Experimental models of vascular dementia and vascular cognitive impairment: A systematic review

Journal of Neurochemistry

Volumn 115, Issue 4, 2010, Pages 814-828

  Jiwa, Nadim S ^a   Garrard, Peter ^a   Hainsworth, Atticus H ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Binswanger's disease; CADASIL; Cognition; Lacunar state; Small vessel disease

Indexed keywords

CANDESARTAN; CILOSTAZOL; ENDOTHELIN 1; MUSCARINIC M5 RECEPTOR; NOTCH3 RECEPTOR;

ATHEROSCLEROSIS; BRAIN EMBOLISM; CADASIL; CAROTID ARTERY OBSTRUCTION; COGNITIVE DEFECT; DEMENTIA; GERBIL; HIPPOCAMPUS; HYPERHOMOCYSTEINEMIA; HYPERTENSION; MEMORY DISORDER; MIDDLE CEREBRAL ARTERY OCCLUSION; MULTIINFARCT DEMENTIA; NEUROPSYCHOLOGY; PRIORITY JOURNAL; REVIEW; STREPTOZOCIN DIABETES; STROKE; SYSTEMATIC REVIEW; TRANSGENIC MOUSE; VASCULAR AMYLOIDOSIS; VASCULAR COGNITIVE IMPAIRMENT; WHITE MATTER;

ANIMALS; CADASIL; CAROTID STENOSIS; COGNITION DISORDERS; DEMENTIA, VASCULAR; DISEASE MODELS, ANIMAL; HUMANS; SPECIES SPECIFICITY;

GERBILLINAE; MUS; ORYCTOLAGUS CUNICULUS; PRIMATES; RATTUS; RODENTIA; SUIDAE;

EID: 77958534673     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06958.x     Document Type: Review

References (117)

1. Alexis N. E., Dietrich W. D., Green E. J., Prado R. and Watson B. D. (1995) Nonocclusive common carotid artery thrombosis in the rat results in reversible sensorimotor and cognitive behavioral deficits. Stroke 26, 2338-2346.
2. Amenta F., Di Tullio M. A. and Tomassoni D. (2003) Arterial hypertension and brain damage - evidence from animal models (review). Clin. Exp. Hypertens. 25, 359-380.
3. Andersen M. B. and Sams-Dodd F. (1998) Impairment of working memory in the T-maze after transient global cerebral ischemia in the Mongolian gerbil. Behav. Brain Res. 91, 15-22.
4. Araya R., Noguchi T., Yuhki M. et al. (2006) Loss of M5 muscarinic acetylcholine receptors leads to cerebrovascular and neuronal abnormalities and cognitive deficits in mice. Neurobiol. Dis. 24, 334-344.
5. Bailey E. L., McCulloch J., Sudlow C. and Wardlaw J. M. (2009) Potential animal models of lacunar stroke: a systematic review. Stroke 40, e451-e458.
6. Baumbach G. L., Sigmund C. D., Bottiglieri T. and Lentz S. R. (2002) Structure of cerebral arterioles in cystathionine beta-synthase-deficient mice. Circ. Res. 91, 931-937.
7. Bennett S. A., Tenniswood M., Chen J. H., Davidson C. M., Keyes M. T., Fortin T. and Pappas B. A. (1998) Chronic cerebral hypoperfusion elicits neuronal apoptosis and behavioral impairment. Neuroreport 9, 161-166.
8. Bernardo A., McCord M., Troen A. M., Allison J. D. and McDonald M. P. (2007) Impaired spatial memory in APP-overexpressing mice on a homocysteinemia-inducing diet. Neurobiol. Aging 28, 1195-1205.
9. Borras D., Ferrer I. and Pumarola M. (1999) Age-related changes in the brain of the dog. Vet. Pathol. 36, 202-211.
10. Bouet V., Freret T., Toutain J., Divoux D., Boulouard M. and Schumann-Bard P. (2007) Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp. Neurol. 203, 555-567.
11. Brown W. R., Blair R. M., Moody D. M., Thore C. R., Ahmed S., Robbins M. E. and Wheeler K. T. (2007) Capillary loss precedes the cognitive impairment induced by fractionated whole-brain irradiation: a potential rat model of vascular dementia. J. Neurol. Sci. 257, 67-71.
