Melatonin prevents memory impairment induced by high-fat diet: Role of oxidative stress

Behavioural Brain Research

Volumn 336, Issue , 2018, Pages 93-98

  Alzoubi, Karem H ^a   Mayyas, Fadia A ^a   Mahafzah, Rania ^a   Khabour, Omar F ^a  

^a JORDAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Jordan)

Author keywords

High fat diet; Hippocampus; Maze; Melatonin; Memory

Indexed keywords

CATALASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; MELATONIN; ANTIOXIDANT; NEUROPROTECTIVE AGENT; SUPEROXIDE DISMUTASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; LIPID DIET; LONG TERM MEMORY; MALE; MAZE TEST; MEMORY DISORDER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SHORT TERM MEMORY; SPATIAL MEMORY; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECT; DRUG THERAPY; METABOLISM; SLEEP DEPRIVATION; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; DIET, HIGH-FAT; HIPPOCAMPUS; MALE; MAZE LEARNING; MELATONIN; MEMORY DISORDERS; MEMORY, LONG-TERM; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS; RATS, WISTAR; SLEEP DEPRIVATION; SPATIAL MEMORY; SUPEROXIDE DISMUTASE;

EID: 85028711619     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2017.08.047     Document Type: Article

References (90)

1. Al-Sawalha, N., Alzoubi, K., Khabour, O., Alyacoub, W., Almahmmod, Y., Eissenberg, T., Effect of prenatal exposure to waterpipe tobacco smoke on learning and memory of adult offspring rats. Nicotine Tob. Res., 2017.
2. Ali, T., Badshah, H., Kim, T.H., Kim, M.O., Melatonin attenuates D-galactose-induced memory impairment, neuroinflammation and neurodegeneration via RAGE/NF-K B/JNK signaling pathway in aging mouse model. J. Pineal Res. 58 (2015), 71–85.
3. Allegra, M., Reiter, R., Tan, D.X., Gentile, C., Tesoriere, L., Livrea, M., The chemistry of melatonin's interaction with reactive species. J. Pineal Res. 34 (2003), 1–10.
4. Alomari, M.A., Khabour, O.F., Alzoubi, K.H., Alzubi, M.A., Forced and voluntary exercises equally improve spatial learning and memory and hippocampal BDNF levels. Behav. Brain Res. 247 (2013), 34–39.
5. Alzoubi, K.H., Abdul-Razzak, K.K., Khabour, O.F., Al-Tuweiq, G.M., Alzubi, M.A., Alkadhi, K.A., Adverse effect of combination of chronic psychosocial stress and high fat diet on hippocampus-dependent memory in rats. Behav. Brain Res. 204 (2009), 117–123.
6. Alzoubi, K.H., Abdul-Razzak, K.K., Khabour, O.F., Al-Tuweiq, G.M., Alzubi, M.A., Alkadhi, K.A., Caffeine prevents cognitive impairment induced by chronic psychosocial stress and/or high fat-high carbohydrate diet. Behav. Brain Res. 237 (2013), 7–14.
7. Alzoubi, K.H., Khabour, O.F., Albawaana, A.S., Alhashimi, F.H., Athamneh, R.Y., Tempol prevents chronic sleep-deprivation induced memory impairment. Brain Res. Bull. 120 (2016), 144–150.
8. Alzoubi, K.H., Khabour, O.F., Rashid, B.A., Damaj, I.M., Salah, H.A., The neuroprotective effect of vitamin E on chronic sleep deprivation-induced memory impairment: the role of oxidative stress. Behav. Brain Res. 226 (2012), 205–210.
9. Alzoubi, K.H., Khabour, O.F., Salah, H.A., Abu Rashid, B.E., The Combined Effect of Sleep Deprivation and Western Diet on Spatial Learning and Memory: Role of BDNF and Oxidative Stress. J Mol Neurosci,., 2012.
10. Alzoubi, K.H., Khabour, O.F., Salah, H.A., Abu Rashid, B.E., The combined effect of sleep deprivation and Western diet on spatial learning and memory: role of BDNF and oxidative stress. J. Mol. Neurosci. 50 (2013), 124–133.
