Neurophysiological features of motor cortex excitability and plasticity in Subcortical Ischemic Vascular Dementia: A TMS mapping study

Clinical Neurophysiology

Volumn 126, Issue 5, 2015, Pages 906-913

  Guerra, Andrea ^a   Petrichella, Sara ^a   Vollero, Luca ^a   Ponzo, David ^a,b   Pasqualetti, Patrizio ^c   Määttä, Sara ^b   Mervaala, Esa ^b   Könönen, Mervi ^b   Bressi, Federica ^a   Iannello, Giulio ^a   Rossini, Paolo Maria ^d,e   Ferreri, Florinda ^a,b  

^a UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

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

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e IRCCS San RaffaelePisana   (Italy)

Author keywords

Hyperexcitability; Mapping; Motor cortex; Plasticity; SIVD; TMS; VaD

Indexed keywords

ACETYLCHOLINE;

ACETYLCHOLINE RELEASE; AGED; ALZHEIMER DISEASE; ANTERIOR POSTERIOR AXIS; ARTICLE; BRAIN MAPPING; CLINICAL ARTICLE; CLINICAL EVALUATION; CONTROLLED STUDY; EXECUTIVE FUNCTION; FEMALE; GRAVITY; HUMAN; LEFT HEMISPHERE; MALE; MOTOR CORTEX; MULTIINFARCT DEMENTIA; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NEUROPHYSIOLOGY; PRIORITY JOURNAL; RIGHT HEMISPHERE; SUBCORTICAL ISCHEMIC VASCULAR DEMENTIA; TRANSCRANIAL MAGNETIC STIMULATION; DEMENTIA, VASCULAR; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; VERY ELDERLY;

AGED; AGED, 80 AND OVER; BRAIN MAPPING; DEMENTIA, VASCULAR; FEMALE; HUMANS; MALE; MIDDLE AGED; MOTOR CORTEX; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84926216166     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2014.07.036     Document Type: Article

References (69)

