Dietary cholesterol concentration and duration degrade long-term memory of classical conditioning of the rabbits nictitating membrane response

International Journal of Alzheimer's Disease

Volumn , Issue , 2012, Pages

  Schreurs, Bernard G ^a,b   Wang, Desheng ^a,b   Smith Bell, Carrie A ^a,b   Burhans, Lauren B ^a,b   Bell, Roger ^a,b   Gonzalez Joekes, Jimena ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; COPPER;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL INTAKE; CONDITIONING; CONTROLLED STUDY; CORRELATION ANALYSIS; LONG TERM MEMORY; MALE; MEMORY DISORDER; NICTITATING MEMBRANE; NONHUMAN; PRIORITY JOURNAL; RABBIT;

EID: 84861088134     PISSN: None     EISSN: 20900252     Source Type: Journal    
DOI: 10.1155/2012/732634     Document Type: Article

References (88)

1. Prasanthi J. R. P., Dasari B., Marwarha G., Larson T., Chen X., Geiger J. D., Ghribi O., Caffeine protects against oxidative stress and Alzheimer's disease-like pathology in rabbit hippocampus induced by cholesterol-enriched diet Free Radical Biology and Medicine 2010 49 7 1212 1220
2. Jaya Prasanthi R. P., Schommer E., Thomasson S., Thompson A., Feist G., Ghribi O., Regulation of -amyloid levels in the brain of cholesterol-fed rabbit, a model system for sporadic Alzheimer's disease Mechanisms of Ageing and Development 2008 129 11 649 655
3. Woodruff-Pak D. S., Animal models of Alzheimer's disease: therapeutic implications Journal of Alzheimer's Disease 2008 15 4 507 521
4. Woodruff-Pak D. S., Agelan A., Valle L. D., A rabbit model of Alzheimer's disease: valid at neuropathological, cogn (Pubitemid 47094031)
5. Ghribi O., Golovko M. Y., Larsen B., Schrag M., Murphy E. J., Deposition of iron and -amyloid plaques is associated with cortical cellular damage in rabbits fed with long-term cholesterol-enriched diets Journal of Neurochemistry 2006 99 2 438 449 (Pubitemid 44477201)
6. Sparks D. L., Schreurs B. G., Trace amounts of copper in water induce -amyloid plaques and learning deficits in a rabbit model of Alzheimer's disease Proceedings of the National Academy of Sciences of the United States of America 2003 100 19 11065 11069 (Pubitemid 37140153)
7. Zatta P., Zambenedetti P., Stella M. P., Licastro F., Astrocytosis, microgliosis, metallothionein-I-II and amyloid expression in high cholesterol-fed rabbits Journal of Alzheimer's Disease 2002 4 1 1 9 (Pubitemid 34240999)
8. Sparks D. L., Kuo Y. M., Roher A., Martin T., Lukas R. J., Alterations of Alzheimer's disease in the cholesterol-fed rabbit, including vascular inflammation. Preliminary observations Annals of the New York Academy of Sciences 2000 903 335 344 (Pubitemid 30251574)
9. Sparks D. L., Dietary cholesterol induces Alzheimer-like -amyloid immunoreactivity in rabbit brain Nutrition, Metabolism and Cardiovascular Diseases 1997 7 3 255 266 (Pubitemid 127554217)
10. Sparks D. L., Scheff S. W., Hunsaker J. C., Liu H., Landers T., Gross D. R., Induction of Alzheimer-like -amyloid immunoreactivity in the brains of rabbits with dietary cholesterol Experimental Neurology 1994 126 1 88 94
11. Lemieux S. K., Smith-Bell C. A., Wells J. R., Ezerioha N. M., Carpenter J. S., Sparks D. L., Schreurs B. G., Neurovascular changes measured by time-of-flight MR angiography in cholesterol-fed rabbits with cortical amyloid -peptide accumulation Journal of Magnetic Resonance Imaging 2010 32 2 306 314
12. Deci S., Lemieux S. K., Smith-Bell C. A., Sparks D. L., Schreurs B. G., Cholesterol increases ventricular volume in a rabbit model of Alzheimer's Disease Journal of Alzheimer's Disease 2012 29 2 283 292
13. Hooijmans C. R., Van der Zee C. E. E. M., Dederen P. J., Brouwer K. M., Reijmer Y. D., van Groen T., Broersen L. M., Ltjohann D., Heerschap A., Kiliaan A. J., DHA and cholesterol containing diets influence Alzheimer-like pathology, cognition and cerebral vasculature in APPSWE / PS1dE9 mice Neurobiology of Disease 2009 33 3 482 498
