Lack of hypocretin attenuates behavioral changes produced by glutamatergic activation of the perifornical-lateral hypothalamic Area

Sleep

Volumn 37, Issue 5, 2014, Pages 1011-1020

  Kostin, Andrey ^a   Siegel, Jerome M ^a,b   Alam, Md Noor ^a,c  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dorsomedial hypothalamus; Hypocretin; Lateral hypothalamus; N methyl D Aspartate; Orexin; Perifornical area; Prepro orexin knockout; Sleep

Indexed keywords

GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; OREXIN; N METHYLASPARTIC ACID; NEUROPEPTIDE; OREXINS; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AROUSAL; ARTICLE; BEHAVIOR CHANGE; BRAIN FORNIX; CATAPLEXY; CONTROLLED STUDY; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; ELECTROENCEPHALOGRAM; ELECTROMYOGRAM; KNOCKOUT MOUSE; LATERAL HYPOTHALAMUS; MALE; MICRODIALYSIS; MOUSE; MUSCLE TONE; NONHUMAN; NONREM SLEEP; PERIFORNICAL AREA; PRIORITY JOURNAL; REM SLEEP; SIGNAL TRANSDUCTION; SLEEP PARAMETERS; SLEEP WAKING CYCLE; WAKEFULNESS; WILD TYPE; ANIMAL; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; METABOLISM; NARCOLEPSY; NERVE CELL; PHYSIOLOGY; SLEEP;

ANIMALS; AROUSAL; GLUTAMIC ACID; HYPOTHALAMIC AREA, LATERAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, KNOCKOUT; N-METHYLASPARTATE; NARCOLEPSY; NEURONS; NEUROPEPTIDES; SLEEP; WAKEFULNESS;

EID: 84899685471     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.5665/sleep.3680     Document Type: Article

References (55)