1. Alagona G., Bella R., Ferri R., Carnemolla A., Pappalardo A., Costanzo E., et al. Transcranial magnetic stimulation in Alzheimer disease: motor cortex excitability and cognitive severity. Neurosci Lett 2001, 314:57-60.
2. Alagona G., Ferri R., Pennisi G., Greco S., Santonocito D., Pappalardo A., et al. Motor cortex excitability in Alzheimer's disease and in subcortical ischemic vascular dementia. Neurosci Lett 2004, 362:95-98.
3. Basso D., Lotze M., Vitale L., Ferreri F., Bisiacchi P., Olivetti Belardinelli M., et al. The role of prefrontal cortex in visuo-spatial planning: a repetitive TMS study. Exp Brain Res 2006, 171:411-415.
4. Becker N., Wierenga C.J., Fonseca R., Bonhoeffer T., Nägerl U.V. LTD induction causes morphological changes of presynaptic boutons and reduces their contacts with spines. Neuron 2008, 60:590-597.
5. Bella R., Ferri R., Pennisi M., Cantone M., Lanza G., Malaguarnera G., et al. Enhanced motor cortex facilitation in patients with vascular cognitive impairment-no dementia. Neurosci Lett 2011, 503:171-175.
6. Burke W.J., Houston M.J., Boust S.J., Roccaforte W.H. Use of the geriatric depression scale in dementia of the Alzheimer type. J Am Geriatr Soc 1989, 37:856-860.
7. Dal Forno G., Chiovenda P., Bressi F., Ferreri F., Grossi E., Brandt J., et al. Use of an Italian version of the telephone interview for cognitive status in Alzheimer's disease. Int J Geriatr Psychiatry 2006, 21:126-133.
8. Di Lazzaro V., Oliviero A., Pilato F., Saturno E., Dileone M., Tonali P.A. Motor cortex hyperexcitability to transcranial magnetic stimulation in Alzheimer's disease: evidence of impaired glutamatergic neurotransmission?. Ann Neurol 2003, 53:824.
9. Di Lazzaro V., Oliviero A., Pilato F., Saturno E., Dileone M., Marra C., et al. Motor cortex hyperexcitability to transcranial magnetic stimulation in Alzheimer's disease. J Neurol Neurosurg Psychiatry 2004, 75:555-559.
10. Di Lazzaro V., Pilato F., Dileone M., Saturno E., Oliviero A., Marra C., et al. In vivo cholinergic circuit evaluation in frontotemporal and Alzheimer dementias. Neurology 2006, 66:1111-1113.
11. Di Lazzaro V., Pilato F., Dileone M., Profice P., Marra C., Ranieri F., et al. In vivo functional evaluation of central cholinergic circuits in vascular dementia. Clin Neurophysiol 2008, 119:2494-2500.
12. Di Rosa M., Dell'Ombra N., Zambito A.M., Malaguarnera M., Nicoletti F., Malaguarnera L. Chitotriosidase and inflammatory mediator levels in Alzheimer's disease and cerebrovasculardementia. Eur J Neurosci 2006, 23:2648-2656.
13. Erkinjuntti T., Inzitari D., Pantoni L., Wallin A., Scheltens P., Rockwood K., et al. Research criteria for subcortical vasculardementia in clinical trials. J Neural Transm Suppl 2000, 59:23-30.
14. Feig S., Lipton P. Pairing the cholinergic agonist carbachol with patterned Schaffer collateral stimulation initiates protein synthesis in hippocampal CA1 pyramidal cell dendrites via a muscarinic, NMDA-dependent mechanism. J Neurosci 1993, 13:1010-1021.
15. Ferreri F., Pauri F., Pasqualetti P., Fini R., Dal Forno G., Rossini P.M. Motor cortex excitability in Alzheimer's disease: a transcranial magnetic stimulation study. Ann Neurol 2003, 53:102-108.
16. Ferreri F., Pasqualetti P., Määttä S., Ponzo D., Guerra A., Bressi F., et al. Motor cortex excitability in Alzheimer's disease: a transcranial magnetic stimulation follow-up study. Neurosci Lett 2011, 492:94-98.
17. Ferreri F., Ponzo D., Hukkanen T., Mervaala E., Könönen M., Pasqualetti P., et al. Human brain cortical correlates of short-latency afferent inhibition: a combined EEG-TMS study. J Neurophysiol 2012, 108:314-323.
18. Ferreri F., Rossini P.M. TMS and TMS-EEG techniques in the study of the excitability, connectivity, and plasticity of the human motor cortex. Rev Neurosci 2013, 24:431-442.
19. Ferreri F., Vecchio F., Ponzo D., Pasqualetti P., Rossini P.M. Time-varying coupling of EEG oscillations predicts excitability fluctuations in the primary motor cortex as reflected by motor evoked potentials amplitude: an EEG-TMS study. Hum Brain Mapp 2014, 35:1969-1980.
20. Folstein M.F., Folstein S.E., McHugh P.R. "Mini Mental State": a practical method for grading the cognitive state of patient for the clinician. J Psychiatr Res 1975, 12:189-198.
