Neurobiological mechanisms of addiction: Focus on corticotropin-releasing factor

Current Opinion in Investigational Drugs

Volumn 11, Issue 1, 2010, Pages 63-71

  Koob, George F ^a   Zorrilla, Eric P ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Addiction; Corticotropin releasing factor; Drug relapse; Drug withdrawal; Stress

Indexed keywords

3 (4 CHLORO 2 MORPHOLIN 4 YL THIAZOL 5 YL) 8 (1 ETHYLPROPYL) 2,6 DIMETHYL IMIDAZO[1,2 B]PYRIDAZINE; 3 (6 DIMETHYLAMINO 4 METHYL 3 PYRIDINYL) 7 DIPROPYLAMINO 2,5 DIMETHYLPYRAZOLO[1,5 A]PYRIMIDINE; ACAMPROSATE; ANTALARMIN; CANNABINOID; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; N,N BIS(2 METHOXYETHYL) 3 (4 METHOXY 2 METHYLPHENYL) 2,5 DIMETHYL PYRAZOLO [1,5A]PYRIMIDIN 7 AMINE; NALTREXONE; NICOTINE; OPIATE; PSYCHOSTIMULANT AGENT; UNCLASSIFIED DRUG;

ADDICTION; ALCOHOLISM; ANTICIPATION; AUTONOMIC NERVOUS SYSTEM; COMPULSION; DRUG DEPENDENCE; DRUG INTOXICATION; DRUG RESPONSE; DRUG TARGETING; HUMAN; MENTAL DISEASE; NEUROBIOLOGY; NEUROPHARMACOLOGY; NONHUMAN; PHARMACOGENETICS; PROTEIN TARGETING; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; STRESS; WITHDRAWAL SYNDROME;

ANIMALS; CORTICOTROPIN-RELEASING HORMONE; DISEASE MODELS, ANIMAL; HUMANS; NEURAL PATHWAYS; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; SUBSTANCE WITHDRAWAL SYNDROME; SUBSTANCE-RELATED DISORDERS;

EID: 74549167795     PISSN: 14724472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (100)

1. Koob GF, Le Moal M: Addiction and the brain antireward system. Annu Rev Psychol (2008) 59:29-53.
2. Koob GF: A role for brain stress systems in addiction. Neuron (2008) 59(1):11-34.
3. Vanderschuren LJ, Everitt BJ: Behavioral and neural mechanisms of compulsive drug seeking. Eur J Pharmacol (2005) 526(1-3):77-88.
4. Koob GF, Le Moal M: Plasticity of reward neurocircuitry and the 'dark side' of drug addiction. Nat Neurosci (2005) 8(11):1442-1444.
5. Bale TL, Vale WW: CRF and CRF receptors: Role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol (2004) 44:525-557.
6. Fekete EM, Zorrilla EP: Physiology, pharmacology, and therapeutic relevance of urocortins in mammals: Ancient CRF paralogs. Front Neuroendocrinol (2007) 28(1):1-27.
7. Heinrichs SC, Koob GF: Corticotropin-releasing factor in brain: A role in activation, arousal, and affect regulation. J Pharmacol Exp Ther (2004) 311(2):427-440.
8. Zorrilla EP, Zhao Y, Koob GF: Anti-CRF. In: Encyclopedia of Stress. Fink H (Ed), Elsevier, Amsterdam, the Netherlands (2007):206-214.
9. Swanson LW, Sawchenko PE, Rivier J, Vale WW: The organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: An immunohistochemical study. Neuroendocrinology (1983) 36(3):165-186.
10. Heinrichs SC, Menzaghi F, Merlo Pich E, Baldwin HA, Rassnick S, Britton KT, Koob GF: Anti-stress action of a corticotropin-releasing factor antagonist on behavioral reactivity to stressors of varying type and intensity. Neuropsychopharmacology (1994) 11(3):179-186.
11. Menzaghi F, Howard RL, Heinrichs SC, Vale W, Rivier J, Koob GF: Characterization of a novel and potent corticotropinreleasing factor antagonist in rats. J Pharmacol Exp Ther (1994) 269(2):564-572.
12. Spina MG, Basso AM, Zorrilla EP, Heyser CJ, Rivier J, Vale W, Merlo-Pich E, Koob GF: Behavioral effects of central administration of the novel CRF antagonist astressin in rats. Neuropsychopharmacology (2000) 22(3):230-239.
