Advertisement

Modeling Relapse in Animals

  • Rémi Martin-Fardon
  • Friedbert WeissEmail author
Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 13)

Abstract

Alcohol addiction is a chronically relapsing disorder characterized by compulsive alcohol seeking and use. Alcohol craving and long-lasting vulnerability to relapse present a great challenge for the successful treatment of alcohol addiction. Therefore, relapse prevention has emerged as a critically important area of research, with the need for effective and valid animal models of relapse. This chapter provides an overview of the repertoire of animal models of craving and relapse presently available and employed in alcoholism research. These models include conditioned reinstatement, stress-induced reinstatement, ethanol priming-induced reinstatement, conditioned place preference, Pavlovian spontaneous recovery, the alcohol deprivation effect, and seeking-taking chained schedules. Thus, a wide array of animal models is available that permit investigation of behaviors directed at obtaining access to alcohol, as well as neurobehavioral mechanisms and genetic factors that regulate these behaviors. These models also are instrumental for identifying pharmacological treatment targets and as tools for evaluating the efficacy of potential medications for the prevention of alcohol craving and relapse.

Keywords

Conditioned reinstatement Conditioned place preference Alcohol deprivation effect Reinstatement Pavlovian spontaneous recovery Alcohol-seeking behavior 

Notes

Acknowledgments

Supported by grants AA10531, AA014351, and AA018010 from the National Institutes of Health/National Institute on Alcohol Abuse and Alcoholism to FW. The authors thank Michael Arends for editorial assistance.

References

  1. Aguilar MA, Rodríguez-Arias M, Miñarro J (2009) Neurobiological mechanisms of the reinstatement of drug-conditioned place preference. Brain Res Rev 59:253–277PubMedGoogle Scholar
  2. Albus M, Zahn TP, Breier A (1992) Anxiogenic properties of yohimbine. I. Behavioral, physiological and biochemical measures. Eur Arch Psychiatry Clin Neurosci 241:337–344PubMedGoogle Scholar
  3. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th edn (Revised Version). American Psychiatric Association, WashingtonGoogle Scholar
  4. Anton RF (1999) What is craving? Models and implications for treatment. Alcohol Res Health 23:165–173PubMedGoogle Scholar
  5. Banna KM, Back SE, Do P, See RE (2010) Yohimbine stress potentiates conditioned cue-induced reinstatement of heroin-seeking in rats. Behav Brain Res 208:144–148PubMedCentralPubMedGoogle Scholar
  6. Bardo MT, Bevins RA (2000) Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology (Berl) 153:31–43Google Scholar
  7. Bell RL, Rodd ZA, Boutwell CL, Hsu CC, Lumeng L, Murphy JM, Li TK, McBride WJ (2004) Effects of long-term episodic access to ethanol on the expression of an alcohol deprivation effect in low alcohol-consuming rats. Alcohol Clin Exp Res 28:1867–1874PubMedGoogle Scholar
  8. Bhutada PS, Mundhada YR, Ghodki YR, Chaware P, Dixit PV, Jain KS, Umathe SN (2012a) Influence of sigma-1 receptor modulators on ethanol-induced conditioned place preference in the extinction-reinstatement model. Behav Pharmacol 23:25–33Google Scholar
  9. Bhutada P, Mundhada Y, Ghodki Y, Dixit P, Umathe S, Jain K (2012b) Acquisition, expression, and reinstatement of ethanol-induced conditioned place preference in mice: effects of exposure to stress and modulation by mecamylamine. J Psychopharmacol 26:315–323Google Scholar
  10. Bienkowski P, Kostowski W, Koros E (1999a) Ethanol-reinforced behaviour in the rat: effects of naltrexone. Eur J Pharmacol 374:321–327PubMedGoogle Scholar
  11. Bienkowski P, Kostowski W, Koros E (1999b) The role of drug-paired stimuli in extinction and reinstatement of ethanol-seeking behaviour in the rat. Eur J Pharmacol 374:315–319PubMedGoogle Scholar
  12. Bienkowski P, Rogowski A, Korkosz A, Mierzejewski P, Radwanska K, Kaczmarek L, Bogucka-Bonikowska A, Kostowski W (2004) Time-dependent changes in alcohol-seeking behaviour during abstinence. Eur Neuropsychopharmacol 14:355–360PubMedGoogle Scholar
  13. Blanchard RJ, Hori K, Tom P, Blanchard C (1987) Social structure and ethanol consumption in laboratory rats. Pharmacol Biochem Behav 28:437–442PubMedGoogle Scholar
