Adenosine: A Mediator of the Sleep-Inducing Effects of Prolonged Wakefulness
Open accessAbstract
Both subjective and electroencephalographic arousal diminish as a function of the duration of prior wakefulness. Data reported here suggest that the major criteria for a neural sleep factor mediating the somnogenic effects of prolonged wakefulness are satisfied by adenosine, a neuromodulator whose extracellular concentration increases with brain metabolism and which, in vitro, inhibits basal forebrain cholinergic neurons. In vivo microdialysis measurements in freely behaving cats showed that adenosine extracellular concentrations in the basal forebrain cholinergic region increased during spontaneous wakefulness as contrasted with slow wave sleep; exhibited progressive increases during sustained, prolonged wakefulness; and declined slowly during recovery sleep. Furthermore, the sleep-wakefulness profile occurring after prolonged wakefulness was mimicked by increased extracellular adenosine induced by microdialysis perfusion of an adenosine transport inhibitor in the cholinergic basal forebrain but not by perfusion in a control noncholinergic region.
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The neurobiological mechanisms underlying the homeostatic hourglass are less characterized than the clock mechanisms; important roles have been assigned to adenosine, increased synaptic density during wakefulness, and cytokines.
“The neurobiological mechanisms underlying the hourglass are not characterized as well as the mechanisms of the clock are. As reviewed elsewhere in the present special issue and several times before, important roles have been assigned to adenosine [66], to an increase in synaptic density during wakefulness [79], and to cytokines [50].”
From Sleep, vigilance, and thermosensitivity (2012) · cites this paper as [66]
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Cites
Two-Process Model of Sleep Regulation
Binder, M. D., Hirokawa, N., & Windhorst, U. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_6166 · Cited by 3,895 · see citing works
Restoration of brain energy metabolism as the function of sleep
Benington, J. H., & Heller, H. C. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(94)00057-o · Cited by 828 · see citing works
Steriade, M., Datta, S., Paré, D., Oakson, G., & Dossi, R. C. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-08-02541.1990 · Cited by 775 · see citing works
Arousal--Revisiting the Reticular Activating System
Steriade, M. (1996) · Science · doi:10.1126/science.272.5259.225 · Cited by 350 · see citing works
Adenosine Inhibition of Mesopontine Cholinergic Neurons: Implications for EEG Arousal
Rainnie, D. G., Grunze, H., McCarley, R. W., & Greene, R. W. (1994) · Science · doi:10.1126/science.8303279 · Cited by 341 · see citing works
Self-citationWylen, D. G. L. V., Park, T. S., Rubio, R., & Berne, R. M. (1986) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1986.97 · Cited by 261 · see citing works
Cerebral O2 metabolism and cerebral blood flow in humans during deep and rapid-eye-movement sleep
Madsen, P. L., Schmidt, J. F., Wildschiødtz, G., Friberg, L., Holm, S., Vorstrup, S., & Lassen, N. A. (1991) · Journal of Applied Physiology · doi:10.1152/jappl.1991.70.6.2597 · Cited by 254 · see citing works
Jones, B. E. (1993) · Progress in brain research · doi:10.1016/s0079-6123(08)62381-x · Cited by 212 · see citing works
Caffeine reversal of sleep deprivation effects on alertness and mood
Penetar, D. M., McCann, U. D., Thorne, D., Kamimori, G. H., Galinski, C., Sing, H. C., Thomas, M., & Belenky, G. L. (1993) · Psychopharmacology · doi:10.1007/bf02244933 · Cited by 208 · see citing works
Winn, H. R., Welsh, J. E., Rubio, R., & Berne, R. M. (1980) · Circulation Research · doi:10.1161/01.res.47.4.568 · Cited by 200 · see citing works
Caffeine Reduces Low-Frequency Delta Activity in the Human Sleep EEG
