Microsphere embolism-induced cortical cholinergic deafferentation and impairments in attentional performance

European Journal of Neuroscience

Volumn 21, Issue 11, 2005, Pages 3117-3132

  Craft, Tara K S ^a   Mahoney, John H ^b   DeVries, A Courtney ^a   Sarter, Martin ^c  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Acetylcholine; Attention; Cortex; Ischemia; Microsphere embolism; Stroke

Indexed keywords

ACETYLCHOLINE; FLUORESCENT DYE; GLIAL FIBRILLARY ACIDIC PROTEIN; MICROSPHERE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; ATTENTION; BRAIN CORTEX; BRAIN EMBOLISM; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN REGION; CHOLINERGIC NERVE; CHOLINERGIC SYSTEM; COGNITIVE DEFECT; COMMON CAROTID ARTERY; CONTROLLED STUDY; DEAFFERENTATION; DEMENTIA; GLOBUS PALLIDUS; HYPOTHESIS; IMMUNOHISTOCHEMISTRY; MALE; MICROSPHERE EMBOLISM; NERVE FIBER; NEUROTRANSMISSION; NONHUMAN; PARIETAL LOBE; PATHOGENESIS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STROKE; TASK PERFORMANCE;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; ALZHEIMER DISEASE; ANIMALS; ATTENTION; BASAL NUCLEUS OF MEYNERT; CEREBRAL CORTEX; CEREBROVASCULAR DISORDERS; CHOLINERGIC FIBERS; COGNITION DISORDERS; CONDITIONING, OPERANT; DISEASE MODELS, ANIMAL; FLUORESCENT DYES; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; INTRACRANIAL EMBOLISM; MALE; MICROCIRCULATION; MICROSPHERES; NEUROPSYCHOLOGICAL TESTS; ORGANIC CHEMICALS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION;

EID: 21444445750     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04136.x     Document Type: Article

References (103)

1. Alkayed, N.J., Harukuni, I., Kimes, A.S., London, E.D., Traystman, R.J. & Hurn, P.D. (1998) Gender-linked brain injury in experimental stroke. Stroke, 29, 159-165.
2. Ando, T., Takagi, N., Takagi, K., Kago, T. & Takeo, S. (2005) Effects of nefiracetam on the levels of brain-derived neurotrophic factor and synapsin I mRNA and protein in the hippocampus of microsphere-embolized rats. Eur. J. Pharmacol., 507, 49-56.
3. Apparsundaram, S., Martinez, V., Parikh, V., Kozak, R. & Sarter, M. (2005) Increased capacity and density of choline transporters situated in synaptic membranes of the right medial prefrontal cortex of attentional task-performing rats. J. Neurosci., 25, 3851-3856.
4. Arnold, H.M., Burk, J.A., Hodgson, E.M., Sarter, M. & Bruno, J.P. (2002) Differential cortical acetylcholine release in rats performing a sustained attention task versus behavioral control tasks that do not explicitly tax attention. Neuroscience, 114, 451-460.
5. Ballard, C., McKeith, I., O'Brien, J., Kalaria, R., Jaros, E., Ince, P. & Perry, R. (2000) Neuropathological substrates of dementia and depression in vascular dementia, with a particular focus on cases with small infarct volumes. Dement. Geriatr. Cogn. Disord., 11, 59-65.
6. Barbelivien, A., Bertrand, N., Besret, L., Beley, A., MacKenzie, E.T. & Dauphin, F. (1999) Neurochemical stimulation of the rat substantia innominata increases cerebral blood flow (but not glucose use) through the parallel activation of cholinergic and non-cholinergic pathways. Brain Res., 840, 115-124.
7. Barbelivien, A., Vaussy, C., Marchalant, Y., Maubert, E., Bertrand, N., Beley, A., Roussel, S., Mackenzie, E.T. & Dauphin, F. (2004) Degeneration of the basalocortical pathway from the cortex induces a functional increase in galaninergic markers in the nucleus basalis magnocellularis of the rat. J. Cereb. Blood Flow Metab., 24, 1255-1266.
8. Bevan, J.A., Buga, G.M., Florence, V.M., Gonsalves, A. & Snowden, A. (1982) Distribution of choline acetyltransferase in cerebral and extracerebral cranial arteries of the cat. Its relationship to neurogenic atropine-sensitive dilation. Circ. Res., 50, 470-476.
