Chronic sleep restriction disrupts sleep homeostasis and behavioral sensitivity to alcohol by reducing the extracellular accumulation of adenosine

Journal of Neuroscience

Volumn 34, Issue 5, 2014, Pages 1879-1891

  Clasadonte, Jerome ^a   McIver, Sally R ^a   Schmitt, Luke I ^a   Halassa, Michael M ^b   Haydon, Philip G ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

Adenosine; Alcohol; Allostasis; EEG; Hippocampus; Sleep

Indexed keywords

2 CHLORO 6 N CYCLOPENTYLADENOSINE; 8 CYCLOPENTYL 1, 3 DIPROPYLXANTHINE; ADENOSINE; ALCOHOL; UNCLASSIFIED DRUG;

ADULT; ALERTNESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CHRONIC SLEEP RESTRICTION; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; HOMEOSTASIS; MALE; MOUSE; NONHUMAN; NONREM SLEEP; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; ROTAROD TEST; SCORING SYSTEM; SLEEP DISORDER; WAKEFULNESS;

ADENOSINE; ALCOHOL; ALLOSTASIS; EEG; HIPPOCAMPUS; SLEEP;

ACTION POTENTIALS; ADENOSINE; ALCOHOLS; ANIMALS; BRAIN WAVES; ELECTROENCEPHALOGRAPHY; EXCITATORY POSTSYNAPTIC POTENTIALS; EXTRACELLULAR FLUID; HIPPOCAMPUS; HOMEOSTASIS; MALE; MICE; MICE, INBRED C57BL; MOVEMENT DISORDERS; NEURONS; PURINERGIC P1 RECEPTOR ANTAGONISTS; SLEEP DEPRIVATION; SLEEP STAGES; THEOPHYLLINE; THIOINOSINE; TIME FACTORS; WAKEFULNESS;

EID: 84893146856     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2870-12.2014     Document Type: Article

References (51)

