The combined effect of sleep deprivation and western diet on spatial learning and memory: Role of BDNF and oxidative stress

Journal of Molecular Neuroscience

Volumn 50, Issue 1, 2013, Pages 124-133

  Alzoubi, Karem H ^a   Khabour, Omar F ^a   Salah, Heba A ^a   Abu Rashid, Baraa E ^a  

^a JORDAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Jordan)

Author keywords

BDNF; Hippocampus; Learning; Maze; Memory; Oxidative stress; Sleep deprivation; Western diet

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CATALASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; COGNITIVE DEFECT; CONTROLLED STUDY; DIET; ENZYME ACTIVITY; HIPPOCAMPUS; LONG TERM MEMORY; MALE; MEMORY DISORDER; MENTAL PERFORMANCE; NONHUMAN; OXIDATIVE STRESS; RAT; SHORT TERM MEMORY; SLEEP DEPRIVATION; SPATIAL LEARNING; WEIGHT GAIN; WESTERN DIET;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DIET; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MEMORY DISORDERS; OXIDATIVE STRESS; RATS; RATS, WISTAR; SLEEP DEPRIVATION;

RATTUS;

EID: 84876142200     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-012-9881-7     Document Type: Article

References (76)

1. Acheson A, Conover JC, Fandl JP, DeChiara TM, Russell M, Thadani A, Squinto SP, Yancopoulos GD, Lindsay RM (1995) A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374:450-453
2. Aleisa AM, Alzoubi KH, Alkadhi KA (2011a) Post-learning REM sleep deprivation impairs long-term memory: reversal by acute nicotine treatment. Neurosci Lett 499:28-31
3. Aleisa AM, Helal G, Alhaider IA, Alzoubi KH, Srivareerat M, Tran TT, Al-Rejaie SS, Alkadhi KA (2011b) Acute nicotine treatment prevents REM sleep deprivation-induced learning and memory impairment in rat. Hippocampus 21:899-909
4. Alhaider IA, Aleisa AM, Tran TT, Alkadhi KA (2010a) Caffeine prevents sleep loss-induced deficits in long-term potentiation and related signaling molecules in the dentate gyrus. Eur J Neurosci 31:1368-1376
5. Alhaider IA, Aleisa AM, Tran TT, Alzoubi KH, Alkadhi KA (2010b) Chronic caffeine treatment prevents sleep deprivation-induced impairment of cognitive function and synaptic plasticity. Sleep 33:437-444
6. Alhaider IA, Aleisa AM, Tran TT, Alkadhi KA (2011) Sleep deprivation prevents stimulation-induced increases of levels of P-CREB and BDNF: protection by caffeine. Mol Cell Neurosci 46:742-751
7. Alzoubi KH, Gerges NZ, Alkadhi KA (2005) Levothyroxin restores hypothyroidism-induced impairment of LTP of hippocampal CA1: electrophysiological and molecular studies. Exp Neurol 195:330-341 (Pubitemid 41297786)
8. Alzoubi KH, Aleisa AM, Gerges NZ, Alkadhi KA (2006) Nicotine reverses adult-onset hypothyroidism-induced impairment of learning and memory: behavioral and electrophysiological studies. J Neurosci Res 84:944-953 (Pubitemid 44521038)
9. Alzoubi KH, Abdul-Razzak KK, Khabour OF, Al-Tuweiq GM, Alzubi MA, Alkadhi KA (2009) Adverse effect of combination of chronic psychosocial stress and high fat diet on hippocampus-dependent memory in rats. Behav Brain Res 204:117-123
10. Alzoubi KH, Khabour OF, Rashid BA, Damaj IM, Salah HA (2012) The neuroprotective effect of vitamin E on chronic sleep deprivation-induced memory impairment: the role of oxidative stress. Behav Brain Res 226:205-210
11. Ansari MA, Roberts KN, Scheff SW (2008) Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury. Free Radic Biol Med 45:443-452
12. Baran SE, Campbell AM, Kleen JK, Foltz CH, Wright RL, Diamond DM, Conrad CD (2005) Combination of high fat diet and chronic stress retracts hippocampal dendrites. Neuroreport 16:39-43 (Pubitemid 40194557)
13. Benzi G, Marzatico F, Pastoris O, Villa RF (1990) Influence of oxidative stress on the age-linked alterations of the cerebral glutathione system. J Neurosci Res 26:120-128 (Pubitemid 20175062)
