A review of sleep deprivation studies evaluating the brain transcriptome

SpringerPlus

Volumn 3, Issue 1, 2014, Pages

  Elliott, Alisa S ^a   Huber, Jason D ^b   O’Callaghan, James P ^c   Rosen, Charles L ^a   Miller, Diane B ^c  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

^c NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

Author keywords

Rodent; Sleep deprivation; Sleep disruption; Transcriptome

Indexed keywords

EID: 84928674440     PISSN: None     EISSN: 21931801     Source Type: Journal    
DOI: 10.1186/2193-1801-3-728     Document Type: Review

References (105)

1. Allada R, Siegel JM: Unearthing the phylogenetic roots of sleep.Curr Biol 2008,18(15):R670-R679. doi:10.1016/j.cub.2008.06.033 10.1016/j.cub.2008.06.033
2. Ayas NT, White DP, Manson JE, Stampfer MJ, Speizer FE, Malhotra A, Hu FB: A prospective study of sleep duration and coronary heart disease in women.Arch Intern Med 2003,163(2):205–209. 10.1001/archinte.163.2.205
3. Barf RP, Desprez T, Meerlo P, Scheurink AJ: Increased food intake and changes in metabolic hormones in response to chronic sleep restriction alternated with short periods of sleep allowance.Am J Physiol Regul Integr Comp Physiol 2012,302(1):R112-R117. doi:10.1152/ajpregu.00326.2011 10.1152/ajpregu.00326.2011
4. Basheer R, Halldner L, Alanko L, McCarley RW, Fredholm BB, Porkka-Heiskanen T: Opposite changes in adenosine A1 and A2A receptor mRNA in the rat following sleep deprivation.Neuroreport 2001,12(8):1577–1580. 10.1097/00001756-200106130-00013
5. Benington JH, Heller HC: Restoration of Brain Energy-Metabolism as the Function of Sleep.Prog Neurobiol 1995,45(4):347–360. 10.1016/0301-0082(94)00057-O
6. Borbely AA: A two process model of sleep regulation.Hum Neurobiol 1982,1(3):195–204.
7. Borbely AA, Achermann P: Sleep homeostasis and models of sleep regulation.J Biol Rhythm 1999,14(6):557–568.
8. Brown MK, Naidoo N: The UPR and the anti-oxidant response: relevance to sleep and sleep loss.Mol Neurobiol 2010,42(2):103–113. doi:10.1007/s12035–010–8114–8 10.1007/s12035-010-8114-8
9. Cappuccio FP, Taggart FM, Kandala NB, Currie A, Peile E, Stranges S, Miller MA: Meta-analysis of short sleep duration and obesity in children and adults.Sleep 2008,31(5):619–626.
10. Chaput JP, Despres JP, Bouchard C, Tremblay A: Association of sleep duration with type 2 diabetes and impaired glucose tolerance.Diabetologia 2007,50(11):2298–2304. doi:10.1007/s00125–007–0786-x 10.1007/s00125-007-0786-x
11. Chen JC, Brunner RL, Ren H, Wassertheil-Smoller S, Larson JC, Levine DW, Allison M, Naughton MJ, Stefanick ML: Sleep Duration and Risk of Ischemic Stroke in Postmenopausal Women.Stroke 2008,39(12):3185–3192. doi:10.1161/Strokeaha.108.521773 10.1161/STROKEAHA.108.521773
12. Cirelli C: Invited review: How sleep deprivation affects gene expression in the brain: a review of recent findings.J Appl Physiol 2002,92(1):394–400.
13. Cirelli C, Tononi G: Differences in gene expression between sleep and waking as revealed by mRNA differential display.Mol Brain Res 1998,56(1–2):293–305.
