Orexin Signaling Via the Orexin 1 Receptor Mediates Operant Responding for Food Reinforcement

Biological Psychiatry

Volumn 67, Issue 8, 2010, Pages 753-760

  Sharf, Ruth ^a   Sarhan, Maysa ^a   Brayton, Catherine E ^a   Guarnieri, Douglas J ^a   Taylor, Jane R ^a   DiLeone, Ralph J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Food reward; hypocretin; instrumental learning; motivation; orexin; SB 334867

Indexed keywords

1 (2 METHYL 6 BENZOXAZOLYL) 3 (1,5 NAPHTHYRIDIN 4 YL)UREA; OREXIN; OREXIN 1 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; COMPENSATION; CONTROLLED STUDY; HYPOTHALAMUS; INSTRUMENTAL CONDITIONING; LEARNING; MALE; MOTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REINFORCEMENT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; TASK PERFORMANCE; TRAINING; WILD TYPE;

ANIMALS; BENZOXAZOLES; CONDITIONING, OPERANT; DATA INTERPRETATION, STATISTICAL; FOOD; HYPOTHALAMIC AREA, LATERAL; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NEUROPEPTIDES; RECEPTORS, NEUROPEPTIDE; REINFORCEMENT (PSYCHOLOGY); REINFORCEMENT SCHEDULE; RNA INTERFERENCE; UREA; VIRUSES;

EID: 77950023073     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2009.12.035     Document Type: Article

References (49)