14. Lefterov I., Fitz N. F., Cronican A., Lefterov P., Staufenbiel M., Koldamova R., Memory deficits in APP23/Abca1+/- mice correlate with the level of A oligomers ASN Neuro 2009 1 2 65 76
15. Granholm A. C., Bimonte-Nelson H. A., Moore A. B., Nelson M. E., Freeman L. R., Sambamurti K., Effects of a saturated fat and high cholesterol diet on memory and hippocampal morphology in the middle-aged rat Journal of Alzheimer's Disease 2008 14 2 133 145 (Pubitemid 352040036)
16. Micale V., Scapagnini G., Colombrita C., Mazzola C., Alkon D. L., Drago F., Behavioral effects of dietary cholesterol in rats tested in experimental models of mild stress and cognition tasks European Neuropsychopharmacology 2008 18 6 462 471
17. Miller S., Wehner J. M., Cholesterol treatment facilitates spatial learning performance in DBA/2Ibg mice Pharmacology Biochemistry and Behavior 1994 49 1 257 261
18. Upchurch M., Wehner J. M., DBA/2Ibg mice are incapable of cholinergically-based learning in the Morris water task Pharmacology Biochemistry and Behavior 1988 29 2 325 329 (Pubitemid 19258268)
19. Dufour F., Liu Q. Y., Gusev P., Alkon D., Atzori M., Cholesterol-enriched diet affects spatial learning and synaptic function in hippocampal synapses Brain Research 2006 1103 1 88 98 (Pubitemid 44080124)
20. Vikar V., Rauvala H., Ikonen E., Cognitive deficit and development of motor impairment in a mouse model of Niemann-Pick type C disease Behavioural Brain Research 2002 132 1 1 10 (Pubitemid 34195453)
21. Xu G., Servatius R. J., Shefer S., Tint G. S., O'Brien W. T., Batta A. K., Salen G., Relationship between abnormal cholesterol synthesis and retarded learning in rats Metabolism: Clinical and Experimental 1998 47 7 878 882 (Pubitemid 28313199)
22. Endo Y., Nishimura J. I., Kimura F., Impairment of maze learning in rats following long-term glucocorticoid treatments Neuroscience Letters 1996 203 3 199 202 (Pubitemid 26040209)
23. O'Brien W. T., Xu G., Batta A., Tint G. S., Salen G., Dyer C. A., Kendler A., Servatius R. J., Developmental sensitivity of associative learning to cholesterol synthesis inhibitors Behavioural Brain Research 2002 129 1-2 141 152 (Pubitemid 34059236)
24. Schreurs B. G., Smith-Bell C. A., Darwish D. S., Stankovic G., Sparks D. L., High dietary cholesterol facilitates classical conditioning of the rabbit's nictitating membrane response Nutritional Neuroscience 2007 10 1-2 31 43 (Pubitemid 46671781)
25. Schreurs B. G., Smith-Bell C. A., Darwish D. S., Wang D., Burhans L. B., Gonzales-Joekes J., Deci S., Stankovic G., Sparks D. L., Cholesterol enhances classical conditioning of the rabbit heart rate response Behavioural Brain Research 2007 181 1 52 63 (Pubitemid 46765002)
26. Schreurs B. G., Smith-Bell C. A., Lochhead J., Sparks D. L., Cholesterol modifies classical conditioning of the rabbit (Oryctolagus cuniculus) nictitating membrane response Behavioral Neuroscience 2003 117 6 1220 1232 (Pubitemid 37549424)
27. Darwish D. S., Wang D., Konat G. W., Schreurs B. G., Dietary cholesterol impairs memory and memory increases brain cholesterol and sulfatide levels Behavioral Neuroscience 2010 124 1 115 123
28. Zambn D., Quintana M., Mata P., Alonso R., Benavent J., Cruz-Snchez F., Gich J., Pocov M., Civeira F., Capurro S., Bachman D., Sambamurti K., Nicholas J., Pappolla M. A., Higher incidence of mild cognitive impairment in familial hypercholesterolemia The American Journal of Medicine 2010 123 3 267 274
29. Solomon A., Kreholt I., Ngandu T., Wolozin B., MacDonald S. W. S., Winblad B., Nissinen A., Tuomilehto J., Soininen H., Kivipelto M., Serum total cholesterol, statins and cognition in non-demented elderly Neurobiology of Aging 2009 30 6 1006 1009
30. Goldstein F. C., Ashley A. V., Endeshaw Y. W., Hanfelt J., Lah J. J., Levey A. I., Effects of hypertension and hypercholesterolemia on cognitive functioning in patients with Alzheimer disease Alzheimer Disease and Associated Disorders 2008 22 4 336 342
