A role for hypocretin/orexin in motivation

Behavioural Brain Research

Volumn 217, Issue 2, 2011, Pages 446-453

  Thompson, Jennifer L ^a   Borgland, Stephanie L ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Addiction; Cocaine; Dopamine; Hypocretin; Motivation; Obesity; Orexin; Synaptic plasticity; VTA

Indexed keywords

ALCOHOL; AMPHETAMINE; COCAINE; DOPAMINE; MORPHINE; NICOTINE; OREXIN;

AROUSAL; BEHAVIOR; DRUG DEPENDENCE; DRUG SELF ADMINISTRATION; LOCOMOTION; MESOLIMBIC DOPAMINERGIC SYSTEM; MOTIVATION; NONHUMAN; OBESITY; OVERNUTRITION; PLACE PREFERENCE; PRIORITY JOURNAL; REINFORCEMENT; REVIEW; REWARD; SATIETY; STIMULUS RESPONSE; VENTRAL TEGMENTUM; WITHDRAWAL SYNDROME;

ANIMALS; CONDITIONING, OPERANT; DOPAMINE; DRUG-SEEKING BEHAVIOR; EATING; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LOCOMOTION; MODELS, BIOLOGICAL; MOTIVATION; NEUROPEPTIDES; SELF ADMINISTRATION; VENTRAL TEGMENTAL AREA;

EID: 78650419195     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.09.028     Document Type: Review

References (82)