14. Cirelli C, Tononi G: Differences in brain gene expression between sleep and waking as revealed by mRNA differential display and cDNA microarray technology.J Sleep Res 1999, 8:44–52. 10.1046/j.1365-2869.1999.00008.x
15. Cirelli C, Tononi G: Differences in gene expression during sleep and wakefulness.Ann Med 1999,31(2):117–124. 10.3109/07853899908998787
16. Cirelli C, Tononi G: Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system.J Neurosci 2000,20(24):9187–9194.
17. Cirelli C, Tononi G: Gene expression in the brain across the sleep-waking cycle.Brain Res 2000,885(2):303–321. 10.1016/S0006-8993(00)03008-0
18. Cirelli C, Tononi G: Uncoupling proteins and sleep deprivation.Arch Ital Biol 2004,142(4):541–549.
19. Cirelli C, Gutierrez CM, Tononi G: Extensive and divergent effects of sleep and wakefulness on brain gene expression.Neuron 2004,41(1):35–43. 10.1016/S0896-6273(03)00814-6
20. Cirelli C, Faraguna U, Tononi G: Changes in brain gene expression after long-term sleep deprivation.J Neurochem 2006,98(5):1632–1645. doi:10.1111/j.1471–4159.2006.04058.x 10.1111/j.1471-4159.2006.04058.x
21. Clinton JM, Davis CJ, Zielinski MR, Jewett KA, Krueger JM: Biochemical regulation of sleep and sleep biomarkers.J Clin Sleep Med 2011,7(5 Suppl):S38-S42. doi:10.5664/JCSM.1360
22. Coenen AM, van Luijtelaar EL: Stress induced by three procedures of deprivation of paradoxical sleep.Physiol Behav 1985,35(4):501–504. 10.1016/0031-9384(85)90130-1
23. Conti B, Maier R, Barr AM, Morale MC, Lu X, Sanna PP, Bilbe G, Hoyer D, Bartfai T: Region-specific transcriptional changes following the three antidepressant treatments electro convulsive therapy, sleep deprivation and fluoxetine.Mol Psychiatry 2007,12(2):167–189. doi:10.1038/sj.mp.4001897 10.1038/sj.mp.4001897
24. Das G, Gopalakrishnan A, Faisal M, Mallick BN: Stimulatory role of calcium in rapid eye movement sleep deprivation-induced noradrenaline-mediated increase in Na-K-ATPase activity in rat brain.Neuroscience 2008,155(1):76–89. doi:10.1016/j.neuroscience.2008.04.069 10.1016/j.neuroscience.2008.04.069
25. Datta A, Jingru Q, Khor TH, Teo MT, Heese K, Sze SK: Quantitative neuroproteomics of an in vivo rodent model of focal cerebral ischemia/reperfusion injury reveals a temporal regulation of novel pathophysiological molecular markers.J Proteome Res 2011,10(11):5199–5213. doi:10.1021/pr200673y 10.1021/pr200673y
26. Dattilo M, Antunes HK, Medeiros A, Monico Neto M, Souza HS, Tufik S, de Mello MT: Sleep and muscle recovery: endocrinological and molecular basis for a new and promising hypothesis.Med Hypotheses 2011,77(2):220–222. doi:10.1016/j.mehy.2011.04.017 10.1016/j.mehy.2011.04.017
27. Dijk DJ, Beersma DG: Effects of SWS deprivation on subsequent EEG power density and spontaneous sleep duration.Electroencephalogr Clin Neurophysiol 1989,72(4):312–320. 10.1016/0013-4694(89)90067-9
28. Dijk DJ, Lockley SW: Integration of human sleep-wake regulation and circadian rhythmicity.J Appl Physiol 2002,92(2):852–862. doi:10.1152/japplphysiol.00924.2001
29. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, Ma G, Bupp S, Shrestha P, Shah RD, Doughty ML, Gong S, Greengard P, Heintz N: Application of a translational profiling approach for the comparative analysis of CNS cell types.Cell 2008,135(4):749–762. doi:10.1016/j.cell.2008.10.029 10.1016/j.cell.2008.10.029
30. Emery B, Barres BA: Unlocking CNS cell type heterogeneity.Cell 2008,135(4):596–598. doi:10.1016/j.cell.2008.10.031 10.1016/j.cell.2008.10.031
31. Everson CA, Szabo A: Repeated exposure to severely limited sleep results in distinctive and persistent physiological imbalances in rats.PLoS One 2011,6(8):e22987. doi:10.1371/journal.pone.0022987 10.1371/journal.pone.0022987
32. Fenzl T, Romanowski CP, Flachskamm C, Honsberg K, Boll E, Hoehne A, Kimura M: Fully automated sleep deprivation in mice as a tool in sleep research.J Neurosci Methods 2007,166(2):229–235. doi:10.1016/j.jneumeth.2007.07.007 10.1016/j.jneumeth.2007.07.007
33. Ferrie JE, Shipley MJ, Cappuccio FP, Brunner E, Miller MA, Kumari M, Marmot MG: A prospective study of change in sleep duration: associations with mortality in the Whitehall II cohort.Sleep 2007,30(12):1659–1666.