21. Fratiglioni L., Launer L.J., Andersen K., Breteler M.M., Copeland J.R., Dartigues J.F., et al. Incidence of dementia and major subtypes in Europe: a collaborative study of population-based cohorts. Neurologic diseases in the elderly research group. Neurology 2000, 54:S10-S15.
22. Gainotti G., Marra C., Villa G. A double dissociation between accuracy and time of execution on attentional tasks in Alzheimer's disease and multi-infarct dementia. Brain 2001, 124:731-738.
23. Gottfries C.G., Blennow K., Karlsson I., Wallin A. The neuro chemistry of vascular dementia. Dementia 1994, 5:163-167.
24. Guerra A., Assenza F., Bressi F., Scrascia F., Del Duca M., Ursini F., et al. Transcranial magnetic stimulation studies in Alzheimer's disease. Int J Alzheimer Dis 2011, 2011:263817.
25. Hallett M., Epstein C.M., Berardelli A., Sackeim H., Maccabee P. Topics in transcranial magnetic stimulation. Suppl Clin Neurophysiol 2000, 53:301-311.
26. Hoeppner J., Wegrzyn M., Thome J., Bauer A., Oltmann I., Buchmann J., et al. Intra- and inter-cortical motor excitability in Alzheimer's disease. J Neural Transm 2012, 119:605-612.
27. Kalaria R. Similarities between Alzheimer's disease and vascular dementia. J Neurol Sci 2002, 203-204:29-34.
28. Kalaria R.N., Ballard C. Overlap between pathology of Alzheimer disease and vascular dementia. Alzheimer Dis Assoc Disord 1999, 13(Suppl. 3). S115-23.
29. Khedr E.M., Ahmed M.A., Darwish E.S., Ali A.M. The relationship between motor cortex excitability and severity of Alzheimer's disease: a transcranial magnetic stimulation study. Neurophysiol Clin 2011, 41:107-113.
30. Lee J.H., Kim S.H., Kim G.H., Seo S.W., Park H.K., Oh S.J., et al. Identification of pure subcortical vascular dementia using 11C-Pitts burgh compound B. Neurology 2011, 77:18-25.
31. Lawton M.P., Brody E.M. Assessment of older people: self maintaining and instrumental activities of daily living. Gerontologist 1969, 9:179-186.
32. Liepert J., Bär K.J., Meske U., Weiller C. Motor cortex disinhibition in Alzheimer's disease. Clin Neurophysiol 2001, 112:1436-1441.
33. Lisman J., Lichtman J.W., Sanes J.R. LTP: perils and progress. Nat Rev Neurosci 2003, 4:926-929.
34. Looi J.C., Sachdev P.S. Differentiation of vascular dementia from AD on neuropsychological tests. Neurology 1999, 53:670-678.
35. Määttä S., Landsness E., Sarasso S., Ferrarelli F., Ferreri F., Ghilardi M.F., et al. The effects of morning training on night sleep: a behavioral and EEG study. Brain Res Bull 2010, 82:118-123.
36. Malaguarnera L., Motta M., Di Rosa M., Anzaldi M., Malaguarnera M. Interleukin-18 and transforming growth factor-beta 1 plasma levels in Alzheimer's disease and vascular dementia. Neuropathology 2006, 26:307-312.
37. Malaguarnera M., Ferri R., Bella R., Alagona G., Carnemolla A., Pennisi G. Homocysteine, vitamin B12 and folate in vascular dementia and in Alzheimer disease. Clin Chem Lab Med 2004, 42:1032-1035.
38. Martin K.C., Barad M., Kandel E.R. Local protein synthesis and its role in synapse specific plasticity. Curr Opin Neurobiol 2000, 10:587-592.
39. Martorana A., Mori F., Esposito Z., Kusayanagi H., Monteleone F., Codecà C., et al. Dopamine modulates cholinergic cortical excitability in Alzheimer's disease patients. Neuropsychopharmacology 2009, 34:2323-2328.
40. McKhann G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984, 34:939-944.
41. Mega M.S., Cummings J.L. Frontal-subcortical circuits and neuropsychiatric disorders. J Neuropsychiatry Clin Neurosci 1994, 6:358-370.
42. Nardone R., Bratti A., Tezzon F. Motor cortex inhibitory circuits in dementia with Lewy bodies and in Alzheimer's disease. J Neural Transm 2006, 113:1679-1684.
43. Nardone R., Bergmann J., Tezzon F., Ladurner G., Golaszewski S. Cholinergic dysfunction in subcortical ischaemic vascular dementia: a transcranial magnetic stimulation study. J Neural Transm 2008, 115:737-743.
44. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 2010, 9:689-701.
45. Pennisi G., Ferri R., Alagona G., Pennisi M., Malaguarnera G., Motta M., et al. Motor cortex hyperexcitability in subcortical ischemic vascular dementia. Arch Gerontol Geriatr 2010, 53:111-113.
