Neurobiology of an endophenotype: Modeling the progression of alcohol addiction in rodents

Current Opinion in Neurobiology

Volumn 23, Issue 4, 2013, Pages 607-614

  Mahoney, Megan K ^a   Olmstead, Mary C ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; ACETYLCHOLINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABINOID 1 RECEPTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROKININ 1 RECEPTOR; NEUROPEPTIDE Y; OREXIN 1 RECEPTOR; OREXIN 2 RECEPTOR; SEROTONIN 1A RECEPTOR; SEROTONIN 3 RECEPTOR; SEROTONIN 6 RECEPTOR;

ALCOHOL CONSUMPTION; ALCOHOLISM; ASSOCIATION; BRAIN REGION; CENTRAL NUCLEUS (AMYGDALA); COMPULSION; DISEASE ASSOCIATION; DISEASE COURSE; DOPAMINE RELEASE; DRUG SEEKING BEHAVIOR; DRUG USE; ENDOPHENOTYPE; GABAERGIC TRANSMISSION; HUMAN; MEDIAN RAPHE NUCLEUS; NEUROBIOLOGY; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION;

EID: 84881022302     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2013.03.006     Document Type: Review

References (103)

1. Weiss F. Alcohol self-administration. Animal Models of Drug Addiction 2011, 133-165. Humana Press. M.C. Olmstead (Ed.).
2. American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders. Washington, DC; 2000.
3. Belin D., Economidou D., Pelloux Y., Everitt B.J. Habit formation and compulsion. Animal Models of Drug Addiction 2011, 337-378. Humana Press. M.C. Olmstead (Ed.).
4. De Bruin N.M.W.J., McCreary A.C., Van Loevezijn A., De Vries T.J., Venhorst J., Van Drimmelen M., Kruse C.G. A novel highly selective 5-HT(6) receptor antagonist attenuates ethanol and nicotine seeking but does not affect inhibitory response control in Wistar rats. Behav Brain Res 2013, 236:157-165.
5. Steensland P., Fredriksson I., Holst S., Feltmann K., Franck J., Schilström B., Carlsson A. The monoamine stabilizer (-)-OSU6162 attenuates voluntary ethanol intake and ethanol-induced dopamine output in nucleus accumbens. Biol Psychiatry 2012, 72:823-831.
6. Chaudhri N., Sahuque L.L., Janak P.H. Ethanol seeking triggered by environmental context is attenuated by blocking dopamine D1 receptors in the nucleus accumbens core and shell in rats. Psychopharmacology (Berl) 2009, 207:303-314.
7. Chaudhri N., Sahuque L.L., Schairer W.W., Janak P.H. Separable roles of the nucleus accumbens core and shell in context- and cue-induced alcohol-seeking. Neuropsychopharmacology 2010, 35:783-791.
8. Wouda J.A., Riga D., De Vries W., Stegeman M., Van Mourik Y., Schetters D., Schoffelmeer A.N.M., Pattij T., De Vries T.J., Vries W., et al. Varenicline attenuates cue-induced relapse to alcohol, but not nicotine seeking, while reducing inhibitory response control. Psychopharmacology (Berl) 2011, 216:267-277.
9. De Bruin N.M.W.J., Lange J.H.M., Kruse C.G., Herremans A.H., Schoffelmeer A.N.M., Van Drimmelen M., De Vries T.J. SLV330, a cannabinoid CB(1) receptor antagonist, attenuates ethanol and nicotine seeking and improves inhibitory response control in rats. Behav Brain Res 2011, 217:408-415.
10. 1 receptors. Br J Pharmacol 2011, 162:880-889.
11. Dayas C.V., Liu X., Simms J.A., Weiss F. Distinct patterns of neural activation associated with ethanol seeking: effects of naltrexone. Biol Psychiatry 2007, 61:979-989.