Landolt, H. (1995) · Neuropsychopharmacology · doi:10.1016/0893-133x(94)00079-f · Cited by 198 · see citing works
Pull, I., & MCILWAIN, H. (1972) · Biochemical Journal · doi:10.1042/bj1260965 · Cited by 193 · see citing works
Huston, J. P., Haas, H. L., Boix, F., Pfister, M., Decking, U. K. M., Schrader, J., & Schwarting, R. K. W. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00021-8 · Cited by 184 · see citing works
Alkylxanthines elevate hippocampal excitability
Dunwiddie, T. V., Hoffer, B. J., & Fredholm, B. B. (1981) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00501365 · Cited by 175 · see citing works
Effects of caffeine on alertness
Zwyghuizen‐Doorenbos, A., Roehrs, T., Lipschutz, L., Timms, V., & Roth, T. G. (1990) · Psychopharmacology · doi:10.1007/bf02245786 · Cited by 173 · see citing works
Increase of adenosine content in cerebral cortex of the cat during bicuculline-induced seizure
Schrader, J., Wahl, M., Kuschinsky, W., et al. (1980) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00580977 · Cited by 126 · see citing works
Effects of N6-cyclopentyladenosine and caffeine on sleep regulation in the rat
Schwierin, B., Borbély, A. A., & Tobler, I. (1996) · European Journal of Pharmacology · doi:10.1016/0014-2999(96)00021-0 · Cited by 125 · see citing works
Craig, C. G., & White, T. D. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb03256.x · Cited by 117 · see citing works
Cerebral glucose utilization during stage 2 sleep in man
Maquet, P., Dive, D., Salmon, É., Sadzot, B., Franco, G., Poirrier, R., & Franck, G. (1992) · Brain Research · doi:10.1016/0006-8993(92)90522-b · Cited by 112 · see citing works
Brundege, J. M., & Dunwiddie, T. V. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-18-05603.1996 · Cited by 111 · see citing works
Homeostatic changes during post-nap sleep maintain baseline levels of delta EEG
Feinberg, I., March, J. D., Floyd, T. C., Jimison, R., Bossom-Demitrack, L., & Katz, P. H. (1985) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(85)91051-x · Cited by 106 · see citing works
Haas, L., & Greene, R. W. (1988) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00182732 · Cited by 99 · see citing works
Self-citationRole of adenosine in sleep in rats.
Radulovacki, M. G. (1985) · PubMed · Cited by 94 · see citing works
Worley, P. F., Baraban, J. M., McCarren, M., et al. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.10.3467 · Cited by 94 · see citing works
Rosenberg, P. A., Knowles, R., Knowles, K., & Li, Y. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-05-02953.1994 · Cited by 89 · see citing works
Gereau, R. W., & Conn, P. J. (1994) · Neuron · doi:10.1016/0896-6273(94)90319-0 · Cited by 87 · see citing works
de Sánchez, V. C., ̃oz, R. H.-M., ́rez, J. S., Vidrio, S., Yáñez, L., & ̃oz, M. D. ́. M. ́. (1993) · Brain Research · doi:10.1016/0006-8993(93)91651-8 · Cited by 77 · see citing works
Effects of caffeine on hippocampal pyramidal cells in vitro
Greene, R. W., Haas, H. L., & Hermann, A. (1985) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1985.tb08843.x · Cited by 65 · see citing works
Self-citationCerebral hypoxia in the pathogenesis of migraine
Rose, F. C., & Amery, W. K. (1982) · Pitman eBooks · Cited by 52 · see citing works
Plasma adenosine and hypoxemia in patients with sleep apnea
Findley, L. J., Boykin, M. P., Fallon, T., & Belardinelli, L. (1988) · Journal of Applied Physiology · doi:10.1152/jappl.1988.64.2.556 · Cited by 46 · see citing works
Wu, P. H., Barraco, R. A., & Phillis, J. W. (1984) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(84)90169-1 · Cited by 41 · see citing works
Shiromani, P. J., Winston, S. H., & McCarley, R. W. (1996) · Molecular Brain Research · doi:10.1016/0169-328x(95)00325-m · Cited by 41 · see citing works