1. Wang G.J., Volkow N.D., Thanos P.K., Fowler J.S. Similarity between obesity and drug addiction as assessed by neurofunctional imaging: a concept review. J. Addict. Dis. 2004, 23:39-53.
2. Wang G.J., Volkow N.D., Logan J., Pappas N.R., Wong C.T., Zhu W., et al. Brain dopamine and obesity. Lancet 2001, 357:354-357.
3. Volkow N.D., Wang G.J., Fowler J.S., Telang F. Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2008, 363:3191-3200.
4. DeLecea L., Kilduff T.S., Peyron C., Gao X.-B., Foye P.E., Danielson P.E., et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:322-327.
5. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., et al. Orexin and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998, 92:573-585.
6. Aston-Jones G., Smith R.J., Sartor G.C., Moorman D.E., Massi L., Tahsili-Fahadan P., et al. Lateral hypothalamic orexin/hypocretin neurons: a role in reward-seeking and addiction. Brain Res. 2010, 1314:74-90.
7. Peyron C., Tighe D.K., van den Pol A., de Lecea L., Heller H.C., Sutcliffe J.G., et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 1998, 18:9996-10015.
8. Fadel J., Deutch A.Y. Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience 2002, 111:379-387.
9. Baldo B.A., Daniel R.A., Berridge C.W., Kelley A.E. Overlapping distributions of orexin/hypocretin- and dopamine-β-hydroxylase immunoreactivity fibers in rat brain regions mediating arousal, motivation, and stress. J. Comp. Neurol. 2003, 464:220-237.
10. Balcita-Pedicino J.J., Sesack S.R. Orexin axons in the rat ventral tegmental area synapse infrequently onto dopamine and gamma-aminobutyric acid neurons. J. Comp. Neurol. 2007, 503:668-685.
11. Robinson T.E., Berridge K.C. The neural basis of drug craving; an incentive-sensitization theory of addiction. Brain Res. Rev. 1993, 18:247-291.
12. Volkow N.D., Wise R.A. How can drug addiction help us understand obesity?. Nat. Neurosci. 2005, 5:555-559.
13. Bassareo V., Di Chiara G. Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience 1999, 89:637-641.
14. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
15. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 2005, 8:1481-1489.
16. Roitman M.F., Wheeler R.A., Wightman R.M., Carelli R.M. Real-time chemical responses in the nucleus accumbens differentiate rewarding and aversive stimuli. Nat. Neurosci. 2008, 11:1376-1377.
17. Salamone J.D., Correa M., Farrar A., Mingote S.M. Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacol 2007, 191:461-482.
18. Salamone J.D., Steinpreis R.E., McCullough L.D., Smith P., Grebel D., Mahan K. Complex motor and sensorimotor functions of striatal and accumbens dopamine: involvement in instrumental behavior processes. Psychopharmacol 1991, 104:515-521.
19. Salamone J.D., Cousins M.S., Bucher S. Anhedonia or anergia? Effects of haloperidol and nucleus accumbens dopamine depletion on instrumental response selection in a T-maze cost/benefit procedure. Behav. Brain Res. 1994, 65:221-229.
20. Bonci A., Malenka R.C. Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area. J. Neurosci. 1999, 19:3723-3730.
21. Overton P.G., Richards C.D., Berry M.S., Clark D. Long-term potentiation at excitatory amino acid synapses on midbrain dopamine neurons. Neuroreport 1999, 10:221-226.
22. Thomas M.T., Malenka R.C., Bonci A. Modulation of long-term depression by dopamine in the mesolimbic system. J. Neurosci. 2000, 20:5581-5586.
23. Ungless M.A., Whistler J.L., Malenka R.C., Bonci A. A single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 2001, 411:583-587.
24. Saal D., Dong Y., Bonci A., Malenka R.C. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 2003, 37:577-582.
25. Borgland S.L., Malenka R., Bonci A. Acute and chronic cocaine-induced potentiation of synaptic strength in the VTA: electrophysiological and behavioral correlates in individual rats. J. Neurosci. 2004, 24:7482-7490.
26. Mathon D.S., Kamal A., Smidt M.P., Ramakers G.M. Modulation of cellular activity and synaptic transmission in the ventral tegmental area. Eur. J. Pharmacol. 2003, 480:97-115.
27. Suaud-Chagny M.F., Chergui K., Chouvet G., Gonon F. Relationship between dopamine release in the rat nucleus accumbens and the discharge activity of dopaminergic neurons during local in vivo application of amino acids in the ventral tegmental area. Neuroscience 1992, 49:63-72.
28. Murase S., Grenhoff J., Chouvet G., Gonon F.G., Svensson T.H. Prefrontal cortex regulates burst firing and transmitter release in rat mesolimbic dopamine neurons studied in vivo. Neurosci. Lett. 1993, 157:53-56.
29. Parker J.G., Zweifel L.S., Clark J.J., Evans S.B., Phillips P.E., Palmiter R.D. Absence of NMDA receptors in dopamine neurons attenuates dopamine release but not conditioned approach during Pavlovian conditioning. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:13491-19496.
