Experience-dependent plasticity in hypocretin/orexin neurones: Re-setting arousal threshold

Acta Physiologica

Volumn 198, Issue 3, 2010, Pages 251-262

  Gao, X B ^a   Wang, A H ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b URSINUS COLLEGE   (United States)

Author keywords

Energy homeostasis; Lateral hypothalamus; Sleep regulation; Synaptic transmission

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; CORTICOTROPIN RELEASING FACTOR; DOPAMINE 1 RECEPTOR; DOPAMINE RECEPTOR; FORSKOLIN; GLUTAMIC ACID; LEPTIN; MODAFINIL; NEUROTRANSMITTER; OREXIN; PROTEIN C FOS; PROTIRELIN;

ACTION POTENTIAL; ADDICTION; ANIMAL BEHAVIOR; AROUSAL; BRAIN REGION; CONFERENCE PAPER; DARKNESS; DIET RESTRICTION; ENVIRONMENTAL FACTOR; FORAGING; HORMONE ACTION; HORMONE RELEASE; HORMONE SYNTHESIS; HUMAN; HYPOTHALAMUS; INNERVATION; LONG TERM POTENTIATION; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSYCHOLOGICAL ASPECT; REM SLEEP; SLEEP DEPRIVATION; SLOW WAVE SLEEP; SURVIVAL; WAKEFULNESS; WITHDRAWAL SYNDROME;

ANIMALS; AROUSAL; BEHAVIOR; DIFFERENTIAL THRESHOLD; HUMANS; HYPOTHALAMUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NEURONAL PLASTICITY; NEURONS; NEUROPEPTIDES; NEUROTRANSMITTER AGENTS; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; SLEEP; SYNAPTIC TRANSMISSION; WAKEFULNESS;

EID: 75749137704     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2009.02047.x     Document Type: Conference Paper

References (78)