Self-citationCraig, C. G., & White, T. D. (1992) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)11440-7 · Cited by 41 · see citing works
Sanderson, G., & Scholfield, C. N. (1986) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00582948 · Cited by 31 · see citing works
Padua, R. A., Geiger, J. D., Dambock, S., et al. (1990) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1990.tb01945.x · Cited by 21 · see citing works
Gu, J. G., & Geiger, J. D. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb10043.x · Cited by 21 · see citing works
MCILWAIN, H., & Poll, J. D. (1985) · Neurochemistry International · doi:10.1016/0197-0186(85)90014-2 · Cited by 19 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- [4]Radulovacki M. Rev Clin Basic Pharmacol. 1985;5:327. [PubMed] [Google Scholar]
- [8]Portas CM, Thakkar M, Rainnie DG, Greene RW, McCarley RW. Neuroscience. in press. This study also demonstrated a concentration-response relation over a four-log-unit concentration range between adenosine perfused into the cholinergic basal forebrain and the extent of reduction of wakefulness. [Google Scholar]
- [9]Ursin R, Sterman MB. A Manual for Standardized Scoring of Sleep and Waking States in the Adult Cat. Brain Information Service, Brain Research Institute, University of California; Los Angeles: 1981. EEG activation was scored in 20-s epochs. [Google Scholar]
- [20]de Sánchez VC, et al. Brain Res. 1993;612:115.Huston JP, et al. Neuroscience. 1996;73:99. doi: 10.1016/0306-4522(96)00021-8.Adenosine appears to have a tighter linkage to sleep after wakefulness than do other putative SWS factors [see review by Krueger JM, Fang J. In: Sleep and Sleep Disorders: From Molecule to Behavior. Hayaishi O, Inoue S, editors. Academic Press and Harcourt Brace; Tokyo, Japan: in press.] · DOI
Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Fredholm, B. B., Bättig, K., Holmén, J., Nehlig, A., & Zvartau, E. E. (1999) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01396-6 · Cited by 2,624 · see citing works
International Union of Pharmacology. XXV. Nomenclature and Classification of Adenosine Receptors
Fredholm, B. B., IJzerman, A. P., Jacobson, K. A., Klotz, K.-N., & Linden, J. (2001) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01511-4 · Cited by 2,585 · see citing works
The two‐process model of sleep regulation: a reappraisal
Borbély, A. A., Daan, S., Wirz‐Justice, A., & Deboer, T. (2016) · Journal of Sleep Research · doi:10.1111/jsr.12371 · Cited by 1,577 · see citing works
Behavioral and Physiological Consequences of Sleep Restriction
Banks, S., & Dinges, D. F. (2007) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.26918 · Cited by 1,505 · see citing works
Control of sleep and wakefulness
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E., & McCarley, R. W. (2012) · Physiological Reviews · doi:10.1152/physrev.00032.2011 · Cited by 1,477 · see citing works
Self-citationAdenosine Receptors as Therapeutic Targets
Jacobson, K. A., & Gao, Z.-G. (2006) · Nature Reviews Drug Discovery · doi:10.1038/nrd1983 · Cited by 1,431 · see citing works
Saper, C. B., Fuller, P. M., Pedersen, N. P., Lu, J., & Scammell, T. E. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.032 · Cited by 1,404 · see citing works
The sleep-deprived human brain
Krause, A. J., Simon, E. B., Mander, B. A., Greer, S. M., Saletin, J. M., Goldstein-Piekarski, A. N., & Walker, M. P. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.55 · Cited by 1,200 · see citing works
<i>Sleep Deprivation and Vigilant Attention</i>
Lim, J., & Dinges, D. F. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1417.002 · Cited by 1,213 · see citing works
Rest in Drosophila is a sleep-like state
Hendricks, J. C., Finn, S. M., Panckeri, K. A., Chavkin, J., Williams, J. A., Sehgal, A., & Pack, A. I. (2000) · Neuron · doi:10.1016/s0896-6273(00)80877-6 · Cited by 1,050 · see citing works
Neural Circuitry of Wakefulness and Sleep