11. Alzoubi, K.H., Khabour, O.F., Salah, H.A., Hasan, Z., Vitamin E prevents high-fat high-carbohydrates diet-induced memory impairment: the role of oxidative stress. Physiol. Behav. 119 (2013), 72–78.
12. Alzoubi, K.H., Khabour, O.F., Salah, H.A., Rashid, B.E.A., The combined effect of sleep deprivation and western diet on spatial learning and memory: role of BDNF and oxidative stress. J. Mol. Neurosci. 50 (2013), 124–133.
13. Alzoubi, K.H., Khabour, O.F., Tashtoush, N.H., Al-Azzam, S.I., Mhaidat, N.M., Evaluation of the effect of pentoxifylline on sleep-deprivation induced memory impairment. Hippocampus 23 (2013), 812–819.
14. Alzoubi, K.H., Malkawi, B.S., Khabour, O.F., El-Elimat, T., Alali, F.Q., Arbutus andrachne, L., Reverses Sleep Deprivation-Induced Memory Impairments in Rats. Mol Neurobiol, 2017.
15. Alzoubi, K.H., Mayyas, F.A., Khabour, O.F., Salama, F.M.B., Alhashimi, F.H., Mhaidat, N.M., Chronic melatonin treatment prevents memory impairment induced by chronic sleep deprivation. Mol. Neurobiol., 2015, 1–9.
16. Alzoubi, K.H., Rababa'h, A.M., Owaisi, A., Khabour, O.F., L-carnitine prevents memory impairment induced by chronic REM-sleep deprivation. Brain Res. Bull. 131 (2017), 176–182.
17. Baydas, G., Ozveren, F., Akdemir, I., Tuzcu, M., Yasar, A., Learning and memory deficits in rats induced by chronic thinner exposure are reversed by melatonin. J. Pineal Res. 39 (2005), 50–56.
18. Beilharz, J.E., Maniam, J., Morris, M.J., Short-term exposure to a diet high in fat and sugar or liquid sugar, selectively impairs hippocampal-dependent memory, with differential impacts on inflammation. Behav. Brain Res. 306 (2016), 1–7.
19. Buettner, R., Schölmerich, J., Bollheimer, L.C., High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity 15 (2007), 798–808.
20. Butterfield, D.A., Drake, J., Pocernich, C., Castegna, A., Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol. Med. 7 (2001), 548–554.
21. Chattoraj, A., Liu, T., Zhang, L.S., Huang, Z., Borjigin, J., Melatonin formation in mammals: in vivo perspectives. Rev. Endocr. Metab. Disord. 10 (2009), 237–243.
22. Chen, Z., Xu, Y.Y., Wu, R., Han, Y.X., Yu, Y., Ge, J.F., Chen, F.H., Impaired learning and memory in rats induced by a high-fat diet: involvement with the imbalance of nesfatin-1 abundance and copine 6 expression. J. Neuroendocrinol., 29, 2017.
23. Cordner, Z.A., Tamashiro, K.L., Effects of high-fat diet exposure on learning & memory. Physiol. Behav. 152 (2015), 363–371.
24. Diamond, D.M., Park, C.R., Heman, K.L., Rose, G.M., Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9 (1999), 542–552.
25. Ding, Y., Zhang, Z., Dai, X., Jiang, Y., Bao, L., Li, Y., Li, Y., Grape seed proanthocyanidins ameliorate pancreatic beta-cell dysfunction and death in low-dose streptozotocin-and high-carbohydrate/high-fat diet-induced diabetic rats partially by regulating endoplasmic reticulum stress. Nutr. Metab., 10, 2013, 1.
26. Dziegiel, P., Podhorska-Okolow, M., Zabel, M., Melatonin: adjuvant therapy of malignant tumors. Med. Sci. Monit. 14 (2008), RA64–RA70.
27. Emet, M., Ozcan, H., Ozel, L., Yayla, M., Halici, Z., Hacimuftuoglu, A., A review of melatonin, its receptors and drugs. Eurasian J. Med 48 (2016), 135–141.