1. Adamantidis, A. de Lecea, L. 2009. The hypocretins as sensors for metabolism and arousal. J Physiol 587, 33 40.
2. Adamantidis, A.R., Zhang, F., Aravanis, A.M., Deisseroth, K. de Lecea, L. 2007. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450, 420 424.
3. Arrieta-Cruz, I. Pfaff, D.W. 2009. Definition of arousal and mechanistic studies in intact and brain-damaged mice. Ann N Y Acad Sci 1157, 24 31.
4. Ballon, J.S. Feifel, D. 2006. A systematic review of modafinil: potential clinical uses and mechanisms of action. J Clin Psychiatry 67, 554 566.
5. Berridge, C.W. 2008. Noradrenergic modulation of arousal. Brain Res Rev 58, 1 17.
6. Blundon, J.A. Zakharenko, S.S. 2008. Dissecting the components of long-term potentiation. Neuroscientist 14, 598 608.
7. Borbély, A.A. 1977. Sleep in the rat during food deprivation and subsequent restitution of food. Brain Res 124, 457 471.
8. Boutrel, B., Kenny, P.J., Specio, S.E., Martin-Fardon, R., Markou, A., Koob, G.F. de Lecea, L. 2005. Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc Natl Acad Sci USA 102, 19168 19173.
9. + channels mediate inhibition of orexin neurons by glucose. Neuron 50, 711 722.
10. Cirelli, C., Gutierrez, C.M. Tononi, G. 2004. Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron. 41, 35 43.
11. Diano, S., Horvath, B., Urbanski, H.F., Sotonyi, P. Horvath, T.L. 2003. Fasting activates the nonhuman primate hypocretin (orexin) system and its postsynaptic targets. Endocrinology 144, 3774 3778.
12. Douglas, R., Markram, H. Martin, K. 2004. Neocortex. In : G.M. Shepherd (ed The Synaptic Organization of the Brain, pp. 499 558. Oxford University Press, New York.
13. Estabrooke, I.V., McCarthy, M.T., Ko, E., Chou, T.C., Chemelli, R.M., Yanagisawa, M., Saper, C.B. Scammell, T.E. 2001. Fos expression in orexin neurons varies with behavioral state. J Neurosci 21, 1656 1662.
14. Flavell, S.W. Greenberg, M.E. 2008. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 31, 563 590.
15. Frey, U., Huang, Y.Y. Kandel, E.R. 1993. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260, 1661 1664.
16. Fujiki, N., Yoshida, Y., Ripley, B., Honda, K., Mignot, E. Nishino, S. 2001. Changes in CSF hypocretin-1 (orexin A) levels in rats across 24 hours and in response to food deprivation. Neuroreport 17, 993 997.
17. Gao, X.B. 2009. Electrophysiological effects of MCH on neurons in the hypothalamus. Peptides. May 20. [Epub ahead of print] PubMed PMID: 19463877.
18. González, J.A., Horjales-Araujo, E., Fugger, L., Broberger, C. Burdakov, D. 2009. Stimulation of orexin/hypocretin neurones by thyrotropin-releasing hormone. J Physiol 587, 1179 1186.
19. Griffith, L.C. Rosbash, M. 2008. Sleep: hitting the reset button. Nat Neurosci 11, 123 124.
20. Guyon, A., Tardy, M.P., Rovère, C., Nahon, J.L., Barhanin, J. Lesage, F. 2009. Glucose inhibition persists in hypothalamic neurons lacking tandem-pore K+ channels. J Neurosci 29, 2528 2533.
21. Hara, J., Gerashchenko, D., Wisor, J.P., Sakurai, T., Xie, X. Kilduff, T.S. 2009. Thyrotropin-releasing hormone increases behavioral arousal through modulation of hypocretin/orexin neurons. J Neurosci 29, 3705 3714.
22. Harris, G.C., Wimmer, M. Aston-Jones, G. 2005. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437, 556 559.
23. Hebb, D.O. 1949. The Organization of Behavior. Wiley, New York.
24. Henny, P. Jones, B.E. 2006. 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 499, 645 661.
25. Horvath, T.L. Gao, X.B. 2005. Input organization and plasticity of hypocretin neurons: possible clues to obesity's association with insomnia. Cell Metab 1, 279 286.
26. Huang, Y.Y. Kandel, E.R. 1995. D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci USA 92, 2446 2450.
27. Hyman, S. E., Malenka, R. C. Nestler, E. J. 2006. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29, 565 598.
28. Jacobs, B.L. McGinty, D.J. 1971. Effects of food deprivation on sleep and wakefulness in the rat. Exp Neurol 30, 212 222.
29. Jones, B.E. 2008. Modulation of cortical activation and behavioral arousal by cholinergic and orexinergic systems. Ann N Y Acad Sci 1129, 26 34.
30. Kessels, H.W. Malinow, R. 2009. Synaptic AMPA receptor plasticity and behavior. Neuron 61, 340 350.