1. Armitage R (2007) Sleep and circadian rhythms in mood disorders. Acta Psychiatr Scand Suppl 433: 104-115. Medline
2. Armitage R, Hoffmann R, Conroy DA, Arnedt JT, Brower KJ (2012) Effects of a 3-hour sleep delay on sleep homeostasis in alcohol dependent adults. Sleep 35: 273-278. CrossRef Medline
3. Arrigoni E, Rainnie DG, McCarley RW, Greene RW (2001) Adenosinemediated presynaptic modulation of glutamatergic transmission in the laterodorsal tegmentum. J Neurosci 21: 1076-1085. Medline
4. Bachmann V, Klaus F, Bodenmann S, Schäfer N, Brugger P, Huber S, Berger W, Landolt HP (2012) Functional ADA polymorphism increases sleep depth and reduces vigilant attention in humans. Cereb Cortex 22: 962-970. CrossRef Medline
5. Banks S, Dinges DF (2007) Behavioral and physiological consequences of sleep restriction. J Clin Sleep Med 3: 519-528. Medline
6. Basheer R, Strecker RE, Thakkar MM, McCarley RW (2004) Adenosine and sleep-wake regulation. Prog Neurobiol 73: 379-396. CrossRef Medline
7. Bjorness TE, Kelly CL, Gao T, Poffenberger V, Greene RW (2009) Control and function of the homeostatic sleep response by adenosine A1 receptors. J Neurosci 29: 1267-1276. CrossRef Medline
8. Boison D (2013) Adenosine kinase: exploitation for therapeutic gain. Pharmacol Rev 65: 906-943. CrossRef Medline
9. Borbély AA, Achermann P (1999) Sleep homeostasis and models of sleep regulation. J Biol Rhythms 14: 557-568. Medline
10. Brower KJ (2003) Insomnia, alcoholism and relapse. Sleep Med Rev 7: 523-539. CrossRef Medline
11. Brower KJ, Perron BE (2010) Sleep disturbance as a universal risk factor for relapse in addictions to psychoactive substances. Med Hypotheses 74: 928-933. CrossRef Medline
12. Brower KJ, Aldrich MS, Robinson EA, Zucker RA, Greden JF (2001) Insomnia, self-medication, and relapse to alcoholism. Am J Psychiatry 158: 399-404. CrossRef Medline
13. Brower KJ, Krentzman A, Robinson EA (2011) Persistent insomnia, abstinence, and moderate drinking in alcohol-dependent individuals. Am J Addict 20: 435-440. CrossRef Medline
14. Bruns RF (1981) Adenosine antagonism by purines, pteridines and benzopteridines in human fibroblasts. Biochem Pharmacol 30: 325-333. CrossRef Medline
15. Choi DS, Cascini MG, Mailliard W, Young H, Paredes P, McMahon T, Diamond I, Bonci A, Messing RO (2004) The type 1 equilibrative nucleoside transporter regulates ethanol intoxication and preference. Nat Neurosci 7: 855-861. CrossRef Medline
16. Cirelli C (2009) The genetic and molecular regulation of sleep: from fruit flies to humans. Nat Rev Neurosci 10: 549-560. CrossRef Medline
17. Clark M, Dar MS (1988) Mediation of acute ethanol-induced motor disturbances by cerebellar adenosine in rats. Pharmacol Biochem Behav 30: 155-161. Medline
18. Dar MS (1990) Central adenosinergic system involvement in ethanol-induced motor incoordination in mice. J Pharmacol Exp Ther 255: 1202-1209. Medline
19. Dar MS (1993) Brain adenosinergic modulation of acute ethanol-induced motor impairment. Alcohol Alcohol Suppl 2: 425-429. Medline
20. Dar MS (2001) Modulation of ethanol-induced motor incoordination by mouse striatal A (1) adenosinergic receptor. Brain Res Bull 55: 513-520. CrossRef Medline
21. Deurveilher S, Rusak B, Semba K (2012) Time-of-day modulation of homeostatic and allostatic sleep responses to chronic sleep restriction in rats. Am J Physiol Regul Integr Comp Physiol 302: R1411-R1425. CrossRef Medline
22. Diamond I, Gordon AS (1994) The role of adenosine in mediating cellular and molecular responses to ethanol. EXS 71: 175-183. Medline
23. Diamond I, Nagy L, Mochly-Rosen D, Gordon A (1991) The role of adenosine and adenosine transport in ethanol-induced cellular tolerance and dependence: possible biologic and genetic markers of alcoholism. Ann N Y Acad Sci 625: 473-487. CrossRef Medline
24. Fellin T, Halassa MM, Terunuma M, Succol F, Takano H, Frank M, Moss SJ, Haydon PG (2009) Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc Natl Acad Sci U S A 106: 15037-15042. CrossRef Medline
25. Greene RW (2011) Adenosine: front and center in linking nutrition and metabolism to neuronal activity. J Clin Invest 121: 2548-2550. CrossRef Medline
26. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY, Abel T, Haydon PG, Frank MG (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61: 213-219. CrossRef Medline
