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Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 10, 2007 - Issue 1-2
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Articles

High dietary cholesterol facilitates classical conditioning of the rabbit's nictitating membrane response

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Pages 31-43 | Published online: 05 Sep 2013

References

  • Alexander GJ, Kopeloff LM. 1971. Induced hypercholesterolemia and decrease susceptibility to seizures in experimental animals. Exp Neurol 32:134–140.
  • Alissa EM, Bahijri SM, Lamb DJ, Ferns GAA. 2004. The effects of coadministration of dietary copper and zinc supplements on atherosclerosis, antioxidant enzymes and indices of lipid peroxidation in the cholesterol-fed rabbit. Int J Exp Pathol 85: 265–275.
  • Atzmon G, Gabriely I, Griener W, Davidson D, Schechter C, Brazilai N. 2002. Plasma HDL levels highly correlate with cognitive function in exceptional longevity. J Gerontol A Biol Sci Med Sci 57A:M712–M715.
  • Barrientos RM, Higgins EA, Biedenkapp JC, Sprunger DB, Wright- Hardesty KJ, Watkins LR, Rudy JW, Maier SF. 2006. Peripheral infection and aging interact to impair hippocampal memory consolidation. Neurobiol Aging 27:723–732.
  • Beaslely CL, Honer WG, von Bergmann K, Falkai P, Lutjohann D, Bayer TA. 2005. Reductions in cholesterol and synaptic markers in association cortex in mood disorders. Bipolar Disord 7: 449–455.
  • Bird KD. 2004. Analysis of variance via confience intervals. London: Sage. p 226.
  • Bjorkhem I. 2002. Do oxysterols control cholesterol homeostasis? J Clin Invest 110:725–730.
  • Bjorkhem I, Meaney S. 2004. Brain cholesterol: Long secret life behind a barrier. Arterioscler Thromb Vasc Biol 24:1–11.
  • Brennan FX, Tieder JBI. 2006. Centrally administered tumor necrosis tactor-a facilitates the avoidance performance of Sprague-Dawley rats. Brain Res 1109:142–145.
  • Brennan FX, Beck KD, Servatius RJ. 2004. Proinflammatory cytokines differentially affect lever press avoidance acquisition in rats. Behav Brain Res 153:351–355.
  • Buck DL, Seager MA, Schreurs BG. 2001. Conditioning-specific reflex modification of the rabbit (Oryctolagus cuniculus) nictitating membrane response: Generality and nature of the phenomenon. Behav Neurosci 115:1039–1047.
  • Cao D, Fukuchi K, Wan H, Kim H, Li L. 2006. Lack of LDL receptor aggravates learning deficits and amyloid deposits in Alzheimer transgenic mice. Neurobiol Aging 27:1632–1643.
  • Coleman SR, Gormezano I. 1971. Classical conditioning of the rabbit’s (Oryctolagus cuniculus) nictitating membrane response under symmetrical CS-US interval shifts. J Comp Physiol Psychol 77:447–455.
  • JACC Study Group Cui R, Iso H, Toyoshima H, Date C, Yamamoto A, Kikuchi S, Kondo T, Watanabe Y, Koizumi A, Inaba Y, Tamakoshi A. JACC Study Group. 2006. Serum cholesterol levels of mortality from stroke and coronary heart disease in Japanese: The JACC study. Atherosclerosis. (In press).
  • Deyo RA, Straube KT, Disterhoft JF. 1989. Nimodipine facilitates associative learning in aging rabbits. Science 243:809–811.
  • Dietschy JM, Turley SD. 2001. Cholesterol metabolism in the brain. Curr Opin Lipidol 12:105–112.
  • Dietschy JM, Turley SD. 2004. Cholesterol metabolism in the central nervous system during early development and in the mature animal. J Lipid Res 45:1375–1397.
  • Dufour F, Liu Q-Y, Gusev P, Alkon DL, Atzori M. 2006. Cholesterol-enriched diet affects spatial learning and synaptic function in hippocampal synapses. Brain Res 1103:88–98.