12. Schank J.R., Goldstein A.L., Rowe K.E., King C.E., Marusich J.A., Wiley J.L., Carroll F.I., Thorsell A., Heilig M. The kappa opioid receptor antagonist JDTic attenuates alcohol seeking and withdrawal anxiety. Addict Biol 2012, 17:634-647.
13. Deehan G.A., Mckinzie D.L., Carroll F.I., McBride W.J., Rodd Z.A. The long-lasting effects of JDTic, a kappa opioid receptor antagonist, on the expression of ethanol-seeking behavior and the relapse drinking of female alcohol-preferring (P) rats. Pharmacol Biochem Behav 2012, 101:581-587.
14. Martin-Fardon R., Weiss F. N-(2-methyl-6-benzoxazolyl)-N'-1,5-naphthyridin-4-yl urea (SB334867), a hypocretin receptor-1 antagonist, preferentially prevents ethanol seeking: comparison with natural reward seeking. Addict Biol 2012, 10.1111/j.1369-1600.2012.00480.x.
15. Stopponi S., Somaini L., Cippitelli A., De Guglielmo G., Kallupi M., Cannella N., Gerra G., Massi M., Ciccocioppo R., Guglielmo G. Pregabalin reduces alcohol drinking and relapse to alcohol seeking in the rat. Psychopharmacology (Berl) 2012, 220:87-96.
16. Willcocks A.L., Mcnally G.P. The role of medial prefrontal cortex in extinction and reinstatement of alcohol-seeking in rats. Eur J Neurosci 2013, 37:173-338.
17. Sinclair C.M., Cleva R.M., Hood L.E., Olive M.F., Gass J.T. mGluR5 receptors in the basolateral amygdala and nucleus accumbens regulate cue-induced reinstatement of ethanol-seeking behavior. Pharmacol Biochem Behav 2012, 101:329-335.
18. Zhao Y., Dayas C.V., Aujla H., Baptista M.A.S., Martin-Fardon R., Weiss F. Activation of group II metabotropic glutamate receptors attenuates both stress and cue-induced ethanol-seeking and modulates c-fos expression in the hippocampus and amygdala. J Neurosci 2006, 26:9967-9974.
19. Kufahl P.R., Martin-Fardon R., Weiss F. Enhanced sensitivity to attenuation of conditioned reinstatement by the mGluR 2/3 agonist LY379268 and increased functional activity of mGluR 2/3 in rats with a history of ethanol dependence. Neuropsychopharmacology 2011, 36:2762-2773.
20. Brown R.M., Mustafa S., Ayoub M.A., Dodd P.R., Pfleger K.D.G., Lawrence A.J. mGlu5 receptor functional interactions and addiction. Front Pharmacol 2012, 3:84.
21. O'Connor E.C., Crombag H.S., Mead A.N., Stephens D.N. The mGluR5 antagonist MTEP dissociates the acquisition of predictive and incentive motivational properties of reward-paired stimuli in mice. Neuropsychopharmacology 2010, 35:1807-1817.
22. Cannady R., Fisher K.R., Durant B., Besheer J., Hodge C.W. Enhanced AMPA receptor activity increases operant alcohol self-administration and cue-induced reinstatement. Addict Biol 2013, 18:54-65.
23. Richards J.K., Simms J.A., Steensland P., Taha S.A., Borgland S.L., Bonci A., Bartlett S.E. Inhibition of orexin-1/hypocretin-1 receptors inhibits yohimbine-induced reinstatement of ethanol and sucrose seeking in Long-Evans rats. Psychopharmacology (Berl) 2008, 199:109-117.
24. Schank J.R., Pickens C.L., Rowe K.E., Cheng K., Thorsell A., Rice K.C., Shaham Y., Heilig M. Stress-induced reinstatement of alcohol-seeking in rats is selectively suppressed by the neurokinin 1 (NK1) antagonist L822429. Psychopharmacology (Berl) 2011, 218:111-119.