30. Stuber G.D., Klanker M., de Ridder B., Bowers M.S., Joosten R.N., Feenstra M.G., et al. Reward predictive cues enhance excitatory synaptic strength onto midbrain dopamine neurons. Science 2008, 321:1690-1692.
31. Zhu Y., Miwa Y., Yamanaka A., Yada T., Shibahara M., Abe Y., et al. Orexin receptor type-1 couples exclusively to pertussis toxin-insensitive G-proteins, while orexin receptor type-2 couples to both pertussis toxin-sensitive and -insensitive G-proteins. J. Pharmacol. Sci. 2003, 92:259-266.
32. Smith R., See R.E., Aston-Jones G. Orexin/hypocretin signalling at the OX1 receptor regulates cue-elicited cocaine seeking. Eur. J. Neurosci. 2009, 30:493-503.
33. Wang B., You Z.-B., Wise R.A. Reinstatement of cocaine seeking by hypocretin (orexin) in the ventral tegmental area: independence from the local corticotropin-releasing factor network. Biol. Psychiatry 2009, 65:857-862.
34. 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 1999, 98:437-451.
35. Akanmu M.A., Honda K. Selective stimulation of orexin receptor type 2 promotes wakefulness in freely behaving rats. Brain Res. 2005, 1048:138-145.
36. Hondo M., Nagai K., Ohno K., Kisanuki Y., Willie J.T., Watanabe T., et al. Histamine-1 receptor is not required as a downstream effector of orexin-2 receptor in maintenance of basal sleep/wake states. Acta Physiol. 2009, 198:287-294.
37. Korotkova T.M., Sergeeva O.A., Eriksson K.S., Haas H.L., Brown R.E. Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexins/hypocretins. J. Neurosci. 2003, 23:7-11.
38. Narita M., Nagumo Y., Hashimoto S., Narita M., Khotib J., Miyatake M., et al. Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine. J. Neurosci. 2006, 26:398-405.
39. Trivedi P., Yu H., MacNeil D.J., Van der Ploeg L.H., Guan X.M. Distribution of orexin receptor mRNA in the rat brain. FEBS Lett. 1998, 438:71-75.
40. Muschamp J.W., Dominguez J.M., Sato S.M., Shen R.Y., Hull E.M. A role for hypocretin (orexin) in male sexual behavior. J. Neurosci. 2007, 27:T2837-2845T.
41. Mileykovskiy B.Y., Kiyashchenko L.I., Siegel J.M. Behavioral correlates of activity in identified Hypocretin/orexin Neurons. Neuron 2005, 46:787-798.
42. Borgland S.L., Taha S., Sarti F., Fields H.L., Bonci A. Orexin A signaling in dopamine neurons is critical for cocaine induced synaptic plasticity and behavioral sensitization. Neuron 2006, 49:589-601.
43. Borgland S.L., Storm E., Bonci A. Orexin B/hypocretin-2 increases glutamatergic synaptic transmission to ventral tegmental area neurons. Eur. J. Neurosci. 2008, 29:1-12.
44. España R.A., Oleson E.B., Locke J.L., Brookshire B.R., Roberts D.C., Jones S.R. The hypocretin-orexin system regulates cocaine self-administration via actions on the mesolimbic dopamine system. Eur. J. Neurosci. 2010, 31:336-348.
45. Narita M., Nagumo Y., Miyatake M., Ikegami D., Kurahashi K., Suzuki T. Implication of protein kinase C in the orexin-induced elevation of extracellular dopamine levels and its rewarding effect. Eur. J. Neurosci. 2007, 25:1537-1545.
46. Vittoz N.M., Berridge C.W. Hypocretin/orexin selectively increases dopamine efflux within the prefrontal cortex: involvement of the ventral tegmental area. Neuropsychopharmacol 2006, 31:384-395.
47. Vittoz N.M., Schmeichel B., Berridge C.W. Hypocretin/orexin preferentially activates caudomedial ventral tegmental area dopamine neurons. Eur. J. Neurosci. 2008, 28:1629-1640.
48. 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. 2003, 23:3106-3111.
49. Sharf R., Sarhan M., Dileone R.J. Orexin mediates the expression of precipitated morphine withdrawal and concurrent activation of the nucleus accumbens shell. Biol. Psychiatry 2008, 64:175-183.
50. Zhou Y., Bendor J., Hofmann L., Randesi M., Ho A., Kreek M.J. Mu opioid receptor and orexin/hypocretin mRNA levels in the lateral hypothalamus and striatum are enhanced by morphine withdrawal. J. Endocrinol. 2006, 191:137-145.
51. Nakamura T., Uramura K., Nambu T., Yada T., Goto K., Yanagisawa M., et al. Orexin-induced hyperlocomotion and stereotypy are mediated by the dopaminergic system. Brain Res. 2000, 873:181-187.
52. Wisor J.P., Nishino S., Sora I., Uhl G.H., Mignot E., Edgar D.M. Dopaminergic role in stimulant-induced wakefulness. J. Neurosci. 2001, 21:1787-1794.
53. Kotz C.M., Wang C., Teske J.A., Thorpe A.J., Novak C.M., Kiwaki K., et al. Orexin A mediation of time spent moving in rats: neural mechanisms. Neuroscience 2006, 142:29-36.