28. Eskelinen, M.H., Ngandu, T., Helkala, E.-L., Tuomilehto, J., Nissinen, A., Soininen, H., Kivipelto, M., Fat intake at midlife and cognitive impairment later in life: a population-based CAIDE study. Int. J. Geriatr. Psychiatry, 23, 2008, 741.
29. Fachinetto, R., Burger, M.E., Wagner, C., Wondracek, D.C., Brito, V.B., Nogueira, C.W., Ferreira, J., Rocha, J.B., High fat diet increases the incidence of orofacial dyskinesia and oxidative stress in specific brain regions of rats. Pharmacol. Biochem. Behav. 81 (2005), 585–592.
30. García, J.J., López‐Pingarrón, L., Almeida‐Souza, A., Tres, P., García‐Gil, D.X., Tan, R.J., Ramírez, J.M., Bernal‐Pérez, M., Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: a review. J. Pineal Res. 56 (2014), 225–237.
31. 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. J. Alzheimer's Dis. 14 (2008), 133–145.
32. Greenwood, C.E., Winocur, G., High-fat diets, insulin resistance and declining cognitive function. Neurobiol. Aging 26 (2005), 42–45.
33. He, P., Ouyang, X., Zhou, S., Yin, W., Tang, C., Laudon, M., Tian, S., A novel melatonin agonist Neu-P11 facilitates memory performance and improves cognitive impairment in a rat model of Alzheimer' disease. Horm. Behav. 64 (2013), 1–7.
34. Kalmijn, S., Foley, D., White, L., Burchfiel, C.M., Curb, J.D., Petrovitch, H., Ross, G.W., Havlik, R.J., Launer, L.J., Metabolic cardiovascular syndrome and risk of dementia in Japanese-American elderly men. The Honolulu-Asia aging study. Arterioscler. Thromb. Vasc. Biol. 20 (2000), 2255–2260.
35. Kalmijn, S., Launer, L.J., Ott, A., Witteman, J., Hofman, A., Breteler, M., Dietary fat intake and the risk of incident dementia in the Rotterdam Study. Ann. Neurol. 42 (1997), 776–782.
36. Kalmijn, S., Launer, L.J., Ott, A., Witteman, J.C., Hofman, A., Breteler, M.M., Dietary fat intake and the risk of incident dementia in the Rotterdam Study. Ann. Neurol. 42 (1997), 776–782.
37. Kanoski, S.E., Davidson, T.L., Western diet consumption and cognitive impairment: links to hippocampal dysfunction and obesity. Physiol. Behav. 103 (2011), 59–68.
38. Khabour, O.F., Alzoubi, K.H., Alomari, M.A., Alzubi, M.A., Changes in spatial memory and BDNF expression to concurrent dietary restriction and voluntary exercise. Hippocampus 20 (2010), 637–645.
39. Khabour, O.F., Alzoubi, K.H., Alomari, M.A., Alzubi, M.A., Changes in spatial memory and BDNF expression to simultaneous dietary restriction and forced exercise. Brain Res. Bull. 90 (2013), 19–24.
40. Kozirog, M., Poliwczak, A.R., Duchnowicz, P., Koter‐Michalak, M., Sikora, J., Broncel, M., Melatonin treatment improves blood pressure, lipid profile, and parameters of oxidative stress in patients with metabolic syndrome. J. Pineal Res. 50 (2011), 261–266.
41. Lauderback, C.M., Hackett, J.M., Huang, F.F., Keller, J.N., Szweda, L.I., Markesbery, W.R., Butterfield, D.A., The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Abeta1–42. J. Neurochem. 78 (2001), 413–416.
42. Ledreux, A., Wang, X., Schultzberg, M., Granholm, A.C., Freeman, L.R., Detrimental effects of a high fat/high cholesterol diet on memory and hippocampal markers in aged rats. Behav. Brain Res. 312 (2016), 294–304.
43. Leon, J., Acuna-Castroviejo, D., Escames, G., Tan, D.X., Reiter, R.J., Melatonin mitigates mitochondrial malfunction. J. Pineal Res. 38 (2005), 1–9.