13. Dunn AJ, Berridge CW: Physiological and behavioral responses to corticotropin-releasing factor administration: Is CRF a mediator of anxiety or stress responses? Brain Res Brain Res Rev (1990) 15(2):71-100.
14. Koob GF, Heinrichs SC, Menzaghi F, Pich EM, Britton KT: Corticotropin releasing factor, stress and behavior. Semin Neurosci (1994) 6(4):221-229.
15. Koob GF, Bartfai T, Roberts AJ: The use of molecular genetic approaches in the neuropharmacology of corticotropinreleasing factor. Int J Comp Psychol (2001) 14(3-4):90-110.
16. Sarnyai Z, Shaham Y, Heinrichs SC: The role of corticotropinreleasing factor in drug addiction. Pharmacol Rev (2001) 53(2):209-243.
17. Koob GF, Heinrichs SC: A role for corticotropin-releasing factor and urocortin in behavioral responses to stressors. Brain Res (1999) 848(1-2):141-152.
18. Spina M, Merlo-Pich E, Chan RKW, Basso AM, Rivier J, Vale W, Koob GF: Appetite-suppressing effects of urocortin, a CRF-related neuropeptide. Science (1996) 273(5281):1561-1564.
19. Pelleymounter MA, Joppa M, Carmouche M, Cullen MJ, Brown B, Murphy B, Grigoriadis DE, Ling N, Foster AC: Role of corticotropinreleasing factor (CRF) receptors in the anorexic syndrome induced by CRF. J Pharmacol Exp Ther (2000) 293(3):799-806.
20. Ho SP, Takahashi LK, Livanov V, Spencer K, Lesher T, Maciag C, Smith MA, Rohrbach KW, Hartig PR, Arneric SP: Attenuation of fear conditioning by antisense inhibition of brain corticotropin releasing factor-2 receptor. Brain Res Mol Brain Res (2001) 89(1-2):29-40.
21. Takahashi LK, Ho SP, Livanov V, Graciani N, Arneric SP: Antagonism of CRF2 receptors produces anxiolytic behavior in animal models of anxiety. Brain Res (2001) 902(2):135-142.
22. Zhao Y, Valdez GR, Fekete EM, Rivier JE, Vale WW, Rice KC, Weiss F, Zorrilla EP: Subtype-selective corticotropin-releasing factor receptor agonists exert contrasting, but not opposite, effects on anxiety-related behavior in rats. J Pharmacol Exp Ther (2007) 323(3):846-854.
23. Koob GF, Kreek MJ: Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am J Psychiatry (2007) 164(8):1149-1159.
24. Heimer L, Alheid G: Piecing together the puzzle of basal forebrain anatomy. In: The Basal Forebrain: Anatomy to Function. Napier TC, Kalivas PW, Hanin I (Eds), Plenum Press, New York, NY, USA (1991):1-42.
25. Merlo-Pich E, Lorang M, Yeganeh M, Rodriguez de Fonseca F, Raber J, Koob GF, Weiss F; Increase of extracellular corticotropinreleasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci (1995) 15(8):5439-5447.
26. Olive MF, Koenig HN, Nannini MA, Hodge CW: Elevated extracellular CRF levels in the bed nucleus of the stria terminalis during ethanol withdrawal and reduction by subsequent ethanol intake. Pharmacol Biochem Behav (2002) 72(1-2):213-220.
27. George O, Ghozland S, Azar MR, Cottone P, Zorrilla EP, Parsons LH, O'Dell LE, Richardson HN, Koob GF: CRF-CRF1 system activation mediates withdrawal-induced increases in nicotine selfadministration in nicotine-dependent rats. Proc Natl Acad Sci USA (2007) 104(43):17198-17203.
28. Richter RM, Weiss F: In vivo CRF release in rat amygdala is increased during cocaine withdrawal in self-administering rats. Synapse (1999) 32(4):254-261.
29. Weiss F, Ciccocioppo R, Parsons LH, Katner S, Liu X, Zorrilla EP, Valdez GR, Ben-Shahar O, Angeletti S, Richter RR: Compulsive drugseeking behavior and relapse: Neuroadaptation, stress, and conditioning factors. In: The Biological Basis of Cocaine Addiction. Quinones-Jenab V (Ed) New York Academy of Sciences, New York, NY, USA (2001):1-26.
30. Rodriguez de Fonseca F, Carrera MR, Navarro M, Koob GF, Weiss F: Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal. Science (1997) 276(5321): 2050-2054.