12. Carboni S., Boschert U., Gaillard P., Gotteland J. P., Gillon J. Y. and Vitte P. A. (2008) AS601245, a c-Jun NH2-terminal kinase (JNK) inhibitor, reduces axon/dendrite damage and cognitive deficits after global cerebral ischaemia in gerbils. Br. J. Pharmacol. 153, 157-163.
13. Chung E., Iwasaki K., Mishima K., Egashira N. and Fujiwara M. (2002) Repeated cerebral ischemia induced hippocampal cell death and impairments of spatial cognition in the rat. Life Sci. 72, 609-619.
14. Cummings B. J., Head E., Ruehl W., Milgram N. W. and Cotman C. W. (1996) The canine as an animal model of human aging and dementia. Neurobiol. Aging 17, 259-268.
15. De Jong G. I., Farkas E., Stienstra C. M., Plass J. R., Keijser J. N., De La Torre J. C. and Luiten P. G. (1999) Cerebral hypoperfusion yields capillary damage in the hippocampal CA1 area that correlates with spatial memory impairment. Neuroscience 91, 203-210.
16. Dietrich W. D., Watson B. D., Busto R., Ginsberg M. D. and Bethea J. R. (1987) Photochemically induced cerebral infarction. I. Early microvascular alterations. Acta Neuropathol. 72, 315-325.
17. Elfenbein H. A., Rosen R. F., Stephens S. L., Switzer R. C., Smith Y., Pare J., Mehta P. D., Warzok R. and Walker L. C. (2007) Cerebral beta-amyloid angiopathy in aged squirrel monkeys. Histol. Histopathol. 22, 155-167.
18. Farkas E., Donka G., De Vos R. A., Mihaly A., Bari F. and Luiten P. G. (2004) Experimental cerebral hypoperfusion induces white matter injury and microglial activation in the rat brain. Acta Neuropathol. 108, 57-64.
19. Farkas E., Luiten P. G. and Bari F. (2007) Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res. Rev. 54, 162-180.
20. Ferrara A., El B. S., Seyen S., Tirelli E. and Plumier J. C. (2009) The usefulness of operant conditioning procedures to assess long-lasting deficits following transient focal ischemia in mice. Behav. Brain Res. 205, 525-534.
21. Fukatsu T., Miyake-Takagi K., Nagakura A., Omino K., Okuyama N., Ando T., Takagi N., Furuya Y. and Takeo S. (2002) Effects of nefiracetam on spatial memory function and acetylcholine and GABA metabolism in microsphere-embolized rats. Eur. J. Pharmacol. 453, 59-67.
22. Gibson C. L. and Murphy S. P. (2004) Progesterone enhances functional recovery after middle cerebral artery occlusion in male mice. J. Cereb. Blood Flow Metab. 24, 805-813.
23. Goldman H., Berman R. F., Gershon S., Murphy S., Morehead M. and Altman H. J. (1992) Cerebrovascular permeability and cognition in the aging rat. Neurobiol. Aging 13, 57-62.
24. Hachinski V., Iadecola C., Petersen R. C. et al. (2006) National Institute of Neurological Disorders and Stroke-Canadian Stroke Network vascular cognitive impairment harmonization standards. Stroke 37, 2220-2241.
25. Hainsworth A. H. and Markus H. S. (2008) Do in vivo experimental models reflect human cerebral small vessel disease? A systematic review. J. Cereb. Blood Flow Metab. 28, 1877-1891.
26. Hamel E., Nicolakakis N., Aboulkassim T., Ongali B. and Tong X. K. (2008) Oxidative stress and cerebrovascular dysfunction in mouse models of Alzheimer's disease. Exp. Physiol. 93, 116-120.
27. Hattori H., Takeda M., Kudo T., Nishimura T. and Hashimoto S. (1992) Cumulative white matter changes in the gerbil brain under chronic cerebral hypoperfusion. Acta Neuropathol. 84, 437-442.
28. Hattori K., Lee H., Hurn P. D., Crain B. J., Traystman R. J. and DeVries A. C. (2000) Cognitive deficits after focal cerebral ischemia in mice. Stroke 31, 1939-1944.
29. Head E., Mehta R., Hartley J., Kameka M., Cummings B. J., Cotman C. W., Ruehl W. W. and Milgram N. W. (1995) Spatial learning and memory as a function of age in the dog. Behav. Neurosci. 109, 851-858.
30. Herzig M. C., Van Nostrand W. E. and Jucker M. (2006) Mechanism of cerebral beta-amyloid angiopathy: murine and cellular models. Brain Pathol. 16, 40-54.