44. Lovell, M.A., Markesbery, W.R., Ratio of 8-hydroxyguanine in intact DNA to free 8-hydroxyguanine is increased in Alzheimer disease ventricular cerebrospinal fluid. Arch. Neurol. 58 (2001), 392–396.
45. Maesako, M., Uemura, K., Kubota, M., Kuzuya, A., Sasaki, K., Hayashida, N., Asada-Utsugi, M., Watanabe, K., Uemura, M., Kihara, T., Exercise is more effective than diet control in preventing high fat diet-induced β-amyloid deposition and memory deficit in amyloid precursor protein transgenic mice. J. Biol. Chem. 287 (2017), 201223024–201223033.
46. Markesbery, W.R., Oxidative stress hypothesis in Alzheimer's disease. Free Radic. Biol. Med. 23 (1997), 134–147.
47. Markesbery, W.R., Lovell, M.A., Four-hydroxynonenal a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol. Aging 19 (1998), 33–36.
48. Matsuzawa-Nagata, N., Takamura, T., Ando, H., Nakamura, S., Kurita, S., Misu, H., Ota, T., Yokoyama, M., Honda, M., Miyamoto, K.-i., Increased oxidative stress precedes the onset of high-fat diet—induced insulin resistance and obesity. Metabolism 57 (2008), 1071–1077.
49. Mattson, F.H., Grundy, S.M., Comparison of effects of dietary saturated, monounsaturated, and polyunsaturated fatty acids on plasma lipids and lipoproteins in man. J. Lipid Res. 26 (1985), 194–202.
50. Mayyas, F., Alzoubi, K.H., Al-Taleb, Z., An evaluation of the effect of pentoxifylline on blood pressure and myocardial oxidative status following intake of western diet. Clin. Exp. Hypertens. 37 (2015), 666–673.
51. Mayyas, F., Alzoubi, K.H., Al-Taleb, Z., An evaluation of the effect of pentoxifylline on blood pressure and myocardial oxidative status following intake of western diet. Clin. Exp. Hypertens. 37 (2015), 666–673.
52. Mayyas, F., Alzoubi, K.H., Al-Taleb, Z., Impact of high fat/high salt diet on myocardial oxidative stress. Clin. Exp. Hypertens. 39 (2017), 126–132.
53. McNay, E.C., Ong, C.T., McCrimmon, R.J., Cresswell, J., Bogan, J.S., Sherwin, R.S., Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol. Learn. Mem. 93 (2010), 546–553.
54. Mehta, K.D., Mehta, A.K., Halder, S., Khanna, N., Tripathi, A.K., Sharma, K.K., Protective effect of melatonin on propoxur-induced impairment of memory and oxidative stress in rats. Environ. Toxicol. 29 (2014), 705–713.
55. Mhaidat, N.M., Alzoubi, K.H., Khabour, O.F., Tashtoush, N.H., Banihani, S.A., Abdul-razzak, K.K., Exploring the effect of vitamin C on sleep deprivation induced memory impairment. Brain Res. Bull. 113 (2015), 41–47.
56. Molteni, R., Barnard, R., Ying, Z., Roberts, C., Gomez-Pinilla, F., A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112 (2002), 803–814.
57. Nicolle, M.M., Gonzalez, J., Sugaya, K., Baskerville, K.A., Bryan, D., Lund, K., Gallagher, M., McKinney, M., Signatures of hippocampal oxidative stress in aged spatial learning-impaired rodents. Neuroscience 107 (2001), 415–431.
58. Nuseir, K.Q., Alzoubi, K.H., Alabwaini, J., Khabour, O.F., Kassab, M.I., Sucrose-induced analgesia during early life modulates adulthood learning and memory formation. Physiol. Behav. 145 (2015), 84–90.
59. Nuseir, K.Q., Alzoubi, K.H., Alhusban, A., Bawaane, A., Al-Azzani, M., Khabour, O.F., Sucrose and naltrexone prevent increased pain sensitivity and impaired long-term memory induced by repetitive neonatal noxious stimulation: role of BDNF and beta-endorphin. Physiol. Behav. 179 (2017), 213–219.