14. Chamorro RA, Duran SA, Reyes SC, Ponce R, Algarin CR, Peirano PD (2011) Sleep deprivation as a risk factor for obesity. Rev Med Chil 139:932-940
15. Chelikani PFI, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61:192-208 (Pubitemid 38183572)
16. D'Almeida V, Lobo LL, Hipolide DC, de Oliveira AC, Nobrega JN, Tufik S (1998) Sleep deprivation induces brain region-specific decreases in glutathione levels. Neuroreport 9:2853-2856 (Pubitemid 28435176)
17. Diamond DM, Park CR, Heman KL, Rose GM (1999) Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9:542-552 (Pubitemid 29509524)
18. Fachinetto R, Burger ME, Wagner C, Wondracek DC, Brito VB, Nogueira CW, Ferreira J, Rocha JB (2005) High fat diet increases the incidence of orofacial dyskinesia and oxidative stress in specific brain regions of rats. Pharmacol Biochem Behav 81:585-592 (Pubitemid 40966806)
19. Falkenberg T, Mohammed AK, Henriksson B, Persson H, Winblad B, Lindefors N (1992) Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci Lett 138:153-156
20. Freedman DS (2011) Obesity - United States, 1988-2008. MMWR Surveill Summ 60(Suppl):73-77
21. Fukui K, Omoi NO, Hayasaka T, Shinnkai T, Suzuki S, Abe K, Urano S (2002) Cognitive impairment of rats caused by oxidative stress and aging, and its prevention by vitamin E. Ann N Y Acad Sci 959:275-284 (Pubitemid 34457568)
22. Garcia-Fuentes E, Murri M, Garrido-Sanchez L, Garcia-Serrano S, Garcia-Almeida JM, Moreno-Santos I, Tinahones FJ, Macias-Gonzalez M (2010) PPARgamma expression after a high-fat meal is associated with plasma superoxide dismutase activity in morbidly obese persons. Obesity (Silver Spring) 18:952-958
23. Gerges NZ, Alzoubi KH, Park CR, Diamond DM, Alkadhi KA (2004) Adverse effect of the combination of hypothyroidism and chronic psychosocial stress on hippocampus-dependent memory in rats. Behav Brain Res 155:77-84 (Pubitemid 39119968)
24. Gerges NZ, Alzoubi KH, Alkadhi KA (2005) Role of phosphorylated CaMKII and calcineurin in the differential effect of hypothyroidism on LTP of CA1 and dentate gyrus. Hippocampus 15:480-490 (Pubitemid 40916295)
25. Grahnstedt S, Ursin R (1985) Platform sleep deprivation affects deep slow wave sleep in addition to REM sleep. Behav Brain Res 18:233-239 (Pubitemid 16176243)
26. Greene R, Siegel J (2004) Sleep: a functional enigma. Neuromol Med 5:59-68 (Pubitemid 38391957)
27. Greenwood CE, Winocur G (1990) Learning and memory impairment in rats fed a high saturated fat diet. Behav Neural Biol 53:74-87 (Pubitemid 20111364)
28. Gupta YK, Gupta M, Kohli K (2003) Neuroprotective role of melatonin in oxidative stress vulnerable brain. Indian J Physiol Pharmacol 47:373-386 (Pubitemid 37151175)
29. Guzman-Marin R, Ying Z, Suntsova N, Methippara M, Bashir T, Szymusiak R, Gomez-Pinilla F, McGinty D (2006) Suppression of hippocampal plasticity-related gene expression by sleep deprivation in rats. J Physiol 575:807-819 (Pubitemid 44323744)
30. Guyton AC, Hall JE (2006) States of brain activity - sleep, brain waves, epilepsy, phycosis sleep: Medical physiology, 11th edn. Elsevier, Philadelphia, pp 739-741
31. Harikesh Kalonia AK (2006) Protective effect of BR-16A (poly herbal preparation) on the behavioural and biochemical alterations in sleep disturbed mice. Annals of Neurosciences 13
32. Harrison Y, Horne JA (2000) Sleep loss and temporal memory. Q J Exp Psychol A 53:271-279
33. Heldt SA, Stanek L, Chhatwal JP, Ressler KJ (2007) Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12:656-670 (Pubitemid 46998249)
34. Jhoo JH, Kim HC, Nabeshima T, Yamada K, Shin EJ, Jhoo WK, Kim W, Kang KS, Jo SA, Woo JI (2004) Beta-amyloid (1-42)-induced learning and memory deficits in mice: involvement of oxidative burdens in the hippocampus and cerebral cortex. Behav Brain Res 155:185-196 (Pubitemid 39208900)
