Cortical plasticity is preserved in nondemented older individuals with severe ischemic small vessel disease

Human Brain Mapping

Volumn 34, Issue 6, 2013, Pages 1464-1476

  List, Jonathan ^a,b   Duning, Thomas ^a   Kürten, Julia ^a   Deppe, Michael ^a   Wilbers, Eike ^a   Flöel, Agnes ^b  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Diffusion tensor imaging; Paired associative stimulation; Transcranial magnetic stimulation; White matter hyperintensities

Indexed keywords

ADULT; AGED; ARTICLE; ASSOCIATION; BRAIN ISCHEMIA; CEREBROVASCULAR DISEASE; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; DISEASE SEVERITY; EXECUTIVE FUNCTION; FEMALE; FRACTIONAL ANISOTROPY; GERIATRIC PATIENT; HUMAN; MALE; MEMORY; MEMORY DISORDER; NERVE CELL PLASTICITY; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIRED ASSOCIATIVE STIMULATION; PARAHIPPOCAMPAL GYRUS; PREFRONTAL CORTEX; PRIORITY JOURNAL; WHITE MATTER;

AGED; ANISOTROPY; BRAIN ISCHEMIA; CEREBRAL CORTEX; COGNITION; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; MALE; MIDDLE AGED; NEURONAL PLASTICITY; NEUROPSYCHOLOGICAL TESTS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84876419781     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22003     Document Type: Article

References (70)