34. Franco-Perez J, Ballesteros-Zebadua P, Fernandez-Figueroa EA, Ruiz-Olmedo I, Reyes-Grajeda P, Paz C: Sleep deprivation and sleep recovery modifies connexin36 and connexin43 protein levels in rat brain.Neuroreport 2012,23(2):103–107. doi:10.1097/WNR.0b013e32834e8fcb 10.1097/WNR.0b013e32834e8fcb
35. Frank MG: Erasing synapses in sleep: is it time to be SHY?Neural Plast 2012, 2012:264378. doi:10.1155/2012/264378
36. Franken P, Chollet D, Tafti M: The homeostatic regulation of sleep need is under genetic control.J Neurosci 2001,21(8):2610–2621.
37. Franken P, Dudley CA, Estill SJ, Barakat M, Thomason R, O'Hara BF, McKnight SL: NPAS2 as a transcriptional regulator of non-rapid eye movement sleep: genotype and sex interactions.Proc Natl Acad Sci U S A 2006,103(18):7118–7123. doi:10.1073/pnas.0602006103 10.1073/pnas.0602006103
38. Friedman L, Bergmann BM, Rechtschaffen A: Effects of sleep deprivation on sleepiness, sleep intensity, and subsequent sleep in the rat.Sleep 1979,1(4):369–391.
39. Gottlieb DJ, Redline S, Nieto FJ, Baldwin CM, Newman AB, Resnick HE, Punjabi NM: Association of usual sleep duration with hypertension: the Sleep Heart Health Study.Sleep 2006,29(8):1009–1014.
40. Heiman M, Schaefer A, Gong S, Peterson JD, Day M, Ramsey KE, Suarez-Farinas M, Schwarz C, Stephan DA, Surmeier DJ, Greengard P, Heintz N: A translational profiling approach for the molecular characterization of CNS cell types.Cell 2008,135(4):738–748. doi:10.1016/j.cell.2008.10.028 10.1016/j.cell.2008.10.028
41. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, Pack AI: Rest in Drosophila is a sleep-like state.Neuron 2000,25(1):129–138. 10.1016/S0896-6273(00)80877-6
42. Howarth C, Gleeson P, Attwell D: Updated energy budgets for neural computation in the neocortex and cerebellum.J Cereb Blood Flow Metab 2012,32(7):1222–1232. doi:10.1038/jcbfm.2012.35 10.1038/jcbfm.2012.35
43. Huber R, Tononi G, Cirelli C: Exploratory behavior, cortical BDNF expression, and sleep homeostasis.Sleep 2007,30(2):129–139.
44. Ikehara S, Iso H, Date C, Kikuchi S, Watanabe Y, Wada Y, Inaba Y, Tamakoshi A, Group JS: Association of sleep duration with mortality from cardiovascular disease and other causes for Japanese men and women: the JACC study.Sleep 2009,32(3):295–301.