35. Jiang F, Shen XM, Li SH, Cui ML, Zhang Y, Wang C, Yu XG, Yan CH (2009) Effects of chronic partial sleep deprivation on growth and learning/memory in young rats. Zhongguo Dang Dai Er Ke Za Zhi 11:128-132
36. Kanoski SE, Davidson TL (2010) Different patterns of memory impairments accompany short- and longer-term maintenance on a high-energy diet. J Exp Psychol Anim Behav Process 36:313-319
37. Kanoski SE, Davidson TL (2011) Western diet consumption and cognitive impairment: links to hippocampal dysfunction and obesity. Physiol Behav 103:59-68
38. Khabour OF, Alzoubi KH, Alomari MA, Alzubi MA (2012) Changes in spatial memory and BDNF expression to simultaneous dietary restriction and forced exercise. Brain Res Bull. doi: 10.1016/j.brainresbull.2012.08.005
39. Khabour OF, Alzoubi KH, Alomari MA, Alzubi MA (2010) Changes in spatial memory and BDNF expression to concurrent dietary restriction and voluntary exercise. Hippocampus 20:637-645
40. Kripke DF, Garfinkel L, Wingard DL, Klauber MR, Marler MR (2002) Mortality associated with sleep duration and insomnia. Arch Gen Psychiatry 59:131-136 (Pubitemid 34137380)
41. Leproult R, Van Cauter E (2010) Role of sleep and sleep loss in hormonal release and metabolism. Endocr Dev 17:11-21
42. Li S, Tian Y, Ding Y, Jin X, Yan C, Shen X (2009) The effects of rapid eye movement sleep deprivation and recovery on spatial reference memory of young rats. Learn Behav 37:246-253
43. Linnarsson S, Bjorklund A, Ernfors P (1997) Learning deficit in BDNF mutant mice. Eur J Neurosci 9:2581-2587 (Pubitemid 28082947)
44. Lopez J, Roffwarg HP, Dreher A, Bissette G, Karolewicz B, Shaffery JP (2008) Rapid eye movement sleep deprivation decreases long-term potentiation stability and affects some glutamatergic signaling proteins during hippocampal development. Neuroscience 153:44-53
45. Mattson MP, Duan W, Guo Z (2003) Meal size and frequency affect neuronal plasticity and vulnerability to disease: cellular and molecular mechanisms. J Neurochem 84:417-431 (Pubitemid 36182240)
46. McCarley RW (2011) Neurobiology of REM sleep. Handb Clin Neurol 98:151-171
47. McDermott CM, Hardy MN, Bazan NG, Magee JC (2006) Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus. J Physiol 570:553-565
48. Mednick SC, Nakayama K, Cantero JL, Atienza M, Levin AA, Pathak N, Stickgold R (2002) The restorative effect of naps on perceptual deterioration. Nat Neurosci 5:677-681 (Pubitemid 34742984)
49. Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711-760 (Pubitemid 13030692)
50. Mizuno M, Yamada K, Olariu A, Nawa H, Nabeshima T (2000) Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 20:7116-7121
51. Molteni R, Barnard RJ, Ying Z, Roberts CK, Gomez-Pinilla F (2002) A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112:803-814 (Pubitemid 34667045)
52. Montplaisir J, Petit D, Gauthier S, Gaudreau H, Decary A (1998) Sleep disturbances and EEG slowing in Alzheimer's disease. Sleep Res Online 1:147-151
53. Ohlmann KK, O'Sullivan MI (2009) The costs of short sleep. AAOHN J 57:381-385, quiz 386-387
54. Park CR, Campbell AM, Diamond DM (2001) Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in adult rats. Biol Psychiatry 50:994-1004 (Pubitemid 34066492)
55. Park HR, Park M, Choi J, Park KY, Chung HY, Lee J (2010) A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci Lett 482:235-239
56. Pistell PJ, Morrison CD, Gupta S, Knight AG, Keller JN, Ingram DK, Bruce-Keller AJ (2010) Cognitive impairment following high fat diet consumption is associated with brain inflammation. J Neuroimmunol 219:25-32
57. Ramanathan L, Gulyani S, Nienhuis R, Siegel JM (2002) Sleep deprivation decreases superoxide dismutase activity in rat hippocampus and brainstem. Neuroreport 13:1387-1390