25. Lê A.D., Funk D., Juzytsch W., Coen K., Navarre B.M., Cifani C., Shaham Y. Effect of prazosin and guanfacine on stress-induced reinstatement of alcohol and food seeking in rats. Psychopharmacology (Berl) 2011, 218:89-99.
26. Nielsen C.K., Simms J.A., Bito-Onon J.J., Li R., Ananthan S., Bartlett S.E. The delta opioid receptor antagonist, SoRI-9409, decreases yohimbine stress-induced reinstatement of ethanol-seeking. Addict Biol 2012, 17:224-234.
27. Lê A.D., Funk D., Coen K., Li Z., Shaham Y. Role of corticotropin-releasing factor in the median raphe nucleus in yohimbine-induced reinstatement of alcohol seeking in rats. Addict Biol 2011, 10.1111/j.1369-1600.2011.00374.x.
28. Simms J.A., Haass-Koffler C.L., Bito-Onon J., Li R., Bartlett S.E. Mifepristone in the central nucleus of the amygdala reduces yohimbine stress-induced reinstatement of ethanol-seeking. Neuropsychopharmacology 2012, 37:906-918.
29. Cippitelli A., Damadzic R., Hansson A.C., Singley E., Sommer W.H., Eskay R., Thorsell A., Heilig M. Neuropeptide Y (NPY) suppresses yohimbine-induced reinstatement of alcohol seeking. Psychopharmacology (Berl) 2010, 208:417-426.
30. Gilpin N.W. Corticotropin-releasing factor (CRF) and neuropeptide Y (NPY): effects on inhibitory transmission in central amygdala, and anxiety- & alcohol-related behaviors. Alcohol 2012, 46:329-337.
31. Lê A.D., Funk D., Harding S., Juzytsch W., Fletcher P.J., Le D. The role of noradrenaline and 5-hydroxytryptamine in yohimbine-induced increases in alcohol-seeking in rats. Psychopharmacology (Berl) 2009, 204:477-488.
32. Lê A.D., Funk D., Harding S., Juzytsch W., Fletcher P.J., Shaham Y. Effects of dexfenfluramine and 5-HT3 receptor antagonists on stress-induced reinstatement of alcohol seeking in rats. Psychopharmacology (Berl) 2006, 186:82-92.
33. Lê A.D., Poulos C.X., Harding S., Watchus J., Juzytsch W., Shaham Y. Effects of naltrexone and fluoxetine on alcohol self-administration and reinstatement of alcohol seeking induced by priming injections of alcohol and exposure to stress. Neuropsychopharmacology 1999, 21:435-444.
34. Peana A.T., Giugliano V., Rosas M., Sabariego M., Acquas E. Effects of l-cysteine on reinstatement of ethanol-seeking behavior and on reinstatement-elicited extracellular signal-regulated kinase phosphorylation in the rat nucleus accumbens shell. Alcohol Clin Exp Res 2012, 37:E1-E43.
35. Wang J., Lanfranco M.F., Gibb S.L., Yowell Q.V., Carnicella S., Ron D. Long-lasting adaptations of the NR2B-containing NMDA receptors in the dorsomedial striatum play a crucial role in alcohol consumption and relapse. J Neurosci 2010, 30:10187-10198.
36. Shoblock J.R., Welty N., Aluisio L., Fraser I., Motley S.T., Morton K., Palmer J., Bonaventure P., Carruthers N.I., Lovenberg T.W., et al. Selective blockade of the orexin-2 receptor attenuates ethanol self-administration, place preference, and reinstatement. Psychopharmacology (Berl) 2011, 215:191-203.
37. Sperling R.E., Gomes S.M., Sypek E.I., Carey A.N., McLaughlin J.P. Endogenous kappa-opioid mediation of stress-induced potentiation of ethanol-conditioned place preference and self-administration. Psychopharmacology (Berl) 2010, 210:199-209.
