Evidence for a Long-Lasting Compulsive Alcohol Seeking Phenotype in Rats

Neuropsychopharmacology

Volumn 43, Issue 4, 2018, Pages 728-738

  Giuliano, Chiara ^a   Peña Oliver, Yolanda ^a   Goodlett, Charles R ^b   Cardinal, Rudolf N ^c   Robbins, Trevor W ^a   Bullmore, Edward T ^a,c,d   Belin, David ^a   Everitt, Barry J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; GSK 1521498; MU OPIATE RECEPTOR ANTAGONIST; UNCLASSIFIED DRUG; INDAN DERIVATIVE; MU OPIATE RECEPTOR; N-((3,5-DIFLUORO-3'-(1H-1,2,4-TRIAZOL-3-YL)-4-BIPHENYLYL)METHYL)-2,3-DIHYDRO-1H-INDEN-2-AMINE; TRIAZOLE DERIVATIVE;

ALCOHOL ABSTINENCE; ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL EFFECTIVENESS; COMPULSION; COMPULSIVE LCOHOL SEEKING; CONTROLLED STUDY; DISEASE PREDISPOSITION; DRINKING BEHAVIOR; DRUG SEEKING BEHAVIOR; EVIDENCE BASED PRACTICE; FEAR CONDITIONING TEST; FOOTSHOCK; MALE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PUNISHMENT; RAT; REINFORCEMENT; RELAPSE; RISK ASSESSMENT; RISK FACTOR; TASK PERFORMANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECT; GENETICS; PHENOTYPE; PHYSIOLOGY; PSYCHOLOGY; TIME FACTOR;

ALCOHOL DRINKING; ANIMALS; COMPULSIVE BEHAVIOR; DRUG-SEEKING BEHAVIOR; ETHANOL; INDANS; MALE; PHENOTYPE; RATS; RECEPTORS, OPIOID, MU; TIME FACTORS; TRIAZOLES;

EID: 85041725655     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2017.105     Document Type: Article

References (58)