31. Hodges H., Katzung N., Sowinski P., Hopewell J. W., Wilkinson J. H., Bywaters T. and Rezvani M. (1998) Late behavioural and neuropathological effects of local brain irradiation in the rat. Behav. Brain Res. 91, 99-114.
32. Horecky J., Baciak L., Kasparova S., Pacheco G., Aliev G. and Vancova O. (2009) Minimally invasive surgical approach for three-vessel occlusion as a model of vascular dementia in the rat-brain bioenergetics assay. J. Neurol. Sci. 283, 178-181.
33. Huber J. D., VanGilder R. L. and Houser K. A. (2006) Streptozotocin-induced diabetes progressively increases blood-brain barrier permeability in specific brain regions in rats. Am. J. Physiol Heart Circ. Physiol 291, H2660-H2668.
34. Joutel A., Monet-Lepretre M., Gosele C. et al. (2010) Cerebrovascular dysfunction and microcirculation rarefaction precede white matter lesions in a mouse genetic model of cerebral ischemic small vessel disease. J. Clin. Invest. 120, 433-445.
35. Kalaria R. N. and Erkinjuntti T. (2009) Small-vessel diseases of the brain, in Vascular Cognitive Impairment in Clinical Practice (Wahlund L. O., Erkinjuntti T. and Gauthier S., eds), pp. 118-134. Cambridge University Press, Cambridge, UK.
36. Kamath A. F., Chauhan A. K., Kisucka J., Dole V. S., Loscalzo J., Handy D. E. and Wagner D. D. (2006) Elevated levels of homocysteine compromise blood-brain barrier integrity in mice. Blood 107, 591-593.
37. Kemper T., Moss M. B., Hollander W. and Prusty S. (1999) Microinfarction as a result of hypertension in a primate model of cerebrovascular disease. Acta Neuropathol. (Berl) 98, 295-303.
38. Kemper T. L., Blatt G. J., Killiany R. J. and Moss M. B. (2001) Neuropathology of progressive cognitive decline in chronically hypertensive rhesus monkeys. Acta Neuropathol. 101, 145-153.
39. Kilkenny C., Browne W. J., Cuthill I. C., Emerson M. and Altman D. G. (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 8, e1000412.
40. Kimura S., Saito H., Minami M., Togashi H., Nakamura N., Nemoto M. and Parvez H. S. (2000) Pathogenesis of vascular dementia in stroke-prone spontaneously hypertensive rats. Toxicology 153, 167-178.
41. Kitagawa K., Yagita Y., Sasaki T., Sugiura S., Omura-Matsuoka E., Mabuchi T., Matsushita K. and Hori M. (2005) Chronic mild reduction of cerebral perfusion pressure induces ischemic tolerance in focal cerebral ischemia. Stroke 36, 2270-2274.
42. Kitamura N., Araya R., Kudoh M. et al. (2009) Beneficial effects of estrogen in a mouse model of cerebrovascular insufficiency. PLoS ONE 4, e5159.
43. Kudo T., Tada K., Takeda M. and Nishimura T. (1990) Learning impairment and microtubule-associated protein 2 decrease in gerbils under chronic cerebral hypoperfusion. Stroke 21, 1205-1209.
44. Kudo T., Takeda M., Tanimukai S. and Nishimura T. (1993) Neuropathologic changes in the gerbil brain after chronic hypoperfusion. Stroke 24, 259-264.
45. Kuhad A. and Chopra K. (2007) Curcumin attenuates diabetic encephalopathy in rats: behavioral and biochemical evidences. Eur. J. Pharmacol. 576, 34-42.
46. Kumar-Singh S. (2009) Hereditary and sporadic forms of abeta-cerebrovascular amyloidosis and relevant transgenic mouse models. Int. J. Mol. Sci. 10, 1872-1895.
47. Kurumatani T., Kudo T., Ikura Y. and Takeda M. (1998) White matter changes in the gerbil brain under chronic cerebral hypoperfusion. Stroke 29, 1058-1062.
48. Lai M., Horsburgh K., Bae S. E. et al. (2007) Forebrain mineralocorticoid receptor overexpression enhances memory, reduces anxiety and attenuates neuronal loss in cerebral ischaemia. Eur. J. Neurosci. 25, 1832-1842.