38. Lê A.D., Lê Dzung A., Funk D., Harding S., Juzytsch W., Li Z., Fletcher P.J. Intra-median raphe nucleus (MRN) infusions of muscimol, a GABA-A receptor agonist, reinstate alcohol seeking in rats: role of impulsivity and reward. Psychopharmacology (Berl) 2008, 195:605-615.
39. Lê A.D., Lo S., Harding S., Juzytsch W., Marinelli P.W., Funk D. Coadministration of intravenous nicotine and oral alcohol in rats. Psychopharmacology (Berl) 2010, 208:475-486.
40. Lê A.D., Wang A., Harding S., Juzytsch W., Shaham Y. Nicotine increases alcohol self-administration and reinstates alcohol seeking in rats. Psychopharmacology (Berl) 2003, 168:216-221.
41. Bhutada P., Mundhada Y., Ghodki Y., Dixit P., Umathe S., Jain K. Acquisition, expression, and reinstatement of ethanol-induced conditioned place preference in mice: effects of exposure to stress and modulation by mecamylamine. J Psychopharmacol 2012, 26:315-323.
42. Bäckström P., Bachteler D., Koch S., Hyytiä P., Spanagel R. mGluR5 antagonist MPEP reduces ethanol-seeking and relapse behavior. Neuropsychopharmacology 2004, 29:921-928.
43. Sidhpura N., Weiss F., Martin-Fardon R. Effects of the mGlu2/3 agonist LY379268 and the mGlu5 antagonist MTEP on ethanol seeking and reinforcement are differentially altered in rats with a history of ethanol dependence. Biol Psychiatry 2010, 67:804-811.
44. Wang Y.T. Probing the role of AMPAR endocytosis and long-term depression in behavioural sensitization: relevance to treatment of brain disorders, including drug addiction. Br J Pharmacol 2008, 153(Suppl):S389-S395.
45. Bachteler D., Economidou D., Danysz W., Ciccocioppo R., Spanagel R. The effects of acamprosate and neramexane on cue-induced reinstatement of ethanol-seeking behavior in rat. Neuropsychopharmacology 2005, 30:1104-1110.
46. Kalivas P.W., LaLumiere R.T., Knackstedt L., Shen H. Glutamate transmission in addiction. Neuropharmacology 2009, 56(Suppl 1):169-173.
47. Tsai G., Coyle J.T. The role of glutamatergic neurotransmission in the pathophysiology of alcoholism. Annu Rev Med 1998, 49:173-184.
48. Spanagel R., Zieglgänsberger W. Anti-craving compounds for ethanol: new pharmacological tools to study addictive processes. Trends Pharmacol Sci 1997, 18:54-59.
49. Spanagel R., Hölter S.M. Pharmacological validation of a new animal model of alcoholism. J Neural Transm 2000, 107:669-680.
50. Spanagel R. Alcoholism: a systems approach from molecular physiology to addictive behavior. Physiol Rev 2009, 89:649-705.
51. Rodd-Henricks Z.A., Mckinzie D.L., Edmundson V.E., Dagon C.L., Murphy J.M., McBride W.J., Lumeng L., Li T.K. Effects of 5-HT(3) receptor antagonists on daily alcohol intake under acquisition, maintenance, and relapse conditions in alcohol-preferring (P) rats. Alcohol 2000, 21:73-85.
52. López-Moreno J.A., González-Cuevas G., Rodríguez de Fonseca F., Navarro M. Long-lasting increase of alcohol relapse by the cannabinoid receptor agonist WIN 55,212-2 during alcohol deprivation. J Neurosci 2004, 24:8245-8252.
53. Kuzmin A., Jerlhag E., Liljequist S., Engel J. Effects of subunit selective nACh receptors on operant ethanol self-administration and relapse-like ethanol-drinking behavior. Psychopharmacology (Berl) 2009, 203:99-108.
54. Gilpin N.W., Stewart R.B., Murphy J.M., Li T.-K., Badia-Elder N.E. Neuropeptide Y reduces oral ethanol intake in alcohol-preferring (P) rats following a period of imposed ethanol abstinence. Alcohol Clin Exp Res 2003, 27:787-794.
