Orexin neurons are necessary for the circadian control of REM sleep

Sleep

Volumn 32, Issue 9, 2009, Pages 1127-1134

  Kantor, Sandor ^a   Mochizuki, Takatoshi ^a   Janisiewicz, Agnieszka M ^a   Clark, Erika ^a   Nishino, Seiji ^b   Scammell, Thomas E ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Ataxin 3; Body temperature; Cataplexy; Circadian rhythm; Constant darkness; Knock out; Narcolepsy; REM sleep; REM sleep latency; REM sleep propensity

Indexed keywords

ATAXIN 3; OREXIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BODY TEMPERATURE; CATAPLEXY; CIRCADIAN RHYTHM; CONTROLLED STUDY; EXPERIMENTAL MODEL; KNOCKOUT MOUSE; LOCOMOTION; MALE; MOUSE; NERVE CELL; NONHUMAN; NONREM SLEEP; PRIORITY JOURNAL; REM SLEEP; SIGNAL TRANSDUCTION; SLEEP WAKING CYCLE; WAKEFULNESS; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, TRANSGENIC; NEURONS; NEUROPEPTIDES; NEUROTRANSMITTER AGENTS; SLEEP, REM; WAKEFULNESS;

EID: 70349252024     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.1093/sleep/32.9.1127     Document Type: Article

References (60)

