Cocaine and Nicotine Research Illustrates a Range of Hypocretin Mechanisms in Addiction

Vitamins and Hormones

Volumn 89, Issue , 2012, Pages 291-313

  Baimel, Corey ^a   Borgland, Stephanie L ^a   Corrigall, William ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Addiction; Arousal; Drug target; Motivation; Nicotine; Synaptic plasticity; Ventral tegmental area

Indexed keywords

EID: 84861465122     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394623-2.00016-0     Document Type: Chapter

References (108)

1. Alderson H.L., Latimer M.P., Winn P. Intravenous self-administration of nicotine is altered by lesions of the posterior, but not anterior, pedunculopontine tegmental nucleus. Eur. J. Neurosci. 2006, 23:2169-2175.
2. Argilli E., Sibley D.R., Malenka R.C., England P.M., Bonci A. Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area. J. Neurosci. 2008, 28:9092-9100.
3. 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(Suppl. 1):112-121.
4. Aston-Jones G., Smith R.J., Sartor G.C., Moorman D.E., Massi L., Tahsili-Fahadan P., Richardson K.A. Lateral hypothalamic orexin/hypocretin neurons: A role in reward-seeking and addiction. Brain Res. 2010, 1314:74-90.
5. 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, 503:668-684.
6. Baldo B.A., Daniel R.A., Berridge C.W., Kelley A.E. Overlapping distributions of orexin/hypocretin- and dopamine-beta-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. J. Comp. Neurol. 2003, 464:220-237.
7. Balfour D.J. The neurobiology of tobacco dependence: A preclinical perspective on the role of the dopamine projections to the nucleus accumbens. Nicotine Tob. Res. 2004, 6:899-912.
8. Balfour D.J. The neuronal pathways mediating the behavioral and addictive properties of nicotine. Handb. Exp. Pharmacol. 2009, 192:209-233.
9. Boileau I., Dagher A., Leyton M., Gunn R.N., Baker G.B., Diksic M., Benkelfat C. Modeling sensitization to stimulants in humans: An [11C]raclopride/positron emission tomography study in healthy men. Arch. Gen. Psychiatry 2006, 63:1386-1395.
10. Borgland S.L., Malenka R.C., Bonci A. Acute and chronic cocaine-induced potentiation of synaptic strength in the ventral tegmental area: Electrophysiological and behavioral correlates in individual rats. J. Neurosci. 2004, 24:7482-7490.
11. Borgland S.L., Taha S.A., Sarti F., Fields H.L., Bonci A. Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 2006, 49:589-601.
12. Borgland S.L., Storm E., Bonci A. Orexin B/hypocretin 2 increases glutamatergic transmission to ventral tegmental area neurons. Eur. J. Neurosci. 2008, 28:1545-1556.
13. Borgland S.L., Chang S.J., Bowers M.S., Thompson J.L., Vittoz N., Floresco S.B., Chou J., Chen B.T., Bonci A. Orexin A/hypocretin-a selectively promotes motivation for positive reinforcers. J. Neurosci. 2009, 29:11215-11225.
14. Boutrel B., Kenny P.J., Specio S.E., Martin-Fardon R., Markou A., Koob G.F., de Lecea L. Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19168-19173.
15. Changeux J.P. Nicotine addiction and nicotine receptors: Lessons learned from genetically modified mice. Nat. Rev. Neurosci. 2010, 11:389-401.
16. Chen B.T., Bowers M.S., Martin M., Hopf F.W., Guillory A.M., Carelli R.M., Chou J.K., Bonci A. Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA. Neuron 2008, 59:288-297.
17. Corrigall W.A. Hypocretin mechanisms in nicotine addiction: Evidence and speculation. Psychopharmacology (Berl.) 2009, 206:23-37.
18. Di Fabio R., Pellacani A., Faedo S., Roth A., Piccoli L., Gerrard P., Porter R.A., Johnson C.N., Thewlis K., Donati D., Stasi L., Spada S., et al. Discovery process and pharmacological characterization of a novel dual orexin 1 and orexin 2 receptor antagonist useful for treatment of sleep disorders. Bioorg. Med. Chem. Lett. 2011, 21:5562-5567.
19. 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.
