Caffeine prevents cognitive impairment induced by chronic psychosocial stress and/or high fat-high carbohydrate diet

Behavioural Brain Research

Volumn 237, Issue 1, 2013, Pages 7-14

  Alzoubi, K H ^a   Abdul Razzak, K K ^a   Khabour, O F ^a   Al Tuweiq, G M ^a   Alzubi, M A ^a   Alkadhi, K A ^b  

^a JORDAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Jordan)

^b UNIVERSITY OF HOUSTON   (United States)

Author keywords

Caffeine; Hippocampus dependent memory; Psychosocial stress; Radial arm water maze; Western diet

Indexed keywords

CAFFEINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CHRONIC STRESS; CONTROLLED STUDY; DRUG MECHANISM; LEARNING DISORDER; LIPID DIET; LONG TERM CARE; LONG TERM MEMORY; MALE; MAZE TEST; MEMORY DISORDER; MENTAL STRESS; MENTAL TASK; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SHORT TERM MEMORY; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHT; CAFFEINE; CENTRAL NERVOUS SYSTEM STIMULANTS; COGNITION DISORDERS; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; MALE; MAZE LEARNING; MEMORY; RATS; RATS, WISTAR; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 84867063148     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.09.018     Document Type: Article

References (81)

1. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiological Reviews 2007, 87:873-904.
2. Sandi C., Pinelo-Nava M.T. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plasticity 2007, 78970.
3. Zoladz P.R., Park C.R., Halonen J.D., Salim S., Alzoubi K.H., Srivareerat M., et al. Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stress-induced amnesia. Hippocampus 2011, 22:577-589.
4. Park C.R., Campbell A.M., Diamond D.M. Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in adult rats. Biological Psychiatry 2001, 50:994-1004.
5. Gerges N.Z., Alzoubi K.H., Park C.R., Diamond D.M., Alkadhi K.A. Adverse effect of the combination of hypothyroidism and chronic psychosocial stress on hippocampus-dependent memory in rats. Behavioural Brain Research 2004, 155:77-84.
6. Aleisa A.M., Alzoubi K.H., Gerges N.Z., Alkadhi K.A. Nicotine blocks stress-induced impairment of spatial memory and long-term potentiation of the hippocampal CA1 region. International Journal of Neuropsychopharmacology 2006, 9:417-426.
7. 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. Behavioural Brain Research 2009, 204:117-123.
8. Lupien S.J., Gaudreau S., Tchiteya B.M., Maheu F., Sharma S., Nair N.P., et al. Stress-induced declarative memory impairment in healthy elderly subjects: relationship to cortisol reactivity. Journal of Clinical Endocrinology and Metabolism 1997, 82:2070-2075.
9. Srivareerat M., Tran T.T., Alzoubi K.H., Alkadhi K.A. Chronic psychosocial stress exacerbates impairment of cognition and long-term potentiation in beta-amyloid rat model of Alzheimer's disease. Biological Psychiatry 2009, 65:918-926.
10. Alkadhi K.A., Alzoubi K.H., Srivareerat M., Tran T.T. Chronic psychosocial stress exacerbates impairment of synaptic plasticity in beta-amyloid rat model of Alzheimer's disease: prevention by nicotine. Current Alzheimer Research 2011, 8:718-731.
11. Alkadhi K.A., Alzoubi K.H., Srivareerat M., Tran T.T. Elevation of BACE in an Abeta rat model of Alzheimer's disease: exacerbation by chronic stress and prevention by nicotine. International Journal of Neuropsychopharmacology 2011, 1-11.
12. Diamond D.M., Rose G.M. Stress impairs LTP and hippocampal-dependent memory. Annals of the New York Academy of Sciences 1994, 746:411-414.
13. Gerges N.Z., Stringer J.L., Alkadhi K.A. Combination of hypothyroidism and stress abolishes early LTP in the CA1 but not dentate gyrus of hippocampus of adult rats. Brain Research 2001, 922:250-260.
14. Gerges N.Z., Aleisa A.M., Schwarz L.A., Alkadhi K.A. Reduced basal CaMKII levels in hippocampal CA1 region: possible cause of stress-induced impairment of LTP in chronically stressed rats. Hippocampus 2004, 14:402-410.
15. Aleisa A.M., Alzoubi K.H., Alkadhi K.A. Chronic but not acute nicotine treatment reverses stress-induced impairment of LTP in anesthetized rats. Brain Research 2006, 1097:78-84.
16. Aleisa A.M., Alzoubi K.H., Gerges N.Z., Alkadhi K.A. Chronic psychosocial stress-induced impairment of hippocampal LTP: possible role of BDNF. Neurobiology of Disease 2006, 22:453-462.