1. American Psychiatric Association (2013). Diagnostic and Statistical Manual of Mental Disorders. Available at ohttp://dsm.psychia tryonline.org/doi/book/10.1176/appi.books.97808904255964.
2. Barkley-Levenson AM, Crabbe JC (2015). Genotypic and sex differences in anxiety-like behavior and alcohol-induced anxio-lysis in High Drinking in the Dark selected mice. Alcohol 49: 29-36.
3. Belin D, Berson N, Balado E, Piazza PV, Deroche-Gamonet V (2011). High-novelty-preference rats are predisposed to compulsive cocaine self-administration. Neuropsychopharmacology 36: 569-579.
4. Belin D, Mar AC, Dalley JW, Robbins TW, Everitt BJ (2008). High impulsivity predicts the switch to compulsive cocaine-taking. Science 320: 1352-1355.
5. Belin-Rauscent A, Fouyssac M, Bonci A, Belin D (2016). How preclinical models evolved to resemble the diagnostic criteria of drug addiction. Biol Psychiatry 79: 39-46.
6. Blasio A, Steardo L, Sabino V, Cottone P (2014). Opioid system in the medial prefrontal cortex mediates binge-like eating. Addict Biol 19: 652-662.
7. Carnicella S, Ron D, Barak S (2014). Intermittent ethanol access schedule in rats as a preclinical model of alcohol abuse. Alcohol 48: 243-252.
8. Chen BT, Yau H-J, Hatch C, Kusumoto-Yoshida I, Cho SL, Hopf FW et al (2013). Rescuing cocaine-induced prefrontal cortex hypoactivity prevents compulsive cocaine seeking. Nature 496: 359-362.
9. Cooper A, Barnea-Ygael N, Levy D, Shaham Y, Zangen A (2007). A conflict rat model of cue-induced relapse to cocaine seeking. Psychopharmacology (Berl) 194: 117-125.
10. Corbit LH, Nie H, Janak PH (2012). Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol Psychiatry 72: 389-395.
11. Czachowski CL, Delory MJ (2009). Acamprosate and naltrexone treatment effects on ethanol and sucrose seeking and intake in ethanol-dependent and nondependent rats. Psychopharmacology (Berl) 204: 335-348.
12. Deroche-Gamonet V, Belin D, Piazza PV (2004). Evidence for addiction-like behavior in the rat. Science 305: 1014-1017.
13. Engeln M, Ansquer S, Dugast E, Bezard E, Belin D, Fernagut P-O (2016). Multi-facetted impulsivity following nigral degeneration and dopamine replacement therapy. Neuropharmacology 109: 69-77.
14. Epstein DH, Preston KL, Stewart J, Shaham Y (2006). Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology (Berl) 189: 1-16.
15. Everitt BJ, Robbins TW (2015). Drug addiction: updating actions to habits to compulsions ten years on. Annu Rev Psychol 67: 23-50.
16. Franck J, Jayaram-Lindström N (2013). Pharmacotherapy for alcohol dependence: status of current treatments. Curr Opin Neurobiol 23: 692-699.
17. Giuliano C, Goodlett CR, Economidou D, García-Pardo MP, Belin D, Robbins TW et al (2015). The novel μ-opioid receptor antagonist GSK1521498 decreases both alcohol seeking and drinking: evidence from a new preclinical model of alcohol seeking. Neuropsychopharmacology 40: 2981-2992.
18. Giuliano C, Robbins TW, Nathan PJ, Bullmore ET, Everitt BJ (2012). Inhibition of opioid transmission at the μ-opioid receptor prevents both food seeking and binge-like eating. Neuropsycho-pharmacology 37: 2643-2652.
19. Giuliano C, Robbins TW, Wille DR, Bullmore ET, Everitt BJ (2013). Attenuation of cocaine and heroin seeking by μ-opioid receptor antagonism. Psychopharmacology (Berl) 227: 137-147.
20. Hendershot CS, Wardell JD, Samokhvalov AV, Rehm J (2016). Effects of naltrexone on alcohol self-administration and craving: meta-analysis of human laboratory studies. Addict Biol 14: (doi:10.1111/adb.12425).
21. Hopf FW, Lesscher HMB (2014). Rodent models for compulsive alcohol intake. Alcohol 48: 253-264.
22. Ignar DM, Goetz AS, Noble KN, Carballo LH, Stroup AE, Fisher JC et al (2011). Regulation of ingestive behaviors in the rat by GSK1521498, a novel micro-opioid receptor-selective inverse agonist. J Pharmacol Exp Ther 339: 24-34.
23. Kelly E, Mundell SJ, Sava A, Roth AL, Felici A, Maltby K et al (2015). The opioid receptor pharmacology of GSK1521498 compared to other ligands with differential effects on compulsive reward-related behaviours. Psychopharmacology (Berl) 232: 305-314.
24. Knight CP, Hauser SR, Deehan GA, Toalston JE, McBride WJ, Rodd ZA (2016). Oral conditioned cues can enhance or inhibit ethanol (EtOH)-seeking and EtOH-relapse drinking by alcohol-preferring (P) rats. Alcohol Clin Exp Res 40: 906-915.
25. Koob GF (2003). Alcoholism: allostasis and beyond. Alcohol Clin Exp Res 27: 232-243.
26. Koob GF, Rassnick S, Heinrichs S, Weiss F (1994). Alcohol, the reward system and dependence. EXS 71: 103-114.
27. Koob GF, Volkow ND (2010). Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238.
28. Lê A, Shaham Y (2002). Neurobiology of relapse to alcohol in rats. Pharmacol Ther 94: 137-156.
29. Marchant NJ, Khuc TN, Pickens CL, Bonci A, Shaham Y (2013). Context-induced relapse to alcohol seeking after punishment in a rat model. Biol Psychiatry 73: 256-262.