31. Zorrilla EP, Valdez GR, Weiss F: Changes in levels of regional CRF-like-immunoreactivity and plasma corticosterone during protracted drug withdrawal in dependent rats. Psychopharmacology (2001) 158(4):374-381.
32. Funk CK, O'Dell LE, Crawford EF, Koob GF: Corticotropin-releasing factor within the central nucleus of the amygdala mediates enhanced ethanol self-administration in withdrawn, ethanoldependent rats. J Neurosci (2006) 26(44):11324-11332.
33. Caberlotto L, Rimondini R, Hansson A, Eriksson S, Heilig M: Corticotropin-releasing hormone (CRH) mRNA expression in rat central amygdala in cannabinoid tolerance and withdrawal: Evidence for an allostatic shift? Neuropsychopharmacology (2004) 29(1):15-22.
34. Roberto M, Cruz MT, Gilpin NW, Sabino V, Schweitzer P, Bajo M, Cottone P, Madamba SM, Souffer DG, Zorrilla EP, Koob GF et al: CRF-induced amygdala GABA release plays a key role in alcohol dependence. Biol Psychiatry (2010) in press.
35. Sarnyai Z, Biro E, Gardi J, Vecsernyes M, Julesz J, Telegdy G: Brain corticotropin-releasing factor mediates 'anxiety-like' behavior induced by cocaine withdrawal in rats. Brain Res (1995) 675(1-2):89-97.
36. Basso AM, Spina M, Rivier J, Vale W, Koob GF: Corticotropinreleasing factor antagonist attenuates the 'anxiogeniclike' effect in the defensive burying paradigm but not in the elevated plus-maze following chronic cocaine in rats. Psychopharmacology (1999) 145(1):21-30.
37. Knapp DJ, Overstreet DH, Moy SS, Breese GR: SB242084, flumazenil, and CRA1000 block ethanol withdrawal-induced anxiety in rats. Alcohol (2004) 32(2):101-111.
38. Overstreet DH, Knapp DJ, Breese GR: Modulation of multiple ethanol withdrawal-induced anxiety-like behavior by CRF and CRF1 receptors. Pharmacol Biochem Behav (2004) 77(2):405-413.
39. Tucci S, Cheeta S, Seth P, File SE: Corticotropin releasing factor antagonist, α-helical CRF9-41, reverses nicotine-induced conditioned, but not unconditioned, anxiety. Psychopharmacology (2003) 167(3):251-256.
40. Skelton KH, Gutman DA, Thrivikraman KV, Nemeroff CB, Owens MJ: The CRF1 receptor antagonist R121919 attenuates the neuroendocrine and behavioral effects of precipitated lorazepam withdrawal. Psychopharmacology (2007) 192(3):385-396.
41. Stinus L, Cador M, Zorrilla EP, Koob GF: Buprenorphine and a CRF1 antagonist block the acquisition of opiate withdrawal-induced conditioned place aversion in rats. Neuropsychopharmacology (2005) 30(1):90-98.
42. Contarino A, Papaleo F: The corticotropin-releasing factor receptor-1 pathway mediates the negative affective states of opiate withdrawal. Proc Natl Acad Sci USA (2005) 102(51): 18649-18654.
43. Bruijnzeel AW, Zislis G, Wilson C, Gold MS: Antagonism of CRF receptors prevents the deficit in brain reward function associated with precipitated nicotine withdrawal in rats. Neuropsychopharmacology (2007) 32(4):955-963.
44. Bruijnzeel AW, Prado M, Isaac S: Corticotropin-releasing factor-1 receptor activation mediates nicotine withdrawal-induced deficit in brain reward function and stress-induced relapse. Biol Psychiatry (2009) 66(2):110-117.
45. Valdez GR, Roberts AJ, Chan K, Davis H, Brennan M, Zorrilla EP, Koob GF: Increased ethanol self-administration and anxietylike behavior during acute ethanol withdrawal and protracted abstinence: Regulation by corticotropin- releasing factor. Alcohol Clin Exp Res (2002) 26(10):1494-1501.
46. Valdez GR, Sabino V, Koob GF: Increased anxiety-like behavior and ethanol self-administration in dependent rats: Reversal via corticotropin-releasing factor-2 receptor activation. Alcohol Clin Exp Res (2004) 28(6):865-872.
47. Sabino V, Cottone P, Koob GF, Steardo L, Lee MJ, Rice KC, Zorrilla EP: Dissociation between opioid and CRF1 antagonist sensitive drinking in Sardinian alcohol-preferring rats. Psychopharmacology (2006) 189(2):175-186.