1. Arsava EM, Rahman R, Rosand J, Lu J, Smith EE, Rost NS, Singhal AB, Lev MH, Furie KL, Koroshetz WJ, Sorensen AG, Ay H ( 2009): Severity of leukoaraiosis correlates with clinical outcome after ischemic stroke. Neurology 72: 1403-1410.
2. Aschenbrenner S, Tucha O, Lange K ( 2001): Regensburger Wortflüssigkeitstest (RWT). Göttingen, Bern: Hogrefe-Verlag GmbH & Co. KG.
3. Barnes DE, Covinsky KE, Whitmer RA, Kuller LH, Lopez OL, Yaffe K ( 2009): Predicting risk of dementia in older adults: The late-life dementia risk index. Neurology 73: 173-179.
4. 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: 1405-1412.
5. Bella R, Ferri R, Pennisi M, Cantone M, Lanza G, Malaguarnera G, Spampinato C, Giordano D, Alagona G, Pennisi G ( 2011): Enhanced motor cortex facilitation in patients with vascular cognitive impairment-no dementia. Neurosci Lett 503: 171-175.
6. Black S, Gao F, Bilbao J ( 2009): Understanding white matter disease: Imaging pathological correlations in vascular cognitive impairment. Stroke 40: S48-S52.
7. Bliss TV, Collingridge GL ( 1993): A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361: 31-39.
8. Buonomano DV, Merzenich MM ( 1998): Cortical plasticity: From synapses to maps. Annu Rev Neurosci 21: 149-186.
9. Bütefisch CM, Netz J, Wessling M, Seitz RJ, Hömberg V ( 2003): Remote changes in cortical excitability after stroke. Brain 126: 470-481.
10. Castel-Lacanal E, Gerdelat-Mas A, Marque P, Loubinoux I, Simonetta-Moreau M ( 2007): Induction of cortical plastic changes in wrist muscles by paired associative stimulation in healthy subjects and post-stroke patients. Exp Brain Res 180: 113-122.
11. Castel-Lacanal E, Marque P, Tardy J, de Boissezon X, Guiraud V, Chollet F, Loubinoux I, Moreau MS ( 2009): Induction of cortical plastic changes in wrist muscles by paired associative stimulation in the recovery phase of stroke patients. Neurorehabil Neural Repair 23: 366-372.
12. Cirillo J, Lavender AP, Ridding MC, Semmler JG ( 2009): Motor cortex plasticity induced by paired associative stimulation is enhanced in physically active individuals. J Physiol 587: 5831-5842.
13. Deppe M, Duning T, Mohammadi S, Schwindt W, Kugel H, Knecht S, Ringelstein EB ( 2007): Diffusion-tensor imaging at 3 T: Detection of white matter alterations in neurological patients on the basis of normal values. Invest Radiol 42: 338-345.
14. Deppe M, Kellinghaus C, Duning T, Moddel G, Mohammadi S, Deppe K, Schiffbauer H, Kugel H, Keller SS, Ringelstein EB. Knecht S ( 2008): Nerve fiber impairment of anterior thalamocortical circuitry in juvenile myoclonic epilepsy. Neurology 71: 1981-1985.
15. Di Lazzaro V, Pilato F, Dileone M, Profice P, Marra, C, Ranieri F, Quaranta D, Gainotti G, Tonali PA ( 2008): In vivo functional evaluation of central cholinergic circuits in vascular dementia. Clin Neurophysiol 119: 2494-2500.
16. Dichgans M ( 2009): Cognition in CADASIL. Stroke 40: S45-S47.
17. Dufouil C, Godin O, Chalmers J, Coskun O, MacMahon S, Tzourio-Mazoyer N, Bousser MG, Anderson C, Mazoyer B, Tzourio C, PROGRESS MRI Substudy Investigators ( 2009): Severe cerebral white matter hyperintensities predict severe cognitive decline in patients with cerebrovascular disease history. Stroke 40: 2219-2221.
18. Duning T, Kugel H, Knecht S ( 2005): Excellent cognitive performance despite massive cerebral white matter changes. Neuroradiology 47: 749-752.
19. Eisenberg DP, Berman KF ( 2010): Executive function, neural circuitry, and genetic mechanisms in schizophrenia. Neuropsychopharmacology 35: 258-277.
20. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA ( 1987): MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am J Roentgenol 149: 351-356.
21. Flöel A, Ruscheweyh R, Krüger K, Willemer C, Winter B, Völker K, Lohmann H, Zitzmann M, Mooren F, Breitenstein C, Knecht S ( 2010): Physical activity and memory functions: Are neurotrophins and cerebral gray matter volume the missing link? Neuroimage 49: 2756-2763.
22. 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: 189-198.