55. Vengeliene V., Bachteler D., Danysz W., Spanagel R. The role of the NMDA receptor in alcohol relapse: a pharmacological mapping study using the alcohol deprivation effect. Neuropharmacology 2005, 48:822-829.
56. Colombo G., Serra S., Vacca G., Carai M.A.M., Gessa G.L. Baclofen-induced suppression of alcohol deprivation effect in Sardinian alcohol-preferring (sP) rats exposed to different alcohol concentrations. Eur J Pharmacol 2006, 550:123-126.
57. Wise R.A. Voluntary ethanol intake in rats following exposure to ethanol on various schedules. Psychopharmacologia 1973, 29:203-210.
58. Holter S.M., Engelmann M., Kirschke C., Liebsch G., Landgraf R., Spanagel R. Long-term ethanol self-administration with repeated ethanol deprivation episodes changes ethanol drinking pattern and increases anxiety-related behaviour during ethanol deprivation in rats. Behav Pharmacol 1998, 9:41-48.
59. Wolffgramm J., Heyne A. From controlled drug intake to loss of control: the irreversible development of drug addiction in the rat. Behav Brain Res 1995, 70:77-94.
60. Nielsen C.K., Simms J.A., Li R., Mill D., Yi H., Feduccia A.A., Santos N., Bartlett S.E. δ-Opioid receptor function in the dorsal striatum plays a role in high levels of ethanol consumption in rats. J Neurosci 2012, 32:4540-4552.
61. Sabino V., Kwak J., Rice K.C., Cottone P. Pharmacological characterization of the 20% alcohol intermittent access model in sardinian alcohol-preferring rats: a model of binge-like drinking. Alcohol Clin Exp Res 2012, 10.1111/acer.12008.
62. Bustamante D., Quintanilla M.E., Tampier L., Gonzalez-Lira V., Israel Y., Herrera-Marschitz M. Ethanol induces stronger dopamine release in nucleus accumbens (shell) of alcohol-preferring (bibulous) than in alcohol-avoiding (abstainer) rats. Eur J Pharmacol 2008, 591:153-158.
63. Logrip M.L., Janak P.H., Ron D. Escalating ethanol intake is associated with altered corticostriatal BDNF expression. J Neurochem 2009, 109:1459-1468.
64. Jeanblanc J., He D.-Y., McGough N.N.H., Logrip M.L., Phamluong K., Janak P.H., Ron D. The dopamine D3 receptor is part of a homeostatic pathway regulating ethanol consumption. J Neurosci 2006, 26:1457-1464.
65. Knapp D.J., Overstreet D.H., Huang M., Wills T.A., Whitman B.A., Angel R.A., Sinnett S.E., Breese G.R. Effects of a stressor and corticotrophin releasing factor on ethanol deprivation-induced ethanol intake and anxiety-like behavior in alcohol-preferring P rats. Psychopharmacology (Berl) 2011, 218:179-189.
66. Hwa L.S., Debold J.F., Miczek K.A. Alcohol in excess: CRF(1) receptors in the rat and mouse VTA and DRN. Psychopharmacology (Berl) 2013, 225:313-327.
67. Cippitelli A., Damadzic R., Singley E., Thorsell A., Ciccocioppo R., Eskay R.L., Heilig M. Pharmacological blockade of corticotropin-releasing hormone receptor 1 (CRH1R) reduces voluntary consumption of high alcohol concentrations in non-dependent Wistar rats. Pharmacol Biochem Behav 2012, 100:522-529.
68. Schroeder J.P., Overstreet D.H., Hodge C.W. The mGluR5 antagonist MPEP decreases operant ethanol self-administration during maintenance and after repeated alcohol deprivations in alcohol-preferring (P) rats. Psychopharmacology (Berl) 2005, 179:262-270.