27. Hanlon EC, Vyazovskiy VV, Faraguna U, Tononi G, Cirelli C (2011) Synaptic potentiation and sleep need: clues from molecular and electrophysiological studies. Curr Top Med Chem 11: 2472-2482. CrossRef Medline
28. Kalinchuk AV, McCarley RW, Porkka-Heiskanen T, Basheer R (2011) The time course of adenosine, nitric oxide (NO) and inducible NO synthase changes in the brain with sleep loss and their role in the non-rapid eye movement sleep homeostatic cascade. J Neurochem 116: 260-272. CrossRef Medline
29. Kim Y, Laposky AD, Bergmann BM, Turek FW (2007) Repeated sleep restriction in rats leads to homeostatic and allostatic responses during recovery sleep. Proc Natl Acad Sci U S A 104: 10697-10702. CrossRef Medline
30. Leemburg S, Vyazovskiy VV, Olcese U, Bassetti CL, Tononi G, Cirelli C (2010) Sleep homeostasis in the rat is preserved during chronic sleep restriction. Proc Natl Acad Sci U S A 107: 15939-15944. CrossRef Medline
31. McCoy JG, Strecker RE (2011) The cognitive cost of sleep lost. Neurobiol Learn Mem 96: 564-582. CrossRef Medline
32. 2A adenosine receptor blockade or stimulation on alcohol intake in alcohol-preferring rats. Psychopharmacology (Berl) 219: 945-957. CrossRef Medline
33. Nagy LE, Diamond I, Casso DJ, Franklin C, Gordon AS (1990) Ethanol increases extracellular adenosine by inhibiting adenosine uptake via the nucleoside transporter. J Biol Chem 265: 1946-1951. Medline
34. Nam HW, McIver SR, Hinton DJ, Thakkar MM, Sari Y, Parkinson FE, Haydon PG, Choi DS (2012) Adenosine and glutamate signaling in neuronglial interactions: implications in alcoholism and sleep disorders. Alcohol Clin Exp Res 36: 1117-1125. CrossRef Medline
35. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310: 113-116. CrossRef Medline
36. Schmitt LI, Sims RE, Dale N, Haydon PG (2012) Wakefulness affects synaptic and network activity by increasing extracellular astrocyte-derived adenosine. J Neurosci 32: 4417-4425. CrossRef Medline
37. Schuckit MA (1994) Low level of response to alcohol as a predictor of future alcoholism. Am J Psychiatry 151: 184-189. Medline
38. Sportiche N, Suntsova N, Methippara M, Bashir T, Mitrani B, Szymusiak R, McGinty D (2010) Sustained sleep fragmentation results in delayed changes in hippocampal-dependent cognitive function associated with reduced dentate gyrus neurogenesis. Neuroscience 170: 247-258. CrossRef Medline
39. Steriade M (2005) In: Principles and practices of sleep medicine (Kryger MH, Roth T, Dement WC, eds.), pp 101-119. Philadelphia, PA: Elsevier.
40. Steriade M, McCarley RW (2005) Brain control of wakefulness and sleep, Ed 2. New York: Plenum.
41. Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10: 49-62. CrossRef Medline
42. Van Dongen HP, Maislin G, Mullington JM, Dinges DF (2003) The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep 26: 117-126. Medline
43. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26: 407-418. Medline
44. Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G (2008) Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat Neurosci 11: 200-208. CrossRef Medline
45. Vyazovskiy VV, Olcese U, Lazimy YM, Faraguna U, Esser SK, Williams JC, Cirelli C, Tononi G (2009) Cortical firing and sleep homeostasis. Neuron 63: 865-878. CrossRef Medline
46. Wall M, Dale N (2008) Activity-dependent release of adenosine: a critical re-evaluation of mechanism. Curr Neuropharmacol 6: 329-337. CrossRef Medline
47. Wall MJ, Dale N (2013) Neuronal transporter and astrocytic ATP exocytosis underlie activity-dependent adenosine release in the hippocampus. J Physiol 591: 3853-3871. CrossRef Medline
48. Whishaw IQ (1972) Hippocampal electroencephalographic activity in the Mongolian gerbil during behaviours and wheel running and in the rat during wheel running and conditioned immobility. Can J Psychol 26: 219-239. Medline
49. Wong MM, Brower KJ, Nigg JT, Zucker RA (2010) Childhood sleep problems, response inhibition, and alcohol and drug outcomes in adolescence and young adulthood. Alcohol Clin Exp Res 34: 1033-1044. CrossRef Medline
50. Wulff K, Gatti S, Wettstein JG, Foster RG (2010) Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nat Rev Neurosci 11: 589-599. CrossRef Medline
51. Zielinski MR, Taishi P, Clinton JM, Krueger JM (2012) 5'-Ectonulceotidaseknock-out mice lack non-REM sleep responses to sleep deprivation. Eur J Neurosci 35: 1789-1798. CrossRef Medline