1. Alam MN, Szymusiak R, McGinty D. Hypocretinergic system: role in REM-sleep regulation. In: Mallick BN, Pandi-Perumal SR, McCarley R, Morrison AR, eds. Rapid eye movement sleep: Cambridge University Press, 2011:234-46
2. Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW. Control of sleep and wakefulness. Physiol Rev 2012;92:1087-187
3. Datta S. Cellular and chemical neuroscience of mammalian sleep. Sleep Med 2010;11:431-40
4. Siegel JM. The neurobiology of sleep. Semin Neurol 2009;29:277-96
5. de Lecea L, Kilduff TS, Peyron C, et al. The hypocretins: hypothalamusspecific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 1998;95:322-7
6. 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
7. Sakurai T, Amemiya A, Ishii M, et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998;92:573-85
8. Ohno K, Sakurai T. Orexin neuronal circuitry: role in the regulation of sleep and wakefulness. Front Neuroendocrinol 2008;29:70-87
9. Takahashi K, Lin JS, Sakai K. Neuronal activity of orexin and nonorexin waking-Active neurons during wake-sleep states in the mouse. Neuroscience 2008;153:860-70
10. Mileykovskiy BY, Kiyashchenko LI, Siegel JM. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 2005;46:787-98
11. Lee MG, Hassani OK, Jones BE. Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. J Neurosci 2005;25:6716-20
12. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 2007;450:420-4
13. Tsunematsu T, Kilduff TS, Boyden ES, Takahashi S, Tominaga M, Yamanaka A. Acute optogenetic silencing of orexin/hypocretin neurons induces slow-wave sleep in mice. J Neurosci 2011;31:10529-39
14. 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;6:991-7
15. Thannickal TC, Moore RY, Nienhuis R, et al. Reduced number of hypocretin neurons in human narcolepsy. Neuron 2000;27:469-74
16. Lin L, Faraco J, Li R, et al. The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 1999;98:365-76
17. Nishino S. The hypothalamic peptidergic system, hypocretin/orexin and vigilance control. Neuropeptides 2007;41:117-33
18. Anaclet C, Parmentier R, Ouk K, et al. Orexin/hypocretin and histamine: distinct roles in the control of wakefulness demonstrated using knock-out mouse models. J Neurosci 2009;29:14423-38
19. Yoshida K, McCormack S, Espana RA, Crocker A, Scammell TE. Afferents to the orexin neurons of the rat brain. J Comp Neurol 2006;494:845-61
20. Methippara MM, Alam MN, Szymusiak R, McGinty D. Effects of lateral preoptic area application of orexin-A on sleep-wakefulness. Neuroreport 2000;11:3423-6
21. Thakkar MM, Ramesh V, Strecker RE, McCarley RW. Microdialysis perfusion of orexin-A in the basal forebrain increases wakefulness in freely behaving rats. Arch Ital Biol 2001;139:313-28
22. Abrahamson EE, Moore RY. The posterior hypothalamic area: chemoarchitecture and afferent connections. Brain Res 2001;889:1-22
23. Henny P, Jones BE. Innervation of orexin/hypocretin neurons by GABAergic, glutamatergic or cholinergic basal forebrain terminals evidenced by immunostaining for presynaptic vesicular transporter and postsynaptic scaffolding proteins. J Comp Neurol 2006;499:645-61
24. Niu JG, Yokota S, Tsumori T, Qin Y, Yasui Y. Glutamatergic lateral parabrachial neurons innervate orexin-containing hypothalamic neurons in the rat. Brain Res;1358:110-22
25. 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;23:10691-702
26. Alam MA, Mallick BN. Glutamic acid stimulation of the perifornicallateral hypothalamic area promotes arousal and inhibits non-REM/REM sleep. Neurosci Lett 2008;439:281-6
27. Li FW, Deurveilher S, Semba K. Behavioural and neuronal activation after microinjections of AMPA and NMDA into the perifornical lateral hypothalamus in rats. Behav Brain Res 2011;224:376-86
28. Khan AM, Curras MC, Dao J, et al. Lateral hypothalamic NMDA receptor subunits NR2A and/or NR2B mediate eating: immunochemical/ behavioral evidence. Am J Physiol 1999;276:R880-91
29. Eyigor O, Centers A, Jennes L. Distribution of ionotropic glutamate receptor subunit mRNAs in the rat hypothalamus. J Comp Neurol 2001;434:101-24
30. Henny P, Brischoux F, Mainville L, Stroh T, Jones BE. Immunohistochemical evidence for synaptic release of glutamate from orexin terminals in the locus coeruleus. Neuroscience 2010;169:1150-7