9. Biesold, D., Inanami, O., Sato, A. & Sato, Y. (1989) Stimulation of the nucleus basalis of Meynert increases cerebral cortical blood flow in rats. Neurosci. Lett., 98, 39-44.
10. Burk, J.A., Herzog, C.D., Porter, M.C. & Sarter, M. (2002) Interactions between aging and cortical cholinergic deafferentation on attention. Neurobiol. Aging, 23, 467-477.
11. Burk, J.A. & Sarter, M. (2001) Dissociation between the attentional functions mediated via basal forebrain cholinergic and GABAergic neurons Neuroscience, 105, 899-909.
12. Bushnell, P.J., Chiba, A.A. & Oshiro, W.M. (1998) Effects of unilateral removal of basal forebrain cholinergic neurons on cued target detection in rats. Behav. Brain Res., 90, 57-71.
13. Chu, Y. Cochran, E.J., Bennett, D.A., Mufson, E.J. & Kordower, J.H. (2001) Down-regulation of trkA mKNA within nucleus basalis neurons in individuals with mild cognitive impairment and Alzheimer's disease. J. Comp. Neurol., 437, 296-307.
14. Date, I., Takagi, N., Takagi, K., Kago, T., Matsumoto, K., Nakamura, T. & Takeo, S. (2004a) Hepatocyte growth factor attenuates cerebral ischemia-induced learning dysfunction. Biochem. Biophys. Res. Commun., 319, 1152-1158.
15. Date, I., Takagi, N., Takagi, K., Kago, T., Matsumoto, K., Nakamura, T. & Takeo, S. (2004b) Hepatocyte growth factor improved learning and memory dysfunction of microsphere-embolized rats. J. Neurosci. Res., 78, 442-453
16. de la Torre, J.C. & Stefano, G.B. (2000) Evidence that Alzheimer's disease is a microvascular disorder: the role of constitutive nitric oxide. Brain Res. Rev., 34, 119-136.
17. Dihne, M., Grommes, C., Lutzenburg, M., Witte, O.W. & Block, F. (2002) Different mechanisms of secondary neuronal damage in thalamic nuclei after focal cerebral ischemia in rats. Stroke, 33, 3006-3011.
18. Everitt, B.J. & Robbins, T.W. (1997) Central cholinergic systems and cognition. Annu. Rev. Psychol., 48, 649-684.
19. Fadel, J., Moore, H., Sarter, M. & Bruno, J.P. (1996) Trans-synaptic stimulation of cortical acetylcholine release after partial 192 IgG-saporin-induced loss of cortical cholinergic afferents. J. Neurosci., 16, 6592-6600.
20. Farkas, E. & Luiten, P.G. (2001) Cerebral microvascular pathology in aging and Alzheimer's disease. Prog. Neurobiol., 64, 575-611.
21. Figueiredo, B.C., Piccardo, P., Maysinger, D., Clarke, P.B. & Cuello, A.C. (1993) Effects of acidic fibroblast growth factor on cholinergic neurons of nucleus basalis magnocellularis and in a spatial memory task following cortical devascularization. Neuroscience, 56, 955-963.
22. Fukatsu, T., Miyake-Takagi, K., Nagakura, A., Omino, K., Okuyama, N., Ando, T., Takagi, N., Furuya, Y. & 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.
23. Geula, C. (1998) Abnormalities of neural circuitry in Alzheimer's disease: hippocampus and cortical cholinergic innervation. Neurology, 51, S18-S29.
24. Gharbawie, O.A. & Whishaw, I.Q. (2003) Cholinergic and serotonergic neocortical projection lesions given singly or in combination cause only mild impairments on tests of skilled movement in rats: evaluation of a model of dementia. Brain Res., 970, 97-109.
25. Gill, T.M., Sarter, M. & Givens, B. (2000) Sustained visual attention performance-associated prefrontal neuronal activity: evidence for cholinergic modulation. J. Neurosci., 20, 4745-4757.
26. Gutierrez, H., Miranda, M.I. & Bermudez-Rattoni, F. (1997) Learning impairment and cholinergic deafferentation after cortical nerve growth factor deprivation. J. Neurosci., 17, 3796-3803.
27. Haga, S., Haga, C., Aizawa, T. & Ikeda, K. (2002) Neuronal degeneration and glial cell-responses following trimethyltin intoxication in the rat. Acta Neuropathol., 103, 575-582.
