, E. Kunesch, L. G. Cohen, R. Benecke, and J. Classen, “Induction of plasticity in the human motor cortex by paired associative stimulation,” Brain, vol. 123, no. 3, pp. 572–584, 2000. View at Google Scholar · View at Scopus
  55. R. Nardone, J. Bergmann, M. Kronbichler et al., “Abnormal short latency afferent inhibition in early Alzheimer's disease: a transcranial magnetic demonstration,” Journal of Neural Transmission, vol. 115, no. 11, pp. 1557–1562, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Martorana, F. Mori, Z. Esposito et al., “Dopamine modulates cholinergic cortical excitability in Alzheimer's disease patients,” Neuropsychopharmacology, vol. 34, no. 10, pp. 2323–2328, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. F. Ferreri, P. Pasqualetti, S. Määttä et al., “Human brain connectivity during single and paired pulse transcranial magnetic stimulation,” NeuroImage, vol. 54, no. 1, pp. 90–102, 2011. View at Publisher · View at Google Scholar
  58. D. Suvà, I. Favre, R. Kraftsik, M. Esteban, A. Lobrinus, and J. Miklossy, “Primary motor cortex involvement in Alzheimer disease,” Journal of Neuropathology and Experimental Neurology, vol. 58, no. 11, pp. 1125–1134, 1999. View at Google Scholar · View at Scopus
  59. J. N. Sanes and J. P. Donoghue, “Plasticity and primary motor cortex,” Annual Review of Neuroscience, vol. 23, pp. 393–415, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. P. Cicinelli, R. Traversa, A. Bassi, G. Scivoletto, and P. M. Rossini, “Interhemispheric differences of hand muscle representation in human motor cortex,” Muscle and Nerve, vol. 20, no. 5, pp. 535–542, 1997. View at Publisher · View at Google Scholar · View at Scopus
  61. V. Di Lazzaro, F. Pilato, M. Dileone et al., “Functional evaluation of cerebral cortex in dementia with Lewy bodies,” NeuroImage, vol. 37, no. 2, pp. 422–429, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. V. Di Lazzaro, F. Pilato, M. Dileone et al., “In vivo functional evaluation of central cholinergic circuits in vascular dementia,” Clinical Neurophysiology, vol. 119, no. 11, pp. 2494–2500, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Solé-Padullés, D. Bartrés-Faz, C. Junqué et al., “Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study,” Cerebral Cortex, vol. 16, no. 10, pp. 1487–1493, 2006. View at Publisher · View at Google Scholar
  64. M. Cotelli, R. Manenti, S. F. Cappa et al., “Effect of transcranial magnetic stimulation on action naming in patients with Alzheimer disease,” Archives of Neurology, vol. 63, no. 11, pp. 1602–1604, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Cotelli, R. Manenti, S. F. Cappa, O. Zanetti, and C. Miniussi, “Transcranial magnetic stimulation improves naming in Alzheimer disease patients at different stages of cognitive decline,” European Journal of Neurology, vol. 15, no. 12, pp. 1286–1292, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Cotelli, M. Calabria, R. Manenti et al., “Improved language performance in Alzheimer disease following brain stimulation,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 82, no. 7, pp. 794–797, 2011. View at Google Scholar
  67. J. Bentwich, E. Dobronevsky, S. Aichenbaum et al., “Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer's disease: a proof of concept study,” Journal of Neural Transmission, vol. 118, no. 3, pp. 463–471, 2011. View at Publisher · View at Google Scholar
  68. S. Rossi and P. M. Rossini, “TMS in cognitive plasticity and the potential for rehabilitation,” Trends in Cognitive Sciences, vol. 8, no. 6, pp. 273–279, 2004. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Julkunen, A. M. Jauhiainen, S. Westerén-Punnonen et al., “Navigated TMS combined with EEG in mild cognitive impairment and Alzheimer's disease: a pilot study,” Journal of Neuroscience Methods, vol. 172, no. 2, pp. 270–276, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. R. J. Ilmoniemi, J. Virtanen, J. Ruohonen et al., “Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity,” Neuroreport, vol. 8, no. 16, pp. 3537–3540, 1997. View at Google Scholar