Scammell, T. E., Arrigoni, E., & Lipton, J. O. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.014 · Cited by 966 · see citing works
The Neurobiology of Sleep: Genetics, cellular physiology and subcortical networks
Pace-Schott, E. F., & Hobson, J. A. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn895 · Cited by 937 · see citing works
Use of sleep hygiene in the treatment of insomnia
Stepanski, E. J., & Wyatt, J. K. (2003) · Sleep Medicine Reviews · doi:10.1053/smrv.2001.0246 · Cited by 733 · see citing works
Adenosine A2A, but not A1, receptors mediate the arousal effect of caffeine
Huang, Z.-L., Qu, W.-M., Eguchi, N., Chen, J.-F., Schwarzschild, M. A., Fredholm, B. B., Urade, Y., & Hayaishi, O. (2005) · Nature Neuroscience · doi:10.1038/nn1491 · Cited by 640 · see citing works
Role of Sleep and Sleep Loss in Hormonal Release and Metabolism
Leproult, R., & Van Cauter, E. (2010) · Endocrine Development · doi:10.1159/000262524 · Cited by 602 · see citing works
Altered brain response to verbal learning following sleep deprivation
Drummond, S. P. A., Brown, G. G., Gillin, J. C., Stricker, J. L., Wong, E. C., & Buxton, R. B. (2000) · Nature · doi:10.1038/35001068 · Cited by 557 · see citing works
Comorbidity of insomnia and depression
Staner, L. (2010) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2009.09.003 · Cited by 481 · see citing works
Circadian system, sleep and endocrinology
Morris, C. J., Aeschbach, D., & Scheer, F. A. J. L. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.09.003 · Cited by 403 · see citing works
Mathematical models of sleep regulation
Achermann, P. (2003) · Frontiers in Bioscience · doi:10.2741/1064 · Cited by 358 · see citing works
Biochemical regulation of non-rapid-eye-movement sleep
Krueger, J. M. (2003) · Frontiers in Bioscience · doi:10.2741/1033 · Cited by 329 · see citing works
The effect of caffeine on subsequent sleep: A systematic review and meta-analysis
Gardiner, C., Weakley, J., Burke, L. M., Roach, G. D., Sargent, C., Maniar, N., Townshend, A., & Halson, S. L. (2023) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2023.101764 · Cited by 315 · see citing works
“As homeostatic sleep pressure is suggested to increase with rising cerebral adenosine concentrations [14,63], the action of caffeine in blocking A1 and A2a receptors may reduce the propensity for sleep [64,65].”
BackgroundKreutzmann, J. C., Havekes, R., Abel, T., & Meerlo, P. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.053 · Cited by 309 · see citing works
<i>Hypothalamic Regulation of Sleep and Arousal</i>
Szymusiak, R., & McGinty, D. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1417.027 · Cited by 294 · see citing works
Sleep homeostasis: a role for adenosine in humans?
Landolt, H.-P. (2008) · Biochemical Pharmacology · doi:10.1016/j.bcp.2008.02.024 · Cited by 290 · see citing works
Schmidt, M. H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.08.001 · Cited by 291 · see citing works
Drugs as instruments: A new framework for non-addictive psychoactive drug use
Müller, C. P., & Schumann, G. (2011) · Behavioral and Brain Sciences · doi:10.1017/s0140525x11000057 · Cited by 286 · see citing works
Kong, J., Shepel, P. N., Holden, C. P., Mackiewicz, M., Pack, A. I., & Geiger, J. D. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05581.2002 · Cited by 281 · see citing works
Alcohol disrupts sleep homeostasis
Thakkar, M. M., Sharma, R., & Sahota, P. (2015) · Alcohol · doi:10.1016/j.alcohol.2014.07.019 · Cited by 262 · see citing works
Self-citationEvidence that sleep deprivation downregulates dopamine D2R in ventral striatum in the human brain
Volkow, N. D., Tomasi, D., Wang, G.-J., Telang, F., Fowler, J. S., Logan, J., Benveniste, H., Kim, R., Thanos, P. K., & Ferré, S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0045-12.2012 · Cited by 254 · see citing works