45. Kalinchuk AV, McCarley RW, Porkka-Heiskanen T, Basheer R: Sleep deprivation triggers inducible nitric oxide-dependent nitric oxide production in wake-active basal forebrain neurons.J Neurosci 2010,30(40):13254–13264. doi:10.1523/JNEUROSCI.0014–10.2010 10.1523/JNEUROSCI.0014-10.2010
46. Kilduff TS, Lein ES, de la Iglesia H, Sakurai T, Fu YH, Shaw P: New developments in sleep research: molecular genetics, gene expression, and systems neurobiology.J Neurosci 2008,28(46):11814–11818. doi:10.1523/JNEUROSCI.3768–08.2008 10.1523/JNEUROSCI.3768-08.2008
47. Kim J, Jo I: Age-Dependent Association Between Sleep Duration and Hypertension in the Adult Korean Population.Am J Hypertens 2010,23(12):1286–1291. doi:10.1038/Ajh.2010.166 10.1038/ajh.2010.166
48. Kim Y, Chen L, McCarley RW, Strecker RE: Sleep allostasis in chronic sleep restriction: the role of the norepinephrine system.Brain Res 2013, 1531:9–16. doi:10.1016/j.brainres.2013.07.048
49. Kohane IS, Valtchinov VI: Quantifying the white blood cell transcriptome as an accessible window to the multiorgan transcriptome.Bioinformatics 2012,28(4):538–545. doi:10.1093/bioinformatics/btr713 10.1093/bioinformatics/btr713
50. Kong J, Shepel PN, Holden CP, Mackiewicz M, Pack AI, Geiger JD: Brain glycogen decreases with increased periods of wakefulness: implications for homeostatic drive to sleep.J Neurosci 2002,22(13):5581–5587.
51. Kushida CA: Countermeasures for sleep loss and deprivation.Curr Treat Options Neurol 2006,8(5):361–366. 10.1007/s11940-006-0025-7
52. Lamond N, Jay SM, Dorrian J, Ferguson SA, Jones C, Dawson D: The dynamics of neurobehavioural recovery following sleep loss.J Sleep Res 2007,16(1):33–41. doi:10.1111/j.1365–2869.2007.00574.x 10.1111/j.1365-2869.2007.00574.x
53. Leenaars CH, Dematteis M, Joosten RN, Eggels L, Sandberg H, Schirris M, Feenstra MG, Van Someren EJ: A new automated method for rat sleep deprivation with minimal confounding effects on corticosterone and locomotor activity.J Neurosci Methods 2011,196(1):107–117. doi:10.1016/j.jneumeth.2011.01.014 10.1016/j.jneumeth.2011.01.014
54. Liew CC, Ma J, Tang HC, Zheng R, Dempsey AA: The peripheral blood transcriptome dynamically reflects system wide biology: a potential diagnostic tool.J Lab Clin Med 2006,147(3):126–132. doi:10.1016/j.lab.2005.10.005 10.1016/j.lab.2005.10.005
55. Luckhaupt SE, Tak S, Calvert GM: The prevalence of short sleep duration by industry and occupation in the National Health Interview Survey.Sleep 2010,33(2):149–159.
56. Luyster FS, Strollo PJ, Zee PC, Walsh JK, Sleep BDAA: Sleep: A Health Imperative.Sleep 2012,35(6):727–734. doi:10.5665/Sleep.1846
57. Mackiewicz M, Nikonova EV, Zimmerman JE, Galante RJ, Zhang L, Cater JR, Geiger JD, Pack AI: Enzymes of adenosine metabolism in the brain: diurnal rhythm and the effect of sleep deprivation.J Neurochem 2003,85(2):348–357. 10.1046/j.1471-4159.2003.01687.x
58. Mackiewicz M, Shockley KR, Romer MA, Galante RJ, Zimmerman JE, Naidoo N, Baldwin DA, Jensen ST, Churchill GA, Pack AI: Macromolecule biosynthesis: a key function of sleep.Physiol Genomics 2007,31(3):441–457. doi:10.1152/physiolgenomics.00275.2006 10.1152/physiolgenomics.00275.2006
59. Mackiewicz M, Zimmerman JE, Shockley KR, Churchill GA, Pack AI: What are microarrays teaching us about sleep?Trends Mol Med 2009,15(2):79–87. doi:10.1016/j.molmed.2008.12.002 10.1016/j.molmed.2008.12.002