60. Okatani, Y., Wakatsuki, A., Kaneda, C., Melatonin increases activities of glutathione peroxidase and superoxide dismutase in fetal rat brain. J. Pineal Res. 28 (2000), 89–96.
61. Ozdemir, D., Tugyan, K., Uysal, N., Sonmez, U., Sonmez, A., Acikgoz, O., Ozdemir, N., Duman, M., Ozkan, H., Protective effect of melatonin against head trauma-induced hippocampal damage and spatial memory deficits in immature rats. Neurosci. Lett. 385 (2005), 234–239.
62. Ozdemir, D., Tugyan, K., Uysal, N., Sonmez, U., Sonmez, A., Acikgoz, O., Ozdemir, N., Duman, M., Ozkan, H., Protective effect of melatonin against head trauma-induced hippocampal damage and spatial memory deficits in immature rats. Neurosci. Lett. 385 (2005), 234–239.
63. Pablos, M.I., Agapito, M.T., Gutierrez, R., Recio, J.M., Reiter, R.J., Barlow‐Walden, L., Acuña‐Castroviejo, D., Menendez‐Pelaez, A., Melatonin stimulates the activity of the detoxifying enzyme glutathione peroxidase in several tissues of chicks. J. Pineal Res. 19 (1995), 111–115.
64. Panchal, S.K., Poudyal, H., Iyer, A., Nazer, R., Alam, A., Diwan, V., Kauter, K., Sernia, C., Campbell, F., Ward, L., High-carbohydrate high-fat diet-nduced metabolic syndrome and cardiovascular remodeling in rats. J. Cardiovasc. Pharmacol. 57 (2011), 51–64.
65. Park, H.R., Park, M., Choi, J., Park, K.-Y., Chung, H.Y., Lee, J., A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci. Lett. 482 (2010), 235–239.
66. Park, H.R., Park, M., Choi, J., Park, K.Y., Chung, H.Y., Lee, J., A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci. Lett. 482 (2010), 235–239.
67. Pintana, H., Apaijai, N., Pratchayasakul, W., Chattipakorn, N., Chattipakorn, S.C., Effects of metformin on learning and memory behaviors and brain mitochondrial functions in high fat diet induced insulin resistant rats. Life Sci. 91 (2012), 409–414.
68. Poeggeler, B., Saarela, S., Reiter, R.J., Tan, D.X., Chen, L.D., Manchester, L.C., Barlow-Walden, L.R., Melatonin—a highly potent endogenous radical scavenger and electron donor: new aspects of the oxidation chemistry of this indole accessed in vitro. Ann. N. Y. Acad. Sci. 738 (1994), 419–420.
69. Reiter, R.J., Tamura, H., Tan, D.X., Xu, X.-Y., Melatonin and the circadian system: contributions to successful female reproduction. Fertil. Steril. 102 (2014), 321–328.
70. Reiter, R.J.-X. Tan, D., Mayo, J.C., Sainz, R.M., Leon, J., Czarnocki, Z., Melatonin as an antioxidant: biochemical mechanisms and pathophysiological implications in humans. Acta Biochim. Pol. Eng. Ed. 50 (2003), 1129–1146.
71. Ren, W., Liu, G., Chen, S., Yin, J., Wang, J., Tan, B., Wu, G., Bazer, F.W., Peng, Y., Li, T., Reiter, R.J., Yin, Y., Melatonin signaling in T cells: functions and applications. J. Pineal Res, 62, 2017.
72. Ribeiro, M.C.P., Barbosa, N.B.d.V., de Almeida, T.M., Parcianello, L.M., Perottoni, J., de Avila, D.S., Rocha, J.B.T., High-fat diet and hydrochlorothiazide increase oxidative stress in brain of rats. Cell Biochem. Funct. 27 (2009), 473–478.
73. Rodriguez, A.B., Nogales, G., Marchena, J.M., Ortega, E., Barriga, C., Suppression of both basal and antigen-induced lipid peroxidation in ring dove heterophils by melatonin. Biochem. Pharmacol. 58 (1999), 1301–1306.
74. Rodriguez, C., Mayo, J.C., Sainz, R.M., Antolin, I., Herrera, F., Martin, V., Reiter, R.J., Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal Res. 36 (2004), 1–9.