28. Harkany, T., Penke, B. & Luiten, P.G. (2000) beta-Amyloid excitotoxicity in rat magnocellular nucleus basalis. Effect of cortical deafferentation on cerebral blood flow regulation and implications for Alzheimer's disease. Ann. N.Y. Acad. Sci., 903, 374-386.
29. Hartig, W., Bauer, A., Brauer, K., Grosche, J., Hortobagyi, T., Penke, B., Schliebs, R. & Harkany, T. (2002) Functional recovery of cholinergic basal forebrain neurons under disease conditions: old problems, new solutions? Rev. Neurosci., 13, 95-165.
30. Holley, L.A., Turchi, J., Apple, C. & Sarter, M. (1995) Dissociation between the attentional effects of infusions of a benzodiazepine receptor agonist and an inverse agonist into the basal forebrain. Psychopharmacology, 120, 99-108.
31. Hopkins, K.J., Wang, G. & Schmued, L.C. (2000) Temporal progression of kainic acid induced neuronal and myelin degeneration in the rat forebrain. Brain Res., 864, 69-80.
32. Hsieh, C.Y., Cruikshank, S.J. & Metherate, R. (2000) Differential modulation of auditory thalamocortical and intracortical synaptic transmission by cholinergic agonist. Brain Res., 880, 51-64.
33. Kalaria, R. (2002) Similarities between Alzheimer's disease and vascular dementia. J. Neurol. Sci., 203-204, 29-34.
34. Kataoka, K., Hayakawa, T., Kuroda, R., Yuguchi, T. & Yamada, K. (1991) Cholinergic deafferentation after focal cerebral infarct in rats. Stroke, 22, 1291-1296.
35. Knox, C.A. & Oliveira, A. (1980) Brain aging in normotensive and hypertensive strains of rats. III. A quantitative study of cerebrovasculature. Acta Neuropathol., 52, 17-25.
36. Lacombe, P., Sercombe, R., Verrecchia, C., Philipson, V., MacKenzie, E.T. & Seylaz, J. (1989) Cortical blood flow increases induced by stimulation of the substantia innominata in the unanesthetized rat. Brain Res., 491, 1-14.
37. Langa, K.M., Foster, N.L. & Larson, E.B. (2004) Mixed dementia: emerging concepts and therapeutic implications. JAMA, 292, 2901-2908.
38. Lehericy, S., Hirsch, E.C., Cervera-Pierot, P., Hersh, L.B., Bakchine, S., Piette, F., Duyckaerts, C., Hauw, J.J., Javoy-Agid, F. & Agid, Y. (1993) Heterogeneity and selectivity of the degeneration of cholinergic neurons in the basal forebrain of patients with Alzheimer's disease. J. Comp. Neurol., 330, 15-31.
39. Liberini, P., Pioro, E.P., Maysinger, D. & Cuello, A.C. (1994) Neocortical infarction in subhuman primates leads to restricted morphological damage of the cholinergic neurons in the nucleus basalis of Meynert. Brain Res., 648, 1-8.
40. Linville, D.G. & Arneric, S.P. (1991) Cortical cerebral blood flow governed by the basal forebrain: age-related impairments. Neurobiol. Aging, 12, 503-510.
41. Linville, D.G., Williams, S. & Arneric, S.P. (1993) Basal forebrain control of cortical cerebral blood flow is independent of local cortical neurons. Brain Res., 622, 26-34.
42. Luiten, P.G., de Jong, G.I., Van der Zee, E.A. & van Dijken, H. (1996) Ultrastructural localization of cholinergic muscarinic receptors in rat brain cortical capillaries. Brain Res., 720, 225-229.
43. Lysakowski, A., Wainer, B.H., Bruce, G. & Hersh, L.B. (1989) An atlas of the regional and laminar distribution of choline acetyltransferase immunoreactivity in rat cerebral cortex. Neuroscience, 28, 291-336.
44. Martinez, V. & Sarter, M. (2004) Lateralized attentional functions of cortical cholinergic inputs. Behav. Neurosci., 118, 984-991.
45. McGaughy, J., Kaiser, T. & Sarter, M. (1996) Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav. Neurosci., 110, 247-265.
46. McGaughy, J. & Sarter, M. (1995) Behavioral vigilance in rats: task validation and effects of age, amphetamine, and benzodiazepine receptor ligands. Psychopharmacology, 117, 340-357.
47. McGaughy, J. & Sarter, M. (1998) Sustained attention performance in rats with intracortical infusions of 192 IgG-saporin-induced cortical cholinergic deafferentation: effects of physostigmine and FG 7142. Behav. Neurosci., 112, 1519-1525.