  • Elias PK, Elias MF, D’Agostino RB, Sullivan LM, Wolf PA. 2005. Serum cholesterol and cognitive performance in the Framingham heart study. Psychosom Med 67:24–30.
  • Endo Y, Nishimura J-I, Kimura F. 1996. Impairment of maze learning in rats following long-term glucocorticoid treatments. Neurosci Lett 203:199–202.
  • Evans RM, Emsley CL, Gao S, Sahota A, Hall KS, Farlow MR, Hendrie H. 2000. Serum cholesterol, APOE genotype, and the risk of Alzheimer’s disease: A population-based study of African Americans. Neurology 54:240–242.
  • Fazio S, Linton MF. 2001. The inflamed plaque: Cytokine production and cellular cholesterol balance in the vessel wall. Am J Cardiol 88A:12E-15E.
  • Giese KP, Storm JF, Reuter D, Fedorov NB, Shao L-R, Leichter T, Pongs O, Silva AJ. 1998. Reduced K+ channel inactivation, spike broadening, and after-hyperpolarization in Kvß 1.1-deficient mice with impaired learning. Learn Mem 5:257–273.
  • Goritz C, Mauch DH, Nagler K, Pfrieger FW. 2002. Role of glial- derived cholesterol in synaptogenesis: New revelations in the synapse-glia affair. J Physiol (Paris) 96:257–263.
  • Gormezano I. 1966. Classical conditioning. In: Sidowski JB, editor. Experimental methods and instrumentation in psychology. New York: McGraw-Hill.
  • Gormezano I, Gibbs CM. 1988. Transduction of the rabbit’s nictitating membrane response. Behav Res Methods Instrum Comput 20:18–21.
  • Gracia KS, Mauk MD, Weidemann G, Kehoe EJ. 2003. Covariation of alternative measures of responding in rabbit (Oryctolagus cuniculus) eyeblink conditioning during acquisition training and tone generalization. Behav Neurosci 117:292–303.
  • Hartmann T. 2001. Cholesterol, Aß and Alzheimer’s disease. Trends Neurosci 11:S45–S48.
  • Henry PD, Bentley KI. 1981. Suppression of atherogenesis in cholesterol-fed rabbit treated with nifedipine. J Clin Invest 68: 1366–1369.
  • Herz J, Chen Y. 2006. Reelin, lipoprotein receptors and synaptic plasticity. Nat Rev Neurosci 7:850–859.
  • Heverin M, Meaney S, Lutjohann D, Diczfalusy U, Wahren J, Bjorkhem I. 2005. Crossing the barrier: Net flux of 27- hydroxycholesterol into the human brain. J Lipid Res 46: 1047–1052.
  • Huang Y, Walker KE, Hanley F, Narula J, Houser SR, Tulenko TN. 2004. Cardiac systolic and diastolic dysfunction after a cholesterol-rich diet. Circulation 109:97–102.
  • Jarvik GP, Wijsman EM, Kukull WA, Schellenberg GD, Yu C, Larson EB. 1995. Interactions of apolipoprotein E genotype, total cholesterol level, age, and sex in prediction of Alzheimer’s disease. Neurology 45:1092–1096.
  • Johnston D, Christie BR, Frick A, Gray R, Hoffman DA, Schexnayder LK, Watanabe S, Yuan L-L. 2003. Active dendrites, potassium channels and synaptic plasticity. Phil Trans R Soc Lond B 358:667–674.
  • Kane KA, Robinson GB. 1999. Effect of chronic nimodipine on spatial learning and on long-term potentiation. Behav Brain Res 98:95–101.
  • Kaul D. 2001. Molecular link between cholesterol, cytokines and atherosclerosis. Mol Cell Neurosci 219:65–71.
  • Kessler AR, Kessler B, Yehuda S. 1986. In vivo modulation of brain cholesterol level and learning performance by a novel plant lipid: Indication of interactions between hippocampal -cortical cholesterol and learning. Life Sci 38:1185–1192.
  • Kivipelto M, Helkala E-L, Hanninen T, Laakso MP, Hallikainen M, Alhainen K, Soininen H, Tuomilehto J, Nissinen A. 2001. Midlife vascular risk factors and late-life mild cognitive impairment: A population-based study. Neurology 56: 1683–1689.