31. Solomon A., Kreholt I., Ngandu T., Winblad B., Nissinen A., Tuomilehto J., Soininen H., Kivipelto M., Serum cholesterol changes after midlife and late-life cognition: twenty-one-year follow-up study Neurology 2007 68 10 751 756 (Pubitemid 46667900)
32. Bocan T. M. A., Mueller S. B., Mazur M. J., Uhlendorf P. D., Brown E. Q., Kieft K. A., The relationship between the degree of dietary-induced hypercholesterolemia in the rabbit and atherosclerotic lesion formation Atherosclerosis 1993 102 1 9 22 (Pubitemid 23269727)
33. Riedmller K., Metz S., Bonaterra G. A., Kelber O., Weiser D., Metz J., Kinscherf R., Cholesterol diet and effect of long-term withdrawal on plaque development and composition in the thoracic aorta of New Zealand White rabbits Atherosclerosis 2010 210 2 407 413
34. Lamb D. J., Avades T. Y., Ferns G. A. A., Biphasic modulation of atherosclerosis induced by graded dietary copper supplementation in the cholesterol-fed rabbit International Journal of Experimental Pathology 2001 82 5 287 294 (Pubitemid 34225160)
35. Henry P. D., Bentley K. I., Suppression of atherogenesis in cholesterol-fed rabbit treated with nifedipine Journal of Clinical Investigation 1981 68 5 1366 1369 (Pubitemid 12235039)
36. Huang Y., Walker K. E., Hanley F., Narula J., Houser S. R., Tulenko T. N., Cardiac systolic and diastolic dysfunction after a cholesterol-rich diet Circulation 2004 109 1 97 102 (Pubitemid 38056028)
37. Schreurs B. G., Alkon D. L., US-US conditioning of the rabbit's nictitating membrane response: emergence of a conditioned response without alpha conditioning Psychobiology 1990 18 3 312 320 (Pubitemid 20304702)
38. Coleman S. R., Gormezano I., Classical conditioning of the rabbit's (Oryctolagus cuniculus) nictitating membrane response under symmetrical CS-US interval shifts Journal of Comparative and Physiological Psychology 1971 77 3 447 455
39. Gormezano I., Sidowski J. B., Classical conditioning Experimental Methods and Instrumentation in Psychology 1966 New York, NY, USA McGraw-Hill 385 420
40. Gormezano I., Gibbs C. M., Transduction of the rabbit's nictitating membrane response Behavior Research Methods, Instruments, Computers 1988 20 18 21
41. Woodruff-Pak D. S., Disterhoft J. F., Where is the trace in trace conditioning? Trends in Neurosciences 2008 31 2 105 112
42. Sparks D. L., Intraneuronal -amyloid immunoreactivity in the CNS Neurobiology of Aging 1996 17 2 291 299
43. Weible A. P., McEchron M. D., Disterhoft J. F., Cortical involvement in acquisition and extinction of trace eyeblink conditioning Behavioral Neuroscience 2000 114 6 1058 1067 (Pubitemid 32001885)
44. Holland D., Brewer J. B., Hagler D. J., Fenema-Notestine C., Dale A. M., Subregional neuroanatomical change as a biomarker for Alzheimer's disease Proceedings of the National Academy of Sciences of the United States of America 2009 106 49 20954 20959
45. Zheng H., Zhang C., Yang W., Wang Y., Lin Y., Yang P., Yu Q., Fan J., Liu E., Fat and cholesterol diet induced lipid metabolic disorders and insulin resistance in rabbit Experimental and Clinical Endocrinology and Diabetes 2009 117 8 400 405
46. Sparks D. L., Cholesterol metabolism and brain amyloidosis: evidence for a role of copper in the clearance of A through the liver Current Alzheimer Research 2007 4 2 165 169 (Pubitemid 46557506)
47. Russell J. C., Proctor S. D., Small animal models of cardiovascular disease: tools for the study of the roles of metabolic syndrome, dyslipidemia, and atherosclerosis Cardiovascular Pathology 2006 15 6 318 330 (Pubitemid 44755356)
48. Yanni A. E., The laboratory rabbit: an animal model of atherosclerosis research Laboratory Animals 2004 38 3 246 256 (Pubitemid 38962073)
49. Sparks D. L., Martin T. A., Gross D. R., Hunsaker J. C., Link between heart disease, cholesterol, and Alzheimer's disease: a review Microscopy Research and Technique 2000 50 4 287 290 (Pubitemid 30651168)