  14. Bouton ME (1988) Context and ambiguity in the extinction of emotional learning: implications for exposure therapy. Behav Res Ther 26:137–149PubMedGoogle Scholar
  15. Bouton ME (2002) Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol Psychiatry 52:976–986PubMedGoogle Scholar
  16. Bouton ME (2004) Context and behavioral processes in extinction. Learn Mem 11:485–494PubMedGoogle Scholar
  17. Bouton ME, Swartzentruber D (1986) Analysis of the associative and occasion-setting properties of contexts participating in a Pavlovian discrimination. J Exp Psychol Anim Behav Process 12:333–350Google Scholar
  18. Bouton ME, Frohardt RJ, Sunsay C, Waddell J, Morris RW (2008) Contextual control of inhibition with reinforcement: adaptation and timing mechanisms. J Exp Psychol Anim Behav Process 34(2):223–236 PMCID: 2877503Google Scholar
  19. Bowers MS, Hopf FW, Chou JK, Guillory AM, Chang S-J, Janak PH, Bonci A, Diamond I (2008) Nucleus accumbens AGS3 expression drives ethanol seeking through G betagamma. Proc Natl Acad Sci U S A 105:12533–12538PubMedCentralPubMedGoogle Scholar
  20. Braus DF, Wrase J, Grusser S, Hermann D, Ruf M, Flor H, Mann K, Heinz A (2001) Alcohol-associated stimuli activate the ventral striatum in abstinent alcoholics. J Neural Transm 108:887–894PubMedGoogle Scholar
  21. Brooks DC (2000) Recent and remote extinction cues reduce spontaneous recovery. Q J Exp Psychol B 53:25–58PubMedGoogle Scholar
  22. Brooks DC, Bouton ME (1993) A retrieval cue for extinction attenuates spontaneous recovery. J Exp Psychol Anim Behav Process 19:77–89PubMedGoogle Scholar
  23. Brower KJ, Perron BE (2010) Prevalence and correlates of withdrawal-related insomnia among adults with alcohol dependence: results from a national survey. Am J Addict 19:238–244. PMCID: 2998536Google Scholar
  24. Brown SA, Vik PW, Patterson TL, Grant I, Schuckit MA (1995) Stress, vulnerability and adult alcohol relapse. J Stud Alcohol 56:538–545PubMedGoogle Scholar
  25. Buffalari DM, See RE (2011) Inactivation of the bed nucleus of the stria terminalis in an animal model of relapse: effects on conditioned cue-induced reinstatement and its enhancement by yohimbine. Psychopharmacology (Berl) 213:19–27Google Scholar
  26. Buller KM, Xu Y, Day TA (1998) Indomethacin attenuates oxytocin and hypothalamic-pituitary-adrenal axis responses to systemic interleukin-1 beta. J Neuroendocrinol 10:519–528PubMedGoogle Scholar
  27. Burattini C, Gill TM, Aicardi G, Janak PH (2006) The ethanol self-administration context as a reinstatement cue: acute effects of naltrexone. Neuroscience 139:877–887PubMedGoogle Scholar
  28. Burish TG, Maisto SA, Cooper AM, Sobell MB (1981) Effects of voluntary short-term abstinence from alcohol on subsequent drinking patterns of college students. Q. J. Stud. Alcohol 42:1013–1020Google Scholar
  29. Camarini R, Pautassi RM, Mendez M, Quadros IM, Souza-Formigoni ML, Boerngen-Lacerda R (2010) Behavioral and neurochemical studies in distinct animal models of ethanol’s motivational effects. Curr Drug Abuse Rev 3:205–221PubMedGoogle Scholar
  30. Cannella N, Economidou D, Kallupi M, Stopponi S, Heilig M, Massi M, Ciccocioppo R (2009) Persistent increase of alcohol-seeking evoked by neuropeptide S: an effect mediated by the hypothalamic hypocretin system. Neuropsychopharmacology 34:2125–2134PubMedGoogle Scholar
  31. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321–352PubMedGoogle Scholar
  32. Carnicella S, Kharazia V, Jeanblanc J, Janak PH, Ron D (2008) GDNF is a fast-acting potent inhibitor of alcohol consumption and relapse. Proc Natl Acad Sci U S A 105:8114–8119PubMedCentralPubMedGoogle Scholar
  33. Charney DS, Heninger GR, Redmond DE Jr (1983) Yohimbine induced anxiety and increased noradrenergic function in humans: effects of diazepam and clonidine. Life Sci 33:19–29PubMedGoogle Scholar
  34. Chen G, Cuzon Carlson VC, Wang J, Beck A, Heinz A, Ron D, Lovinger DM, Buck KJ (2011) Striatal involvement in human alcoholism and alcohol consumption, and withdrawal in animal models. Alcohol Clin Exp Res 35(10):1739–1748Google Scholar
  35. Ciccocioppo R, Angeletti S, Weiss F (2001) Long-lasting resistance to extinction of response reinstatement induced by ethanol-related stimuli: role of genetic ethanol preference. Alcohol Clin Exp Res 25:1414–1419PubMedGoogle Scholar