20. España R.A., Melchior J.R., Roberts D.C., Jones S.R. Hypocretin 1/orexin A in the ventral tegmental area enhances dopamine responses to cocaine and promotes cocaine self-administration. Psychopharmacology (Berl.) 2011, 214:415-426.
21. Exley R., Clements M.A., Hartung H., McIntosh J.M., Cragg S.J. Alpha6-containing nicotinic acetylcholine receptors dominate the nicotine control of dopamine neurotransmission in nucleus accumbens. Neuropsychopharmacology 2008, 33:2158-2166.
22. Exley R., Maubourguet N., David V., Eddine R., Evrard A., Pons S., Marti F., Threlfell S., Cazala P., McIntosh J.M., Changeux J.P., Maskos U., et al. Distinct contributions of nicotinic acetylcholine receptor subunit alpha4 and subunit alpha6 to the reinforcing effects of nicotine. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:7577-7582.
23. Fadel J., Deutch A.Y. Anatomical substrates of orexin-dopamine interactions: Lateral hypothalamic projections to the ventral tegmental area. Neuroscience 2002, 111:379-387.
24. Fitzgerald L.W., Ortiz J., Hamedani A.G., Nestler E.J. Drugs of abuse and stress increase the expression of GluR1 and NMDAR1 glutamate receptor subunits in the rat ventral tegmental area: Common adaptations among cross-sensitizing agents. J. Neurosci. 1996, 16:274-282.
25. Fowler C.D., Lu Q., Johnson P.M., Marks M.J., Kenny P.J. Habenular α5 nicotinic receptor subunit signalling controls nicotine intake. Nature 2011, 471:597-601.
26. Gotti C., Zoli M., Clementi F. Brain nicotinic acetylcholine receptors: Native subtypes and their relevance. Trends Pharmacol. Sci. 2006, 27:482-491.
27. Gotti C., Guiducci S., Tedesco V., Corbioli S., Zanetti L., Moretti M., Zanardi A., Rimondini R., Mugnaini M., Clementi F., Chiamulera C., Zoli M. Nicotinic acetylcholine receptors in the mesolimbic pathway: Primary role of ventral tegmental area alpha6beta2* receptors in mediating systemic nicotine effects on dopamine release, locomotion, and reinforcement. J. Neurosci. 2010, 30:5311-5325.
28. Grady S.R., Salminen O., Laverty D.C., Whiteaker P., McIntosh J.M., Collins A.C., Marks M.J. The subtypes of nicotinic acetylcholine receptors on dopaminergic terminals of mouse striatum. Biochem. Pharmacol. 2007, 74:1235-11246.
29. Graef S., Schönknecht P., Sabri O., Hegerl U. Cholinergic receptor subtypes and their role in cognition, emotion, and vigilance control: An overview of preclinical and clinical findings. Psychopharmacology (Berl.) 2011, 215:205-229.
30. Harpsøe K., Ahring P.K., Christensen J.K., Jensen M.L., Peters D., Balle T. Unraveling the high- and low-sensitivity agonist responses of nicotinic acetylcholine receptors. J. Neurosci. 2011, 31:10759-10766.
31. Harris G.C., Wimmer M., Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 2005, 437:556-559.
32. 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.
33. Haydar S.N., Dunlop J. Neuronal nicotinic acetylcholine receptors-Targets for the development of drugs to treat cognitive impairment associated with schizophrenia and Alzheimer's disease. Curr. Top. Med. Chem. 2010, 10:144-152.
34. Heidbreder C.A., Newman A.H. Current perspectives on selective dopamine D(3) receptor antagonists as pharmacotherapeutics for addictions and related disorders. Ann. N. Y. Acad. Sci. 2010, 1187:4-34.
35. Hollander J.A., Lu Q., Cameron M.D., Kamenecka T.M., Kenny P.J. Insular hypocretin transmission regulates nicotine reward. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:19480-19485.
36. Huang H., Xu Y., van den Pol A. Nicotine excites hypothalamic arcuate anorexigenic proopiomelanocortin neurons and orexigenic neuropeptide Y neurons: Similarities and differences. J. Neurophysiol. 2011, 106:1191-1202.
37. 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.
38. Jones S., Bonci A. Synaptic plasticity and drug addiction. Curr. Opin. Pharmacol. 2005, 5:20-25.
39. Jose Lança A., Sanelli T.R., Corrigall W.A. Nicotine-induced fos expression in the pedunculopontine mesencephalic tegmentum in the rat. Neuropharmacology 2000, 39:2808-2817.