1. Dantz B, Edgar DM, Dement WC. Circadian rhythms in narcolepsy: studies on a 90 minute day. Electroencephalogr Clin Neurophysiol 1994;90:24-35. (Pubitemid 24057706)
2. Selbach O, Haas HL. Hypocretins: the timing of sleep and waking. Chronobiol Int 2006;23:63-70.
3. Broughton R, Krupa S, Boucher B, Rivers M, Mullington J. Impaired circadian waking arousal in narcolepsy-cataplexy. Sleep Res Online 1998;1:159-165
4. Lavie P. REM periodicity under ultrashort sleep/wake cycle in narcoleptic patients. Can J Psychol 1991;45:185-193
5. Mistlberger RE. Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res Brain Res Rev 2005;49:429-454
6. Edgar DM, Dement WC, Fuller CA. Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J Neurosci 1993;13:1065-1079
7. Mayer G, Hellmann F, Leonhard E, Meier-Ewert K. Circadian temperature and activity rhythms in unmedicated narcoleptic patients. Pharmacol Biochem Behav 1997;58:395-402. (Pubitemid 27394291)
8. Crocker A, Espana RA, Papadopoulou M, et al. Concomitant loss of dynorphin, NARP, and orexin in narcolepsy. Neurology 2005;65:1184-1188
9. Thannickal TC, Moore RY, Nienhuis R, et al. Reduced number of hypocretin neurons in human narcolepsy. Neuron 2000;27:469-474 (Pubitemid 30951849)
10. Peyron C, Faraco J, Rogers W, et al. A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat Med 2000;6:991-997
11. Abrahamson EE, Leak RK, Moore RY. The suprachiasmatic nucleus projects to posterior hypothalamic arousal systems. Neuroreport 2001;12:435-440
12. Lu J, Zhang YH, Chou TC, et al. Contrasting effects of ibotenate lesions of the paraventricular nucleus and subparaventricular zone on sleep-wake cycle and temperature regulation. J Neurosci 2001;21:4864-4874 (Pubitemid 32565644)
13. Chou TC, Scammell TE, Gooley JJ, Gaus SE, Saper CB, Lu J. Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J Neurosci 2003;23:10691-10702 (Pubitemid 37485283)
14. Deurveilher S, Semba K. Indirect projections from the suprachiasmatic nucleus to major arousal-promoting cell groups in rat: implications for the circadian control of behavioural state. Neuroscience 2005;130:165-183 (Pubitemid 39550423)
15. Peyron C, Tighe DK, van den Pol AN, et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 1998;18:9996-10015. (Pubitemid 28543775)
16. Aston-Jones G, Chen S, Zhu Y, Oshinsky ML. A neural circuit for circadian regulation of arousal. Nat Neurosci 2001;4:732-738 (Pubitemid 32595412)
17. Yoshida K, McCormack S, Espana RA, Crocker A, Scammell TE. Afferents to the orexin neurons of the rat brain. J Comp Neurol 2006;494:845-861 (Pubitemid 43054230)
18. Deboer T, Overeem S, Visser NA, et al. Convergence of circadian and sleep regulatory mechanisms on hypocretin-1. Neuroscience 2004;129:727-732 (Pubitemid 39487123)
19. Zhang S, Zeitzer JM, Yoshida Y, et al. Lesions of the suprachiasmatic nucleus eliminate the daily rhythm of hypocretin-1 release. Sleep 2004;27:619-627 (Pubitemid 38823358)
20. Yoshida Y, Fujiki N, Nakajima T, et al. Fluctuation of extracellular hypocretin-1 (orexin A) levels in the rat in relation to the light-dark cycle and sleep-wake activities. Eur J Neurosci 2001;14:1075-1081 (Pubitemid 35463751)
21. Gerashchenko D, Kohls MD, Greco M, et al. Hypocretin-2-saporin lesions of the lateral hypothalamus produce narcoleptic-like sleep behavior in the rat. J Neurosci 2001;21:7273-7283 (Pubitemid 32846974)
22. Chemelli RM, Willie JT, Sinton CM, et al. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 1999;98:437-451
23. Hara J, Beuckmann CT, Nambu T, et al. Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron 2001;30:345-354 (Pubitemid 32530580)
24. Chou TC, Lee CE, Lu J, et al. Orexin (hypocretin) neurons contain dynorphin. J Neurosci 2001;21:RC168.
25. Baumann CR, Clark EL, Pedersen NP, Hecht JL, Scammell TE. Do enteric neurons make hypocretin? Regul Pept 2008;147:1-3.
26. Mochizuki T, Crocker A, McCormack S, Yanagisawa M, Sakurai T, Scammell TE. Behavioral state instability in orexin knock-out mice. J Neurosci 2004;24:6291-6300 (Pubitemid 38944219)
27. Scammell TE, Willie JT, Guilleminault C, Siegel JM. A consensus definition of cataplexy in mouse models of narcolepsy. Sleep 2009;32:111-116
28. Fujiki N, Cheng T, Yoshino F, Nishino S. Specificity of direct transitions from wake to REM sleep in orexin/ataxin-3 narcoleptic mice. Sleep 2006;29:A225.
29. Espana RA, McCormack SL, Mochizuki T, Scammell TE. Running promotes wakefulness and increases cataplexy in orexin knockout mice. Sleep 2007;30:1417-1425 (Pubitemid 350036969)
30. Seroka CD, Johnson CE, Heideman PD. Variation in nocturnality and circadian activity rhythms between photoresponsive F344 and nonphotoresponsive Sprague Dawley rats. J Circ Rhythms 2008;6:8.