  36. Ciccocioppo R, Martin-Fardon R, Weiss F (2002) Effect of selective blockade of mu(1) or delta opioid receptors on reinstatement of alcohol-seeking behavior by drug-associated stimuli in rats. Neuropsychopharmacology 27:391–399PubMedGoogle Scholar
  37. Ciccocioppo R, Economidou D, Fedeli A, Angeletti S, Weiss F, Heilig M, Massi M (2003a) Attenuation of ethanol self-administration and of conditioned reinstatement of alcohol-seeking behaviour by the antiopioid peptide nociceptin/orphanin FQ in alcohol-preferring rats. Psychopharmacology (Berl) 172:170–178Google Scholar
  38. Ciccocioppo R, Lin D, Martin-Fardon R, Weiss F (2003b) Reinstatement of ethanol-seeking behavior by drug cues following single versus multiple ethanol intoxication in the rat: effects of naltrexone. Psychopharmacology (Berl) 168:208–215Google Scholar
  39. Ciccocioppo R, Economidou D, Cippitelli A, Cucculelli M, Ubaldi M, Soverchia L, Lourdusamy A, Massi M (2006) Genetically selected Marchigian Sardinian alcohol-preferring (msP) rats: an animal model to study the neurobiology of alcoholism. Addict Biol 11:339–355PubMedCentralPubMedGoogle Scholar
  40. Cooney NL, Gillespie RA, Baker LH, Kaplan RF (1987) Cognitive changes after alcohol cue exposure. J Consult Clin Psychol 55:150–155PubMedGoogle Scholar
  41. Cooney NL, Litt MD, Morse PA, Bauer LO, Gaupp L (1997) Alcohol cue reactivity, negative-mood reactivity, and relapse in treated alcoholic men. J Abnorm Psychol 106:243–250PubMedGoogle Scholar
  42. Corbit LH, Janak PH (2007) Ethanol-associated cues produce general pavlovian-instrumental transfer. Alcohol Clin Exp Res 31:766–774PubMedGoogle Scholar
  43. Crombag HS, Shaham Y (2002) Renewal of drug seeking by contextual cues after prolonged extinction in rats. Behav Neurosci 116:169–173PubMedGoogle Scholar
  44. Crombag HS, Grimm JW, Shaham Y (2002) Effect of dopamine receptor antagonists on renewal of cocaine seeking by reexposure to drug-associated contextual cues. Neuropsychopharmacology 27:1006–1015PubMedGoogle Scholar
  45. Crombag HS, Bossert JM, Koya E, Shaham Y (2008) Context-induced relapse to drug seeking: a review. Philos Trans R Soc Lond B Biol Sci 363:3233–3243PubMedGoogle Scholar
  46. Cunningham CL, Niehus JS, Noble D (1993) Species difference in sensitivity to ethanol’s hedonic effects. Alcohol 10:97–102PubMedGoogle Scholar
  47. Cunningham CL, Gremel CM, Groblewski PA (2006) Drug-induced conditioned place preference and aversion in mice. Nat Protoc 1:1662–1670PubMedGoogle Scholar
  48. Czachowski CL, Santini LA, Legg BH, Samson HH (2002) Separate measures of ethanol seeking and drinking in the rat: effects of remoxipride. Alcohol 28:39–46PubMedGoogle Scholar
  49. Daglish MR, Nutt DJ (2003) Brain imaging studies in human addicts. Eur Neuropsychopharmacol 13:453–458PubMedGoogle Scholar
  50. Davis M, Redmond DE Jr, Baraban JM (1979) Noradrenergic agonists and antagonists: effects on conditioned fear as measured by the potentiated startle paradigm. Psychopharmacology (Berl) 65:111–118Google Scholar
  51. Dayas CV, Buller KM, Day TA (1999) Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala. Eur J Neurosci 11:2312–2322PubMedGoogle Scholar
  52. Dayas CV, Liu X, Simms JA, Weiss F (2007) Distinct patterns of neural activation associated with ethanol seeking: effects of naltrexone. Biol Psychiatry 61:979–989PubMedCentralPubMedGoogle Scholar
  53. Dhaher R, Hauser SR, Getachew B, Bell RL, McBride WJ, McKinzie DL, Rodd ZA (2010) The orexin-1 receptor antagonist SB-334867 reduces alcohol relapse drinking, but not alcohol-seeking, in alcohol-preferring (P) rats. J Addict Med 4:153–159PubMedCentralPubMedGoogle Scholar
  54. Epstein DH, Preston KL, Stewart J, Shaham Y (2006a) “All models are wrong, but some are useful”: an assessment of the validity of the reinstatement procedure as a model of drug relapse and craving. Psychopharmacology 189:1–16Google Scholar
  55. Epstein DH, Preston KL, Stewart J, Shaham Y (2006b) Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology (Berl) 189:1–16Google Scholar
  56. Eravci M, Grosspietsch T, Pinna G, Schulz O, Kley S, Bachmann M, Wolffgramm J, Gotz E, Heyne A, Meinhold H, Baumgartner A (1997) Dopamine receptor gene expression in an animal model of ‘behavioral dependence’ on ethanol. Brain Res Mol Brain Res 50:221–229PubMedGoogle Scholar