48. Mesulam, M. (2004) The cholinergic lesion of Alzheimer's disease: pivotal factor or side show? Learn. Mem., 11, 43-49.
49. Metherate, R. & Weinberger, N.M. (1990) Cholinergic modulation of responses to single tones produces tone-specific receptive field alterations in cat auditory cortex. Synapse, 6, 133-145.
50. Meyer, J., Xu, G., Thornby, J., Chowdhury, M. & Quach, M. (2002) Longitudinal analysis of abnormal domains comprising mild cognitive impairment (MCI) during aging. J. Neurol. Sci., 201, 19-25.
51. Milner, T.A., Aoki, C., Sheu, K.F., Blass, J.P. & Pickel, V.M. (1987) Light microscopic immunocytochemical localization of pyruvate dehydrogenase complex in rat brain: topographical distribution and relation to cholinergic and catecholaminergic nuclei. J. Neurosci., 7, 3171-3190.
52. Miyake, K., Takeo, S. & Kaijihara, H. (1993) Sustained decrease in brain regional blood flow after microsphere embolism in rats. Stroke, 24, 415-420.
53. Montaldi, D., Brooks, D.N., McColl, J.H., Wyper, D., Patterson, J., Barron, E. & McCulloch, J. (1990) Measurements of regional cerebral blood flow and cognitive performance in Alzheimer's disease. J. Neurol. Neurosurg. Psychiary, 53, 33-38.
54. Mufson, E.J., Ma, S.Y., Cochran, E.J., Bennett, D.A., Beckett, L.A., Jaffar, S., Saragovi, H.U. & Kordower, J.H. (2000) Loss of nucleus basalis neurons containing trkA immunoreactivity in individuals with mild cognitive impairment and early Alzheimer's disease. J. Comp. Neurol., 427, 19-30.
55. Mufson, E.J., Ma, S.Y., Dills, J., Cochran, E.J., Leurgans, S., Wuu, J., Bennett, D.A., Jaffar, S., Gilmor, M.L., Levey, A.I. & Kordower, J.H. (2002) Loss of basal forebrain P75 (NTR) immunoreactivity in subjects with mild cognitive impairment and Alzheimer's disease. J. Comp. Neurol., 443, 136-153.
56. Murphy, P.C. & Sillito, A.M. (1991) Cholinergic enhancement of direction selectivity in the visual cortex of the cat. Neuroscience, 40, 13-20.
57. Oldford, E. & Castro-Alamancos, M.A. (2003) Input-specific effects of acetylcholine on sensory and intracortical evoked responses in the 'barrel cortex' in vivo. Neuroscience, 117, 769-778.
58. Oshiro, W.M., Bushnell, P.J. & Chiba, A.A. (2000) A comparison of the effects of bilateral and unilateral infusions of muscimol into the basal forebrain on cued detection of visual targets in rats. Behav. Neurosci., 114, 137-149.
59. Palmer, A.M. (1996) Neurochemical studies of Alzheimer's disease. Neurodegeneration, 5, 381-391.
60. Pappas, B.A., Bayley, P.J., Bui, B.K., Hansen, L.A. & Thal, L.J. (2000) Choline acetyltransferase activity and cognitive domain scores of Alzheimer's patients. Neurobiol. Aging, 21, 11-17.
61. Pearson, R.C., Gatter, K.C. & Powell, T.P. (1983) Retrograde cell degeneration in the basal nucleus in monkey and man. Brain Res., 261, 321-326.
62. Penschuck, S., Chen-Bee, C.H., Prakash, N. & Frostig, R.D. (2002) In vivo modulation of a cortical functional sensory representation shortly after topical cholinergic agent application. J. Comp. Neurol., 452, 38-50.
63. Perry, E.K., Blessed, G., Tomlinson, B.E., Perry, R.H., Crow, T.J., Cross, A.J., Dockray, G.J., Dimaline, R. & Arregui, A. (1981) Neurochemical activities in human temporal lobe related to aging and Alzheimer-type changes. Neurobiol. Aging, 2, 251-256.
64. Pinard, E., Nallet, H., MacKenzie, E.T., Seylaz, J. & Roussel, S. (2002) Penumbral microcirculatory changes associated with peri-infarct depolarizations in the rat. Stroke, 33, 606-612.