23. Frantseva MV, Fitzgerald PB, Möller B, Daigle M, Daskalakis ZJ ( 2008): Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill learning. Cereb Cortex 18: 990-996.
24. Frisoni GB, Fox NC, Jack CR, Scheltens P, Thompson PM ( 2010): The clinical use of structural MRI in Alzheimer disease. Nat Rev Neurol 6: 67-77.
25. Geerlings MI, Appelman AP, Vincken KL, Mali WP, van der Graaf Y ( 2009): Association of white matter lesions and lacunar infarcts with executive functioning: The SMART-MR study. Am J Epidemiol 170: 1147-1155.
26. Hautzinger M, Bailer M, Worall H, Keller F ( 1994): Beck-Depressions-Inventar (BDI). Bern: Huber.
27. Helmstaedter C, Lendt M, Lux M ( 2001): Verbaler Lern und Merkfähigkeitstest. Göttingen (Germany): Beltz.
28. Ihara K, Tomimoto H, Ishizu M, Mukai T, Yoshida H, Sawamoto N, Inoue M, Doi T, Hashikawa K, Konishi J, Shibasaki H, Fukuyama H ( 2004): Decrease in cortical benzodiazepine receptors in symptomatic patients with leukoaraiosis: A positron emission tomography study. Stroke 35: 942-947.
29. Khan ZU, Muly EC ( 2011): Molecular mechanisms of working memory. Behav Brain Res 219: 329-341.
30. Kleim JA, Jones TA ( 2008): Principles of experience-dependent neural plasticity: Implications for rehabilitation after brain damage. J Speech Lang Hear Res 51: S225-S239.
31. Knecht S, Wersching H, Lohmann H, Bruchmann M, Duning T, Dziewas R, Berger K, Ringelstein EB ( 2008): High normal blood pressure is adapted with poor cognitive performance. Hypertension 51: 663-668.
32. Kuo MF, Paulus W, Nitsche MA ( 2008): Boosting focally-induced brain plasticity by dopamine. Cereb Cortex 18: 648-651.
33. Lezak MD ( 2004): Neuropsychological Assessment. New York, Oxford: Oxford University Press.
34. List J, Duning T, Meinzer M, Kürten J, Schirmacher A, Deppe M, Evers S, Young P, Flöel A ( 2011): Enhanced rapid-onset cortical plasticity in CADASIL as a possible mechanism for preserved cognition. Cereb Cortex 21: 2774-2787.
35. Lyden P, Lu M, Jackson C, Marler J, Kothari R, Brott T, Zivin J ( 1999): Underlying structure of the National Institutes of Health Stroke Scale: Results of a factor analysis. NINDS tPA Stroke Trial Investigators. Stroke 30: 2347-2354.
36. Mattson MP, Maudsle S, Martin B ( 2004): BDNF and 5-HT: A dynamic duo in age-related neuronal plasticity and neurodegenerative disorders. Trends Neurosci 27: 589-594.
37. Mohammadi S, Moller HE, Kugel H, Muller DK, Deppe M ( 2010): Correcting eddy current and motion effects by affine whole-brain registrations: Evaluation of three-dimensional distortions and comparison with slicewise correction. Magn Reson Med 64: 1047-1056.
38. Müller-Dahlhaus JF, Orekhov Y, Liu Y, Ziemann U ( 2008): Interindividual variability and age-dependency of motor cortical plasticity induced by paired associative stimulation. Exp Brain Res 187: 467-475.
39. O'Brien JT, Erkinjuntti T, Reisberg B, Roman G, Sawada T, Pantoni L, Bowler JV, Ballard C, DeCarli C, Gorelick PB, Rockwood K, Burns A, Gauthier S, DeKosky ST ( 2003): Vascular cognitive impairment. Lancet Neurol 2: 89-98.
40. O'sullivan M ( 2008): Leukoaraiosis. Pract Neurol 8: 26-38.
41. O'sullivan M ( 2010): Imaging small vessel disease: Lesion topography, networks, and cognitive deficits investigated with MRI. Stroke 41: S154-S158.
42. Oldfield RC ( 1971): The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9: 97-113.
43. Osterrieth P ( 1944): Le test de copie d'une figure complexe. Arch Psychol 30: 286-350.
44. Pantoni L, Pescini F, Nannucci S, Sarti C, Bianchi S, Dotti MT, Federico A, Inzitari D ( 2010): Comparison of clinical, familial, and MRI features of CADASIL and NOTCH3-negative patients. Neurology 74: 57-63.
45. Park DC, Reuter-Lorenz P ( 2009): The adaptive brain: Aging and neurocognitive scaffolding. Annu Rev Psychol 60: 173-196.
46. Pennisi G, Ferri R, Alagona G, Pennisi M, Malaguarnera G, Motta M, Bella R ( 2011): Motor cortex hyperexcitability in subcortical ischemic vascular dementia. Arch Gerontol Geriatr 53: e111-e113.