  57. Erb S, Stewart J (1999) A role for the bed nucleus of the stria terminalis, but not the amygdala, in the effects of corticotropin-releasing factor on stress- induced reinstatement of cocaine seeking. J Neurosci 19:RC35Google Scholar
  58. Eriksen L, Gotestam KG (1984) Conditioned abstinence in alcoholics: a controlled experiment. Int J Addict 19:287–294PubMedGoogle Scholar
  59. Ettenberg A (1990) Haloperidol prevents the reinstatement of amphetamine-rewarded runway responding in rats. Pharmacol Biochem Behav 36:635–638PubMedGoogle Scholar
  60. Ettenberg A (2009) The runway model of drug self-administration. Pharmacol Biochem Behav 91:271–277PubMedCentralPubMedGoogle Scholar
  61. Ettenberg A, MacConell LA, Geist TD (1996) Effects of haloperidol in a response-reinstatement model of heroin relapse. Psychopharmacology (Berl) 124:205–210Google Scholar
  62. Feltenstein MW, See RE (2006) Potentiation of cue-induced reinstatement of cocaine-seeking in rats by the anxiogenic drug yohimbine. Behav Brain Res 174:1–8PubMedGoogle Scholar
  63. Fox HC, Talih M, Malison R, Anderson GM, Kreek MJ, Sinha R (2005) Frequency of recent cocaine and alcohol use affects drug craving and associated responses to stress and drug-related cues. Psychoneuroendocrinology 30:880–891PubMedGoogle Scholar
  64. Fuchs RA, Feltenstein MW, See RE (2006) The role of the basolateral amygdala in stimulus-reward memory and extinction memory consolidation and in subsequent conditioned cued reinstatement of cocaine seeking. Eur J Neurosci 23:2809–2813PubMedGoogle Scholar
  65. Gass JT, Olive MF (2007) Reinstatement of ethanol-seeking behavior following intravenous self-administration in Wistar rats. Alcohol Clin Exp Res 31:1441–1445PubMedGoogle Scholar
  66. George MS, Anton RF, Bloomer C, Teneback C, Drobes DJ, Lorberbaum JP, Nahas Z, Vincent DJ (2001) Activation of prefrontal cortex and anterior thalamus in alcoholic subjects on exposure to alcohol-specific cues. Arch Gen Psychiatry 58:345–352PubMedGoogle Scholar
  67. Goldstein RZ, Volkow ND (2002) Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry 159:1642–1652PubMedCentralPubMedGoogle Scholar
  68. Greeley JD, Swift W, Prescott J, Heather N (1993) Reactivity to alcohol-related cues in heavy and light drinkers. J Stud Alcohol 54:359–368PubMedGoogle Scholar
  69. Gremel CM, Cunningham CL (2007) Role of test activity in ethanol-induced disruption of place preference expression in mice. Psychopharmacology (Berl) 191:195–202Google Scholar
  70. Gremel CM, Cunningham CL (2008) Roles of the nucleus accumbens and amygdala in the acquisition and expression of ethanol-conditioned behavior in mice. J Neurosci 28:1076–1084PubMedGoogle Scholar
  71. Grimm JW, Hope BT, Wise RA, Shaham Y (2001) Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature 412:141–142PubMedCentralPubMedGoogle Scholar
  72. Grusser SM, Wrase J, Klein S, Hermann D, Smolka MN, Ruf M, Weber-Fahr W, Flor H, Mann K, Braus DF, Heinz A (2004) Cue-induced activation of the striatum and medial prefrontal cortex is associated with subsequent relapse in abstinent alcoholics. Psychopharmacology (Berl) 175:296–302Google Scholar
  73. Heilig M, Egli M, Crabbe JC, Becker HC (2010) Acute withdrawal, protracted abstinence and negative affect in alcoholism: are they linked? Addict Biol 15:169–184PubMedCentralPubMedGoogle Scholar
  74. Heinz A, Siessmeier T, Wrase J, Buchholz HG, Grunder G, Kumakura Y, Cumming P, Schreckenberger M, Smolka MN, Rosch F, Mann K, Bartenstein P (2005) Correlation of alcohol craving with striatal dopamine synthesis capacity and D2/3 receptor availability: a combined [18F]DOPA and [18F]DMFP PET study in detoxified alcoholic patients. Am J Psychiatry 162:1515–1520PubMedGoogle Scholar
  75. Heinz A, Beck A, Mir J, Grusser SM, Grace AA, Wrase J (2010) Alcohol craving and relapse prediction: imaging studies. In: Cynthia M. Kuhn GFK (eds) Advances in the neuroscience of addiction. CRC Press, Taylor & Francis Group, Boca Raton pp 137–162Google Scholar
  76. Heyne A, Swodlowska G, Wolffgramm J (1991) Physical dependence on ethanol vs. rebound phenomena in an animal model of alcoholism. Naunyn Schmiedeberg’s Arch Pharmacol Suppl 344:R70Google Scholar