Unraveling the evolutionary determinants of sleep
Joiner, W. J. (2016) · Current Biology · doi:10.1016/j.cub.2016.08.068 · Cited by 232 · see citing works
Identification of a population of sleep-active cerebral cortex neurons
Gerashchenko, D., Wisor, J. P., Burns, D., Reh, R. K., Shiromani, P. J., Sakurai, T., de la Iglesia, H. O., & Kilduff, T. S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803125105 · Cited by 207 · see citing works
Circadian and wakefulness-sleep modulation of cognition in humans
Wright, K. P., Lowry, C. A., & LeBourgeois, M. K. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00050 · Cited by 209 · see citing works
The Neurobiology of Sleep and Wakefulness
Schwartz, M. D., & Kilduff, T. S. (2015) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2015.07.002 · Cited by 207 · see citing works
Prostaglandin D2 and sleep/wake regulation
Urade, Y., & Hayaishi, O. (2011) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2011.08.003 · Cited by 200 · see citing works
Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats
Guzmán‐Marín, R., Suntsova, N., Stewart, D. R., Gong, H., Szymusiak, R., & McGinty, D. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.041665 · Cited by 197 · see citing works
Sleep and wakefulness out of phase with internal biological time impairs learning in humans
Wright, K. P., Hull, J. T., Hughes, R. J., Ronda, J. M., & Czeisler, C. A. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.4.508 · Cited by 191 · see citing works
Adenosine, caffeine, and sleep–wake regulation: state of the science and perspectives
Reichert, C. F., Deboer, T., & Landolt, H. (2022) · Journal of Sleep Research · doi:10.1111/jsr.13597 · Cited by 183 · see citing works
“…came from the observations that extracellular adenosine levels in different brain areas in rats and cats tended to increase during wakefulness, decrease during sleep, and to be enhanced after prolonged wakefulness (Huston et al., 1996; Porkka-Heiskanen et al., 1997; Porkka-Heiskanen et al., 2000).”
BackgroundMethodInfluentialMechanisms of modafinil: A review of current research
Gerrard, P., & Malcolm, R. (2007) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.a911 · Cited by 160 · see citing works
Sleep, its regulation and possible mechanisms of sleep disturbances
Porkka‐Heiskanen, T., Zitting, K. ‐., & Wigren, H. ‐. (2013) · Acta Physiologica · doi:10.1111/apha.12134 · Cited by 157 · see citing works
Self-citationSleep Neurobiology for the Clinician
(2004) · Sleep · doi:10.1093/sleep/27.4.811 · Cited by 151 · see citing works
Evidence for Neuroinflammatory and Microglial Changes in the Cerebral Response to Sleep Loss
Wisor, J. P., Schmidt, M. A., & Clegern, W. C. (2011) · Sleep · doi:10.1093/sleep/34.3.261 · Cited by 141 · see citing works
Mascetti, G. G. (2016) · Nature and Science of Sleep · doi:10.2147/nss.s71970 · Cited by 119 · see citing works
Locus Ceruleus Control of Slow-Wave Homeostasis
Cirelli, C., Huber, R., Gopalakrishnan, A., Southard, T. L., & Tononi, G. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4845-04.2005 · Cited by 119 · see citing works
Caffeine Consumption and Sleep Quality in Australian Adults
Watson, E., Coates, A., Kohler, M., & Banks, S. (2016) · Nutrients · doi:10.3390/nu8080479 · Cited by 109 · see citing works
Sleep, vigilance, and thermosensitivity
Romeijn, N., Raymann, R. J. E. M., Møst, E., Te Lindert, B., Van Der Meijden, W. P., Fronczek, R., Gomez-Herrero, G., & Van Someren, E. J. W. (2012) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-011-1042-2 · Cited by 105 · see citing works
Photic Entrainment of the Circadian System
Ashton, A., Foster, R., & Jagannath, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020729 · Cited by 106 · see citing works
Neurobiological and Hormonal Mechanisms Regulating Women’s Sleep
Dorsey, A., de Lecea, L., & Jennings, K. J. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.625397 · Cited by 100 · see citing works