17. Alzoubi K.H., Aleisa A.M., Alkadhi K.A. The sliding threshold of modification hypothesis: application to the effect of hypothyroidism or chronic psychosocial stress and nicotine on synaptic plasticity. Neuroscience Letters 2008, 430:203-206.
18. Hirata R., Togashi H., Matsumoto M., Yamaguchi T., Izumi T., Yoshioka M. Characterization of stress-induced suppression of long-term potentiation in the hippocampal CA1 field of freely moving rats. Brain Research 2008, 1226:27-32.
19. Foy M.R., Stanton M.E., Levine S., Thompson R.F. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behavioral and Neural Biology 1987, 48:138-149.
20. 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. Annals of Neurology 1997, 42:776-782.
21. Thirumangalakudi L., Prakasam A., Zhang R., Bimonte-Nelson H., Sambamurti K., Kindy M.S., et al. High cholesterol-induced neuroinflammation and amyloid precursor protein processing correlate with loss of working memory in mice. Journal of Neurochemistry 2008, 106:475-485.
22. Li D., Du C.Y., Tang X.J., Jin Y.X., Lei T., Yao Y., et al. Changes of heart rate variability and impairment of learning and memory induced by cerebral ischemia/reperfusion in rats. Sheng Li Xue Bao 2007, 59:35-41.
23. Wu A., Molteni R., Ying Z., Gomez-Pinilla F. A saturated-fat diet aggravates the outcome of traumatic brain injury on hippocampal plasticity and cognitive function by reducing brain-derived neurotrophic factor. Neuroscience 2003, 119:365-375.
24. Goldbart A.D., Row B.W., Kheirandish-Gozal L., Cheng Y., Brittian K.R., Gozal D. High fat/refined carbohydrate diet enhances the susceptibility to spatial learning deficits in rats exposed to intermittent hypoxia. Brain Research 2006, 1090:190-196.
25. Stranahan A.M., Norman E.D., Lee K., Cutler R.G., Telljohann R.S., Egan J.M., et al. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 2008, 18:1085-1088.
26. Molteni R., Barnard R.J., Ying Z., Roberts C.K., Gomez-Pinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 2002, 112:803-814.
27. Wu A., Ying Z., Gomez-Pinilla F. The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. European Journal of Neuroscience 2004, 19:1699-1707.
28. Floel A., Witte A.V., Lohmann H., Wersching H., Ringelstein E.B., Berger K., et al. Lifestyle and memory in the elderly. Neuroepidemiology 2008, 31:39-47.
29. Nicholson A.N., Stone B.M. Heterocyclic amphetamine derivatives and caffeine on sleep in man. British Journal of Clinical Pharmacology 1980, 9:195-203.
30. Gevaerd M.S., Takahashi R.N., Silveira R., Da Cunha C. Caffeine reverses the memory disruption induced by intra-nigral MPTP-injection in rats. Brain Research Bulletin 2001, 55:101-106.
31. Dall'Igna O.P., Fett P., Gomes M.W., Souza D.O., Cunha R.A., Lara D.R. Caffeine and adenosine A(2a) receptor antagonists prevent beta-amyloid (25-35)-induced cognitive deficits in mice. Experimental Neurology 2007, 203:241-245.
32. Ascherio A., Zhang S.M., Hernan M.A., Kawachi I., Colditz G.A., Speizer F.E., et al. Prospective study of caffeine consumption and risk of Parkinson's disease in men and women. Annals of Neurology 2001, 50:56-63.
33. Maia L., de Mendonca A. Does caffeine intake protect from Alzheimer's disease?. European Journal of Neurology 2002, 9:377-382.
34. Alhaider I.A., Aleisa A.M., Tran T.T., Alzoubi K.H., Alkadhi K.A. Chronic caffeine treatment prevents sleep deprivation-induced impairment of cognitive function and synaptic plasticity. Sleep 2010, 33:437-444.
35. Alhaider I.A., Aleisa A.M., Tran T.T., Alkadhi K.A. Sleep deprivation prevents stimulation-induced increases of levels of P-CREB and BDNF: protection by caffeine. Molecular and Cellular Neurosciences 2011, 46:742-751.
36. Nehlig A., Daval J.L., Debry G. Caffeine and the central nervous system: mechanisms of action, biochemical, metabolic and psychostimulant effects. Brain Research. Brain Research Reviews 1992, 17:139-170.
37. Takahashi R.N., Pamplona F.A., Prediger R.D. Adenosine receptor antagonists for cognitive dysfunction: a review of animal studies. Frontiers in Bioscience 2008, 13:2614-2632.