  77. Heyser CJ, Schulteis G, Koob GF (1997) Increased ethanol self-administration after a period of imposed ethanol deprivation in rats trained in a limited access paradigm. Alcohol Clin Exp Res 21:784–791PubMedGoogle Scholar
  78. Heyser CJ, Schulteis G, Durbin P, Koob GF (1998) Chronic acamprosate eliminates the alcohol deprivation effect while having limited effects on baseline responding for ethanol in rats. Neuropsychopharmacology 18:125–133PubMedGoogle Scholar
  79. Heyser CJ, Moc K, Koob GF (2003) Effects of naltrexone alone and in combination with acamprosate on the alcohol deprivation effect in rats. Neuropsychopharmacology 28:1463–1471PubMedGoogle Scholar
  80. Higley JD, Hasert MF, Suomi SJ, Linnoila M (1991) Nonhuman primate model of alcohol abuse: effect of early experience, personality, and stress on alcohol consumption. Proc Natl Acad Sci U S A 88:7261–7265PubMedCentralPubMedGoogle Scholar
  81. Holter SM, Linthorst AC, Reul JM, Spanagel R (2000) Withdrawal symtoms in a long-term model of voluntary alcohol drinking in Wistar rats. Pharmacol Biochem Behav 66:143–151PubMedGoogle Scholar
  82. Hopf FW, Chang SJ, Sparta DR, Bowers MS, Bonci A (2010) Motivation for alcohol becomes resistant to quinine adulteration after 3 to 4 months of intermittent alcohol self-administration. Alcohol Clin Exp Res 34:1565–1573. PMCID: 2997761Google Scholar
  83. Itzhak Y, Martin JL (2002) Cocaine-induced conditioned place preference in mice: induction, extinction and reinstatement by related psychostimulants. Neuropsychopharmacology 26:130–134PubMedGoogle Scholar
  84. Jaffe JH, Cascella NG, Kumor KM, Sherer MA (1989) Cocaine-induced cocaine craving. Psychopharmacology 97:59–64PubMedGoogle Scholar
  85. Janak PH, Chaudhri N (2010) The potent effect of environmental context on relapse to alcohol-seeking after extinction. Open Addict J 3:76–87PubMedCentralPubMedGoogle Scholar
  86. Kalivas PW, Volkow ND (2005) The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162:1403–1413PubMedGoogle Scholar
  87. Kaplan RF, Meyer RE, Stroebel CF (1983) Alcohol dependence and responsivity to an ethanol stimulus as predictors of alcohol consumption. Br J Addict 78:259–267PubMedGoogle Scholar
  88. Kaplan RF, Meyer RE, Virgilio LM (1984) Physiological reactivity to alcohol cues and the awareness of an alcohol effect in a double-blind placebo design. Br J Addict 79:439–442PubMedGoogle Scholar
  89. Kaplan RF, Cooney NL, Baker LH, Gillespie RA, Meyer RE, Pomerleau OF (1985) Reactivity to alcohol-related cues: physiological and subjective responses in alcoholics and nonproblem drinkers. J Stud Alcohol 46:267–272PubMedGoogle Scholar
  90. Kareken DA, Claus ED, Sabri M, Dzemidzic M, Kosobud AE, Radnovich AJ, Hector D, Ramchandani VA, O’Connor SJ, Lowe M, Li TK (2004) Alcohol-related olfactory cues activate the nucleus accumbens and ventral tegmental area in high-risk drinkers: preliminary findings. Alcohol Clin Exp Res 28:550–557PubMedGoogle Scholar
  91. Katner SN, Weiss F (1999) Ethanol-associated olfactory stimuli reinstate ethanol-seeking behavior after extinction and modify extracellular dopamine levels in the nucleus accumbens. Alcohol Clin Exp Res 23:1751–1760PubMedGoogle Scholar
  92. Katner SN, Magalong JG, Weiss F (1999) Reinstatement of alcohol-seeking behavior by drug-associated discriminative stimuli after prolonged extinction in the rat. Neuropsychopharmacology 20:471–479PubMedGoogle Scholar
  93. Katz JL, Higgins ST (2003) The validity of the reinstatement model of craving and relapse to drug use. Psychopharmacology (Berl) 168:21–30Google Scholar
  94. Kearns DN, Weiss SJ, Panlilio LV (2002) Conditioned suppression of behavior maintained by cocaine self-administration. Drug Alcohol Depend 65:253–261PubMedGoogle Scholar
  95. Knackstedt LA, Ettenberg A (2005) Ethanol consumption reduces the adverse consequences of self-administered intravenous cocaine in rats. Psychopharmacology (Berl). 178:143–150PubMedGoogle Scholar
  96. Knackstedt LA, Ben-Shahar O, Ettenberg A (2006) Alcohol consumption is preferred to water in rats pretreated with intravenous cocaine. Pharmacol Biochem Behav 85:281–286PubMedGoogle Scholar
  97. Koob GF (2003) Alcoholism: allostasis and beyond. Alcohol Clin Exp Res 27:232–243PubMedGoogle Scholar
