Repeated sleep restriction in adolescent rats altered sleep patterns and impaired spatial learning/memory ability

Sleep

Volumn 35, Issue 6, 2012, Pages 849-859

  Yang, Su Rong ^a   Sun, Hui ^a   Huang, Zhi Li ^a   Yao, Ming Hui ^a   Qu, Wei Min ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

Adolescent rat; Morris water maze test (WMT); Repeated sleep restriction (RSR); Slow wave activity (SWA)

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; LEARNING DISORDER; MALE; MAZE TEST; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; REM SLEEP; SLEEP DEPRIVATION; SLEEP PATTERN; SLEEP QUALITY; SLOW WAVE SLEEP;

AGE FACTORS; ANIMALS; BRAIN; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; MALE; MAZE LEARNING; MEMORY DISORDERS; RATS; RATS, SPRAGUE-DAWLEY; SLEEP; SLEEP DEPRIVATION;

EID: 84861869386     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.5665/sleep.1888     Document Type: Article

References (49)

1. Yoo SS, Hu PT, Gujar N, Jolesz FA, Walker MP. A deficit in the ability to form new human memories without sleep. Nat Neurosci 2007;10:385-92.
2. Mueller AD, Pollock MS, Lieblich SE, Epp JR, Galea LA, Mistlberger RE. Sleep deprivation can inhibit adult hippocampal neurogenesis independent of adrenal stress hormones. Am J Physiol Regul Integr Comp Physiol 2008;294:R1693-1703.
3. Boonstra TW, Stins JF, Daffertshofer A, Beek PJ. Effects of sleep deprivation on neural functioning: an integrative review. Cell Mol Life Sci 2007;64:934-46. (Pubitemid 46597758)
4. Skaggs WE, McNaughton BL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 1996;271:1870-3. (Pubitemid 26112314)
5. Featherby T, van den Buuse M, Lubman DI, Lawrence AJ. Persistent downregulation of hippocampal CREB mRNA parallels a Y-maze deficit in adolescent rats following semi-chronic amphetamine administration. Br J Pharmacol 2008;154:417-28. (Pubitemid 351670593)
6. Stickgold R, Walker MP. Sleep-dependent memory consolidation and reconsolidation. Sleep Med 2007;8:331-43. (Pubitemid 46706355)
7. Hennevin E, Huetz C, Edeline JM. Neural representations during sleep: from sensory processing to memory traces. Neurobiol Learn Mem 2007;87:416-40. (Pubitemid 46137012)
8. Walsh CM, Booth V, Poe GR. Spatial and reversal learning in the Morris water maze are largely resistant to six hours of REM sleep deprivation following training. Learn Mem 2011;18:422-34.
9. Hagewoud R, Bultsma LJ, Barf RP, Koolhaas JM, Meerlo P. Sleep deprivation impairs contextual fear conditioning and attenuates subsequent behavioural, endocrine and neuronal responses. J Sleep Res 2011;20:259-66.
10. Van Der Werf YD, Van Der Helm E, Schoonheim MM, Ridderikhoff A, Van Someren EJ. Learning by observation requires an early sleep window. Proc Natl Acad Sci U S A 2009;106:18926-30.
11. Loessl B, Valerius G, Kopasz M, Hornyak M, Riemann D, Voderholzer U. Are adolescents chronically sleep-deprived? An investigation of sleep habits of adolescents in the Southwest of Germany. Child Care Health Dev 2008;34:549-56.
12. Sturman DA, Mandell DR, Moghaddam B. Adolescents exhibit behavioral differences from adults during instrumental learning and extinction. Behav Neurosci 2010;124:16-25.
13. Johnson KP. Adolescent sleep patterns: biological, social, and psychological influences. J Am Acad Child Adolesc Psychiatry 2004;43:374-5.
14. Carskadon MA. Patterns of sleep and sleepiness in adolescents. Pediatrician 1990;17:5-12. (Pubitemid 20094954)
15. Longordo F, Kopp C, Luthi A. Consequences of sleep deprivation on neurotransmitter receptor expression and function. Eur J Neurosci 2009;29:1810-19.
16. Vecsey CG, Baillie GS, Jaganath D, et al. Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 2009;461:1122-5.
17. Casement MD, Broussard JL, Mullington JM, Press DZ. The contribution of sleep to improvements in working memory scanning speed: a study of prolonged sleep restriction. Biol Psychol 2006;72:208-12.
18. Jiang F, VanDyke RD, Zhang J, Li F, Gozal D, Shen X. Effect of chronic sleep restriction on sleepiness and working memory in adolescents and young adults. J Clin Exp Neuropsychol 2011;33:892-900.
19. Van Dongen HP, Maislin G, Mullington JM, Dinges DF. The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep 2003;26:117-26. (Pubitemid 39610686)
20. Tobler I, Borbely AA. The effect of 3-h and 6-h sleep deprivation on sleep and EEG spectra of the rat. Behav Brain Res 1990;36:73-8. (Pubitemid 20026606)
21. Schwierin B, Borbely AA, Tobler I. Prolonged effects of 24-h total sleep deprivation on sleep and sleep EEG in the rat. Neurosci Lett 1999;261:61-4. (Pubitemid 29100076)
22. Akerstedt T, Kecklund G, Ingre M, Lekander M, Axelsson J. Sleep homeostasis during repeated sleep restriction and recovery: support from EEG dynamics. Sleep 2009;32:217-22.