38. Pires V.A., Pamplona F.A., Pandolfo P., Fernandes D., Prediger R.D., Takahashi R.N. Adenosine receptor antagonists improve short-term object-recognition ability of spontaneously hypertensive rats: a rodent model of attention-deficit hyperactivity disorder. Behavioural Pharmacology 2009, 20:134-145.
39. Subcommittee on Laboratory Animal Nutrition, Committee on Animal Nutrition, Board on Agriculture, National Research Council General Considerations for Feeding and Diet Formulation. Nutrient requirements of laboratory animals 1995, National Academy Press, Washington, D.C., pp. 1-9. 4th ed.
40. Alkadhi K.A., Alzoubi K.H., Aleisa A.M., Tanner F.L., Nimer A.S. Psychosocial stress-induced hypertension results from in vivo expression of long-term potentiation in rat sympathetic ganglia. Neurobiology of Disease 2005, 20:849-857.
41. Rigoulot M.A., Leroy C., Koning E., Ferrandon A., Nehlig A. Prolonged low-dose caffeine exposure protects against hippocampal damage but not against the occurrence of epilepsy in the lithium-pilocarpine model in the rat. Epilepsia 2003, 44:529-535.
42. Alhaider I.A., Aleisa A.M., Tran T.T., Alkadhi K.A. Caffeine prevents sleep loss-induced deficits in long-term potentiation and related signaling molecules in the dentate gyrus. European Journal of Neuroscience 2010, 31:1368-1376.
43. Wolff M., Benhassine N., Costet P., Hen R., Segu L., Buhot M.C. Delay-dependent working memory impairment in young-adult and aged 5-HT1BKO mice as assessed in a radial-arm water maze. Learning and Memory 2003, 10(5):401-409.
44. Shukitt-Hale B., McEwen J.J., Szprengiel A., Joseph J.A. Effect of age on the radial arm water maze-a test of spatial learning and memory. Neurobiology of Aging 2004, 25:223-229.
45. Srivareerat M., Tran T.T., Salim S., Aleisa A.M., Alkadhi K.A. Chronic nicotine restores normal Abeta levels and prevents short-term memory and E-LTP impairment in Abeta rat model of Alzheimer's disease. Neurobiology of Aging 2011, 32:834-844.
46. Diamond D.M., Fleshner M., Ingersoll N., Rose G.M. Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behavioral Neuroscience 1996, 110:661-672.
47. 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 1999, 9:542-552.
48. Zoladz P.R., Conrad C.D., Fleshner M., Diamond D.M. Acute episodes of predator exposure in conjunction with chronic social instability as an animal model of post-traumatic stress disorder. Stress 2008, 11:259-281.
49. Alzoubi K.H., Aleisa A.M., Gerges N.Z., Alkadhi K.A. Nicotine reverses adult-onset hypothyroidism-induced impairment of learning and memory: behavioral and electrophysiological studies. Journal of Neuroscience Research 2006, 84:944-953.
50. Alzoubi K.H., Gerges N.Z., Aleisa A.M., Alkadhi K.A. Levothyroxin restores hypothyroidism-induced impairment of hippocampus-dependent learning and memory: behavioral, electrophysiological, and molecular studies. Hippocampus 2009, 19:66-78.
51. 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, 14:133-145.
52. 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. Behavioural Brain Research 2012, 226:205-210.
53. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
54. Diamond D.M., Campbell A.M., Park C.R., Woodson J.C., Conrad C.D., Bachstetter A.D., et al. Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus 2006, 16:571-576.
55. Block G., Rosenberger W.F., Patterson B.H. Calories, fat and cholesterol: intake patterns in the US population by race, sex and age. American Journal of Public Health 1988, 78:1150-1155.
56. Velloso L.A. The brain is the conductor: diet-induced inflammation overlapping physiological control of body mass and metabolism. Arquivos Brasileiros de Endocrinologia e Metabologia 2009, 53:151-158.
57. White C.L., Pistell P.J., Purpera M.N., Gupta S., Fernandez-Kim S.O., Hise T.L., et al. Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet. Neurobiology of Disease 2009, 35:3-13.
58. Bornhoeft J., Castaneda D., Nemoseck T., Wang P., Henning S.M., Hong M.Y. The protective effects of green tea polyphenols: lipid profile, inflammation, and antioxidant capacity in rats fed an atherogenic diet and dextran sodium sulfate. Journal of Medicinal Food 2012, 15:726-732.