49. Laukka E. J., Jones S., Small B. J., Fratiglioni L. and Backman L. (2004) Similar patterns of cognitive deficits in the preclinical phases of vascular dementia and Alzheimer's disease. J. Int. Neuropsychol. Soc. 10, 382-391.
50. Launer L. J., Petrovitch H., Ross G. W., Markesbery W. and White L. R. (2008) AD brain pathology: vascular origins? Results from the HAAS autopsy study. Neurobiol. Aging 29, 1587-1590.
51. Lecrux C., McCabe C., Weir C. J., Gallagher L., Mullin J., Touzani O., Muir K. W., Lees K. R. and Macrae I. M. (2008) Effects of magnesium treatment in a model of internal capsule lesion in spontaneously hypertensive rats. Stroke 39, 448-454.
52. Lee H., Kim J. M., Kim H. J., Lee I. and Chang N. (2005) Folic acid supplementation can reduce the endothelial damage in rat brain microvasculature due to hyperhomocysteinemia. J. Nutr. 135, 544-548.
53. Matsuoka Y., Hasegawa H., Okuda S., Muraki T., Uruno T. and Kubota K. (1995) Ameliorative effects of tea catechins on active oxygen-related nerve cell injuries. J. Pharmacol. Exp. Ther. 274, 602-608.
54. Mickel H. S., Kempski O., Feuerstein G., Parisi J. E. and Webster H. D. (1990) Prominent white matter lesions develop in Mongolian gerbils treated with 100% normobaric oxygen after global brain ischemia. Acta Neuropathol. 79, 465-472.
55. Mikael L. G., Wang X. L., Wu Q., Jiang H., Maclean K. N. and Rozen R. (2009) Hyperhomocysteinemia is associated with hypertriglyceridemia in mice with methylenetetrahydrofolate reductase deficiency. Mol. Genet. Metab 98, 187-194.
56. Miki K., Ishibashi S., Sun L., Xu H., Ohashi W., Kuroiwa T. and Mizusawa H. (2009) Intensity of chronic cerebral hypoperfusion determines white/gray matter injury and cognitive/motor dysfunction in mice. J. Neurosci. Res. 87, 1270-1281.
57. Minami M., Kimura S., Endo T. et al. (1997) Dietary docosahexaenoic acid increases cerebral acetylcholine levels and improves passive avoidance performance in stroke-prone spontaneously hypertensive rats. Pharmacol. Biochem. Behav. 58, 1123-1129.
58. Miyamoto N., Tanaka R., Shimura H., Watanabe T., Mori H., Onodera M., Mochizuki H., Hattori N. and Urabe T. (2010) Phosphodiesterase III inhibition promotes differentiation and survival of oligodendrocyte progenitors and enhances regeneration of ischemic white matter lesions in the adult mammalian brain. J. Cereb. Blood Flow Metab. 30, 299-310.
59. Moore T. L., Killiany R. J., Rosene D. L., Prusty S., Hollander W. and Moss M. B. (2002) Impairment of executive function induced by hypertension in the rhesus monkey (Macaca mulatta). Behav. Neurosci. 116, 387-396.
60. Moorhouse P. and Rockwood K. (2008) Vascular cognitive impairment: current concepts and clinical developments. Lancet Neurol. 7, 246-255.
61. Moss M. B. and Jonak E. (2007) Cerebrovascular disease and dementia: a primate model of hypertension and cognition. Alzheimers. Dement. 3, S6-S15.
62. Nishio K., Ihara M., Yamasaki N. et al. (2010) A mouse model characterizing features of vascular dementia with hippocampal atrophy. Stroke 41, 1278-1284.
63. O'Brien J. T., Erkinjuntti T., Reisberg B. et al. (2003) Vascular cognitive impairment. Lancet Neurol. 2, 89-98.
64. Ohta H., Nishikawa H., Kimura H., Anayama H. and Miyamoto M. (1997) Chronic cerebral hypoperfusion by permanent internal carotid ligation produces learning impairment without brain damage in rats. Neuroscience 79, 1039-1050.
65. Pantoni L., Garcia J. H. and Gutierrez J. A. (1996) Cerebral white matter is highly vulnerable to ischemia. Stroke 27, 1641-1646.
66. Pappas B. A., De La Torre J. C., Davidson C. M., Keyes M. T. and Fortin T. (1996) Chronic reduction of cerebral blood flow in the adult rat: late-emerging CA1 cell loss and memory dysfunction. Brain Res. 708, 50-58.