  • Kolsch H, Heun R, Kerksiek A, Bergmann Kv, Maier W, Lutjohann D. 2004. Altered levels of plasma 24S- and 27-hydroxycholes- terol in demented patients. Neurosci Lett 368:303–308.
  • Koudinov AR, Koudinova NV 2001. Essential role of cholesterol in synaptic plasticity and neuronal degeneration. FASEB J 15: 1858–1860.
  • Lamb DJ, Avades TY, Ferns GAA. 2001. Biphasic modulation of atherosclerosis induced by graded dietary copper supplementation in the cholesterol-fed rabbit. Int J Exp Pathol 82: 287–294.
  • Li L, Cao D, Kim H, Lester R, Fukuchi K. 2006. Simvastatin enhances learning and memory independent of amyloid load in mice. Ann Neurol 60:729–739.
  • Locatelli S, Lutjohann D, Schmidt HH-J, Otto C, Beisiegel U, von Bergmann K. 2002. Reduction of plasma 24S-hydroxycholes- terol (cerebrosterol) levels using high-dosage simvastatin in patients with hypercholesterolemia. Evidence that simvastatin affects cholesterol metabolism in the human brain. Arch Neurol 59:213–216.
  • Maier SF, Watkins LR. 2003. Immune-to-central nervous system communication an its role in modulating pain and cognition: Implications for cancer and cancer treatment. Brain Behav Immun 17:S125–S131.
  • Mauch DH, Nagler K, Schumacher S, Goritz C, Muller E-C, Otto A, Pfrieger FW. 2001. CNS synaptogenesis promoted by glial- derived cholesterol. Science 294:1354–1357.
  • Miller S, Wehner JM. 1994. Cholesterol treatment facilitates spatial learning performance in DBA/2Ibg mice. Pharmacol Biochem Behav 49:257–261.
  • Muldoon MF, Ryan CM, Matthews KA, Manuck SB. 1997. Serum cholesterol and intellectual performance. Psychosom Med 59: 382–387.
  • Naslund J, Haroutunian V, Mohs R, Davis KL, Davies P, Greengard P, Buxbaum JD. 2000. Correlation between elevated levels of amyloid ß-peptide in the brain and cognitive decline. JAMA 283: 1571–1577.
  • Nayler WG. 1999. Review of preclinical data of calcium channel blockers and atherosclerosis. J Cardiovasc Pharmacol 33: S7–S11.
  • Nelson TJ, Schreurs BG, Alkon DL. 1999. Memory storage mechanisms: GTP-binding proteins and conservation across species. In: Adelman G, Smith BH, editors. Elsevier’s encyclopedia ofneuroscience. NewYork: Elseiver. p 1138–1141.
  • Notkola I-L, Sulkava R, Pekkanen J, Erkinjunti T, Ehnholm C, Kivinen P, Tuomilehto J, Nissinen A. 1998. Serum total cholesterol, apolipoprotein Es4 allele, and Alzheimer’s disease. Neuroepidemiology 17:14–20.
  • O’Brien WT, Xu G, Batta A, Tint GS, Salen G, Dyer CA, Kendler A, Servatius RJ. 2002. Developmental sensitivity of associative learning to cholesterol synthesis inhibitors. Behav Brain Res 129: 141–152.
  • Papassotiropoulos A, Wollmer MA, Tsolaki M, Brunner F, Molyva D, Lutjohann D, Nitsch R, Hock C. 2005. A cluster of cholesterol-related genes confers susceptibility for Alzheimer’s disease. J Clin Psychiatry 66:940–947.
  • Pearson HA, Peers C. 2006. Physiological roles for amyloid ß peptides. J Physiol (Lond) 575:5–10.
  • Plant LD, Boyle JP, Smith IF, Peers C, Pearson HA. 2003. The production of amyloid ß peptide is a critical requirement for the viability of central neurons. J Neurosci 23:5531–5535.