59. Roussinov K.S., Yonkov D.I. Cholinergic mechanisms in the learning and memory facilitating effect of caffeine. Acta Physiologica et Pharmacologica Bulgarica 1976, 2:61-68.
60. Cestari V., Castellano C. Caffeine and cocaine interaction on memory consolidation in mice. Archives Internationales de Pharmacodynamie et de Therapie 1996, 331:94-104.
61. Riedel W.J., Jolles J. Cognition enhancers in age-related cognitive decline. Drugs and Aging 1996, 8:245-274.
62. Howell L.L., Coffin V.L., Spealman R.D. Behavioral and physiological effects of xanthines in nonhuman primates. Psychopharmacology 1997, 129:1-14.
63. Loke W.H. Effects of caffeine on mood and memory. Physiology and Behavior 1988, 44:367-372.
64. Furusawa K. Drug effects on cognitive function in mice determined by the non-matching to sample task using a 4-arm maze. Japanese Journal of Pharmacology 1991, 56:483-493.
65. Hudzik T.J., Wenger G.R. Effects of drugs of abuse and cholinergic agents on delayed matching-to-sample responding in the squirrel monkey. Journal of Pharmacology and Experimental Therapeutics 1993, 265:120-127.
66. Fisher S., Guillet R. Neonatal caffeine alters passive avoidance retention in rats in an age- and gender-related manner. Brain Research. Developmental Brain Research 1997, 98:145-149.
67. Sutherland G.R., Peeling J., Lesiuk H.J., Brownstone R.M., Rydzy M., Saunders J.K., et al. The effects of caffeine on ischemic neuronal injury as determined by magnetic resonance imaging and histopathology. Neuroscience 1991, 42:171-182.
68. Prediger R.D., Pamplona F.A., Fernandes D., Takahashi R.N. Caffeine improves spatial learning deficits in an animal model of attention deficit hyperactivity disorder (ADHD) - the spontaneously hypertensive rat (SHR). International Journal of Neuropsychopharmacology 2005, 8:583-594.
69. Riedel W., Hogervorst E., Leboux R., Verhey F., van Praag H., Jolles J. Caffeine attenuates scopolamine-induced memory impairment in humans. Psychopharmacology 1995, 122:158-168.
70. Norris C.M., Halpain S., Foster T.C. Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging. Journal of Neurophysiology 1998, 80:1567-1570.
71. Alzoubi K.H., Gerges N.Z., Alkadhi K.A. Levothyroxin restores hypothyroidism-induced impairment of LTP of hippocampal CA1: electrophysiological and molecular studies. Experimental Neurology 2005, 195:330-341.
72. Gerges N.Z., Alzoubi K.H., Alkadhi K.A. Role of phosphorylated CaMKII and calcineurin in the differential effect of hypothyroidism on LTP of CA1 and dentate gyrus. Hippocampus 2005, 15:480-490.
73. Sawin C.T., Chopra D., Azizi F., Mannix J.E., Bacharach P. The aging thyroid, Increased prevalence of elevated serum thyrotropin levels in the elderly. JAMA: the journal of the American Medical Association 1979, 242:247-250.
74. Ritchie K., Carriere I., de Mendonca A., Portet F., Dartigues J.F., Rouaud O., et al. The neuroprotective effects of caffeine: a prospective population study (the Three City Study). Neurology 2007, 69:536-545.
75. Smellie F.W., Davis C.W., Daly J.W., Wells J.N. Alkylxanthines: inhibition of adenosine-elicited accumulation of cyclic AMP in brain slices and of brain phosphodiesterase activity. Life Sciences 1979, 24:2475-2482.
76. McPherson P.S., Kim Y.K., Valdivia H., Knudson C.M., Takekura H., Franzini-Armstrong C., et al. The brain ryanodine receptor: a caffeine-sensitive calcium release channel. Neuron 1991, 7:17-25.
77. Fredholm B.B. Astra Award Lecture. Adenosine, adenosine receptors and the actions of caffeine. Pharmacology & Toxicology 1995, 76:93-101.
78. de Mendonca A., Ribeiro J.A. Endogenous adenosine modulates long-term potentiation in the hippocampus. Neuroscience 1994, 62:385-390.
79. Dunwiddie T.V., Masino S.A. The role and regulation of adenosine in the central nervous system. Annual Review of Neuroscience 2001, 24:31-55.
80. Costa M.S., Botton P.H., Mioranzza S., Ardais A.P., Moreira J.D., Souza D.O., et al. Caffeine improves adult mice performance in the object recognition task and increases BDNF and TrkB independent on phospho-CREB immunocontent in the hippocampus. Neurochemistry International 2008, 53:89-94.
81. Molteni R., Wu A., Vaynman S., Ying Z., Barnard R.J., Gomez-Pinilla F. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neuroscience 2004, 123:429-440.