46. Pennisi G., Ferri R., Lanza G., Cantone M., Pennisi M., Puglisi V., et al. Transcranial magnetic stimulation in Alzheimer's disease: a neurophysiological marker of cortical hyperexcitability. J Neural Transm 2011, 118:587-598.
47. Pennisi G., Ferri R., Cantone M., Lanza G., Pennisi M., Vinciguerra L., et al. A review of transcranial magnetic stimulation in vascular dementia. Dement Geriatr Cogn Disord 2011, 31:71-80.
48. Pepin J.L., Bogacz D., de Pasqua V., Delwaide P.J. Motor cortex inhibition is not impaired in patients with Alzheimer's disease: evidence from paired transcranial magnetic stimulation. J Neurol Sci 1999, 170:119-123.
49. Pfurtscheller G., Kalcher J., Neuper C., Flotzinger D., Pregenzer M. On-line EEG classification during externally-paced hand movements using a neural network based classifier. Electroencephalogr Clin Neurophysiol 1996, 99:416-425.
50. Pierantozzi M., Panella M, Palmieri M.G., Koch G., Giordano A., Marciani M.G., et al. Different TMS patterns of intracortical inhibition in early onset Alzheimer dementia and frontotemporal dementia. Clin Neurophysiol 2004, 115:2410-2418.
51. Polania R., Nitsche M.A., Paulus W. Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation. Hum Brain Mapp 2011, 32:1236-1249.
52. Polania R., Paulus W., Antal A., Nitsche M.A. Introducing graph theory to track for neuroplastic alterations in the resting human brain: a transcranial direct current stimulation study. Neuroimage 2011, 54:2287-2296.
53. Roh J.H., Lee J.H. Recent updates on subcortical ischemic vascular dementia. J Stroke 2014, 16:18-26.
54. Romàn G.C., Tatemichi T.K., Erkinjuntti T., Cummings J.L., Masdeu J.C., Garcia J.H., et al. Vascular dementia: diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology 1993, 43:250-260.
55. Romàn G.C., Erkinjuntti T., Wallin A., Pantoni L., Chui H.C. Subcortical ischaemic vascular dementia. Lancet Neurol 2002, 1:426-436.
56. Rossi S., Hallett M., Rossini P.M., Pascual-Leone A. Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009, 120:2008-2039.
57. Rossini P.M., Barker A.T., Berardelli A., Caramia M.D., Caruso G., Cracco R.Q., et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Electroencephalogr Clin Neurophysiol 1994, 91:79-92.
58. Rossini P.M., Berardelli A., Deuschl G., Hallett M., Maertens de Noordhout A.M., Paulus W., et al. Applications of magnetic cortical stimulation. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol 1999, 52:171-185.
59. Rossini P.M., Pauri F. Neuromagnetic integrated methods tracking human brain mechanisms of sensorimotor areas 'plastic' reorganisation. Brain Res Brain Res Rev 2000, 33:131-154.
60. Rossini P.M., Rossini L., Ferreri F. Brain-behavior relations: transcranial magnetic stimulation: a review. IEEE Eng Med Biol Mag 2010, 29:84-95.
61. Rossini P.M., Ferilli M.A., Rossini L., Ferreri F. Clinical neurophysiology of brain plasticity in aging brain. Curr Pharm Des 2013, 19:6426-6439.
62. Rothwell J.C., Hallett M., Berardelli A., Eisen A., Rossini P., Paulus W. Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol 1999, 52:97-103.
63. Sato A., Sato Y., Uchida S. Activation of the intracerebral cholinergic nerve fibers originating in the basal forebrain increases regional cerebral blood flow in the rat's cortex and hippocampus. Neurosci Lett 2004, 361:90-93.
64. Sporns O., Chialvo D.R., Kaiser M., Hilgetag C.C. Organization, development and function of complex brain networks. Trends Cogn Sci 2004, 8:418-425.
65. Sporns O. The non-random brain: efficiency, economy, and complex dynamics. Front Comput Neurosci 2011, 5:5.
66. Tayebati S.K., Tomassoni D., Amenta F. Spontaneously hypertensive rat as a model of vascular brain disorder: microanatomy, neurochemistry and behavior. J Neurol Sci 2012, 322:241-249.
67. Toni N., Buchs P.A., Nikonenko I., Bron C.R., Muller D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 1999, 402:421-425.
68. Tononi G., Sporns O., Edelman G.M. A measure for brain complexity: relating functional segregation and integration in the nervous system. Proc Natl Acad Sci USA 1994, 91:5033-5037.
69. Vecchio F., Babiloni C., Ferreri F., Buffo P., Cibelli G., Curcio G., et al. Mobile phone emission modulates inter-hemispheric functional coupling of EEG alpha rhythms in elderly compared to young subjects. Clin Neurophysiol 2010, 121:163-171.