  • Plant LD, Webster NJ, Boyle JP, Ramsden M, Frier DB, Peers C, Pearson HA. 2006. Amyloid ß peptide as a physiological modulator of neuronal “A”-type K+ current. Neurobiol Aging 27:1673–1683.
  • Poirier J. 2005. Apolipoportein E, cholesterol transport and synthesis in sporadic Alzheimer’s disease. Neurobiol Aging 26: 355–361.
  • Qiu S, Korwek KM, Weeber EJ. 2005. A fresh look at an ancient family: Emerging roles for low density lipoprotein receptors in synaptic plasticity and memory formation. Neurobiol Learn Mem 85:16–29.
  • Quartermain D. 2000. Chronic administration of the Ca2+ channel blocker amlodipine facilitates learning and memory in mice. Eur J Pharmacol 399:57–63.
  • Rahman SMA, Van Dam A-M, Schultzberg M, Crisby M. 2005. High cholesterol diet results in increased expression of interleukin-6 and caspase-1 in the brain of apolipoprotein E knockout and wild type mice. J Neuroimmunol 169:59–67.
  • Reitan RM, Shipley RE. 1963. The relationship of serum cholesterol changes to psychological abilities. J Gerontol 18: 350–357.
  • Reitz C, Luchsinger JA, Tang M-X, Manly J, Mayeux R. 2005. Impact of plasma lipids and time on memory performance in healthy elderly without dementia. Neurology 64:1378–1383.
  • Rockwood K. 2006. Epidemiological and clinical trials evidence about a preventive role for statins in Alzheimer’s disease. Acta Neurol Scand 114:s71–s77.
  • Rockwood K, Kirkland S, Hogan DB, McKnight C, Merry H, Verreault R, Wolfson C, McDowell I. 2002. Use of lipidlowering agents, indication bias, and the risk of dementia in community-dwelling elderly people. Arch Neurol 59:223–227.
  • Schachter M. 1997. Calcium antagonists and atherosclerosis. Int J Cardiol 62:S9–S15.
  • Schonknecht P, Lutjohann D, Pantel J, Bardenheuer H, Hartmann T, von Bergmann K, Beyreuther K, Schroder J. 2002. Cerebrospinal fluid 24S-hydroxycholesterol is increased in patients with Alzheimer’s disease compared to healthy controls. Neurosci Lett 324:83–85.
  • Schrader LA, Anderson AE, Varga AW, Levy M, Sweatt JD. 2002. The other half of Hebb: K+ channels and the regulation of neuronal excitability in the hippocampus. Mol Neurobiol 25: 51–66.
  • Schreurs BG. 2003. Classical conditioning and modification of the rabbit’s (Oryctolagus cuniculus) unconditioned nictitating membrane response. Behav Cogn Neurosci Rev 2:83–96.
  • Schreurs BG, Alkon DL. 1990. US-US conditioning of the rabbit’s nictitating membrane response: Emergence of a conditioned response without alpha conditioning. Psychobiology 18: 312–320.
  • Schreurs BG, Oh MM, Hirashima C, Alkon DL. 1995. Conditioning-specific modification ofthe rabbit’s unconditioned nictitating membrane response. Behav Neurosci 109:24–33.
  • Schreurs BG, Gusev PA, Tomsic D, Alkon DL, Shi T. 1998. Intracellular correlates of acquisition and long-term memory of classical conditioning in Purkinje cell dendrites in slices ofrabbit cerebellar lobule HVI. J Neurosci 18:5498–5507.
  • Schreurs BG, Shi T, Pineda SI, Buck DL. 2000. Conditioning the unconditioned response: Modification of the rabbit’s (Oryctola- gus cuniculus) unconditioned nictitating membrane response. J Exp Psychol Anim Behav Process 26:144–156.
  • Schreurs BG, Smith-Bell CA, Lochhead J, Sparks DL. 2003. Cholesterol modifies classical conditioning of the rabbit (Oryctolagus cuniculus) nictitating membrane response. Behav Neurosci 117:1220–1232.