31. Rosin DL, Weston MC, Sevigny CP, Stornetta RL, Guyenet PG. Hypothalamic orexin (hypocretin) neurons express vesicular glutamate transporters VGLUT1 or VGLUT2. J Comp Neurol 2003;465:593-603
32. Torrealba F, Yanagisawa M, Saper CB. Colocalization of orexin a and glutamate immunoreactivity in axon terminals in the tuberomammillary nucleus in rats. Neuroscience 2003;119:1033-44
33. John J, Ramanathan L, Siegel JM. Rapid changes in glutamate levels in the posterior hypothalamus across sleep-wake states in freely behaving rats. Am J Physiol Regul Integr Comp Physiol 2008;295:R2041-9
34. Li Y, Gao XB, Sakurai T, van den Pol AN. Hypocretin/Orexin excites hypocretin neurons via a local glutamate neuron-A potential mechanism for orchestrating the hypothalamic arousal system. Neuron 2002;36:1169-81
35. Chemelli RM, Willie JT, Sinton CM, et al. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 1999;98:437-51
36. Kayaba Y, Nakamura A, Kasuya Y, et al. Attenuated defense response and low basal blood pressure in orexin knockout mice. Am J Physiol Regul Integr Comp Physiol 2003;285:R581-93
37. Paxinos G, Franklin KJ. The mouse brain in stereotaxic coordinates. Second ed. San Diego: Academic Press, 2001
38. Espana RA, Valentino RJ, Berridge CW. Fos immunoreactivity in hypocretin-synthesizing and hypocretin-1 receptor-expressing neurons: effects of diurnal and nocturnal spontaneous waking, stress and hypocretin-1 administration. Neuroscience 2003;121:201-17
39. Estabrooke IV, McCarthy MT, Ko E, et al. Fos expression in orexin neurons varies with behavioral state. J Neurosci 2001;21:1656-62
40. Kumar S, Szymusiak R, Bashir T, Rai S, McGinty D, Alam MN. Effects of serotonin on perifornical-lateral hypothalamic area neurons in rat. Eur J Neurosci 2007;25:201-12
41. Alam MN, Kumar S, Bashir T, et al. GABA-mediated control of hypocretin- but not melanin-concentrating hormone-immunoreactive neurones during sleep in rats. J Physiol 2005;563:569-82
42. Franken P, Malafosse A, Tafti M. Genetic determinants of sleep regulation in inbred mice. Sleep 1999;22:155-69
43. Scammell TE, Willie JT, Guilleminault C, Siegel JM. A consensus definition of cataplexy in mouse models of narcolepsy. Sleep 2009;32:111-6
44. Quan N, Blatteis CM. Microdialysis: a system for localized drug delivery into the brain. Brain Res Bull 1989;22:621-5
45. Hassani OK, Henny P, Lee MG, Jones BE. GABAergic neurons intermingled with orexin and MCH neurons in the lateral hypothalamus discharge maximally during sleep. Eur J Neurosci 2010;32:448-57
46. Hassani OK, Lee MG, Jones BE. Melanin-concentrating hormone neurons discharge in a reciprocal manner to orexin neurons across the sleep-wake cycle. Proc Natl Acad Sci U S A 2009;106:2418-22
47. Konadhode RR, Pelluru D, Blanco-Centurion C, et al. Optogenetic stimulation of MCH neurons increases sleep. J Neurosci 2013;33:10257-63
48. Alam MN, Gong H, Alam T, Jaganath R, McGinty D, Szymusiak R. Sleepwaking discharge patterns of neurons recorded in the rat perifornical lateral hypothalamic area. J Physiol 2002;538:619-31
49. Luppi PH, Clement O, Fort P. Paradoxical (REM) sleep genesis by the brainstem is under hypothalamic control. Curr Opin Neurobiol 2013;23:786-92
50. Martins PJ, DAlmeida V, Pedrazzoli M, Lin L, Mignot E, Tufik S. Increased hypocretin-1 (orexin-A) levels in cerebrospinal fluid of rats after short-term forced activity. Regul Pept 2004;117:155-8
51. Mieda M, Willie JT, Hara J, Sinton CM, Sakurai T, Yanagisawa M. Orexin peptides prevent cataplexy and improve wakefulness in an orexin neuron-Ablated model of narcolepsy in mice. Proc Natl Acad Sci U S A 2004;101:4649-54
52. Rai S, Kumar S, Alam MA, Szymusiak R, McGinty D, Alam MN. A1 receptor mediated adenosinergic regulation of perifornical-lateral hypothalamic area neurons in freely behaving rats. Neuroscience 2010;167:40-8
53. Chou TC, Lee CE, Lu J, et al. Orexin (hypocretin) neurons contain dynorphin. J Neurosci 2001;21:RC168
54. Blouin AM, Thannickal TC, Worley PF, Baraban JM, Reti IM, Siegel JM. Narp immunostaining of human hypocretin (orexin) neurons: loss in narcolepsy. Neurology 2005;65:1189-92
55. Eriksson KS, Sergeeva OA, Selbach O, Haas HL. Orexin (hypocretin)/ dynorphin neurons control GABAergic inputs to tuberomammillary neurons. Eur J Neurosci 2004;19:1278-84