40. Kalivas P.W. Cocaine and amphetamine-like psychostimulants: Neurocircuitry and glutamate neuroplasticity. Dialogues Clin. Neurosci. 2007, 9:389-397.
41. Kalivas P.W., Alesdatter J.E. Involvement of N-methyl-d-aspartate receptor stimulation in the ventral tegmental area and amygdala in behavioral sensitization to cocaine. J. Pharmacol. Exp. Ther. 1993, 267:486-495.
42. Kane J.K., Parker S.L., Matta S.G., Fu Y., Sharp B.M., Li M.D. Nicotine up-regulates expression of orexin and its receptors in rat brain. Endocrinology 2000, 141:3623-3629.
43. Kane J.K., Parker S.L., Li M.D. Hypothalamic orexin-A binding sites are downregulated by chronic nicotine treatment in the rat. Neurosci. Lett. 2001, 298:1-4.
44. Kauer J.A. Learning mechanisms in addiction: Synaptic plasticity in the ventral tegmental area as a result of exposure to drugs of abuse. Annu. Rev. Physiol. 2004, 66:447-475.
45. Kauer J.A., Malenka R.C. Synaptic plasticity and addiction. Nat. Rev. Neurosci. 2007, 8:844-858.
46. Kilduff T.S., Peyron C. The hypocretin/orexin ligand-receptor system: Implications for sleep and sleep disorders. Trends Neurosci. 2000, 23:359-365.
47. 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.
48. Korotkova T.M., Brown R.E., Sergeeva O.A., Ponomarenko A.A., Haas H.L. Effects of arousal- and feeding-related neuropeptides on dopaminergic and GABAergic neurons in the ventral tegmental area of the rat. Eur. J. Neurosci. 2006, 23:2677-2685.
49. Lambe E.K., Olausson P., Horst N.K., Taylor J.R., Aghajanian G.K. Hypocretin and nicotine excite the same thalamocortical synapses in prefrontal cortex: Correlation with improved attention in rat. J. Neurosci. 2005, 25:5225-5229.
50. Lança A.J., Adamson K.L., Coen K.M., Chow B.L., Corrigall W.A. The pedunculopontine tegmental nucleus and the role of cholinergic neurons in nicotine self-administration in the rat: A correlative neuroanatomical and behavioral study. Neuroscience 2000, 96:735-742.
51. Laviolette S.R., Alexson T.O., van der Kooy D. Lesions of the tegmental pedunculopontine nucleus block the rewarding effects and reveal the aversive effects of nicotine in the ventral tegmental area. J. Neurosci. 2002, 22:8653-8660.
52. 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.
53. LeSage M.G., Perry J.L., Kotz C.M., Shelley D., Corrigall W.A. Nicotine self-administration in the rat: Effects of hypocretin antagonists and changes in hypocretin mRNA. Psychopharmacology (Berl.) 2010, 209:203-212.
54. Livingstone P.D., Wonnacott S. Nicotinic acetylcholine receptors and the ascending dopamine pathways. Biochem. Pharmacol. 2009, 78:744-755.
55. Luscher C., Malenka R.C. Drug-evoked synaptic plasticity in addiction: From molecular changes to circuit remodeling. Neuron 2011, 69:650-663.
56. Mameli M., Halbout B., Creton C., Engblom D., Parkitna J.R., Spanagel R., Luscher C. Cocaine-evoked synaptic plasticity: Persistence in the VTA triggers adaptations in the NAc. Nat. Neurosci. 2009, 12:1036-1041.
57. Marcus J.N., Aschkenasi C.J., Lee C.E., Chemelli R.M., Saper C.B., Yanagisawa M., Elmquist J.K. Differential expression of orexin receptors 1 and 2 in the rat brain. J. Comp. Neurol. 2001, 435:6-25.
58. Martin M., Chen B.T., Hopf F.W., Bowers M.S., Bonci A. Cocaine self-administration selectively abolishes LTD in the core of the nucleus accumbens. Nat. Neurosci. 2006, 9:868-869.
59. Mileykovskiy B.Y., Kiyashchenko L.I., Siegel J.M. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 2005, 46:787-798.