  98. Koob GF, Le Moal M (2008) Review. Neurobiological mechanisms for opponent motivational processes in addiction. Philos Trans R Soc Lond B Biol Sci 363:3113–3123PubMedGoogle Scholar
  99. Kornet M, Goosen C, Van Ree JM (1990) The effect of interrupted alcohol supply on spontaneous alcohol consumption by rhesus monkeys. Alcohol Alcoholism 25:407–412PubMedGoogle Scholar
  100. Kornet M, Goosen C, Van Ree JM (1991) Effects of naltrexone on alcohol consumption during chronic alcohol drinking and after a period of imposed abstinence in free-choice drinking rhesus monkeys. Psychopharmacol 104:367–376Google Scholar
  101. Kreek MJ, Koob GF (1998) Drug dependence: stress and dysregulation of brain reward pathways. Drug Alcohol Depend 51:23–47PubMedGoogle Scholar
  102. Kufahl PR, Martin-Fardon R, Weiss F (2011) 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 36(13):2762–2773Google Scholar
  103. Kuzmin A, Sandin J, Terenius L, Ogren SO (2003) Acquisition, expression, and reinstatement of ethanol-induced conditioned place preference in mice: effects of opioid receptor-like 1 receptor agonists and naloxone. J Pharmacol Exp Ther 304:310–318PubMedGoogle Scholar
  104. Laberg JC (1986) Alcohol and expectancy: subjective, psychophysiological and behavioral responses to alcohol stimuli in severely, moderately and non-dependent drinkers. Br J Addict 81:797–808PubMedGoogle Scholar
  105. Lang WJ, Gershon S (1963) Effects of psychoactive drugs on yohimbine induced responses in conscious dogs. A proposed screening procedure for anti-anxiety agents. Arch Int Pharmacodyn Ther 142:457–472PubMedGoogle Scholar
  106. Lauener H (1963) Conditioned suppression in rats and the effect of pharmacological agents thereon. Psychopharmacologia 4:311–325PubMedGoogle Scholar
  107. Le A, Shaham Y (2002) Neurobiology of relapse to alcohol in rats. Pharmacol Ther 94:137–156PubMedGoogle Scholar
  108. Le AD, Quan B, Juzytch W, Fletcher PJ, Joharchi N, Shaham Y (1998) Reinstatement of alcohol-seeking by priming injections of alcohol and exposure to stress in rats. Psychopharmacology (Berl) 135:169–174Google Scholar
  109. Le AD, Poulos CX, Harding S, Watchus J, Juzytsch W, Shaham Y (1999) 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 21:435–444 PubMedGoogle Scholar
  110. Le AD, Harding S, Juzytsch W, Watchus J, Shalev U, Shaham Y (2000) The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats. Psychopharmacology (Berl) 150:317–324Google Scholar
  111. Le AD, Wang A, Harding S, Juzytsch W, Shaham Y (2003) Nicotine increases alcohol self-administration and reinstates alcohol seeking in rats. Psychopharmacology (Berl) 168:216–221Google Scholar
  112. Le AD, Harding S, Juzytsch W, Funk D, Shaham Y (2005) Role of alpha-2 adrenoceptors in stress-induced reinstatement of alcohol seeking and alcohol self-administration in rats. Psychopharmacology (Berl) 179:366–373Google Scholar
  113. Le AD, Funk D, Coen K, Li Z, Shaham Y (2011a) Role of corticotropin-releasing factor in the median raphe nucleus in yohimbine-induced reinstatement of alcohol seeking in rats. Addict BiolGoogle Scholar
  114. Le AD, Funk D, Juzytsch W, Coen K, Navarre BM, Cifani C, Shaham Y (2011b) Effect of prazosin and guanfacine on stress-induced reinstatement of alcohol and food seeking in rats. Psychopharmacology (Berl) 218:89–99Google Scholar
  115. Lee B, Tiefenbacher S, Platt DM, Spealman RD (2004) Pharmacological blockade of alpha2-adrenoceptors induces reinstatement of cocaine-seeking behavior in squirrel monkeys. Neuropsychopharmacology 29:686–693PubMedGoogle Scholar
  116. Li TK, Lumeng L, McBride WJ, Waller MB (1979) Progress towards a voluntary oral consumption model of alcoholism. Drug Alcohol Depend 4:45–60PubMedGoogle Scholar
  117. Liu X, Weiss F (2002a) Additive effect of stress and drug cues on reinstatement of ethanol seeking: exacerbation by history of dependence and role of concurrent activation of corticotropin-releasing factor and opioid mechanisms. J Neurosci 22:7856–7861PubMedGoogle Scholar
  118. Liu X, Weiss F (2002b) Reversal of ethanol-seeking behavior by D1 and D2 antagonists in an animal model of relapse: differences in antagonist potency in previously ethanol-dependent versus nondependent rats. J Pharmacol Exp Ther 300:882–889PubMedGoogle Scholar