67. Park L., Anrather J., Girouard H., Zhou P. and Iadecola C. (2007) Nox2-derived reactive oxygen species mediate neurovascular dysregulation in the aging mouse brain. J. Cereb. Blood Flow Metab. 27, 1908-1918.
68. Petito C. K., Olarte J. P., Roberts B., Nowak Jr T. S. and Pulsinelli W. A. (1998) Selective glial vulnerability following transient global ischemia in rat brain. J. Neuropathol. Exp. Neurol. 57, 231-238.
69. Plaschke K., Yun S. W., Martin E., Hoyer S. and Bardenheuer H. J. (1999) Interrelation between cerebral energy metabolism and behaviour in a rat model of permanent brain vessel occlusion. Brain Res. 830, 320-329.
70. Pratt J., Boudeau P., Uzan A., Imperato A. and Stutzmann J. (1998) Enoxaparin reduces cerebral edemaafter photothrombotic injury in the rat. Haemostasis 28, 78-85.
71. Pulsinelli W. A. and Brierley J. B. (1979) A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 10, 267-272.
72. Rapp J. H., Pan X. M., Neumann M., Hong M., Hollenbeck K. and Liu J. (2008) Microemboli composed of cholesterol crystals disrupt the blood-brain barrier and reduce cognition. Stroke 39, 2354-2361.
73. Rasmussen R. S., Overgaard K., Hildebrandt-Eriksen E. S. and Boysen G. (2006) D-amphetamine improves cognitive deficits and physical therapy promotes fine motor rehabilitation in a rat embolic stroke model. Acta Neurol. Scand. 113, 189-198.
74. Rhyu I. J., Bytheway J. A., Kohler S. J. et al. (2010) Effects of aerobic exercise training on cognitive function and cortical vascularity in monkeys. Neuroscience 167, 1239-1248.
75. Roof R. L., Schielke G. P., Ren X. and Hall E. D. (2001) A comparison of long-term functional outcome after 2 middle cerebral artery occlusion models in rats. Stroke 32, 2648-2657.
76. Roos M. W. and Ericsson A. (1999) N-tert-butyl-alpha-phenylnitrone reduces the number of microinfarctions in the rabbit brain cortex. Exp. Brain Res. 124, 271-272.
77. Sakai N., Yanai K., Ryu J. H., Nagasawa H., Hasegawa T., Sasaki T., Kogure K. and Watanabe T. (1996) Behavioral studies on rats with transient cerebral ischemia induced by occlusion of the middle cerebral artery. Behav. Brain Res. 77, 181-188.
78. Saksida L. M. and Bussey T. J. (2010) Animal models of amnesia. Neuropsychologia 48, 2231-2233.
79. Sarti C. and Pantoni L. (2003) Experimental models of vascular dementia: a focus on white matter disease and incomplete infarction, in Vascular Cognitive Impairment: preventable dementia (Bowler J. V. and Hachinski V., eds), pp. 76-92. Oxford University Press, Oxford, UK.
80. Sarti C., Pantoni L., Bartolini L. and Inzitari D. (2002) Persistent impairment of gait performances and working memory after bilateral common carotid artery occlusion in the adult Wistar rat. Behav. Brain Res. 136, 13-20.
81. Sato Y., Chin Y., Kato T. et al. (2009) White matter activated glial cells produce BDNF in a stroke model of monkeys. Neurosci. Res. 65, 71-78.
82. Schneider J. A., Bienias J. L., Wilson R. S., Berry-Kravis E., Evans D. A. and Bennett D. A. (2005) The apolipoprotein E epsilon4 allele increases the odds of chronic cerebral infarction [corrected] detected at autopsy in older persons. Stroke 36, 954-959.
83. Shibata M., Ohtani R., Ihara M. and Tomimoto H. (2004) White matter lesions and glial activation in a novel mouse model of chronic cerebral hypoperfusion. Stroke 35, 2598-2603.
84. Shibata M., Yamasaki N., Miyakawa T., Kalaria R. N., Fujita Y., Ohtani R., Ihara M., Takahashi R. and Tomimoto H. (2007) Selective impairment of working memory in a mouse model of chronic cerebral hypoperfusion. Stroke 38, 2826-2832.
85. Shughrue P. J. and Merchenthaler I. (2003) Estrogen prevents the loss of CA1 hippocampal neurons in gerbils after ischemic injury. Neuroscience 116, 851-861.