1. Chemelli R.M., Willie J.T., Sinton C.M., Elmquist J.K., Scammell T., Lee C., et al. Narcolepsy in orexin knockout mice: Molecular genetics of sleep regulation. Cell 98 (1999) 437-451
2. Lin L., Faraco J., Li R., Kadotani H., Rogers W., Lin X., et al. The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98 (1999) 365-376
3. Peyron C., Faraco J., Rogers W., Ripley B., Overeem S., Charnay Y., et al. A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat Med 6 (2000) 991-997
4. Sutcliffe J.G., and De Lecea L. The hypocretins: Setting the arousal threshold. Nat Rev Neurosci 3 (2002) 339-349
5. Willie J.T., Chemelli R.M., Sinton C.M., and Yanagisawa M. To eat or to sleep?. Orexin in the regulation of feeding and wakefulness. Annu Rev Neurosci 24 (2001) 429-458
6. Harris G.C., Wimmer M., and Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437 (2005) 556-559
7. Georgescu D., Zachariou V., Barrot M., Mieda M., Willie J.T., Eisch A.J., et al. Involvement of the lateral hypothalamic peptide orexin in morphine dependence and withdrawal. J Neurosci 23 (2003) 3106-3111
8. Sharf R., Sarhan M., and DiLeone R.J. Orexin mediates the expression of precipitated morphine withdrawal and concurrent activation of the nucleus accumbens shell. Biol Psychiatry 64 (2008) 175-183
9. Zhou Y., Bendor J., Hofmann L., Randesi M., Ho A., and Kreek M.J. Mu opioid receptor and orexin/hypocretin mRNA levels in the lateral hypothalamus and striatum are enhanced by morphine withdrawal. J Endocrinol 191 (2006) 137-145
10. Peyron C., Tighe D.K., van den Pol A.N., de Lecea L., Heller H.C., Sutcliffe J.G., et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18 (1998) 9996-10015
11. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., et al. Orexins and orexin receptors: A family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92 (1998) 573-585
12. Date Y., Ueta Y., Yamashita H., Yamaguchi H., Matsukura S., Kangawa K., et al. Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc Natl Acad Sci U S A 96 (1999) 748-753
13. De Lecea L., Kilduff T.S., Peyron C., Gao X., Foye P.E., Danielson P.E., et al. The hypocretins: Hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 95 (1998) 322-327
14. Marcus J.N., Aschkenasi C.J., Lee C.E., Chemelli R.M., Saper C.B., Yanagisawa M., et al. Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 435 (2001) 6-25
15. Bardo M.T. Neuropharmacological mechanisms of drug reward: Beyond dopamine in the nucleus accumbens. Crit Rev Neurobiol 12 (1998) 37-67
16. Beninger R.J. The role of dopamine in locomotor activity and learning. Brain Res 287 (1983) 173-196
17. Wise R.A. Catecholamine theories of reward: A critical review. Brain Res 152 (1978) 215-247
18. Wise R.A., and Rompre P.P. Brain dopamine and reward. Annu Rev Psychol 40 (1989) 191-225
19. Boutrel B., Kenny P.J., Specio S.E., Martin-Fardon R., Markou A., Koob G.F., et al. Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc Natl Acad Sci U S A 102 (2005) 19168-19173
20. Borgland S.L., Taha S.A., Sarti F., Fields H.L., and Bonci A. Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49 (2006) 589-601
21. Kunii K., AYamanaka A., Nambu T., Matsuzaki I., Goto K., and Sakurai T. Orexins/hypocretins regulate drinking behaviour. Brain Res 842 (1999) 256-261
22. Lubkin M., and Stricker-Krongrad A. Independent feeding and metabolic actions of orexins in mice. Biochem Biophys Res Commun 253 (1998) 241-245
23. Sweet D.C., Levine A.S., Billington C.J., and Kotz C.M. Feeding response to central orexins. Brain Res 821 (1999) 535-538
24. Borgland S.L., Chang S.J., Bowers M.S., Thompson J.L., Vittoz N., Floresco S.B., et al. Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J Neurosci 29 (2009) 11215-11225
25. Nair S.G., Golden S.A., and Shaham Y. Differential effects of the hypocretin 1 receptor antagonist SB 334867 on high-fat food self-administration and reinstatement of food seeking in rats. Br J Pharmacol 154 (2008) 406-416
26. Richards J.K., Simms J.A., Steensland P., Taha S.A., Borgland S.L., Bonci A., et al. Inhibition of orexin-1/hypocretin-1 receptors inhibits yohimbine-induced reinstatement of ethanol and sucrose seeking in Long-Evans rats. Psychopharmacology 199 (2008) 109-117
27. Hollander J.A., Lu Q., Cameron M.D., Kamenecka T.M., and Kenny P.J. Insular hypocretin transmission regulates nicotine reward. Proc Natl Acad Sci U S A 105 (2008) 19480-19485
28. Gourley S.L., Wu F.J., Kiraly D.D., Ploski J.E., Kedves A.T., Duman R.S., et al. Regionally specific regulation of ERK MAP kinase in a model of antidepressant-sensitive chronic depression. Biol Psychiatry 63 (2008) 353-359
29. Skjoldager P., Pierre P.J., and Mittleman G. Reinforcer magnitude and progressive ratio responding in the rat: Effects of increased effort, prefeeding, and extinction. Learn Motiv 24 (1993) 303-343
30. Lawrence A.J., Cowen M.S., Yang H.J., Chen F., and Oldfield B. The orexin system regulates alcohol-seeking in rats. Br J Pharmacol 148 (2006) 752-759
31. Rodgers R.J., Halford J.C., Nunes de Souza R.L., Canto de Souza A.L., Piper D.C., Arch J.R., et al. SB-334867, a selective orexin-1 receptor antagonist, enhances behavioural satiety and blocks the hyperphagic effect of orexin-A in rats. Eur J Neurosci 13 (2001) 1444-1452
32. Hommel J.D., Sears R.M., Georgescu D., Simmons D.L., and DiLeone R.J. Local gene knockdown in the brain using viral-mediated RNA interference. Nat Med 9 (2003) 1539-1544
33. Hommel J.D., Trinko R., Sears R.M., Georgescu D., Liu Z.W., Gao X.B., et al. Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51 (2006) 801-810
34. Hagan J.J., Leslie R.A., Patel S., Evans M.L., Wattam T.A., Holmes S., et al. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci U S A 96 (1999) 10911-10916
35. Kilduff T.S., and Peyron C. The hypocretin/orexin ligand-receptor system: Implications for sleep and sleep disorders. Trends Neurosci 23 (2000) 359-365
36. Haynes A.C., Jackson B., Overend P., Buckingham R.E., Wilson S., Tadayyon M., et al. Effects of single and chronic intracerebroventricular administration of the orexins on feeding in the rat. Peptides 20 (1999) 1099-1105
37. Haynes A.C., Jackson B., Chapman H., Tadayyon M., Johns A., Porter R.A., et al. A selective orexin-1 receptor antagonist reduces food consumption in male and female rats. Regul Pept 96 (2000) 45-51
38. White C.L., Ishii Y., Mendoza T., Upton N., Stasi L.P., and Bray G.A. Effect of a selective ox 1R antagonist on food intake and body weight in two strains of rats that differ in susceptibility to dietary-induced obesity. Peptides 26 (2005) 2331-2338
39. Telegdy G., and Adamik A. The action of orexin A on passive avoidance learning. Involvement of transmitters. Regul Pept 104 (2002) 105-110
40. Jaeger L.B., Farr S.A., Banks W.A., and Morley J.E. Effects of orexin-A on memory processing. Peptides 23 (2002) 1683-1688
41. Akbari E., Motamedi F., Naghdi N., and Noorbakhshnia M. The effect of antagonization of orexin 1 receptors in CA1 and dentate gyrus regions on memory processing in passive avoidance task. Behav Brain Res 187 (2008) 172-177
42. Akbari E., Naghdi N., and Motamedi F. Functional inactivation of orexin 1 receptors in CA1 region impairs acquisition, consolidation and retrieval in Morris water maze task. Behav Brain Res 173 (2006) 47-52
43. Akbari E., Naghdi N., and Motamedi F. The selective orexin 1 receptor antagonist SB-334867-A impairs acquisition and consolidation but not retrieval of spatial memory in Morris water maze. Peptides 28 (2007) 650-656
44. Harris G.C., Wimmer M., Randall-Thompson J.F., and Aston-Jones G. Lateral hypothalamic orexin neurons are critically involved in learning to associate an environment with morphine reward. Behav Brain Res 183 (2007) 43-51
45. Zheng H., Patterson L.M., and Berthoud H.R. Orexin signaling in the ventral tegmental area is required for high-fat appetite induced by opioid stimulation of the nucleus accumbens. J Neurosci 27 (2007) 11075-11082
46. Funato H., Tsai A.L., Willie J.T., Kisanuki Y.Y., Williams S.C., Sakurai T., et al. Enhanced orexin receptor-2 signaling prevents diet-induced obesity and improves leptin sensitivity. Cell Metab 9 (2009) 64-76
47. Duxon M.S., Stretton J., Starr K., Jones D.N., Holland V., Riley G., et al. Evidence that orexin-A-evoked grooming in the rat is mediated by orexin-1 (OX1) receptors, with downstream 5-HT2C receptor involvement. Psychopharmacology 153 (2001) 203-209
48. Killeen P.R., Hanson S.J., and Osborne S.R. Arousal: Its genesis and manifestation as response rate. Psychol Rev 85 (1978) 571-581
49. Killeen P.R., and Sitomer M.T. MPR. Behav Processes 62 (2003) 49-64