60. Mallick BN, Singh A: REM sleep loss increases brain excitability: role of noradrenaline and its mechanism of action.Sleep Med Rev 2011,15(3):165–178. doi:10.1016/j.smrv.2010.11.001 10.1016/j.smrv.2010.11.001
61. Maret S, Dorsaz S, Gurcel L, Pradervand S, Petit B, Pfister C, Hagenbuchle O, O'Hara BF, Franken P, Tafti M: Homer1a is a core brain molecular correlate of sleep loss.Proc Natl Acad Sci U S A 2007,104(50):20090–20095. doi:10.1073/pnas.0710131104 10.1073/pnas.0710131104
62. Martins PJ, Fernandes L, de Oliveira AC, Tufik S, D'Almeida V: Type of diet modulates the metabolic response to sleep deprivation in rats.Nutr Metab 2011,8(1):86. doi:10.1186/1743–7075–8-86 10.1186/1743-7075-8-86
63. McEwen BS: Sleep deprivation as a neurobiologic and physiologic stressor: Allostasis and allostatic load.Metab Clin Exp 2006,55(10 Suppl 2):S20-S23. doi:10.1016/j.metabol.2006.07.008
64. McGlincy NJ, Valomon A, Chesham JE, Maywood ES, Hastings MH, Ule J: Regulation of alternative splicing by the circadian clock and food related cues.Genome Biol 2012,13(6):R54. doi:10.1186/gb-2012–13–6-r54 10.1186/gb-2012-13-6-r54
65. Meerlo P, Koehl M, van der Borght K, Turek FW: Sleep restriction alters the hypothalamic-pituitary-adrenal response to stress.J Neuroendocrinol 2002,14(5):397–402. 10.1046/j.0007-1331.2002.00790.x
66. Moller-Levet CS, Archer SN, Bucca G, Laing EE, Slak A, Kabiljo R, Lo JC, Santhi N, von Schantz M, Smith CP, Dijk DJ: Effects of insufficient sleep on circadian rhythmicity and expression amplitude of the human blood transcriptome.Proc Natl Acad Sci U S A 2013,110(12):E1132-E1141. doi:10.1073/pnas.1217154110 10.1073/pnas.1217154110
67. Mongrain V, Hernandez SA, Pradervand S, Dorsaz S, Curie T, Hagiwara G, Gip P, Heller HC, Franken P: Separating the contribution of glucocorticoids and wakefulness to the molecular and electrophysiological correlates of sleep homeostasis.Sleep 2010,33(9):1147–1157.
68. Mongrain V, La Spada F, Curie T, Franken P: Sleep loss reduces the DNA-binding of BMAL1, CLOCK, and NPAS2 to specific clock genes in the mouse cerebral cortex.PLoS One 2011,6(10):e26622. doi:10.1371/journal.pone.0026622 10.1371/journal.pone.0026622
69. Naidoo N, Giang W, Galante RJ, Pack AI: Sleep deprivation induces the unfolded protein response in mouse cerebral cortex.J Neurochem 2005,92(5):1150–1157. doi:10.1111/j.1471–4159.2004.02952.x 10.1111/j.1471-4159.2004.02952.x
70. Nelson SE, Duricka DL, Campbell K, Churchill L, Krueger JM: Homer1a and 1bc levels in the rat somatosensory cortex vary with the time of day and sleep loss.Neurosci Lett 2004,367(1):105–108. doi:10.1016/j.neulet.2004.05.089 10.1016/j.neulet.2004.05.089
71. Nikonova EV, Naidoo N, Zhang L, Romer M, Cater JR, Scharf MT, Galante RJ, Pack AI: Changes in components of energy regulation in mouse cortex with increases in wakefulness.Sleep 2010,33(7):889–900.
72. Nurminen M, Karjalainen A: Epidemiologic estimate of the proportion of fatalities related to occupational factors in Finland.Scand J Work Environ Health 2001,27(3):161–213. 10.5271/sjweh.605
73. Petit JM, Tobler I, Kopp C, Morgenthaler F, Borbely AA, Magistretti PJ: Metabolic response of the cerebral cortex following gentle sleep deprivation and modafinil administration.Sleep 2010,33(7):901–908.