86. Smith S. E., Hodges H., Sowinski P., Man C. M., Leach M. J., Sinden J. D., Gray J. A. and Meldrum B. S. (1997) Long-term beneficial effects of BW619C89 on neurological deficit, cognitive deficit and brain damage after middle cerebral artery occlusion in the rat. Neuroscience 77, 1123-1135.
87. Sonnen J. A., Larson E. B., Crane P. K., Haneuse S., Li G., Schellenberg G. D., Craft S., Leverenz J. B. and Montine T. J. (2007) Pathological correlates of dementia in a longitudinal, population-based sample of aging. Ann. Neurol. 62, 406-413.
88. Storozheva Z. I., Proshin A. T., Sherstnev V. V., Storozhevykh T. P., Senilova Y. E., Persiyantseva N. A., Pinelis V. G., Semenova N. A., Zakharova E. I. and Pomytkin I. A. (2008) Dicholine salt of succinic acid, a neuronal insulin sensitizer, ameliorates cognitive deficits in rodent models of normal aging, chronic cerebral hypoperfusion, and beta-amyloid peptide-(25-35)-induced amnesia. BMC. Pharmacol. 8, 1.
89. Su M. Y., Head E., Brooks W. M., Wang Z., Muggenburg B. A., Adam G. E., Sutherland R., Cotman C. W. and Nalcioglu O. (1998) Magnetic resonance imaging of anatomic and vascular characteristics in a canine model of human aging. Neurobiol. Aging 19, 479-485.
90. Takeda S., Sato N., Uchio-Yamada K., Sawada K., Kunieda T., Takeuchi D., Kurinami H., Shinohara M., Rakugi H. and Morishita R. (2010) Diabetes-accelerated memory dysfunction via cerebrovascular inflammation and Abeta deposition in an Alzheimer mouse model with diabetes. Proc. Natl Acad. Sci. USA 107, 7036-7041.
91. Tanaka Y., Imai H., Konno K. et al. (2008) Experimental model of lacunar infarction in the gyrencephalic brain of the miniature pig: neurological assessment and histological, immunohistochemical, and physiological evaluation of dynamic corticospinal tract deformation. Stroke 39, 205-212.
92. Tapp P. D., Chu Y., Araujo J. A., Chiou J. Y., Head E., Milgram N. W. and Su M. Y. (2005) Effects of scopolamine challenge on regional cerebral blood volume. A pharmacological model to validate the use of contrast enhanced magnetic resonance imaging to assess cerebral blood volume in a canine model of aging. Prog. Neuropsychopharmacol. Biol. Psychiatry 29, 399-406.
93. Togashi H., Kimura S., Matsumoto M., Yoshioka M., Minami M. and Saito H. (1996) Cholinergic changes in the hippocampus of stroke-prone spontaneously hypertensive rats. Stroke 27, 520-525.
94. Torp R., Head E., Milgram N. W., Hahn F., Ottersen O. P. and Cotman C. W. (2000) Ultrastructural evidence of fibrillar beta-amyloid associated with neuronal membranes in behaviorally characterized aged dog brains. Neuroscience 96, 495-506.
95. De La Torre J. C., Fortin T., Park G. A., Butler K. S., Kozlowski P., Pappas B. A., De S. H., Saunders J. K. and Richard M. T. (1992) Chronic cerebrovascular insufficiency induces dementia-like deficits in aged rats. Brain Res. 582, 186-195.
96. Troen A. M., Shea-Budgell M., Shukitt-Hale B., Smith D. E., Selhub J. and Rosenberg I. H. (2008) B-vitamin deficiency causes hyperhomocysteinemia and vascular cognitive impairment in mice. Proc. Natl Acad. Sci. USA 105, 12474-12479.
97. Tsukuda K., Mogi M., Li J. M., Iwanami J., Min L. J., Sakata A., Fujita T., Iwai M. and Horiuchi M. (2007) Amelioration of cognitive impairment in the type-2 diabetic mouse by the angiotensin II type-1 receptor blocker candesartan. Hypertension 50, 1099-1105.
98. Ueno K. I., Togashi H., Mori K., Matsumoto M., Ohashi S., Hoshino A., Fujita T., Saito H., Minami M. and Yoshioka M. (2002) Behavioural and pharmacological relevance of stroke-prone spontaneously hypertensive rats as an animal model of a developmental disorder. Behav. Pharmacol. 13, 1-13.