48. Funk CK, Zorrilla EP, Lee MJ, Rice KC, Koob GF: Corticotropinreleasing factor 1 antagonists selectively reduce ethanol self-administration in ethanol-dependent rats. Biol Psychiatry (2007) 61(1):78-86.
49. Richardson HN, Zhao Y, Fekete EM, Funk CK, Wirsching P, Janda KD, Zorrilla EP, Koob GF: MPZP: A novel small molecule corticotropinreleasing factor type 1 receptor (CRF1) antagonist. Pharmacol Biochem Behav (2008) 88(4):497-510.
50. Chu K, Koob GF, Cole M, Zorrilla EP, Roberts AJ: Dependenceinduced increases in ethanol self-administration in mice are blocked by the CRF1 receptor antagonist antalarmin and by CRF1 receptor knockout. Pharmacol Biochem Behav (2007) 86(4):813-821.
51. Gilpin NW, Richardson HN, Koob GF: Effects of CRF1-receptor and opioid-receptor antagonists on dependence-induced increases in alcohol drinking by alcohol-preferring (P) rats. Alcohol Clin Exp Res (2008) 32(9):1535-1542.
52. Sommer WH, Rimondini R, Hansson AC, Hipskind PA, Gehlert DR, Barr CS, Heilig MA: Upregulation of voluntary alcohol intake, behavioral sensitivity to stress, and amygdala Crhr1 expression following a history of dependence. Biol Psychiatry (2008) 63(2):139-145.
53. Gehlert DR, Cippitelli A, Thorsell A, Le AD, Hipskind PA, Hamdouchi C, Lu J, Hembre EJ, Cramer J, Song M, McKinzie D et al: 3-(4-Chloro-2- morpholin-4-yl-thiazol-5-yl)-8-(1-ethylpropyl)-2,6-dimethylimidazo[ 1,2-b]pyridazine: A novel brain-penetrant, orally available corticotropin- releasing factor receptor 1 antagonist with efficacy in animal models of alcoholism. J Neurosci (2007) 27(10):2718-2726.
54. Specio SE, Wee S, O'Dell LE, Boutrel B, Zorrilla EP, Koob GF: CRF1 receptor antagonists attenuate escalated cocaine selfadministration in rats. Psychopharmacology (2008) 196(3):473-482.
55. Greenwell TN, Funk CK, Cottone P, Richardson HN, Chen SA, Rice K, Zorrilla EP, Koob GF: Corticotropin-releasing factor-1 receptor antagonists decrease heroin self-administration in long- but not short-access rats. Addict Biol (2009) 14(2):130-143.
56. Marlatt GA, Gordon JR: Determinants of relapse: Implications for the maintenance of behavioral change. In: Behavioral Medicine: Changing Health Lifestyles. Davidson P, Davidson SH (Eds), Brunner/Mazel, New York, NY, USA (1980):410-452.
57. Alling C, Balldin J, Bokstrom K, Gottfries CG, Karlsson I, Langstrom G: Studies on duration of a late recovery period after chronic abuse of ethanol: A cross-sectional study of biochemical and psychiatric indicators. Acta Psychiatr Scand (1982) 66(5):384-397.
58. Hershon HI: Alcohol withdrawal symptoms and drinking behavior. J Stud Alcohol (1977) 38(5):953-971.
59. Annis HM, Sklar SM, Moser AE: Gender in relation to relapse crisis situations, coping, and outcome among treated alcoholics. Addict Behav (1998) 23(1):127-131.
60. Zywiak WH, Connors GJ, Maisto SA, Westerberg VS: Relapse research and the Reasons for Drinking Questionnaire: A factor analysis of Marlatt's relapse taxonomy. Addiction (1996) 91(Suppl):S121-S130.
61. Lowman C, Allen J, Stout RL: Replication and extension of Marlatt's taxonomy of relapse precipitants: Overview of procedures and results. The Relapse Research Group. Addiction (1996) 91(Suppl):S51-S71.
62. Childress AR, Ehrman R, McLellan AT, MacRae J, Natale M, O'Brien CP: Can induced moods trigger drug-related responses in opiate abuse patients? J Subst Abuse Treatment (1994) 11(1):17-23.
63. Cooney NL, Litt MD, Morse PA, Bauer LO, Gaupp L: Alcohol cue reactivity, negative-mood reactivity, and relapse in treated alcoholic men. J Abnorm Psychol (1997) 106(2):243-250.