31. Kim, Y., Laposky, A.D., Bergmann, B.M. Turek, F.W. 2007. Repeated sleep restriction in rats leads to homeostatic and allostatic responses during recovery sleep. Proc Natl Acad Sci USA 104, 10697 10702.
32. Kopp, C., Longordo, F. Luthi, A. 2007. Experience-dependent changes in NMDA receptor composition at mature central synapses. Neuropharmacology 53, 1 9.
33. Korotkova, T.M., Klyuch, B.P., Ponomarenko, A.A., Lin, J.S., Haas, H.L. Sergeeva, O.A. 2007. Modafinil inhibits rat midbrain dopaminergic neurons through D2-like receptors. Neuropharmacology 52, 626 633.
34. de Lecea, L., Kilduff, T.S., Peyron, C., Gao, X., Foye, P.E., Danielson, P.E., Fukuhara, C., Battenberg, E.L., Gautvik, V.T., Bartlett, F.S., 2nd., Frankel, W.N., van den Pol, A.N., Bloom, F.E., Gautvik, K.M. Sutcliffe, J.G. 1998. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95, 322 327.
35. Lee, M.G., Hassani, O.K. Jones, B.E. 2005. Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. J Neurosci 25, 6716 6720.
36. Li, Y., Gao, X.-B., Sakurai, T. van den Pol, A.N. 2002. Hypocretin/orexin excites hypocretin neurons via a local glutamate neuron - a potential mechanism for orchestrating the hypothalamic arousal system. Neuron 36, 1169 1181.
37. Lin, J.S., Sakai, K., Vanni-Mercier, G. Jouvet, M. 1989. A critical role of the posterior hypothalamus in the mechanisms of wakefulness determined by microinjection of muscimol in freely moving cats. Brain Res 479, 225 240.
38. Lisman, J. Raghavachari, S. 2006. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE 356, re11.
39. Malenka, R.C. Bear, M.F. 2004. LTP and LTD: an embarrassment of riches. Neuron 44, 5 21.
40. Marsh, D.J., Weingarth, D.T., Novi, D.E., Chen, H.Y., Trumbauer, M.E., Chen, A.S., Guan, X.M., Jiang, M.M., Feng, Y., Camacho, R.E. et al. 2002. Melanin-concentrating hormone 1 receptor-deficient mice are lean, hyperactive, and hyperphagic and have altered metabolism. Proc Natl Acad Sci USA 99, 3240 3245.
41. McNaughton, B.L., Barnes, C.A., Rao, G., Baldwin, J. Rasmussen, M. 1986. Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information. J Neurosci 6, 563 571.
42. Mileykovskiy, B.Y., Kiyashchenko, L.I. Siegel, J.M. 2005. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46, 787 798.
43. Modirrousta, M., Mainville, L. Jones, B.E. 2005. Orexin and MCH neurons express c-Fos differently after sleep deprivation vs. recovery and bear different adrenergic receptors. Eur J Neurosci 21, 2807 2816.
44. Nauta, W.J.H. 1946. Hypothalamic regulation of sleep in rats: an experimental study. J Neurophysiol 9, 285 316.
45. Otmakhov, N., Khibnik, L., Otmakhova, N., Carpenter, S., Riahi, S., Asrican, B. Lisman, J. 2004. Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J Neurophysiol 91, 1955 1962.
46. Pinto, S., Roseberry, A.G., Liu, H., Diano, S., Shanabrough, M., Cai, X., Friedman, J.M. Horvath, T.L. 2004. Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304, 110 115.
47. van den Pol, A.N., Wuarin, J.P. Dudek, F.E. 1990. Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. Science 250, 1276 1278.
48. Ranson, S.W. 1939. Somnolence caused by hypothalamic lesions in the monkey. Arch. Neurol. Psychiatry 41, 1 23.
49. Rao, Y., Liu, Z.W., Borok, E., Rabenstein, R.L., Shanabrough, M., Lu, M., Picciotto, M.R., Horvath, T.L. Gao, X.B. 2007. Prolonged wakefulness induces experience-dependent synaptic plasticity in mouse hypocretin/orexin neurons. J Clin Invest 117, 4022 4033.
50. Rao, Y., Lu, M., Ge, F., Marsh, D.J., Qian, S., Wang, A.H., Picciotto, M.R. Gao, X.B. 2008. Regulation of synaptic efficacy in hypocretin/orexin- containing neurons by melanin concentrating hormone in the lateral hypothalamus. J Neurosci 28, 9101 9110.
51. Ribeiro, A.C., Sawa, E., Carren-LeSauter, I., LeSauter, J., Silver, R. Pfaff, D.W. 2007. Two forces for arousal: pitting hunger versus circadian influences and identifying neurons responsible for changes in behavioral arousal. Proc Natl Acad Sci USA 104, 20078 20083.
52. Rioult-Pedotti, M.S., Friedman, F. Donoghue, J.P. 2000. Learning-induced LTP in neocortex. Science 290, 533 536.
53. Sakurai, T. 2007. The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 8, 171 181.
54. Sakurai, T., Amemiya, A., Ishii, M., Matsuzaki, I., Chemelli, R.M., Tanaka, H., Williams, S.C., Richardson, J.A., Kozlowski, G.P., Wilson, S. et al. 1998. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573 585.