65. Procter, A.W. (1996) Neurochemical correlates of dementia. Neurodegeneration, 5, 403-407.
66. Raszkiewicz, J.L., Linville, D.G., Kerwin, J.F. Jr, Wagenaar, F. & Arneric, S.P. (1992) Nitric oxide synthase is critical in mediating basal forebrain regulation of cortical cerebral circulation. J. Neurosci. Res., 33, 129-135.
67. Reed, B.R. (2004) Vascular dementia. Arch. Neurol., 61, 433-435.
68. Sarter, M. & Bruno, J.P. (2004) Developmental origins of the age-related decline in cortical cholinergic function and associated cognitive abilities. Neurobiol. Aging, 25, 1127-1139.
69. Sarter, M., Givens, B. & Bruno, J.P. (2001) The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res. Rev., 35, 146-160.
70. Sarter, M., Hasselmo, M.E., Bruno, J.P. & Givens, B. (2005) Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and top-down cholinergic modulation of signal detection. Brain Res. Rev., 48, 98-111.
71. Schallert, T., Fleming, S.M., Leasure, J.L., Tillerson, J.L. & Bland, S.T. (2000) CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology, 39, 777-787.
72. Schmued, L.C. & Hopkins, K.J. (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res., 874, 123-130.
73. Sekiguchi, M., Sugiyama, Y., Takagi, K., Takagi, N., Takeo, S., Tanaka, O., Yamato, I., Torigoe, K. & Nowakowski, R.S. (2003) Rapid appearance of pathological changes of neurons and glia cells in the cerebellum of microsphere-embolized rats. Brain Res., 978, 228-232.
74. Sekiguchi, M., Takagi, K., Takagi, N., Date, I., Takeo, S., Tanaka, O., Yamato, I., Kobashikawa, S., Torigoe, K. & Nowakowski, R.S. (2005) Time course and sequence of pathological changes in the cerebellum of microsphere-embolized rats. Exp. Neurol., 191, 266-275.
75. Seshadri, S., Beiser, A., Selhub, J., Jacques, P.F., Rosenberg, I.H., D'Agostino, R.B., Wilson, P.W. & Wolf, P.A. (2002) Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N. Engl. J. Med., 346, 476-483.
76. Sims, N.R., Bowen, D.M., Allen, S.J., Smith, C.C., Neary, D., Thomas, D.J. & Davison, A.N. (1983) Presynaptic cholinergic dysfunction in patients with dementia. J. Neurochem., 40, 503-509.
77. Soblosky, J.S., Tabor, S.L., Matthews, M.A., Davidson, J.F., Chorney, D.A. & Carey, M.E. (1996) Reference memory and allocentric spatial localization deficits after unilateral cortical brain injury in the rat. Behav. Brain Res., 80. 185-194.
78. Sofroniew, M.V., Galletly, N.P., Isacson, O. & Svendsen, C.N. (1990) Survival of adult basal forebrain cholinergic neurons after loss of target neurons. Science, 247, 338-342.
79. Stichel, C.C. & Singer, W. (1987) Quantitative analysis of the choline acetyltransferase-immunoreactive axonal network in the cat primary visual cortex. I. Adult cats. J. Comp. Neurol., 258, 91-98.
80. Szutowicz, A., Tomaszewicz, M., Jankowska, A., Madziar, B. & Bielarczyk, H. (2000) Acetyl-CoA metabolism in cholinergic neurons and their susceptibility to neurotoxic inputs. Metab. Brain Dis., 15, 29-44.
81. Tago, H., Kimura, H. & Maeda, T. (1986) Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J. Histochem. Cytochem., 34, 1431-1438.
82. Takagi, N., Miyake, K., Taguchi, T., Sugita, N., Takagi, K., Tamada, H. & Takeo, S. (1997b) Changes in cholinergic neurons and failure in learning function after microsphere embolism-induced cerebral ischemia. Brain Res. Bull., 43, 87-92.
83. Takagi, N., Miyake, K., Taguchi, T., Tamada, H., Takagi, K., Sugita, N. & Takeo, S. (1997a) Failure in learning task and loss of cortical cholingergic fibers in microsphere-embolized rats. Exp. Brain Res., 114, 279-287.
84. Takagi, N., Miyake-Takagi, K., Takagi, K., Tamura, H. & Takeo, S. (2002) Altered extracellular signal-regulated kinase signal transduction by the muscarinic acetylcholine and metabotropic glutamate receptors after cerebral ischemia. J. Biol. Chem., 277, 6382-6390.
85. Takagi, N., Tsuru, H., Yamamura, M. & Takeo, S. (1995) Changes in striatal dopamine metabolism after microsphere embolism in rats. Stroke, 26, 1101-1106.