60. Moorman D.E., Aston-Jones G. Orexin/hypocretin modulates response of ventral tegmental dopamine neurons to prefrontal activation: Diurnal influences. J. Neurosci. 2010, 30:15585-15599.
61. 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.
62. 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, 27:2837-2845.
63. 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.
64. Nakamura T., Uramura K., Nambu T., Yada T., Goto K., Yanagisawa M., Sakurai T. Orexin-induced hyperlocomotion and stereotypy are mediated by the dopaminergic system. Brain Res. 2000, 873:181-187.
65. Naqvi N.H., Rudrauf D., Damasio H., Bechara A. Damage to the insula disrupts addiction to cigarette smoking. Science 2007, 315:531-534.
66. Narita M., Nagumo Y., Hashimoto S., Khotib J., Miyatake M., Sakurai T., Yanagisawa M., Nakamachi T., Shioda S., Suzuki T. 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.
67. 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.
68. Nelson M.E., Kuryatov A., Choi C.H., Zhou Y., Lindstrom J. Alternate stoichiometries of alpha4beta2 nicotinic acetylcholine receptors. Mol. Pharmacol. 2003, 63:332-341.
69. Nogueira L., Kalivas P.W., Lavin A. Long-term neuroadaptations produced by withdrawal from repeated cocaine treatment: Role of dopaminergic receptors in modulating cortical excitability. J. Neurosci. 2006, 26:12308-12313.
70. Overton P., Clark D. Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat. Synapse 1992, 10:131-140.
71. Pasumarthi R.K., Fadel J. Activation of orexin/hypocretin projections to basal forebrain and paraventricular thalamus by acute nicotine. Brain Res. Bull. 2008, 77:367-373.
72. Pasumarthi R.K., Fadel J. Stimulation of lateral hypothalamic glutamate and acetylcholine efflux by nicotine: Implications for mechanisms of nicotine-induced activation of orexin neurons. J. Neurochem. 2010, 113:1023-1035.
73. Pasumarthi R.K., Reznikov L.R., Fadel J. Activation of orexin neurons by acute nicotine. Eur. J. Pharmacol. 2006, 535:172-176.
74. Plaza-Zabala A., Martín-García E., de Lecea L., Maldonado R., Berrendero F. Hypocretins regulate the anxiogenic-like effects of nicotine and induce reinstatement of nicotine-seeking behavior. J. Neurosci. 2010, 30:2300-2310.
75. Plaza-Zabala A., Flores A., Maldonado R., Berrendero F. Hypocretin/orexin signaling in the hypothalamic paraventricular nucleus is essential for the expression of nicotine withdrawal. Biol. Psychiatry 2011, 71:214-223.
76. Polosa R., Benowitz N.L. Treatment of nicotine addiction: Present therapeutic options and pipeline developments. Trends Pharmacol. Sci. 2011, 32:281-289.
77. Pons S., Fattore L., Cossu G., Tolu S., Porcu E., McIntosh J.M., Changeux J.P., Maskos U., Fratta W. Crucial role of alpha4 and alpha6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J. Neurosci. 2008, 28:12318-12327.
78. 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.
79. Robinson T.E., Berridge K.C. The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Res. Brain Res. Rev. 1993, 18:247-291.
80. Rodgers R.J., Halford J.C., Nunes de Souza R.L., Canto de Souze A.L., Piper D.C., Arch J.R., Upton N., Porter R.A., Johns A., Blundell J.E. SB-334867, a selective orexin-1 receptor antagonist, enhances behavioural satiety and blocks the hyperphagic effect of orexin-A in rats. Eur. J. Neurosci. 2001, 13:1444-1452.
81. Roecker A.J., Coleman P.J. Orexin receptor antagonists: Medicinal chemistry and therapeutic potential. Curr. Top. Med. Chem. 2008, 8:977-987.
82. 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.
83. Saccone N.L., Culverhouse R.C., Schwantes-An T.H., Cannon D.S., Chen X., Cichon S., Giegling I., Han S., Han Y., Keskitalo-Vuokko K., Kong X., Landi M.T., et al. Multiple independent loci at chromosome 15q25.1 affect smoking quantity: A meta-analysis and comparison with lung cancer and COPD. PLoS Genet. 2010, 6. pii: e1001053.
84. Scammell T.E., Winrow C.J. Orexin receptors: Pharmacology and therapeutic opportunities. Annu. Rev. Pharmacol. Toxicol. 2011, 51:243-266.