47. Pennisi G, Ferri R, Cantone M, Lanza G, Pennisi M, Vinciguerra L, Malaguarnera G, Bella R ( 2011a): A review of transcranial magnetic stimulation in vascular dementia. Dement Geriatr Cogn Disord 31: 71-80.
48. Pennisi G, Ferri R, Lanza G, Cantone M, Pennisi M, Puglisi V, Malaguarnera G, Bella R ( 2011b): Transcranial magnetic stimulation in Alzheimer's Disease: A neurophysiological marker of cortical hyperexcitability. J Neural Transm 118: 587-598.
49. Peters N, Opherk C, Danek A, Ballard C, Herzog J, Dichgans M ( 2005): The pattern of cognitive performance in CADASIL: A monogenic condition leading to subcortical ischemic vascular dementia. Am J Psychiatry 162: 2078-2085.
50. R Development Core Team ( 2010): R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing.
51. Reddy H, Stefano ND, Mortilla M, Federico A, Matthews PM ( 2002): Functional reorganization of motor cortex increases with greater axonal injury from CADASIL. Stroke 33: 502-508.
52. Rioult-Pedotti MS, Friedman D, Donoghue JP ( 2000): Learning-induced LTP in neocortex. Science 290: 533-536.
53. Rogalski EJ, Murphy CM, deToledo-Morrell L, Shah RC, Moseley ME, Bammer R, Stebbins GT ( 2009): Changes in parahippocampal white matter integrity in amnestic mild cognitive impairment: a diffusion tensor imaging study. Behav Neurol 21: 51-61.
54. Rosenberg GA ( 2009): Inflammation and white matter damage in vascular cognitive impairment. Stroke 40: S20-S23.
55. Rosenzweig ES, Barnes CA ( 2003): Impact of aging on hippocampal formation: Plasticity, network dynamics and cognition. Prog Neurobiol 69: 143-179.
56. Sato Y, Chin Y, Kato T, Tanaka Y, Tozuka Y, Mase M, Ageyama N, Ono F, Terao K, Yoshikawa Y, Hisatsune T ( 2009): White matter activated glial cells produce BDNF in a stroke model of monkeys. Neurosci Res 65: 71-78.
57. Sawaki L, Yaseen Z, Kopylev L, Cohen LG ( 2003): Age-dependent changes in the ability to encode a novel elementary motor memory. Ann Neurol 53: 521-524.
58. Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A, Stefano ND ( 2002): Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17: 479-489.
59. Squire LR, Zola-Morgan S ( 1991): The medial temporal lobe memory system. Science 253: 1380-1386.
60. Stagg CJ, Best JG, Stephenson MC, O'Shea J, Wylezinska M, Kincses ZT, Morris PG, Matthews PM, Johansen-Berg H ( 2009): Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci 29: 5202-5206.
61. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J ( 2000): Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123: 572-584.
62. Stoub TR, deToledo-Morrell L, Stebbins GT, Leurgans S, Bennett DA, Shah RC ( 2006): Hippocampal disconnection contributes to memory dysfunction in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci USA 103: 10041-10045.
63. Tombaugh TN ( 2004): Trail Making Test A and B: normative data stratified by age and education. Arch Clin Neuropsychol 19: 203-214.
64. van Praag H ( 2009): Exercise and the brain: Something to chew on. Trends Neurosci 32: 283-290.
65. van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J ( 1988): Interobserver agreement for the assessment of handicap in stroke patients. Stroke 19: 604-607.
66. Vermeer SE, Prins ND, den Heijer T, Hofman A, Koudstaal PJ, Breteler MM ( 2003): Silent brain infarcts and the risk of dementia and cognitive decline. N Engl J Med 348: 1215-1222.
67. Voineskos AN, Rajji TK, Lobaugh NJ, Miranda D, Shenton ME, Kennedy JL, Pollock BG, Mulsant BH ( 2012): Age-related decline in white matter tract integrity and cognitive performance: A DTI tractography and structural equation modeling study. Neurobiol Aging 33: 21-34.
68. Weise D, Schramm A, Stefan K, Wolters A, Reiners K, Naumann M, Classen J ( 2006): The two sides of associative plasticity in writer's cramp. Brain 129: 2709-2721.
69. Won SJ, Kim DY, Gwag BJ ( 2002): Cellular and molecular pathways of ischemic neuronal death. J Biochem Mol Biol 35: 67-86.
70. Ziemann U, Ilíc TV, Pauli C, Meintzschel F, Ruge D ( 2004): Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 24: 1666-1672.