Influence of chronic moderate sleep restriction and exercise training on anxiety, spatial memory, and associated neurobiological measures in mice

Behavioural Brain Research

Volumn 250, Issue , 2013, Pages 74-80

  Zielinski, Mark R ^a   Davis, J Mark ^b   Fadel, James R ^c   Youngstedt, Shawn D ^b,d  

^a VA BOSTON HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d WJB Dorn VA Medical Center   (United States)

Author keywords

Anxiety; BDNF; Exercise training; Memory; Moderate; Sleep restriction

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; PROTEIN C FOS;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BRAIN REGION; CELLULAR DISTRIBUTION; CHRONIC DISEASE; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE SEVERITY; EXERCISE; EXPERIMENTAL MOUSE; HIPPOCAMPUS; MALE; MAZE TEST; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NEUROLOGIC EXAMINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECALL; SITTING; SLEEP DEPRIVATION; SPATIAL LEARNING; SPATIAL MEMORY;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; MALE; MAZE LEARNING; MEMORY DISORDERS; MENTAL RECALL; MICE; MICE, INBRED C57BL; PHYSICAL CONDITIONING, ANIMAL; PROTO-ONCOGENE PROTEINS C-FOS; SLEEP DEPRIVATION; SPACE PERCEPTION; TIME FACTORS;

EID: 84878710034     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.04.038     Document Type: Article

References (42)