69. Gilpin N.W., Misra K., Koob G.F. Neuropeptide Y in the central nucleus of the amygdala suppresses dependence-induced increases in alcohol drinking. Pharmacol Biochem Behav 2008, 90:475-480.
70. Koob G.F. A role for brain stress systems in addiction. Neuron 2008, 59:11-34.
71. Walker B.M. Conceptualizing withdrawal-induced escalation of alcohol self-administration as a learned, plasticity-dependent process. Alcohol 2012, 46:339-348.
72. Gilpin N.W., Misra K., Herman M.A., Cruz M.T., Koob G.F., Roberto M. Neuropeptide Y opposes alcohol effects on gamma-aminobutyric acid release in amygdala and blocks the transition to alcohol dependence. Biol Psychiatry 2011, 69:1091-1099.
73. Roberto M., Cruz M.T., Gilpin N.W., Sabino V., Schweitzer P., Bajo M., Cottone P., Madamba S.G., Stouffer D.G., Zorrilla E.P., et al. Corticotropin releasing factor-induced amygdala gamma-aminobutyric acid release plays a key role in alcohol dependence. Biol Psychiatry 2010, 67:831-839.
74. Vendruscolo L.F., Barbier E., Schlosburg J.E., Misra K.K., Whitfield T.W., Logrip M.L., Rivier C., Repunte-Canonigo V., Zorrilla E.P., Sanna P.P., et al. Corticosteroid-dependent plasticity mediates compulsive alcohol drinking in rats. J Neurosci 2012, 32:7563-7571.
75. George O., Sanders C., Freiling J., Grigoryan E., Vu S., Allen C.D., Crawford E., Mandyam C.D., Koob G.F. Recruitment of medial prefrontal cortex neurons during alcohol withdrawal predicts cognitive impairment and excessive alcohol drinking. Proc Natl Acad Sci U S A 2012, 109:18156-18161.
76. Funk C.K., O'Dell L.E., Crawford E.F., Koob G.F. Corticotropin-releasing factor within the central nucleus of the amygdala mediates enhanced ethanol self-administration in withdrawn, ethanol-dependent rats. J Neurosci 2006, 26:11324-11332.
77. Nealey K.A., Smith A.W., Davis S.M., Smith D.G., Walker B.M. κ-Opioid receptors are implicated in the increased potency of intra-accumbens nalmefene in ethanol-dependent rats. Neuropharmacology 2011, 61:35-42.
78. Gilpin N.W., Koob G.F. Effects of β-adrenoceptor antagonists on alcohol drinking by alcohol-dependent rats. Psychopharmacology (Berl) 2010, 212:431-439.
79. Walker B.M., Rasmussen D.D., Raskind M.A., Koob G.F. Alpha1-noradrenergic receptor antagonism blocks dependence-induced increases in responding for ethanol. Alcohol 2008, 42:91-97.
80. Maccioni P., Zaru A., Loi B., Lobina C., Carai M.A.M., Gessa G.L., Capra A., Mugnaini C., Pasquini S., Corelli F., et al. Comparison of the effect of the GABA(B) receptor agonist, baclofen, and the positive allosteric modulator of the GABA(B) receptor, GS39783, on alcohol self-administration in 3 different lines of alcohol-preferring rats. Alcohol Clin Exp Res 2012, 36:1748-1766.
81. Walker B.M., Koob G.F. The gamma-aminobutyric acid-B receptor agonist baclofen attenuates responding for ethanol in ethanol-dependent rats. Alcohol Clin Exp Res 2007, 31:11-18.
82. 1 receptor antagonist SB-334867 dissociates the motivational properties of alcohol and sucrose in rats. Brain Res 2011, 1391:54-59.
83. Economidou D., Mattioli L., Cifani C., Perfumi M., Massi M., Cuomo V., Trabace L., Ciccocioppo R. Effect of the cannabinoid CB1 receptor antagonist SR-141716A on ethanol self-administration and ethanol-seeking behaviour in rats. Psychopharmacology (Berl) 2006, 183:394-403.