75. Saxena, G., Bharti, S., Kamat, P.K., Sharma, S., Nath, C., Melatonin alleviates memory deficits and neuronal degeneration induced by intracerebroventricular administration of streptozotocin in rats. Pharmacol. Biochem. Behav. 94 (2010), 397–403.
76. Sharma, S., Taliyan, R., Neuroprotective role of Indirubin-3′-monoxime, a GSKβ-inhibitor in high fat diet induced cognitive impairment in mice. Biochem. Biophys. Res. Commun. 452 (2014), 1009–1015.
77. Soontornniyomkij, V., Kesby, J.P., Soontornniyomkij, B., Kim, J.J., Kisseleva, T., Achim, C.L., Semenova, S., Jeste, D.V., Age and high-fat diet effects on glutamine synthetase immunoreactivity in liver and hippocampus and recognition memory in mice. Curr. Aging Sci. 9 (2016), 301–309.
78. Tan, D.X., Manchester, L.C., Terron, M.P., Flores, L.J., Reiter, R.J., One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species?. J. Pineal Res. 42 (2007), 28–42.
79. Terron, M.P., Marchena, J.M., Shadi, F., Harvey, S., Lea, R.W., Rodriguez, A.B., Melatonin: an antioxidant at physiological concentrations. J. Pineal Res. 31 (2001), 95–96.
80. Tongjaroenbuangam, W., Ruksee, N., Mahanam, T., Govitrapong, P., Melatonin attenuates dexamethasone-induced spatial memory impairment and dexamethasone-induced reduction of synaptic protein expressions in the mouse brain. Neurochem. Int. 63 (2013), 482–491.
81. Tuzcu, M., Baydas, G., Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats. Eur. J. Pharmacol. 537 (2006), 106–110.
82. Vandal, M., White, P.J., Tremblay, C., St-Amour, I., Chevrier, G., Emond, V., Lefrancois, D., Virgili, J., Planel, E., Giguere, Y., Marette, A., Calon, F., Insulin reverses the high-fat diet-induced increase in brain abeta and improves memory in an animal model of alzheimer disease. Diabetes 63 (2014), 4291–4301.
83. Williams, W.P. 3rd, McLin, D.E. 3rd, Dressman, M.A., Neubauer, D.N., Comparative review of approved melatonin agonists for the treatment of circadian rhythm sleep-Wake disorders. Pharmacotherapy 36 (2016), 1028–1041.
84. Winiarska, K., Fraczyk, T., Malinska, D., Drozak, J., Bryla, J., Melatonin attenuates diabetes-induced oxidative stress in rabbits. J. Pineal Res. 40 (2006), 168–176.
85. Winocur, G., Greenwood, C.E., Studies of the effects of high fat diets on cognitive function in a rat model. Neurobiol. Aging 26 (2005), 46–49.
86. Xia, Z., Storm, D., Role of circadian rhythm and REM sleep for memory consolidation. Neurosci. Res. 118 (2017), 13–20.
87. Xie, W., Du, L., High-cholesterol diets impair short-term retention of memory in alloxan-induced diabetic mice, but not acquisition of memory nor retention of memory in prediabetic mice. Life Sci. 77 (2005), 481–495.
88. Yang, X., Yang, Y., Fu, Z., Li, Y., Feng, J., Luo, J., Zhang, Q., Wang, Q., Tian, Q., Melatonin ameliorates Alzheimer-like pathological changes and spatial memory retention impairment induced by calyculin A. J. Psychopharmacol. 25 (2011), 1118–1125.
89. Zhang, L., Zhang, H.-Q., Liang, X.-Y., Zhang, H.-F., Zhang, T., Liu, F.-E., Melatonin ameliorates cognitive impairment induced by sleep deprivation in rats: role of oxidative stress, BDNF and CaMKII. Behav. Brain Res. 256 (2013), 72–81.
90. Zhang, X., Dong, F., Ren, J., Driscoll, M.J., Culver, B., High dietary fat induces NADPH oxidase-associated oxidative stress and inflammation in rat cerebral cortex. Exp. Neurol. 191 (2005), 318–325.