30. Mayo LM, de Wit H (2016). Acquisition of conditioned responses to a novel alcohol-paired cue in social drinkers. J Stud Alcohol Drugs 77: 317-326.
31. McBride WJ, Rodd ZA, Bell RL, Lumeng L, Li T-K (2014). The alcohol-preferring (P) and high-alcohol-drinking (HAD) rats-animal models of alcoholism. Alcohol 48: 209-215.
32. McKim TH, Shnitko TA, Robinson DL, Boettiger CA (2016). Translational research on habit and alcohol. Curr Addict Rep 3: 37-49.
33. Merlo E, Milton AL, Goozée ZY, Theobald DE, Everitt BJ (2014). Reconsolidation and extinction are dissociable and mutually exclusive processes: behavioral and molecular evidence. J Neurosci 34: 2422-2431.
34. Monti PM, Rohsenow DJ, Hutchison KE, Swift RM, Mueller TI, Colby SM et al (1999). Naltrexone's effect on cue-elicited craving among alcoholics in treatment. Alcohol Clin Exp Res 23: 1386-1394.
35. Murray JE, Belin-Rauscent A, Simon M, Giuliano C, Benoit-Marand M, Everitt BJ et al (2015). Basolateral and central amygdala differentially recruit and maintain dorsolateral striatum-dependent cocaine-seeking habits. Nat Commun 6: 10088.
36. O'Brien CP, Childress AR, McLellan AT, Ehrman R (1992). Classical conditioning in drug-dependent humans. Ann N Y Acad Sci 654: 400-415.
37. Pelloux Y, Everitt BJ, Dickinson A (2007). Compulsive drug seeking by rats under punishment: effects of drug taking history. Psychopharmacology (Berl) 194: 127-137.
38. Peña-Oliver Y, Giuliano C, Economidou D, Goodlett CR, Robbins TW, Dalley JW et al (2015). Alcohol-preferring rats show goal oriented behaviour to food incentives but are neither sign-trackers nor impulsive. PLoS ONE 10: e0131016.
39. Richardson NR, Roberts DC (1996). Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J Neurosci Methods 66: 1-11.
40. Ripley TL, Sanchez-Roige S, Bullmore ET, Mugnaini M, Maltby K, Miller SR et al (2015). The novel mu-opioid antagonist, GSK1521498, reduces ethanol consumption in C57BL/6J mice. Psychopharmacology (Berl) 232: 3431-3441.
41. Rösner S, Hackl-Herrwerth A, Leucht S, Vecchi S, Srisurapanont M, Soyka M (2010). Opioid antagonists for alcohol dependence. Cochrane Database Syst Rev 8: CD001867.
42. Russo SJ, Murrough JW, Han M-H, Charney DS, Nestler EJ (2012). Neurobiology of resilience. Nat Neurosci 15: 1475-1484.
43. Seif T, Chang S-J, Simms JA, Gibb SL, Dadgar J, Chen BT et al (2013). Cortical activation of accumbens hyperpolarization-active NMDARs mediates aversion-resistant alcohol intake. Nat Neurosci 16: 1094-1100.
44. Spanagel R (2000). Recent animal models of alcoholism. Alcohol Res Health 24: 124-131.
45. Spanagel R, Hölter SM (1999). Long-term alcohol self-administration with repeated alcohol deprivation phases: an animal model of alcoholism? Alcohol Alcohol 34: 231-243.
46. Tabakoff B, Saba L, Printz M, Flodman P, Hodgkinson C, Goldman D et al (2009). Genetical genomic determinants of alcohol consumption in rats and humans. BMC Biol 7: 70.
47. Turyabahika-Thyen K, Wolffgramm J (2006). Loss of flexibility in alcohol-taking rats: promoting factors. Eur Addict Res 12: 210-221.
48. Tye KM, Cone JJ, Schairer WW, Janak PH (2010). Amygdala neural encoding of the absence of reward during extinction. J Neurosci 30: 116-125.
49. Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC (2013). Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 16: 42-47.
50. Vendruscolo LF, Barbier E, Schlosburg JE, Misra KK, Whitfield TW, Logrip ML et al (2012). Corticosteroid-dependent plasticity mediates compulsive alcohol drinking in rats. J Neurosci 32: 7563-7571.
51. Vengeliene V, Bilbao A, Molander A, Spanagel R (2008). Neuro-pharmacology of alcohol addiction. Br J Pharmacol 154: 299-315.
52. Vengeliene V, Bilbao A, Spanagel R (2014). The alcohol deprivation effect model for studying relapse behavior: a comparison between rats and mice. Alcohol 48: 313-320.
53. Vengeliene V, Celerier E, Chaskiel L, Penzo F, Spanagel R (2009). Compulsive alcohol drinking in rodents. Addict Biol 14: 384-396.
54. Weiss F, Ciccocioppo R, Parsons LH, Katner S, Liu X, Zorrilla EP et al (2001). Compulsive drug-seeking behavior and relapse. Ann N Y Acad Sci 937: 1-26.
55. Wolffgramm J (1991). An ethopharmacological approach to the development of drug addiction. Neurosci Biobehav Rev 15: 515-519.
56. Zapata A, Minney VL, Shippenberg TS (2010). Shift from goal-directed to habitual cocaine seeking after prolonged experience in rats. J Neurosci 30: 15457-15463.
57. Ziauddeen H, Chamberlain SR, Nathan PJ, Koch A, Maltby K, Bush M et al (2013). Effects of the mu-opioid receptor antagonist GSK1521498 on hedonic and consummatory eating behaviour: a proof of mechanism study in binge-eating obese subjects. Mol Psychiatry 18: 1287-1293.
58. Ziauddeen H, Nestor LJ, Subramaniam N, Dodds C, Nathan PJ, Miller SR et al (2016). Opioid antagonists and the A118G polymorphism in the μ-opioid receptor gene: effects of GSK1521498 and naltrexone in healthy drinkers stratified by OPRM1 genotype. Neuropsychopharmacology 41: 2647-2657.