50. Schreurs B. G., Long-term memory and extinction of rabbit nictitating membrane trace conditioning Learning and Motivation 1998 29 1 68 82 (Pubitemid 128343463)
51. Schreurs B. G., Long-term memory and extinction of the classically conditioned rabbit nictitating membrane response Learning and Motivation 1993 24 3 293 302
52. Williams K. J., Feig J. E., Fisher E. A., Rapid regression of atherosclerosis: insights from the clinical and experimental literature Nature Clinical Practice Cardiovascular Medicine 2008 5 2 91 102 (Pubitemid 351168064)
53. Prasad K., Regression of hypercholesterolemic atherosclerosis in rabbits by secoisolariciresinol diglucoside isolated from flaxseed Atherosclerosis 2008 197 1 34 42 (Pubitemid 351273270)
54. Stein Y., Stein O., Does therapeutic intervention achieve slowing of progression or bona fide regression of atherosclerotic lesions? Arteriosclerosis, Thrombosis, and Vascular Biology 2001 21 2 183 188 (Pubitemid 32125363)
55. Adams C. W. M., Morgan R. S., Regression of atheroma in the rabbit Atherosclerosis 1977 28 4 399 404 (Pubitemid 8247239)
56. Collin B., Busseuil D., Zeller M., Perrin C., Barthez O., Duvillard L., Vergely C., Bardou M., Dumas M., Cottin Y., Rochette L., Increased superoxide anion production is associated with early atherosclerosis and cardiovascular dysfunctions in a rabbit model Molecular and Cellular Biochemistry 2007 294 1-2 225 235 (Pubitemid 46188904)
57. Van Lenten B. J., Wagner A. C., Navab M., Anantharamaiah G. M., Hama S., Reddy S. T., Fogelman A. M., Lipoprotein inflammatory properties and serum amyloid A levels but not cholesterol levels predict lesion area in cholesterol-fed rabbits Journal of Lipid Research 2007 48 11 2344 2353 (Pubitemid 350058746)
58. Tronson N. C., Taylor J. R., Molecular mechanisms of memory reconsolidation Nature Reviews Neuroscience 2007 8 4 262 275 (Pubitemid 46452320)
59. Frankland P. W., Bontempi B., The organization of recent and remote memories Nature Reviews Neuroscience 2005 6 2 119 130 (Pubitemid 40188946)
60. Bouton M. E., Context and behavioral processes in extinction Learning and Memory 2004 11 5 485 494 (Pubitemid 39299694)
61. Rudy J. W., Huff N. C., Matus-Amat P., Understanding contextual fear conditioning: insights from a two-process model Neuroscience and Biobehavioral Reviews 2004 28 7 675 685 (Pubitemid 39535865)
62. Servatius R. J., Beck K. D., Mild interoceptive stressors affect learning and reactivity to contextual cues: toward understanding the development of unexplained illnesses Neuropsychopharmacology 2005 30 8 1483 1491 (Pubitemid 41153120)
63. Hein A. M., O'Banion M. K., Neuroinflammation and memory: the role of prostaglandins Molecular Neurobiology 2009 40 1 15 32
64. Barrientos R. M., Higgins E. A., Biedenkapp J. C., Sprunger D. B., Wright-Hardesty K. J., Watkins L. R., Rudy J. W., Maier S. F., Peripheral infection and aging interact to impair hippocampal memory consolidation Neurobiology of Aging 2006 27 5 723 732
65. Cai W. H., Blundell J., Han J., Greene R. W., Powell C. M., Postreactivation glucocorticoids impair recall of established fear memory Journal of Neuroscience 2006 26 37 9560 9566 (Pubitemid 44396869)
66. Hopkins S. J., Central nervous system recognition of peripheral inflammation: a neural, hormonal collaboration Acta Bio-Medica: Atenei Parmensis 2007 78, supplement 1 231 247
67. Siegel S., Ramos B. M. C., Applying laboratory research: drug anticipation and the treatment of drug addiction Experimental and Clinical Psychopharmacology 2002 10 3 162 183 (Pubitemid 34919927)
68. Woods S. C., Ramsay D. S., Pavlovian influences over food and drug intake Behavioural Brain Research 2000 110 1-2 175 182 (Pubitemid 30236301)
69. Siegel S., Multiple chemical sensitivity as a conditional response Toxicology and Industrial Health 1999 15 3-4 323 330 (Pubitemid 30030690)