74. Porkka-Heiskanen T, Strecker RE, Thakkar M, Bjorkum AA, Greene RW, McCarley RW: Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness.Science 1997,276(5316):1265–1268. 10.1126/science.276.5316.1265
75. Qureshi AI, Giles WH, Croft JB, Bliwise DL: Habitual sleep patterns and risk for stroke and coronary heart disease: a 10-year follow-up from NHANES I.Neurology 1997,48(4):904–911. 10.1212/WNL.48.4.904
76. Raizen DM, Zimmerman JE, Maycock MH, Ta UD, You YJ, Sundaram MV, Pack AI: Lethargus is a Caenorhabditis elegans sleep-like state (vol 451, pg 569, 2008).Nature 2008,453(7197):952–952. 10.1038/nature07044
77. Rechtschaffen A, Gilliland MA, Bergmann BM, Winter JB: Physiological correlates of prolonged sleep deprivation in rats.Science 1983,221(4606):182–184. 10.1126/science.6857280
78. Rechtschaffen A, Bergmann BM, Gilliland MA, Bauer K: Effects of method, duration, and sleep stage on rebounds from sleep deprivation in the rat.Sleep 1999,22(1):11–31.
79. Sabanayagam C, Shankar A: Sleep duration and cardiovascular disease: results from the National Health Interview Survey.Sleep 2010,33(8):1037–1042.
80. Schultes B, Schmid S, Peters A, Born J, Fehm HL: Sleep loss and the development of diabetes: a review of current evidence.Exp Clin Endocrinol Diabetes 2005,113(10):563–567. doi:10.1055/s-2005–872944 10.1055/s-2005-872944
81. Sgoifo A, Buwalda B, Roos M, Costoli T, Merati G, Meerlo P: Effects of sleep deprivation on cardiac autonomic and pituitary-adrenocortical stress reactivity in rats.Psychoneuroendocrinology 2006,31(2):197–208. doi:10.1016/j.psyneuen.2005.06.009 10.1016/j.psyneuen.2005.06.009
82. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G: Correlates of sleep and waking in Drosophila melanogaster.Science 2000,287(5459):1834–1837. 10.1126/science.287.5459.1834
83. Shaw PJ, Tononi G, Greenspan RJ, Robinson DF: Stress response genes protect against lethal effects of sleep deprivation in Drosophila.Nature 2002,417(6886):287–291. doi:10.1038/417287a 10.1038/417287a
84. Siegel JM: Clues to the functions of mammalian sleep.Nature 2005,437(7063):1264–1271. doi:10.1038/nature04285 10.1038/nature04285
85. Simons K, Toomre D: Lipid rafts and signal transduction.Nat Rev Mol Cell Biol 2000,1(1):31–39. doi:10.1038/35036052 10.1038/35036052
86. Singh S, Amar M, Mallick BN: Rapid eye movement sleep deprivation modulates SynapsinI expression in rat brain.Neurosci Lett 2012. doi:10.1016/j.neulet.2012.05.031
87. Spiegel K, Knutson K, Leproult R, Tasali E, Van Cauter E: Sleep loss: a novel risk factor for insulin resistance and Type 2 diabetes.J Appl Physiol 2005,99(5):2008–2019. doi:10.1152/japplphysiol.00660.2005 10.1152/japplphysiol.00660.2005
88. Tadavarty R, Rajput PS, Wong JM, Kumar U, Sastry BR: Sleep-deprivation induces changes in GABA(B) and mGlu receptor expression and has consequences for synaptic long-term depression.PLoS One 2011,6(9):e24933. doi:10.1371/journal.pone.0024933 10.1371/journal.pone.0024933
89. Taishi P, Sanchez C, Wang Y, Fang J, Harding JW, Krueger JM: Conditions that affect sleep alter the expression of molecules associated with synaptic plasticity.Am J Physiol Regul Integr 2001,281(3):R839-R845.