54. Quarta D., Valerio E., Hutcheson D.M., Hedou G., Heidbreder C. The orexin-1 receptor antagonist SB-334867 reduces amphetamine-evoked dopamine outflow in the shell of the nucleus accumbens and decreases the expression of amphetamine sensitization. Neurochem. Int. 2009, 56:11-15.
55. Sharf R., Guarnieri D.J., Taylor J.R., DiLeone R.J. Orexin mediates morphine place preference, but not morphine-induced hyperactivity or sensitization. Brain Res. 2010, 1317:24-32.
56. España R.A., McCormack S.L., Mochizuki T., Scammell T.E. Running promotes wakefulness and increases cataplexy in orexin knockout mice. Sleep 2007, 30:1417-1425.
57. Harris G.C., Wimmer W., Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 2005, 437:556-559.
58. Harris G.C., Wimmer M., Randall-Thompson J.F., Aston-Jones G. Lateral hypothalamic orexin neurons are critically involved in learning to associate an environment with morphine reward. Behav. Brain Res. 2007, 183:43-51.
59. Zhou Y., Cui C.L., Schlussman S.D., Choi J.C., Ho A., Han J.S., et al. Effects of cocaine place conditioning, chronic escalating-dose " binge" pattern cocaine administration and acute withdrawal on orexin/hypocretin and preprodynorphin gene expressions in lateral hypothalamus of Fischer and Sprague-Dawley rats. Neuroscience 2008, 153:1225-12234.
60. Lawrence A.J., Cowen M.S., Yang H.-J., Chen F., Oldfield B. The orexin system regulates alcohol-seeking in rats. Br. J. Pharmacol. 2006, 148:752-759.
61. Dayas C.V., McGranahan T.M., Martin-Fardon R., Weiss F. Stimuli linked to ethanol availability activate hypothalamic CART and orexin neurons in a reinstatement model of relapse. Biol. Psychiatry 2008, 63:152-157.
62. Hamlin A.S., Clemens K.J., McNally G.P. Renewal of extinguished cocaine-seeking. Neuroscience 2008, 151:659-670.
63. Crombag H.S., Grimm J.W., Shaham Y. Effect of dopamine receptor antagonists on renewal of cocaine seeking by reexposure to drug-associated contextual cues. Neuropsychopharmacol 2002, 27:1006-1015.
64. Smith R.J., Tahsili-Fahadan P., Aston-Jones G. Orexin/hypocretin is necessary for context-driven cocaine-seeking. Neuropharmacol 2010, 58:179-184.
65. 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. 2009, 29:11215-11225.
66. Schneider E.R., Rada P., Darby R.D., Leibowitz S.F., Hoebel B.J. Orexingeneic peptides and alcohol intake: differential effects of orexin, galanin and ghrelin. Alcohol Clin. Exp. Res. 2007, 31:1858-1865.
67. Hollander J., Lu Q., Cameron M., Kamenecka T., Kenny P. Insular hypocretin transmission regulates nicotine reward. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:19480-19485.
68. Thorpe A., Cleary J., Levine A., Kotz C. Centrally administered orexin A increases motivation for sweet pellets in rats. Psychopharmacol 2005, 182:75-83.
69. Sharf R., Sarhan M., Brayton C.E., Guarnieri D.J., Taylor J.R., DiLeone R.J. Orexin signaling via the orexin 1 receptor mediates operant responding for food reinforcement. Biol. Psychiatry 2010, 67:753-760.
70. Nair S.G., Golden S.A., 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. 2008, 154:406-416.
71. 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. 2005, 102:19168-19173.
72. 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. Psychopharmacol 2008, 199:109-117.
73. Richardson N., Roberts D. Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J. Neurosci. Methods 1996, 66:1-11.
74. España R.A., Roberts D.C., Jones S.R. Hypocretin/orexin promotes cocaine self-administration and enhances the effects of cocaine on dopamine signalling program no. 387. 10. 2009. Neuroscience Meeting Planner 2009.
75. Zhang M., Balmadrid C., Kelley A.E. Nucleus accumbens opioid GABaergic, and dopaminergic modulation of palatable food motivation: contrasting effects revealed by a progressive ratio study in the rat. Behav. Neurosci. 2003, 117:202-211.
76. Clegg D.J., Air E.L., Woods S.C., Seeley R.J. Eating elicited by orexin-A, but not melanin-concentrating hormone. Is Opioid Mediated. Endocrinol. 2002, 143:2995-3000.
77. Zheng H., Patterson L.M., 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. 2007, 27:11075-11082.
78. Mignot E. Sleep, sleep disorders and hypocretin (orexin). Sleep Med. 2004, 5(Suppl 1):S2-8.
79. Clark E.L., Baumann C.R., Cano G., Scammell T.E., Mochizuki T. Feeding-elicited cataplexy in orexin knockout mice. Neuroscience 2009, 161:970-977.
80. Aston-Jones G., Smith R.J., Moorman D.E., Richardson K.A. Role of lateral hypothalamic orexin neurons in reward processing and addiction. Neuropharmacology 2009, 56:112-121.
81. Adamantidis A., de Lecea L. The hypocretins as sensors for metabolism and arousal. J. Physiol. 2009, 587:33-40.
82. Johnson S.W., Seutin V., North R.A. Burst firing in dopamine neurons induced by N-methyl-D-aspartate: role of electrogenic sodium pump. Science 1992, 258:665-667.