  • Schreurs BG, Gonzales-Joekes J, Smith-Bell CA. 2006. Conditioning-specific reflex modification of the rabbit (Oryctolagus cuniculus) nictitating membrane response is sensitive to context. Learn Behav 34:315–324.
  • Seager MA, Smith-Bell CA, Schreurs BG. 2003. Conditioning- specific reflex modification of the rabbit (Oryctolagus cuniculus) nictitating membrane response: US intensity effects. Learn Behav 31:292–298.
  • Servatius RJ, Beck KD. 2003. Facilitated acquisition of the classically conditioned eyeblink response in male rats after systemic IL-1ß. Integr Physiol Behav Sci 38:169–178.
  • Shobab LA, Hsiung G-Y, Feldman HH. 2005. Cholesterol in Alzheimer’s disease. Lancet Neurol 4:841–852.
  • Simons M, Keller P, Dichgans J, Schulz JB. 2001. Cholesterol and Alzheimer’s disease: Is there a link? Neurology 57:1089–1093.
  • Simons M, Schwarzler F, Lutjohann D, von Bergmann K, Beyreuther K, Dichgans J, Wormstall H, Hartmann T, Schulz JB. 2002. Treatment with simvastatin in normocholesterolemic patients with Alzheimer’s disease: A 26-week randomized, placebo-controlled, double-blind trial. Ann Neurol 52: 346–350.
  • Sooksawate T, Simmonds MA. 2001a. Effects of membrane cholesterol on the sensitivity of the GABAA receptor to GABA in acutely dissociated rat hippocampal neurones. Neuropharmacology 40:178–184.
  • Sooksawate T, Simmonds MA. 2001b. Influence of membrane cholesterol on modulation of the GABAa receptor by neuroactive steroids and other potentiators. Br J Pharmacol 134:1303–1311.
  • Sparks DL. 1997a. Coronary artery disease, hypertension, ApoE and cholesterol: A link to Alzheimer’s disease. Ann NY Acad Sci 826:128–146.
  • Sparks DL. 1997b. Dietary cholesterol induces Alzheimer-like ß- amyloid immunoreactivity in rabbit brain. Nutr Metab Cardiovasc Dis 7:255–266.
  • Sparks DL, Schreurs BG. 2003. Trace amounts of copper in water induce ß-amyloid plaques and learning deficits in a rabbit model of Alzheimer’s disease. Proc Natl Acad Sci USA 100: 11065–11069.
  • Sparks DL, Hunsaker JC, III, Scheff SW, Kryscio RJ, Henson JL, Markesbery WR. 1990. Cortical senile plaques in coronary heart disease, aging and Alzheimer’s disease. Neurobiol Aging 11: 601–607.
  • Sparks DL, Scheff SW, Hunsaker JC, III, Liu H, Landers T, Gross DR. 1994. Induction of Alzheimer-like ß-amyloid immunor- eactivity in the brains of rabbits with dietary cholesterol. Exp Neurol 126:88–94.
  • Sparks DL, Lochhead J, Horstman D, Wagoner T, Martin T. 2002. Water quality has a pronounced effect on cholesterol-induced accumulation of Alzheimer amyloid (aß) in rabbit brain. J Alzheimers Dis 4:523–529.
  • Sparks DL, Connor DJ, Sabbagh MN, Petersen RB, Lopez J, Browne P. 2006a. Circulating cholesterol levels, apolipoprotein E genotype and dementia severity influence the benefit of atorvastatin treatment in Alzheimer’s disease: Results of the Alzheimer’s disease cholesterol-lowering treatment (ADCLT) trial. Acta Neurol Scand 114:s3–s7.
  • Sparks DL, Friedland R, Petanceska S, Schreurs BG, Shi J, Perry G, Smith MA, Sharma A, DeRosa S, Ziolkowski C, Stankovic G. 2006b. Trace copper levels in the drinking water, but not zinc or aluminum influence CNS Alzheimer-like pathology. J Nutr Health Aging 10:247–254.
  • Stewart R, Russ C, Richards M, Brayne C, Lovestone S, Mann A. 2001. Apolipoprotein E genotype, vascular risk and early cognitive impairment in an African Caribbean population. Dement Geriatr Cogn Disord 12:251–256.