99. Vicente E., Degerone D., Bohn L. et al. (2009) Astroglial and cognitive effects of chronic cerebral hypoperfusion in the rat. Brain Res. 1251, 204-212.
100. Wakita H., Tomimoto H., Akiguchi I. and Kimura J. (1994) Glial activation and white matter changes in the rat brain induced by chronic cerebral hypoperfusion: an immunohistochemical study. Acta Neuropathol. 87, 484-492.
101. Wakita H., Tomimoto H., Akiguchi I. and Kimura J. (1995) Protective effect of cyclosporin A on white matter changes in the rat brain after chronic cerebral hypoperfusion. Stroke 26, 1415-1422.
102. Wakita H., Tomimoto H., Akiguchi I., Lin J. X., Ihara M., Ohtani R. and Shibata M. (2003) Ibudilast, a phosphodiesterase inhibitor, protects against white matter damage under chronic cerebral hypoperfusion in the rat. Brain Res. 992, 53-59.
103. Walker E. J. and Rosenberg G. A. (2010) Divergent role for MMP-2 in myelin breakdown and oligodendrocyte death following transient global ischemia. J. Neurosci. Res. 88, 764-773.
104. Wang F., Geng X., Tao H. Y. and Cheng Y. (2010a) The restoration after repetitive transcranial magnetic stimulation treatment on cognitive ability of vascular dementia rats and its impacts on synaptic plasticity in hippocampal CA1 area. J. Mol. Neurosci. 41, 145-155.
105. Wang J., Zhang H. Y. and Tang X. C. (2010b) Huperzine a improves chronic inflammation and cognitive decline in rats with cerebral hypoperfusion. J. Neurosci. Res. 88, 807-815.
106. Whitehead S., Cheng G., Hachinski V. and Cechetto D. F. (2005a) Interaction between a rat model of cerebral ischemia and beta-amyloid toxicity: II. Effects of triflusal. Stroke 36, 1782-1789.
107. Whitehead S. N., Hachinski V. C. and Cechetto D. F. (2005b) Interaction between a rat model of cerebral ischemia and beta-amyloid toxicity: inflammatory responses. Stroke 36, 107-112.
108. Wiard R. P., Dickerson M. C., Beek O., Norton R. and Cooper B. R. (1995) Neuroprotective properties of the novel antiepileptic lamotrigine in a gerbil model of global cerebral ischemia. Stroke 26, 466-472.
109. Wilcock D. M. and Colton C. A. (2009) Immunotherapy, vascular pathology, and microhemorrhages in transgenic mice. CNS Neurol. Disord. Drug Targets 8, 50-64.
110. Yamada M., Lamping K. G., Duttaroy A. et al. (2001) Cholinergic dilation of cerebral blood vessels is abolished in M(5) muscarinic acetylcholine receptor knockout mice. Proc. Natl Acad. Sci. USA 98, 14096-14101.
111. Yamaguchi M., Sugimachi K., Nakano K., Fujimoto M., Takahashi M., Chikugo T. and Ogawa H. (1994) Memory deficit accompanying cerebral neurodegeneration after stroke in stroke-prone spontaneously hypertensive rats (SHRSP). Acta Neurochir. Suppl. (Wien) 60, 200-202.
112. Yamaguchi M., Calvert J. W., Kusaka G. and Zhang J. H. (2005) One-stage anterior approach for four-vessel occlusion in rat. Stroke 36, 2212-2214.
113. Yamamoto Y., Shioda N., Han F. et al. (2009) Nobiletin improves brain ischemia-induced learning and memory deficits through stimulation of CaMKII and CREB phosphorylation. Brain Res. 1295, 218-229.
114. Yamori Y., Horie R., Handa H., Sato M. and Fukase M. (1976) Pathogenetic similarity of strokes in stroke-prone spontaneously hypertensive rats and humans. Stroke 7, 46-53.
115. Yonemori F., Yamaguchi T., Yamada H. and Tamura A. (1999) Spatial cognitive performance after chronic focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 19, 483-494.
116. Yoshizaki K., Adachi K., Kataoka S., Watanabe A., Tabira T., Takahashi K. and Wakita H. (2008) Chronic cerebral hypoperfusion induced by right unilateral common carotid artery occlusion causes delayed white matter lesions and cognitive impairment in adult mice. Exp. Neurol. 210, 585-591.
117. Young J. W., Powell S. B., Risbrough V., Marston H. M. and Geyer M. A. (2009) Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia. Pharmacol. Ther. 122, 150-202.