1. McCoy J.G., Strecker R.E. The cognitive cost of sleep lost. Neurobiology of Learning and Memory 2011, 96:564-582.
2. Roy-Byrne P.P., Uhde T.W., Post R.M. Effects of one night's sleep deprivation on mood and behavior in panic disorder. Patients with panic disorder compared with depressed patients and normal controls. Archives of General Psychiatry 1986, 43:895-899.
3. Killgore W.D. Effects of sleep deprivation on cognition. Progress in Brain Research 2010, 185:105-129.
4. Novati A., Hulshof H.J., Kookhaas J.M., Lucassen P.J., Meerlo P. Chronic sleep restriction causes a decrease in hippocampal volume in adolescent rats, which is not explained by changes in glucocorticoid levels or neurogenesis. Neuroscience 2011, 190:145-155.
5. Suchecki D., Tiba P.A., Tufik S. Hormonal and behavioral responses of paradoxical sleep-deprived rats to the elevated plus maze. Journal of Neuroendocrinology 2002, 14:549-554.
6. Hairston I.S., Little M.T., Scanlon M.D., Barakat M.T., Palmer T.D., Sapolsky R.M., et al. Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. Journal of Neurophysiology 2005, 94:4224-4233.
7. Yang S., Sun H., Huang Z., Yao M., Qu W. Repeated sleep restriction inn adolescent rats altered sleep patterns and impaired spatial learning/memory ability. Sleep 2012, 35:849-859.
8. Guan Z., Peng X., Fang J. Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus. Brain Research 2004, 1018:38-47.
9. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
10. Poe G.R., Nitz D.A., McNaughton B.L., Barnes C.A. Experience dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Research 2000, 855:176-180.
11. Sutherland G.R., McNaughton B. Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Current Opinion in Neurobiology 2000, 10:180-186.
12. McCoy J.G., Christie M.A., Kim Y., Brennan R., Poeta D.L., McCarley R.W., et al. Chronic sleep restriction impairs spatial memory in rats. Neuroreport 2013, 24:91-95.
13. Roman V., Walstra I., Luiten P.G., Meerlo P. Too little sleep gradually desensitizes the serotonin 1A receptor system. Sleep 2005, 28:1505-1510.
14. Kim Y., Laposky A.D., Bergmann B.M., Turek F.W. Repeated sleep restriction in rats leads to homeostatic and allostatic responses during recovery sleep. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:10697-10702.
15. Youngstedt S.D., Kline C.E., Zielinski M.R., Kripke D.F., Devlin T.M., Bogan R.K., et al. Tolerance of chronic 90-minute time-in-bed restriction in older long sleepers. Sleep 2009, 32:1467-1479.
16. Zielinski M.R., Kline C.E., Kripke D.F., Bogan R.K., Youngstedt S.D. No effect of 8-week time in bed restriction on glucose tolerance in older long sleepers. Journal of Sleep Research 2008, 17:412-419.
17. Strohle A. Physical activity, exercise, depression and anxiety disorders. Journal of Neural Transmission 2009, 116:777-784.
18. Cotman C.W., Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends in Neurosciences 2002, 25:295-301.
19. Erickson K.I., Kramer A.F. Aerobic exercise effects on cognitive and neural plasticity in older adults. British Journal of Sports Medicine 2009, 43:22-24.
20. Garcia-Capdevila S., Portell-Cortes I., Torras-Garcia M., Coll-Andreu M., Costa-Miserachs D. Effects of long-term voluntary exercise on learning and memory processes: dependency of the task and level of exercise. Behavioural Brain Research 2009, 202:162-170.
21. Lalanza J.F., Sanchez-Roige S., Gagliano H., Fuentes S., Bayod S., Camins A., et al. Physiological and behavioural consequences of long-term moderate treadmill exercise. Psychoneuroendocrinology 2012, 37:1745-1754.
22. Alaei H., Moloudi R., Sarkaki A.R. Effects of treadmill running on mid-term memory and swim speed in the rat with Morris water maze test. Journal of Bodywork and Movement Therapies 2008, 12:72-75.
23. Scott J.P., McNaughton L.R., Polman R.C. Effects of sleep deprivation and exercise on cognitive, motor performance and mood. Physiology and Behavior 2006, 87:396-408.
24. Vollert C., Zagaar M., Hovatta I., Taneja M., Vu A., Dao A., et al. Exercise prevents sleep deprivation-associated anxiety-like behavior in rats: potential role of oxidative stress mechanisms. Behavioural Brain Research 2011, 224:233-240.
25. Pierard C., Liscia P., Phillippin J.N., Mons N., Lafon T., Chauveau F., et al. Modafinil restores memory performance and neural activity impaired by sleep deprivation in mice. Pharmacology Biochemistry and Behavior 2007, 88:55-63.
26. Gorski J.A., Zeiler S.R., Tamowski S., Jones K.R. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. Journal of Neuroscience 2003, 23:6856-6865.
27. Neeper S.A., Gomez-Pinilla F., Choi J., Cotman C. Exercise and brain neurotrophins. Nature 1995, 373:109.
28. Zielinski M.R., Davis J.M., Fadel J.R., Youngstedt S.D. Influence of chronic moderate sleep restriction and exercise on inflammation and carcinogenesis in mice. Brain, Behavior, and Immunity 2012, 26:672-679.
29. Walf A.A., Frye C.A. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nature Protocols 2007, 2:322-328.
30. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Research. Brain Research Reviews 2001, 36:60-90.
31. Zielinski M.R., Taishi P., Clinton J.M., Krueger J.M. 5'-Ectonucleotidase-knockout mice lack non-REM sleep responses to sleep deprivation. European Journal of Neuroscience 2012, 35:1789-1798.
32. Fulk L.J., Stock H.S., Lynn A., Marshall J., Wilson M.A., Hand G.A. Chronic physical exercise reduces anxiety-like behavior in rats. International Journal of Sports Medicine 2004, 25:78-82.
33. Pietrelli A., Lopez-Costa J.J., Goni R., Lopez E.M., Brusco A., Basso N. Effects of moderate and chronic exercise on the nitrergic system and behavioral parameters in rats. Brain Research 2011, 1389:71-82.
34. Jiang F., VanDyke R.D., Zhang J., Li F., Gozal D., Shen X. Effect of chronic sleep restriction on sleepiness and working memory in adolescents and young adults. Journal of Clinical and Experimental Neuropsychology 2011, 33:892-900.
35. Fordyce D.E., Wehner J.M. Physical activity enhances spatial learning performance with an associated alteration in hippocampal protein kinase C activity in C57BL/6 and DBA/2 mice. Brain Research 1993, 619:111-119.
36. Zagaar M., Alhaider I., Dao A., Levine A., Alkarawi A., Alzubaidy M., et al. The beneficial effect of regular exercise on cognition in REM sleep deprivation: behavioral, electrophysiolgical and molecular evidence. Neurobiology of Disease 2012, 45:1153-1162.
37. McDermott C.M., Hardy M.N., Bazan N.G., Magee J.C. Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus. Journal of Physiology 2006, 570:553-565.
38. Erickson K.I., Voss M.W., Prakash R.S., Basak C., Szabo A., Chaddock L., et al. Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:3017-3022.
39. VanPraag H., Christie B.R., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:13427-13431.
40. Guzman-Marin R., Ying Z., Suntsova N., Methippara M., Bashir T., Szymusiak R., et al. Suppression of hippocampal plasticity-related gene expression by sleep deprivation in rats. Journal of Physiology 2006, 575:807-819.
41. Berchtold N.C., Kesslak J.P., Cotman C.W. Hippocampal brain derived neurotrphic factor gene regulation by exercise and the medial septum. Journal of Neuroscience Research 2002, 68:511-521.
42. Schmidt C., Collette F., Cajochen C., Peigneux P. A time to think: circadian rhythms in human cognition. Cognitive Neuropsychology 2007, 24:755-789.