64. Sinha R, Fuse T, Aubin LR, O'Malley SS: Psychological stress, drugrelated cues and cocaine craving. Psychopharmacology (2000) 152(2):140-148.
65. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J: The reinstatement model of drug relapse: History, methodology and major findings. Psychopharmacology (2003) 168(1-2):3-20.
66. Lu L, Shepard JD, Hall FS, Shaham Y: Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: A review. Neurosci Biobehav Rev (2003) 27(5):457-491.
67. Le AD, Harding S, Juzytsch W, Watchus J, Shalev U, Shaham Y: The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats. Psychopharmacology (2000) 150(3):317-324.
68. Shaham Y, Erb S, Leung S, Buczek Y, Stewart J: CP-154,526, a selective, non-peptide antagonist of the corticotropinreleasing factor1 receptor attenuates stress-induced relapse to drug seeking in cocaine- and heroin-trained rats. Psychopharmacology (1998) 137(2):184-190.
69. Marinelli PW, Funk D, Juzytsch W, Harding S, Rice KC, Shaham Y, Lê AD: The CRF1 receptor antagonist antalarmin attenuates yohimbine-induced increases in operant alcohol selfadministration and reinstatement of alcohol seeking in rats. Psychopharmacology (2007) 195(3):345-355.
70. Ungless MA, Singh V, Crowder TL, Yaka R, Ron D, Bonci A: Corticotropin-releasing factor requires CRF binding protein to potentiate NMDA receptors via CRF receptor 2 in dopamine neurons. Neuron (2003) 39(3):401-407.
71. Wang B, You ZB, Rice KC, Wise RA: Stress-induced relapse to cocaine seeking: Roles for the CRF2 receptor and CRFbinding protein in the ventral tegmental area of the rat. Psychopharmacology (2007) 193(2):283-294.
72. Tagliaferro P, Morales M. Synapses between corticotropinreleasing factor-containing axon terminals and dopaminergic neurons in the ventral tegmental area are predominantly glutamatergic. J Comp Neurol (2008) 506(4):616-626.
73. Wang B, Shaham Y, Zitzman D, Azari S, Wise RA, You ZB: Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin- releasing factor: A role in stressinduced relapse to drug seeking. J Neuroscience (2005) 25(22):5389-5396.
74. Hahn J, Hopf FW, Bonci A: Chronic cocaine enhances corticotropin- releasing factor-dependent potentiation of excitatory transmission in ventral tegmental area dopamine neurons. J Neurosci (2009) 29(20):6535-16244
75. Behan DP, de Souza EB, Lowry PJ, Potter E, Sawchenko P, Vale WW: Corticotropin releasing factor (CRF) binding protein: A novel regulator of CRF and related peptides. Front Neuroendocrinol (1995) 16(4):362-382.
76. Erb S, Shaham Y, Stewart J: The role of corticotropin-releasing factor and corticosterone in stress- and cocaine-induced relapse to cocaine seeking in rats. J Neurosci (1998) 18(14): 5529-5536.
77. Shaham Y, Funk D, Erb S, Brown TJ, Walker CD, Stewart J: Corticotropin-releasing factor, but not corticosterone, is involved in stress-induced relapse to heroin-seeking in rats. J Neurosci (1997) 17(7):2605-2614.
78. Brown ZJ, Tribe E, D'souza NA, Erb S: Interaction between noradrenaline and corticotrophin-releasing factor in the reinstatement of cocaine seeking in the rat. Psychopharmacology (2009) 203(1):121-130.
79. Ghitza UE, Gray SM, Epstein DH, Rice KC, Shaham Y: The anxiogenic drug yohimbine reinstates palatable food seeking in a rat relapse model: A role of CRF1 receptors. Neuropsychopharmacology (2006) 31(10):2188-2196.
80. Volkow ND, Fowler JS: Addiction, a disease of compulsion and drive: Involvement of the orbitofrontal cortex. Cereb Cortex (2000) 10(3):318-325.
81. Binneman B, Feltner D, Kolluri S, Shi Y, Qiu R, Stiger T: A 6-week randomized, placebo-controlled trial of CP-316,311 (a selective CRH1 antagonist) in the treatment of major depression. Am J Psychiatry (2008) 165(5):617-620.
82. Zobel AW, Nickel T, Kunzel HE, Ackl N, Sonntag A, Ising M, Holsboer F: Effects of the high-affinity corticotropin-releasing hormone receptor 1 antagonist R121919 in major depression: The first 20 patients treated. J Psychiatr Res (2000) 34(3):171-181.