  119. Liu X, Weiss F (2003) Stimulus conditioned to foot-shock stress reinstates alcohol-seeking behavior in an animal model of relapse. Psychopharmacology (Berl) 168:184–191Google Scholar
  120. Liu Y, Le Foll B, Liu Y, Wang X, Lu L (2008) Conditioned place preference induced by licit drugs: establishment, extinction, and reinstatement. Sci World J 8:1228–1245Google Scholar
  121. Ludwig AM, Wikler A (1974) “Craving” and relapse to drink. Q J Stud Alcohol 35:108–130Google Scholar
  122. Ludwig AM, Wikler A, Stark LH (1974) The first drink: psychobiological aspects of craving. Arch Gen Psychiatry 30:539–547PubMedGoogle Scholar
  123. Maas LC, Lukas SE, Kaufman MJ, Weiss RD, Daniels SL, Rogers VW, Kukes TJ, Renshaw PF (1998) Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. Am J Psychiatry 155:124–126PubMedGoogle Scholar
  124. Majchrowicz E (1989) Reversal in central nervous system function during ethanol withdrawal in humans and experimental animals. Fed Proc 40:2065–2072Google Scholar
  125. Marinelli PW, Funk D, Juzytsch W, Harding S, Rice KC, Shaham Y, Le AD (2007) The CRF1 receptor antagonist antalarmin attenuates yohimbine-induced increases in operant alcohol self-administration and reinstatement of alcohol seeking in rats. Psychopharmacology (Berl) 195:345–355Google Scholar
  126. Marlatt GA (1985) Relapse prevention: introduction and overview of the model. In: Marlatt GA, Gordon JR (eds) Relapse prevention: maintenance strategies in the treatment fo addictive behaviors. Guilford, London, pp 3–70Google Scholar
  127. Martin-Fardon R, Ciccocioppo R, Massi M, Weiss F (2000) Nociceptin prevents stress-induced ethanol- but not cocaine-seeking behavior in rats. Neuroreport 11:1939–1943PubMedGoogle Scholar
  128. Martinotti G, Nicola MD, Reina D, Andreoli S, Focà F, Cunniff A, Tonioni F, Bria P, Janiri L (2008) Alcohol protracted withdrawal syndrome: the role of anhedonia. Subst Use Misuse 43:271–284PubMedGoogle Scholar
  129. Maurice T, Casalino M, Lacroix M, Romieu P (2003) Involvement of the sigma 1 receptor in the motivational effects of ethanol in mice. Pharmacol Biochem Behav 74:869–876PubMedGoogle Scholar
  130. McBride WJ, Li TK (1998) Animal models of alcoholism: neurobiology of high alcohol-drinking behavior in rodents. Crit Rev Neurobiol 12:339–369PubMedGoogle Scholar
  131. McBride WJ, Le AD, Noronha A (2002) Central nervous system mechanisms in alcohol relapse. Alcohol Clin Exp Res 26:280–286PubMedGoogle Scholar
  132. McKay JR, Rutherford MJ, Alterman AI, Cacciola JS, Kaplan MR (1995) An examination of the cocaine relapse process. Drug Alcohol Dep 38:35–43Google Scholar
  133. McLellan AT, Lewis DC, O’Brien CP, Kleber HD (2000) Drug dependence, a chronic medical illness: implications for treatment, insurance, and outcomes evaluation. JAMA 284(13):1689–1695Google Scholar
  134. Merlo Pich E, Lorang M, Yeganeh M, Rodriguez de Fonseca F, Raber J, Koob GF, Weiss F (1995) Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci 15:5439–5447Google Scholar
  135. Meyer RE (1996) The disease called addiction: emerging evidence in a 200 year debate. Lancet 347:162–166 Google Scholar
  136. Miller NS, Goldsmith RJ (2001) Craving for alcohol and drugs in animals and humans: biology and behavior. J Addict Dis 20:87–104PubMedGoogle Scholar
  137. Mollenauer S, Bryson R, Robinson M, Sardo J, Coleman C (1993) EtOH Self-administration in anticipation of noise stress in C57BL/6 J mice. Pharmacol Biochem Behav 46:35–38PubMedGoogle Scholar
  138. Monti PM, Binkoff JA, Abrams DB, Zwick WR, Nirenberg TD, Liepman MR (1987) Reactivity of alcoholics and nonalcoholics to drinking cues. J Abnorm Psychol 96:122–126PubMedGoogle Scholar
  139. Monti PM, Rohsenow DJ, Rubonis AV, Niaura RS, Sirota AD, Colby SM, Abrams DB (1993) Alcohol cue reactivity: effects of detoxification and extended exposure. J Stud Alcohol 54:235–245PubMedGoogle Scholar
  140. Monti PM, Rohsenow DJ, Hutchison KE, Swift RM, Mueller TI, Colby SM, Brown RA, Gulliver SB, Gordon A, Abrams DB (1999) Naltrexone’s effect on cue-elicited craving among alcoholics in treatment. Alcohol Clin Exp Res 23:1386–1394PubMedGoogle Scholar
  141. Mueller D, Stewart J (2000) Cocaine-induced conditioned place preference: reinstatement by priming injections of cocaine after extinction. Behav Brain Res 115:39–47PubMedGoogle Scholar