85. Schneider E.R., Rada P., Darby R.D., Leibowitz S.F., Hoebel B.G. Orexigenic peptides and alcohol intake: Differential effects of orexin, galanin, and ghrelin. Alcohol. Clin. Exp. Res. 2007, 31:1858-1865.
86. Sesack S.R., Pickel V.M. Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J. Comp. Neurol. 1992, 320:145-160.
87. Sesack S.R., Deutch A.Y., Roth R.H., Bunney B.S. Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 1989, 290:213-242.
88. 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.
89. Shoblock J.R., Welty N., Aluisio L., Fraser I., Motley S.T., Morton K., Palmer J., Bonaventure P., Carruthers N.I., Lovenberg T.W., Boggs J., Galici R. Selective blockade of the orexin-2 receptor attenuates ethanol self-administration, place preference, and reinstatement. Psychopharmacology (Berl.) 2011, 215:191-203.
90. Smith R.J., See R.E., Aston-Jones G. Orexin/hypocretin signaling at the orexin 1 receptor regulates cue-elicited cocaine-seeking. Eur. J. Neurosci. 2009, 30:493-503.
91. 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.
92. Thomas M.J., Beurrier C., Bonci A., Malenka R.C. Long-term depression in the nucleus accumbens: A neural correlate of behavioral sensitization to cocaine. Nat. Neurosci. 2001, 4:1217-12123.
93. Thomas M.J., Kalivas P.W., Shaham Y. Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Br. J. Pharmacol. 2008, 154:327-342.
94. Tong Z.Y., Overton P.G., Clark D. Antagonism of NMDA receptors but not AMPA/kainate receptors blocks bursting in dopaminergic neurons induced by electrical stimulation of the prefrontal cortex. J. Neural Transm. 1996, 103:889-904.
95. Ungless M.A., Whistler J.L., Malenka R.C., Bonci A. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 2001, 411:583-587.
96. 2+ signaling in dopamine neurons of the ventral tegmental area. Neuroreport 2001, 12:1885-1889.
97. Uteshev V.V., Stevens D.R., Haas H.L. Alpha-bungarotoxin-sensitive nicotinic responses in rat tuberomammillary neurons. Pflugers Arch. 1996, 432:607-613.
98. Uteshev V.V., Meyer E.M., Papke R.L. Activation and inhibition of native neuronal alpha-bungarotoxin-sensitive nicotinic ACh receptors. Brain Res. 2002, 948:33-46.
99. Vittoz N.M., Berridge C.W. Hypocretin/orexin selectively increases dopamine efflux within the prefrontal cortex: Involvement of the ventral tegmental area. Neuropsychopharmacology 2006, 31:384-395.
100. 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.
101. von der Goltz C., Koopmann A., Dinter C., Richter A., Rockenbach C., Grosshans M., Nakovics H., Wiedemann K., Mann K., Winterer G., Kiefer F. Orexin and leptin are associated with nicotine craving: A link between smoking, appetite and reward. Psychoneuroendocrinology 2010, 35:570-577.
102. Voorhees C.M., Cunningham C.L. Involvement of the orexin/hypocretin system in ethanol conditioned place preference. Psychopharmacology (Berl.) 2011, 214:805-818.
103. Wada H., Inagaki N., Yamatodani A., Watanabe T. Is the histaminergic neuron system a regulatory center for whole-brain activity?. Trends Neurosci. 1991, 14:415-418.
104. 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.
105. Wolf M.E., Ferrario C.R. AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci. Biobehav. Rev. 2010, 35:185-211.
106. Wolf M.E., Sun X., Mangiavacchi S., Chao S.Z. Psychomotor stimulants and neuronal plasticity. Neuropharmacology 2004, 47(Suppl. 1):61-79.
107. Wonnacott S., Sidhpura N., Balfour D.J. Nicotine: From molecular mechanisms to behaviour. Curr. Opin. Pharmacol. 2005, 5:53-59.
108. Zhao-Shea R., Liu L., Soll L.G., Improgo M.R., Meyers E.E., McIntosh J.M., Grady S.R., Marks M.J., Gardner P.D., Tapper A.R. Nicotine-mediated activation of dopaminergic neurons in distinct regions of the ventral tegmental area. Neuropsychopharmacology 2011, 36:1021-1032.