58. Reimund E (1994) The free radical flux theory of sleep. Med Hypotheses 43:231-233 (Pubitemid 24324120)
59. Sei H, Saitoh D, Yamamoto K, Morita K, Morita Y (2000) Differential effect of short-term REM sleep deprivation on NGF and BDNF protein levels in the rat brain. Brain Res 877:387-390
60. Silber MH, Ancoli-Israel S, Bonnet MH, Chokroverty S, Grigg-Damberger MM, Hirshkowitz M, Kapen S, Keenan SA, Kryger MH, Penzel T, Pressman MR, Iber C (2007) The visual scoring of sleep in adults. J Clin Sleep Med 3:121-131 (Pubitemid 46649103)
61. Silva RH, Abilio VC, Takatsu AL, Kameda SR, Grassl C, Chehin AB, Medrano WA, Calzavara MB, Registro S, Andersen ML, Machado RB, Carvalho RC, Ribeiro Rde A, Tufik S, Frussa-Filho R (2004) Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice. Neuropharmacology 46:895-903 (Pubitemid 38368922)
62. Smith C, Kelly G (1988) Paradoxical sleep deprivation applied two days after end of training retards learning. Physiol Behav 43:213-216
63. Smith C, Rose GM (1997) Posttraining paradoxical sleep in rats is increased after spatial learning in the Morris water maze. Behav Neurosci 111:1197-1204 (Pubitemid 28010897)
64. Spiegel K, Tasali E, Penev P, Van Cauter E (2004) Brief communication: sleep curtailment in healthy young men is associated with decreased leptin levels, elevated ghrelin levels, and increased hunger and appetite. Ann Intern Med 141:846-850 (Pubitemid 39601178)
65. Srivareerat M, Tran TT, Alzoubi KH, Alkadhi KA (2009) Chronic psychosocial stress exacerbates impairment of cognition and long-term potentiation in beta-amyloid rat model of Alzheimer's disease. Biol Psychiatry 65:918-926
66. Studzinski CM, Li F, Bruce-Keller AJ, Fernandez-Kim SO, Zhang L, Weidner AM, Markesbery WR, Murphy MP, Keller JN (2009) Effects of short-term Western diet on cerebral oxidative stress and diabetes related factors in APP × PS1 knock-in mice. J Neurochem 108:860-866
67. Taheri S, Lin L, Austin D, Young T, Mignot E (2004) Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index. PLoS Med 1:e62 (Pubitemid 40418884)
68. Vorona RD, Winn MP, Babineau TW, Eng BP, Feldman HR, Ware JC (2005) Overweight and obese patients in a primary care population report less sleep than patients with a normal body mass index. Arch Intern Med 165:25-30 (Pubitemid 40096078)
69. White CL, Pistell PJ, Purpera MN, Gupta S, Fernandez-Kim SO, Hise TL, Keller JN, Ingram DK, Morrison CD, Bruce-Keller AJ (2009) Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet. Neurobiol Dis 35:3-13
70. Xie W, Du L (2005) 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 77:481-495 (Pubitemid 40719882)
71. Yamada K, Nabeshima T (2003) Brain-derived neurotrophic factor/TrkB signaling in memory processes. J Pharmacol Sci 91:267-270 (Pubitemid 36581946)
72. Yu H, Bi Y, Ma W, He L, Yuan L, Feng J, Xiao R (2010) Long-term effects of high lipid and high energy diet on serum lipid, brain fatty acid composition, and memory and learning ability in mice. Int J Dev Neurosci 28:271-276
73. Zagaar M, Alhaider I, Dao A, Levine A, Alkarawi A, Alzubaidy M, Alkadhi K (2012) The beneficial effects of regular exercise on cognition in REM sleep deprivation: behavioral, electrophysiological and molecular evidence. Neurobiol Dis 45:1153-1162
74. Zeeni N, Chaumontet C, Moyse E, Fromentin G, Tardivel C, Tome D, Jean A, Darcel N (2009) A positive change in energy balance modulates TrkB expression in the hypothalamus and nodose ganglia of rats. Brain Res 1289:49-55
75. Zelko IN, Mariani TJ, Folz RJ (2002) Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 33:337-349 (Pubitemid 34790245)
76. Zhang X, Dong F, Ren J, Driscoll MJ, Culver B (2005) High dietary fat induces NADPH oxidase-associated oxidative stress and inflammation in rat cerebral cortex. Exp Neurol 191:318-325 (Pubitemid 40092875)