23. Machado RB, Suchecki D, Tufik S. Sleep homeostasis in rats assessed by a long-term intermittent paradoxical sleep deprivation protocol. Behav Brain Res 2005;160:356-64. (Pubitemid 40603532)
24. Machado RB, Tufik S, Suchecki D. Modulation of sleep homeostasis by corticotropin releasing hormone in REM sleep-deprived rats. Int J Endocrinol 2010;2010:1-12.
25. Hairston IS, Little MT, Scanlon MD, et al. Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. J Neurophysiol 2005;94:4224-33. (Pubitemid 41691781)
26. Kim Y, Laposky AD, Bergmann BM, Turek FW. Repeated sleep restriction in rats leads to homeostatic and allostatic responses during recovery sleep. Proc Natl Acad Sci U S A 2007;104:10697-702. (Pubitemid 47185727)
27. Ward CP, McCoy JG, McKenna JT, Connolly NP, McCarley RW, Strecker RE. Spatial learning and memory deficits following exposure to 24 h of sleep fragmentation or intermittent hypoxia in a rat model of obstructive sleep apnea. Brain Res 2009;1294:128-37.
28. Tartar JL, McKenna JT, Ward CP, McCarley RW, Strecker RE, Brown RE. Sleep fragmentation reduces hippocampal CA1 pyramidal cell excitability and response to adenosine. Neurosci Lett 2010;469:1-5.
29. Spear LP. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000;24:417-63. (Pubitemid 30243061)
30. Kohtoh S, Taguchi Y, Matsumoto N, Wada M, Huang ZL, Urade Y. Algorithm for sleep scoring in experimental animals based on fast Fourier transform power spectrum analysis of the electroencephalogram. Sleep Biol Rhythms 2008;6:163-71. (Pubitemid 352015670)
31. Oishi Y, Huang ZL, Fredholm BB, Urade Y, Hayaishi O. Adenosine in the tuberomammillary nucleus inhibits the histaminergic system via A1 receptors and promotes non-rapid eye movement sleep. Proc Natl Acad Sci U S A 2008;105:19992-7.
32. Huang ZL, Qu WM, Eguchi N, et al. Adenosine A2A, but not A1, receptors mediate the arousal effect of caffeine. Nat Neurosci 2005;8:858-9.
33. Huang ZL, Mochizuki T, Qu WM, et al. Altered sleep-wake characteristics and lack of arousal response to H3 receptor antagonist in histamine H1 receptor knockout mice. Proc Natl Acad Sci U S A 2006;103:4687-92.
34. Mendelson WB, Bergmann BM. EEG delta power during sleep in young and old rats. Neurobiol Aging 1999;20:669-73. (Pubitemid 30064413)
35. Trachsel L, Tobler I, Borbely AA. Electroencephalogram analysis of non-rapid eye movement sleep in rats. Am J Physiol 1988;255:R27-37.
36. Leemburg S, Vyazovskiy VV, Olcese U, Bassetti CL, Tononi G, Cirelli C. Sleep homeostasis in the rat is preserved during chronic sleep restriction. Proc Natl Acad Sci U S A 2010;107:15939-44.
37. Toppila J, Alanko L, Asikainen M, Tobler I, Stenberg D, Porkka-Heiskanen T. Sleep deprivation increases somatostatin and growth hormone-releasing hormone messenger RNA in the rat hypothalamus. J Sleep Res 1997;6:171-8. (Pubitemid 27414457)
38. Tobler I, Deboer T, Fischer M. Sleep and sleep regulation in normal and prion protein-deficient mice. J Neurosci 1997;17:1869-79. (Pubitemid 27089831)
39. Vorhees CV, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 2006;1:848-58.
40. Moore M, Meltzer LJ. The sleepy adolescent: causes and consequences of sleepiness in teens. Paediatr Respir Rev 2008;9:114-21.
41. Kopasz M, Loessl B, Hornyak M, et al. Sleep and memory in healthy children and adolescents: a critical review. Sleep Med Rev 2010;14:167-77.
42. Segalowitz SJ, Santesso DL, Jetha MK. Electrophysiological changes during adolescence: a review. Brain Cogn 2010;72:86-100.
43. Sanford LD, Yang L, Wellman LL, Liu X, Tang X. Differential effects of controllable and uncontrollable footshock stress on sleep in mice. Sleep 2010;33:621-30.
44. Hagewoud R, Havekes R, Novati A, Keijser JN, Van der Zee EA, Meerlo P. Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. J Sleep Res 2010;19:280-8.
45. Zavada A, Strijkstra AM, Boerema AS, Daan S, Beersma DG. Evidence for differential human slow-wave activity regulation across the brain. J Sleep Res 2009;18:3-10.
46. Poe GR, Walsh CM, Bjorness TE. Both duration and timing of sleep are important to memory consolidation. Sleep 2010;33:1277-8.
47. Novati A, Roman V, Cetin T, et al. Chronically restricted sleep leads to depression-like changes in neurotransmitter receptor sensitivity and neuroendocrine stress reactivity in rats. Sleep 2008;31:1579-85.
48. Meerlo P, Mistlberger RE, Jacobs BL, Heller HC, McGinty D. New neurons in the adult brain: the role of sleep and consequences of sleep loss. Sleep Med Rev 2009;13:187-94.
49. Barf RP, Meerlo P, Scheurink AJ. Chronic sleep disturbance impairs glucose homeostasis in rats. Int J Endocrinol 2010;2010:1-6.