90. Terao A, Greco MA, Davis RW, Heller HC, Kilduff TS: Region-specific changes in immediate early gene expression in response to sleep deprivation and recovery sleep in the mouse brain.Neuroscience 2003,120(4):1115–1124. 10.1016/S0306-4522(03)00395-6
91. Terao A, Steininger TL, Hyder K, Apte-Deshpande A, Ding J, Rishipathak D, Davis RW, Heller HC, Kilduff TS: Differential increase in the expression of heat shock protein family members during sleep deprivation and during sleep.Neuroscience 2003,116(1):187–200. 10.1016/S0306-4522(02)00695-4
92. Terao A, Wisor JP, Peyron C, Apte-Deshpande A, Wurts SW, Edgar DM, Kilduff TS: Gene expression in the rat brain during sleep deprivation and recovery sleep: an Affymetrix GeneChip study.Neuroscience 2006,137(2):593–605. doi:10.1016/j.neuroscience.2005.08.059 10.1016/j.neuroscience.2005.08.059
93. Thompson CL, Wisor JP, Lee CK, Pathak SD, Gerashchenko D, Smith KA, Fischer SR, Kuan CL, Sunkin SM, Ng LL, Lau C, Hawrylycz M, Jones AR, Kilduff TS, Lein ES: Molecular and anatomical signatures of sleep deprivation in the mouse brain.Front Neurosci 2010, 4:165. doi:10.3389/fnins.2010.00165
94. Tononi G, Cirelli C: Sleep and synaptic homeostasis: a hypothesis.Brain Res Bull 2003,62(2):143–150. 10.1016/j.brainresbull.2003.09.004
95. Van Buskirk C, Sternberg PW: Epidermal growth factor signaling induces behavioral quiescence in Caenorhabditis elegans.Nat Neurosci 2007,10(10):1300–1307. doi:10.1038/nn1981 10.1038/nn1981
96. 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(2):117–126.
97. Veasey S: Sleep homeostasis: finding Odysseus among the mnesteres.Sleep 2010,33(9):1131–1132.
98. Volkow ND, Tomasi D, Wang GJ, Telang F, Fowler JS, Logan J, Benveniste H, Kim R, Thanos PK, Ferre S: Evidence That Sleep Deprivation Downregulates Dopamine D2R in Ventral Striatum in the Human Brain.J Neurosci 2012,32(19):6711–6717. doi:10.1523/JNEUROSCI. 0045–12.2012 10.1523/JNEUROSCI.0045-12.2012
99. Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, Tononi G: Local sleep in awake rats.Nature 2011,472(7344):443–447. doi:10.1038/nature10009 10.1038/nature10009
100. Wang H, Liu Y, Briesemann M, Yan J: Computational analysis of gene regulation in animal sleep deprivation.Physiol Genomics 2010,42(3):427–436. doi:10.1152/physiolgenomics.00205.2009 10.1152/physiolgenomics.00205.2009
101. Weil ZM, Norman GJ, Karelina K, Morris JS, Barker JM, Su AJ, Walton JC, Bohinc S, Nelson RJ, DeVries AC: Sleep deprivation attenuates inflammatory responses and ischemic cell death.Exp Neurol 2009,218(1):129–136. doi:10.1016/j.expneurol.2009.04.018 10.1016/j.expneurol.2009.04.018
102. Wisor JP, O'Hara BF, Terao A, Selby CP, Kilduff TS, Sancar A, Edgar DM, Franken P: A role for cryptochromes in sleep regulation.BMC Neurosci 2002, 3:20. 10.1186/1471-2202-3-20
103. Wisor JP, Schmidt MA, Clegern WC: Evidence for neuroinflammatory and microglial changes in the cerebral response to sleep loss.Sleep 2011,34(3):261–272.
104. Yokogawa T, Marin W, Faraco J, Pezeron G, Appelbaum L, Zhang J, Rosa F, Mourrain P, Mignot E: Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants.PLoS Biol 2007,5(10):2379–2397. doi:10.1371/journal.pbio.0050277
105. Zhdanova IV, Wang SY, Leclair OU, Danilova NP: Melatonin promotes sleep-like state in zebrafish.Brain Res 2001,903(1–2):263–268.