31. Landry GJ, Yamakawa GR, Mistlberger RE. Robust food anticipatory circadian rhythms in rats with complete ablation of the thalamic paraventricular nucleus. Brain Res 2007;1141:108-118
32. Zhang S, Zeitzer JM, Sakurai T, Nishino S, Mignot E. Sleep/wake fragmentation disrupts metabolism in a mouse model of narcolepsy. J Physiol 2007;581:649-663 (Pubitemid 46831762)
33. Vitaterna MH, King DP, Chang AM, et al. Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 1994;264:719-725
34. Zhang S, Lin L, Kaur S, et al. The development of hypocretin (orexin) deficiency in hypocretin/ataxin-3 transgenic rats. Neuroscience 2007;148:34-43. (Pubitemid 47211625)
35. Beuckmann CT, Sinton CM, Williams SC, et al. Expression of a poly-glutamine-ataxin-3 transgene in orexin neurons induces narcolepsy-cataplexy in the rat. J Neurosci 2004;24:4469-4477 (Pubitemid 38608158)
36. Deboer T, Ruijgrok G, Meijer JH. Short light-dark cycles affect sleep in mice. Eur J Neurosci 2007;26:3518-3523 (Pubitemid 350243535)
37. Miller AM, Obermeyer WH, Behan M, Benca RM. The superior colliculus-pretectum mediates the direct effects of light on sleep. Proc Natl Acad Sci U S A 1998;95:8957-8962 (Pubitemid 28350596)
38. Beersma DG, Dijk DJ, Blok CG, Everhardus I. REM sleep deprivation during 5 hours leads to an immediate REM sleep rebound and to suppression of non-REM sleep intensity. Electroencephalogr Clin Neurophysiol 1990;76:114-122 (Pubitemid 20254881)
39. Benington JH, Heller HC. REM-sleep timing is controlled homeostatically by accumulation of REM-sleep propensity in non- REM sleep. Am J Physiol 1994;266:R1992-2000.
40. Endo T, Schwierin B, Borbely AA, Tobler I. Selective and total sleep deprivation: effect on the sleep EEG in the rat. Psychiatry Res 1997;66:97-110. (Pubitemid 27085356)
41. Shea JL, Mochizuki T, Sagvaag V, Aspevik T, Bjorkum AA, Datta S. Rapid eye movement (REM) sleep homeostatic regulatory processes in the rat: changes in the sleep-wake stages and electroencephalographic power spectra. Brain Res 2008;1213:48-56.
42. Dijk DJ, Czeisler CA. Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans. J Neurosci 1995;15:3526-3538
43. Wurts SW, Edgar DM. Circadian and homeostatic control of rapid eye movement (REM) sleep: promotion of REM tendency by the suprachiasmatic nucleus. J Neurosci 2000;20:4300-4310
44. Carskadon MA, Dement WC. Sleepiness and sleep state on a 90-min schedule. Psychophysiology 1977;14:127-133
45. Estabrooke IV, McCarthy MT, Ko E, et al. Fos expression in orexin neurons varies with behavioral state. J Neurosci 2001;21:1656-1662 (Pubitemid 32182206)
46. Lee MG, Hassani OK, Jones BE. Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. J Neurosci 2005;25:6716-6720
47. Mileykovskiy BY, Kiyashchenko LI, Siegel JM. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 2005;46:787-798
48. Takahashi K, Lin JS, Sakai K. Neuronal activity of orexin and non-orexin waking-active neurons during wake-sleep states in the mouse. Neuroscience 2008;153:860-870
49. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 2007;450:420-424 (Pubitemid 350126754)
50. Eriksson KS, Sergeeva OA, Selbach O, Haas HL. Orexin (hypocretin)/ dynorphin neurons control GABAergic inputs to tuberomammillary neurons. Eur J Neurosci 2004;19:1278-1284 (Pubitemid 38387204)
51. Lu J, Sherman D, Devor M, Saper CB. A putative flip-flop switch for control of REM sleep. Nature 2006;441:589-594 (Pubitemid 43927285)
52. Fuller PM, Saper CB, Lu J. The pontine REM switch: past and present. J Physiol 2007;584:735-741 (Pubitemid 350031919)
53. McCarley RW. Neurobiology of REM and NREM sleep. Sleep Med 2007;8:302-330
54. Thorpe AJ, Kotz CM. Orexin A in the nucleus accumbens stimulates feeding and locomotor activity. Brain Res 2005;1050:156-162
55. Shirasaka T, Nakazato M, Matsukura S, Takasaki M, Kannan H. Sympathetic and cardiovascular actions of orexins in conscious rats. Am J Physiol 1999;277:R1780-5. (Pubitemid 30043787)
56. Harris GC, Wimmer M, Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 2005;437:556-559 (Pubitemid 41613553)
57. Boutrel B, Kenny PJ, Specio SE, et al. Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc Natl Acad Sci U S A 2005;102:19168-19173 (Pubitemid 43049584)
58. Lubkin M, Stricker-Krongrad A. Independent feeding and metabolic actions of orexins in mice. Biochem Biophys Res Commun 1998;253:241-245 (Pubitemid 29026688)
59. Scammell TE. Wakefulness: an eye-opening perspective on orexin neurons. Curr Biol 2001;11:R769-71.
60. Sakurai T. The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 2007;8:171-181 (Pubitemid 46294664)