  • Thomson LM, Sutherland RJ. 2005. Systemic administration of lipopolysaccharide and interleukin-1ß have different effects on memory consolidation. Brain Res Bull 67:24–29.
  • Tuma PL, Hubbard AL. 2003. Transcytosis: Crossing cellular barriers. Physiol Rev 83:871–932.
  • Upchurch M, Wehner JM. 1988. DBA/2Ibg mice are incapable of cholinergically-based learning in the Morris water maze. Pharmacol Biochem Behav 29:325–329.
  • van Exel E, de Craen AJM, Gussekloo J, Houx P, Bootsma-van der Weil A, Macfarlane PW, Blauw GJ, Westendorp RGP. 2002. Association between high-density lipoprotein and cognitive impairment in the oldest old. Ann Neurol 51:716–721.
  • Vauthey C, de Freitas GR, van Melle G, Devuyst G, Bogousslavsky J. 2000. Better outcome after stroke with higher serum cholesterol levels. Neurology 54:1944–1949.
  • Voikar V, Rauvala H, Ikonen E. 2002. Cognitive deficit and development of motor impairment in a mouse model of Niemann-Pick type C disease. Behav Brain Res 132:1–10.
  • Whitmer RA, Sidney S, Selby J, Johnston SC, Yaffe K. 2005. Midlife cardiovascular risk factors and risk of dementia in late life. Neurology 64:277–281.
  • Wolozin B, Kellman W, Celesia GC, Siegel G. 2000. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3- methyglutaryl coenzyme A reductase inhibitors. Arch Neurol 57: 1439–1443.
  • Woodruff-Pak DS, Chi J, Li Y-T, Pak MH, Fanelli RJ. 1997. Nimodipine ameliorates impaired eyeblink classical conditioning in order rabbits in the long-delay paradigm. Neurobiol Aging 18: 641–649.
  • Wood WG, Igbavboa U, Exkert GP, Johnson-Anuna LN, Muller WE. 2005. Is hypercholesterolemia a risk factor for Alzheimer’s disease. Mol Neurobiol 31:185–192.
  • Xi L, Ghosh S, Wang X, Das A, Anderson FP, Kukreja RC. 2006. Hypercholestrolemia enhances tolerance to lethal systemic hypoxia in middle-aged mice: Possible role of VEGF down- regulation in brain. Mol Cell Biochem 291:205–211.
  • Xu J, Kang J. 2005. The mechanisms and functions of activity- dependent long-term potentiation of intrinsic excitability. Rev Neurosci 16:311–323.
  • Xu G, Servatius RJ, Shefer S, Tint GS, O’Brien WT, Batta AK, Salen G. 1998. Relationship between abnormal cholesterol synthesis and retarded learning in rats. Metabolism 47: 878–882.
  • Yaffe K, Barret-Connor E, Lin F, Grady D. 2002. Serum lipoprotein levels, statin use, and cognitive function in older women. Arch Neurol 59:378–384.
  • Yanagisawa K. 2003. Cholesterol and Aß aggregation. Pharmacopsychiatry 36:S127–S129.
  • Yehuda S, Carasso RL. 1993. Modulation of learning, pain thresholds, and thermoregulation in the rat by preparations of free purified a-linolenic and linoleic acids: Determination of the optimal v3-to-v6 ratio. Proc Natl Acad Sci USA 90: 10345–10349.
  • Yehuda S, Rabinovitz S, Motofsky DI. 1998. Modulationoflearning and neuronal membrane composition in the rat by essential fatty acid preparation: Time-course analysis. Neurochem Res 23: 627–634.
  • Zhang W, Linden DJ. 2003. The other side of the engram: Experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4:885–900.
  • Zuliani G, Cherubini A, Atti AR, Ble A, Vavalle C, Di Todaro F, Benedetti C, Volpato S, Marinescu MG, Senin U, Fellin R. 2004. Low cholesterol levels are associated with short-term mortality in older patients with ischemic stroke. J Gerentol Med Sci 59A:293–297.

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