70. Wang S. H., Morris R. G. M., Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation Annual Review of Psychology 2010 61 49 79
71. Takashima A., Nieuwenhuis I. L. C., Jensen O., Talamini L. M., Rijpkema M., Fernndez G., Shift from hippocampal to neocortical centered retrieval network with consolidation Journal of Neuroscience 2009 29 32 10087 10093
72. Dbiec J., Doyre V., Nader K., LeDoux J. E., Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala Proceedings of the National Academy of Sciences of the United States of America 2006 103 9 3428 3433 (Pubitemid 43346485)
73. Inda M. C., Delgado-Garcia J. M., Carrion A. M., Acquisition, consolidation, reconsolidation, and extinction of eyelid conditioning responses require de novo protein synthesis Journal of Neuroscience 2005 25 8 2070 2080 (Pubitemid 40289412)
74. Johansen J. P., Cain C. K., Ostroff L. E., Ledoux J. E., Molecular mechanisms of fear learning and memory Cell 2011 147 3 509 524
75. Nader K., Hardt O., A single standard for memory: the case for reconsolidation Nature Reviews Neuroscience 2009 10 3 224 234
76. Duvarci S., Ben Mamou C., Nader K., Extinction is not a sufficient condition to prevent fear memories from undergoing reconsolidation in the basolateral amygdala European Journal of Neuroscience 2006 24 1 249 260 (Pubitemid 44050684)
77. Suzuki A., Josselyn S. A., Frankland P. W., Masushige S., Silva A. J., Kida S., Memory reconsolidation and extinction have distinct temporal and biochemical signatures Journal of Neuroscience 2004 24 20 4787 4795 (Pubitemid 38668203)
78. Ghribi O., Larsen B., Schrag M., Herman M. M., High cholesterol content in neurons increases BACE, -amyloid, and phosphorylated tau levels in rabbit hippocampus Experimental Neurology 2006 200 2 460 467 (Pubitemid 44107924)
79. Robleto K., Poulos A. M., Thompson R. F., Brain mechanisms of extinction of the classically conditioned eyeblink response Learning and Memory 2004 11 5 517 524 (Pubitemid 39299698)
80. Perrett S. P., Mauk M. D., Extinction of conditioned eyelid responses requires the anterior lobe of cerebellar cortex Journal of Neuroscience 1995 15 3 I 2074 2080
81. Delamater A. R., Experimental extinction in Pavlovian conditioning: behavioural and neuroscience perspectives Quarterly Journal of Experimental Psychology Section B 2004 57 2 97 132 (Pubitemid 38483860)
82. Pavlov I. P., Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex. (G. V. Anrep, Trans.) 1927 London, UK Oxford University Press
83. Rescorla R. A., Wagner A. R., Black A. H., Prokasy W. F., A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement Classicl Conditioning II: Current Research and Theory 1972 New York, NY, USA Appleton-Century-Crofts 64 99
84. Heverin M., Meaney S., Ltjohann D., Diczfalusy U., Wahren J., Bjrkhem I., Crossing the barrier: net flux of 27-hydroxycholesterol into the human brain Journal of Lipid Research 2005 46 5 1047 1052
85. Yehuda S., Rabinovitz S., Mostofsky D. I., Mediation of cognitive function by high fat diet following stress and inflammation Nutritional Neuroscience 2005 8 5-6 309 315
86. Rahman S. M. A., Van Dam A. M., Schultzberg M., Crisby M., High cholesterol diet results in increased expression of interleukin-6 and caspase-1 in the brain of apolipoprotein E knockout and wild type mice Journal of Neuroimmunology 2005 169 1-2 59 67 (Pubitemid 41527092)
87. Schreurs B. G., Smith-Bell C. A., Darwish D. S., Stankovic G., Sparks D. L., Classical conditioning of the rabbit's nictitating membrane response is a function of the duration of dietary cholesterol Nutritional Neuroscience 2007 10 3-4 159 168 (Pubitemid 47490015)
88. Berkman Z., Tanriover G., Acar G., Sati L., Altug T., Demir R., Changes in the brain cortex of rabbits on a cholesterol-rich diet following supplementation with a herbal extract of Tribulus terrestris Histology and Histopathology 2009 24 6 683 692