86. Takeo, S., Fukatsu, T., Miyake-Takagi, K., Takagi, N., Niimura, M., Nagakura, A., Ando, T. & Tanonaka, K. (2003) Persistent effects of delayed treatment with nefiracetam on the water maze task in rats with sustained cerebral ischemia. J. Pharmacol. Exp. Ther., 304, 513-523.
87. Takeo, S., Taguchi, T., Tanonaka, K., Miyake, K., Horiguchi, T., Takagi, N. & Fujimori, K. (1992) Sustained damage to energy metabolism of brain regions after microsphere embolism in rats. Stroke, 23, 62-68.
88. Terry, A.V. Jr & Buccafusco, J.J. (2003) The cholinergic hypothesis of age and Alzheimer's disease-related cognitive deficits: recent challenges and their implications for novel drug development. J. Pharmacol. Exp. Ther., 306, 821-827.
89. Tong, X.K. & Hamel, E. (1999) Regional cholinergic denervation of cortical microvessels and nitric oxide synthase-containing neurons in Alzheimer's disease. Neuroscience, 92, 163-175.
90. Tremblay, N., Warren, R.A. & Dykes, R.W. (1990) Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. J. Neurophysiol., 64, 1212-1222.
91. Turchi, J. & Sarter, M. (2000) Cortical cholinergic inputs mediate processing capacity: effects of 192 IgG-saporin-induced lesions on olfactory span performance. Eur. J. Neurosci., 12. 4505-4514.
92. Turchi, J. & Sarter, M. (2001) Antisense oligodeoxynucleotide-induced suppression of basal forebrain NMDA-NR1 subunits selectively impairs visual attentional performance in rats. Eur. J. Neurosci., 14, 103-117.
93. Vaucher, E., Borredon, J., Bonvento, G., Seylaz, J. & Lacombe, P. (1997b) Autoradiographic evidence for flow-metabolism uncoupling during stimulation of the nucleus basalis of Meynert in the conscious rat. J. Cereb. Blood Flow Metab., 17, 686-694.
94. Vaucher, E. & Hamel, E. (1995) Cholinergic basal forebrain neurons project to cortical microvessels in the rat: electron microscopic study with anterogradely transported Phaseolus vulgaris leucoagglutinin and choline acetyltransferase immunocytochemistry. J. Neurosci., 15, 7427-7441.
95. Vaucher, E., Linville, D. & Hamel, E. (1997a) Cholinergic basal forebrain projections to nitric oxide synthase-containing neurons in the rat cerebral cortex. Neuroscience, 79, 827-836.
96. Waite, J.J., Holschneider, D.P. & Scremin, O.U. (1999) Selective immunotoxin-induced cholinergic deafferentation alters blood flow distribution in the cerebral cortex. Brain Res., 818, 1-11.
97. Ward, N.M., Sharkey, J. & Brown, V.J. (1997) Assessment of sensorimotor neglect after occlusion of the middle cerebral artery in the rat. Behav. Neurosci., 111, 1133-1145.
98. Ward, N.M., Sharkey, J., Marston, H.M. & Brown, V.J. (1998) Simple and choice reaction-time performance following occlusion of the anterior cerebral arteries in the rat. Exp. Brain Res., 123, 269-281.
99. Yamada, M., Lamping, K.G., Duttaroy, A., Zhang, W., Cui, Y., Bymaster, F.P., McKinzie, D.L., Felder, C.C., Deng, C.X., Faraci, F.M. & Wess, J. (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.
100. Zar, J.H. (1974) Biostatistical Analysis. Prentice Hall, Englewood Cliffs, N.J.
101. Zekry, D., Duyckaerts, C., Belmin, J., Geoffre, C., Herrmann, F., Moulias, R. & Hauw, J.J. (2003) The vascular lesions in vascular and mixed dementia: the weight of functional neuroanatomy. Neurobiol. Aging, 24, 213-219.
102. Zhang, P., Eckman, C., Younkin, S., Hsiao, K.K. & Iadecola, C. (1997) Increased susceptibility to ischemic brain damage in transgenic mice overexpressing the amyloid precursor protein. J. Neurosci., 17, 7655-7661.
103. Zlokovic, B.V. (2002) Vascular disorder in Alzheimer's disease: role in pathogenesis of dementia and therapeutic targets. Adv. Drug Deliv. Rev., 54, 1553-1559.