Sleep, circadian rhythms, and type 2 diabetes mellitus
Parameswaran, G., & Ray, D. W. (2022) · Clinical Endocrinology · doi:10.1111/cen.14607 · Cited by 85 · see citing works
Effects of caffeine on daytime recovery sleep: A double challenge to the sleep–wake cycle in aging
Carrier, J., Paquet, J., Fernandez-Bolanos, M., Girouard, L., Roy, J., Selmaoui, B., & Filipini, D. (2009) · Sleep Medicine · doi:10.1016/j.sleep.2009.01.001 · Cited by 82 · see citing works
The why and how of sleep-dependent synaptic down-selection
Cirelli, C., & Tononi, G. (2022) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2021.02.007 · Cited by 74 · see citing works
Animal Studies on the Role of Sleep in Memory: From Behavioral Performance to Molecular Mechanisms
Havekes, R., Meerlo, P., & Abel, T. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_369 · Cited by 78 · see citing works
What keeps us awake?–the role of clocks and hourglasses, light, and melatonin
Cajochen, C., Chellappa, S., & Schmidt, C. (2010) · International review of neurobiology · doi:10.1016/s0074-7742(10)93003-1 · Cited by 73 · see citing works
Sleepwalking, sleep terrors, sexsomnia and other disorders of arousal: the old and the new
Idir, Y., Oudiette, D., & Arnulf, I. (2022) · Journal of Sleep Research · doi:10.1111/jsr.13596 · Cited by 61 · see citing works
Mitochondrial origins of the pressure to sleep
Sarnataro, R., Velasco, C. D., Monaco, N., Kempf, A., & Miesenböck, G. (2025) · Nature · doi:10.1038/s41586-025-09261-y · Cited by 62 · see citing works
Takelle, G. M., Muluneh, N. Y., & Biresaw, M. S. (2022) · BMJ Open · doi:10.1136/bmjopen-2021-056564 · Cited by 35 · see citing works
Increased volatile anesthetic requirement in short-sleeping Drosophila mutants
Weber, B., Schaper, C., Bushey, D., Rohlfs, M., Steinfath, M., Tononi, G., Cirelli, C., Scholz, J., & Bein, B. (2009) · Anesthesiology · doi:10.1097/aln.0b013e3181942df2 · Cited by 26 · see citing works
Resetting intrinsic purinergic modulation of neural activity: an associative mechanism?
Dale, N. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-23-10461.2002 · Cited by 23 · see citing works
Silva, H., Del Coso, J., & Pickering, C. (2025) · Sports Medicine · doi:10.1007/s40279-025-02245-y · Cited by 21 · see citing works
- Authors
- Porkka-Heiskanen, T., Strecker, R. E., Thakkar, M., Bjørkum, A. A., Greene, R. W., & McCarley, R. W.
- Affiliations
- T. Porkka-Heiskanen, Department of Psychiatry, Harvard Medical School, Brockton Veterans Administration Medical Center (VAMC), 116 A, 940 Belmont Street, Brockton, MA 02401, USA, and Institute of Biomedicine, University of Helsinki, Helsinki, Finland.
- University of Helsinki (FI)
- Corresponding author
- McCarley, Robert W.
- Venue
- Science
- Published
- 1997-05-23
- Volume
- 276
- Issue
- 5316
- Pages
- 1265-1268
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3599777
- OpenAlex
- W2045815714
- Cited by
- 1,252
- References
- 37
- Citations by year
- 2026: 31 · 2025: 44 · 2024: 40 · 2023: 32 · 2022: 53 · 2021: 43 · 2020: 78 · 2019: 51 · 2018: 44 · 2017: 45 · 2016: 37 · 2015: 51 · 2014: 39 · 2013: 49 · 2012: 55
- FWCI
- 17.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- NORA - Norwegian Open Research Archives (submittedVersion, other-oa)
- Funders
- National Institute of Mental Health (R01MH039683, R37 MH39)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Keywords
- adenosine, sleep induction, prolonged wakefulness, arousal, basal forebrain cholinergic neurons, slow-wave sleep, recovery sleep, sleep-wake cycle, microdialysis, cats
- MeSH terms
- Adenosine, Animals, Cats, Electrophysiology, Sleep, Sleep Deprivation, Thioinosine, Time Factors, Wakefulness, Prosencephalon, Microdialysis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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