84. Besheer J., Faccidomo S., Grondin J.J.M., Hodge C.W. Regulation of motivation to self-administer ethanol by mGluR5 in alcohol-preferring (P) rats. Alcohol Clin Exp Res 2008, 32:209-221.
85. Verplaetse T.L., Rasmussen D.D., Froehlich J.C., Czachowski C.L. Effects of prazosin, an α1-adrenergic receptor antagonist, on the seeking and intake of alcohol and sucrose in alcohol-preferring (P) rats. Alcohol Clin Exp Res 2012, 36:881-886.
86. Czachowski C.L., Santini L.A., Legg B.H., Samson H.H. Separate measures of ethanol seeking and drinking in the rat: effects of remoxipride. Alcohol 2002, 28:39-46.
87. Sharpe A.L., Samson H.H. Effect of naloxone on appetitive and consummatory phases of ethanol self-administration. Alcohol Clin Exp Res 2001, 25:1006-1011.
88. Dickinson A., Wood N., Smith J.W. Alcohol seeking by rats: action or habit?. Q J Exp Psychol B 2002, 55:331-348.
89. Hopf F.W., Chang S.-J., Sparta D.R., Bowers M.S., Bonci A. Motivation for alcohol becomes resistant to quinine adulteration after 3 to 4 months of intermittent alcohol self-administration. Alcohol Clin Exp Res 2010, 34:1565-1573.
90. Mangieri R.A., Cofresí R.U., Gonzales R.A. Ethanol seeking by Long Evans rats is not always a goal-directed behavior. PLoS ONE 2012, 7:e42886.
91. Corbit L.H., Nie H., Janak P.H. Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol Psychiatry 2012, 72:389-395.
92. Lingawi N., Balleine B. Amygdala central nucleus interacts with dorsolateral striatum to regulate the acquisition of habits. J Neurosci 2012, 32:1073-1081.
93. Marchant N.J., Khuc T.N., Pickens C.L., Bonci A., Shaham Y. Context-induced relapse to alcohol seeking after punishment in a rat model. Biol Psychiatry 2012, 10.1016/j.biopsych.2012.07.007.
94. Ahmed S.H. The science of making drug-addicted animals. Neuroscience 2012, 211:107-125.
95. Lesscher H.M.B., Vanderschuren L.J.M.J. Compulsive drug use and its neural substrates. Rev Neurosci 2012, 23:731-745.
96. Schwabe L., Dickinson A., Wolf O.T. Stress, habits, and drug addiction: a psychoneuroendocrinological perspective. Exp Clin Psychopharm 2011, 19:53-63.
97. Badiani A., Belin D., Epstein D., Calu D., Shaham Y. Opiate versus psychostimulant addiction: the differences do matter. Nat Rev Neurosci 2011, 12:685-700.
98. Edwards S., Koob G.F. Neurobiology of dysregulated motivational systems in drug addiction. Future Neurol 2010, 5:393-401.
99. Breese G.R., Sinha R., Heilig M. Chronic alcohol neuroadaptation and stress contribute to susceptibility for alcohol craving and relapse. Pharmacol Ther 2011, 129:149-171.
100. Heilig M., Egli M., Crabbe J., Becker H. Acute withdrawal, protracted abstinence and negative affect in alcoholism: are they linked?. Addict Biol 2010, 15:169-184.
101. Paterson N., Markou A. Animal models and treatments for addiction and depression co-morbidity. Neurotox Res 2007, 11:1-32.
102. Belin D., Mar A.C., Dalley J.W., Robbins T.W., Everitt B.J. High impulsivity predicts the switch to compulsive cocaine-taking. Science 2008, 320:1352-1355.
103. Belin D., Balado E., Piazza P.V., Deroche-Gamonet V. Pattern of intake and drug craving predict the development of cocaine addiction-like behavior in rats. Biol Psychiatry 2009, 65:863-868.