55. Sakurai, T., Nagata, R., Yamanaka, A., Kawamura, H., Tsujino, N., Muraki, Y., Kageyama, H., Kunita, S., Takahashi, S., Goto, K., Koyama, Y., Shioda, S. Yanagisawa, M. 2005. Input of orexin/hypocretin neurons revealed by a genetically encoded tracer in mice. Neuron 46, 297 308.
56. Saper, C.B., Scammell, T.E. Lu, J. 2005. Hypothalamic regulation of sleep and circadian rhythms. Nature 437, 1257 1263. (Pubitemid 41568665)
57. Scammell, T.E., Estabrooke, I.V., McCarthy, M.T., Chemelli, R.M., Yanagisawa, M., Miller, M.S. Saper, C.B. 2000. Hypothalamic arousal regions are activated during modafinil-induced wakefulness. J Neurosci 20, 8620 8628.
58. Selbach, O. Haas, H.L. 2006. Hypocretins: the timing of sleep and waking. Chronobiol Int 23, 63 70.
59. Selbach, O., Doreulee, N., Bohla, C., Eriksson, K.S., Sergeeva, O.A., Poelchen, W., Brown, R.E. Haas, H.L. 2004. Orexins/hypocretins cause sharp wave- and theta-related synaptic plasticity in the hippocampus via glutamatergic, gabaergic, noradrenergic, and cholinergic signaling. Neuroscience 127, 519 528.
60. Sutcliffe, J.G. de Lecea, L. 2002. The hypocretins: setting the arousal threshold. Nat Rev Neurosci. 3, 339 349.
61. Swett, C. Hobson, J. 1968. The effects of posterior hypothalamic lesions on behavioral and electrographic manifestations of sleep and waking in cats. Arch Ital Biol 106, 270 282.
62. Szymusiak, R. McGinty, D. 2008. Hypothalamic regulation of sleep and arousal. Ann N Y Acad Sc 1129, 275 286.
63. Terao, A., Wisor, J.P., Peyron, C., Apte-Deshpande, A., Wurts, S.W., Edgar, D.M. Kilduff, T.S. 2006. Gene expression in the rat brain during sleep deprivation and recovery sleep: an Affymetrix GeneChip study. Neuroscience 137, 593 605.
64. Tononi, G. Cirelli, C. 2007. Staying awake puts pressure on brain arousal systems. J Clin Invest 117, 3648 3650.
65. Von Economo, C. 1930. Sleep as a problem of localization. J Nerv Ment Dis 71, 249 259.
66. Vyazovskiy, V.V., 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.
67. Waites, C.L., Craig, A.M. Garner, C.C. 2005. Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci 28, 251 274.
68. Webb, I.C., Patton, D.F., Hamson, D.K. Mistlberger, R.E. 2008. Neural correlates of arousal-induced circadian clock resetting: hypocretin/orexin and the intergeniculate leaflet. Eur J Neurosci 27, 828 835.
69. Whitlock, J.R., Heynen, A.J., Shuler, M.G. Bear, M.F. 2006. Learning induces long-term potentiation in the hippocampus. Science 313, 1093 1097.
70. Winsky-Sommerer, R., Yamanaka, A., Diano, S., Borok, E., Roberts, A.J., Sakurai, T., Kilduff, T.S., Horvath, T.L. de Lecea, L. 2004. Interaction between the corticotropin-releasing factor system and hypocretins (orexins): a novel circuit mediating stress response. J Neurosci 24, 11439 11448.
71. Wisor, J.P., Nishino, S., Sora, I., Uhl, G.H., Mignot, E. Edgar, D.M. 2001. Dopaminergic role in stimulant-induced wakefulness. J Neurosci 21, 1787 1794.
72. Xie, X., Crowder, T.L., Yamanaka, A., Morairty, S.R., Lewinter, R.D., Sakurai, T. Kilduff, T.S. 2006. GABA(B) receptor-mediated modulation of hypocretin/orexin neurones in mouse hypothalamus. J Physiol 574, 399 414.
73. Yamanaka, A., Beuckmann, C.T., Willie, J.T., Hara, J., Tsujino, N., Mieda, M., Tominaga, M., Yagami, K., Sugiyama, F., Goto, K., Yanagisawa, M. Sakurai, T. 2003. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 38, 701 713.
74. Yin, H.H. Knowlton, B.J. 2006. The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 7, 464 476.
75. Yoshida, Y., Fujiki, N., Nakajima, T., Ripley, B., Matsumura, H., Yoneda, H., Mignot, E. Nishino, S. 2001. 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 14, 1075 1081.
76. Yoshida, K., McCormack, S., Espana, R.A., Crocker, A. Scammell, T.E. 2006. Afferents to the orexin neurons of the rat brain. J Comp Neurol 494, 845 861.
77. Zeitzer, J.M., Buckmaster, C.L, Parker, K.J., Hauck, C. M., Lyons, D.M. Mignot, E. 2003. Circadian and homeostatic regulation of hypocretin in a primate model: implications for the consolidation of wakefulness. J Neurosci 23, 3555 3560.
78. Ziemann, U., Ilic, T.V., Pauli, C., Meintzschel, F. Ruge, D. 2004. Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 24, 1666 1672.