83. Held K, Künzel H, Ising M, Schmid DA, Zobel A, Murck H, Holsboer F, Steiger A: Treatment with the CRH1-receptor-antagonist R121919 improves sleep-EEG in patients with depression. J Psychiatr Res (2004) 38(2):129-136.
84. Zorrilla EP, Koob GF: The therapeutic potential of CRF1 antagonists for anxiety. Expert Opin Invest Drugs (2004) 13(7):799-828.
85. Steckler T, Dautzenberg FM: Corticotropin-releasing factor receptor antagonists in affective disorders and drug dependence - An update. CNS Neurol Disord Drug Targets (2006) 5(2):147-165.
86. Holsboer F, Ising M: Central CRH system in depression and anxiety: Evidence from clinical studies with CRH1 receptor antagonists. Eur J Pharmacol (2008) 583(2-3):350-357.
87. Blomeyer D, Treutlein J, Esser G, Schmidt MH, Schumann G, Laucht M: Interaction between CRHR1 gene and stressful life events predicts adolescent heavy alcohol use. Biol Psychiatry (2008) 63(2):146-151.
88. Hansson AC, Cippitelli A, Sommer WH, Fedeli A, Bjork K, Soverchia L, Terasmaa A, Massi M, Heilig M, Ciccocioppo R: Variation at the rat Crhr1 locus and sensitivity to relapse into alcohol seeking induced by environmental stress. Proc Natl Acad Sci USA (2006) 103(41):15236-15241.
89. Hansson AC, Cippitelli A, Sommer WH, Ciccocioppo R, Heilig M: Region-specific down-regulation of Crhr1 gene expression in alcohol-preferring msP rats following ad lib access to alcohol. Addict Biol (2007) 12(1):30-34.
90. Barr CS, Dvoskin RL, Yuan Q, Lipsky RH, Gupte M, Hu X, Zhou Z, Schwandt ML, Lindell SG, McKee M, Becker ML et al: CRH haplotype as a factor influencing cerebrospinal fluid levels of corticotropin-releasing hormone, hypothalamic-pituitaryadrenal axis activity, temperament, and alcohol consumption in rhesus macaques. Arch Gen Psychiatry (2008) 65(8):934-944.
91. Bruijnzeel AW, Gold MS: The role of corticotropin-releasing factor-like peptides in cannabis, nicotine, and alcohol dependence. Brain Res Brain Res Rev (2005) 49(3):505-528.
92. American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders, 4th edition. American Psychiatric Press, Washington DC, USA (1994).
93. Altshuler HL, Phillips PE, Feinhandler DA: Alteration of ethanol selfadministration by naltrexone. Life Sci (1980) 26(9):679-688.
94. Heyser CJ, Moc K, Koob GF: Effects of naltrexone alone and in combination with acamprosate on the alcohol deprivation effect in rats. Neuropsychopharmacology (2003) 28(8):1463-1471.
95. Simms JA, Steensland P, Medina B, Abernathy KE, Chandler LJ, Wise R, Bartlett SE: Intermittent access to 20% ethanol induces high ethanol consumption in Long-Evans and Wistar rats. Alcohol Clin Exp Res (2008) 32(10):1816-1823.
96. Ji D, Gilpin NW, Richardson HN, Rivier CL, Koob GF: Effects of naltrexone, duloxetine, and a corticotropin-releasing factor type 1 receptor antagonist on binge-like alcohol drinking in rats. Behav Pharmacol (2008) 19(1):1-12.
97. Heilig M, Koob GF, Ekman R, Britton KT: Corticotropin-releasing factor and neuropeptide Y: Role in emotional integration. Trends Neurosci (1994) 17(2):80-85.
98. Le Magnen J, Tran G, Durlach J, Martin C: Dose-dependent suppression of the high alcohol intake of chronically intoxicated rats by Ca-acetyl homotaurinate. Alcohol (1987) 4(2):97-102.
99. Liu X, Weiss F: Additive effect of stress and drug cues on reinstatement of ethanol seeking: Exacerbation by history of dependence and role of concurrent activation of corticotropinreleasing factor and opioid mechanisms. J Neurosci (2002) 22(18):7856-7861.
100. Bachteler D, Economidou D, Danysz W, Ciccocioppo R, Spanagel R: The effects of acamprosate and neramexane on cueinduced reinstatement of ethanol-seeking behavior in rat. Neuropsychopharmacology (2005) 30(6):1104-1110.