  142. Myrick H, Anton RF, Li X, Henderson S, Drobes D, Voronin K, George MS (2004) Differential brain activity in alcoholics and social drinkers to alcohol cues: relationship to craving. Neuropsychopharmacology 29:393–402PubMedGoogle Scholar
  143. Nair SG, Gray SM, Ghitza UE (2006) Role of food type in yohimbine- and pellet-priming-induced reinstatement of food seeking. Physiol Behav 88:559–566PubMedCentralPubMedGoogle Scholar
  144. Nash J Jr, Maickel RP (1988) The role of the hypothalamic-pituitary-adrenocortical axis in post- stress induced ethanol consumption by rats. Prog Neuropsychopharmacol Biol Psychiatry 12:653–671PubMedGoogle Scholar
  145. Nielsen CK, Simms JA, Bito-Onon JJ, Li R, Ananthan S, Bartlett SE (2011) The delta opioid receptor antagonist, SoRI-9409, decreases yohimbine stress-induced reinstatement of ethanol-seeking. Addict Biol 15:81–87Google Scholar
  146. O’Brien CP, McLellan AT (1996) Myths about the treatment of addiction. Lancet 347:237–240PubMedGoogle Scholar
  147. O’Brien CP, Volpicelli LA, Volpicelli JR (1996) Naltrexone in the treatment of alcoholism: a clinical review. Alcohol 13:35–39PubMedGoogle Scholar
  148. O’Brien CP, Childress AR, Ehrman R, Robbins SJ (1998) Conditioning factors in drug abuse: can they explain compulsion? J Psychopharmacol 12:15–22PubMedGoogle Scholar
  149. O’Donnel PJ (1984) The abstinence violation effect and circumstances surrounding relapse as a predictor of outcome status in male alcoholic outposts. J Psychol 117:257–262Google Scholar
  150. Olive MF, Koenig HN, Nannini MA, Hodge CW (2002) Elevated extracellular CRF levels in the bed nucleus of the stria terminalis during ethanol withdrawal and reduction by subsequent ethanol intake. Pharmacol Biochem Behav 72:213–220PubMedGoogle Scholar
  151. Pavlov IP (1927) Conditioned reflexes (GV Anrep trans). Oxford University Press, LondonGoogle Scholar
  152. Pelloux Y, Everitt BJ, Dickinson A (2007) Compulsive drug seeking by rats under punishment: effects of drug taking history. Psychopharmacology (Berl) 194:127–137Google Scholar
  153. Radwanska K, Wrobel E, Korkosz A, Rogowski A, Kostowski W, Bienkowski P, Kaczmarek L (2008) Alcohol relapse induced by discrete cues activates components of AP-1 transcription factor and ERK pathway in the rat basolateral and central amygdala. Neuropsychopharmacology 33:1835–1846PubMedGoogle Scholar
  154. Rankin HR, Hogson R, Stockwell T (1979) The concept of craving and its measurement. Behav Res Ther 17:389–396PubMedGoogle Scholar
  155. Richards JK, Simms JA, Steensland P, Taha SA, Borgland SL, Bonci A, Bartlett SE (2008) Inhibition of orexin-1/hypocretin-1 receptors inhibits yohimbine-induced reinstatement of ethanol and sucrose seeking in Long-Evans rats. Psychopharmacology (Berl) 199:109–117Google Scholar
  156. Rodd ZA, Bell RL, Sable HJ, Murphy JM, McBride WJ (2004) Recent advances in animal models of alcohol craving and relapse. Pharmacol Biochem Behav 79:439–450PubMedGoogle Scholar
  157. Rodd ZA, McKinzie DL, Bell RL, McQueen VK, Murphy JM, Schoepp DD, McBride WJ (2006) The metabotropic glutamate 2/3 receptor agonist LY404039 reduces alcohol-seeking but not alcohol self-administration in alcohol-preferring (P) rats. Behav Brain Res 171:207–215PubMedGoogle Scholar
  158. Rodd-Henricks ZA, Bell RL, Kuc KA, Murphy JM, McBride WJ, Lumeng L, Li TK (2002a) Effects of ethanol exposure on subsequent acquisition and extinction of ethanol self-administration and expression of alcohol-seeking behavior in adult alcohol-preferring (P) rats: I Periadolescent exposure. Alcohol Clin Exp Res 26:1632–1641PubMedGoogle Scholar
  159. Rodd-Henricks ZA, Bell RL, Kuc KA, Murphy JM, McBride WJ, Lumeng L, Li TK (2002b) Effects of ethanol exposure on subsequent acquisition and extinction of ethanol self-administration and expression of alcohol-seeking behavior in adult alcohol-preferring (P) rats: II Adult exposure. Alcohol Clin Exp Res 26:1642–1652PubMedGoogle Scholar
  160. Rohsenow DJ, Monti PM, Hutchison KE, Swift RM, Colby SM, Kaplan GB (2000) Naltrexone’s effects on reactivity to alcohol cues among alcoholic men. J Abnorm Psychol 109:738–742PubMedGoogle Scholar
  161. Romieu P, Meunier J, Garcia D, Zozime N, Martin-Fardon R, Bowen WD, Maurice T (2004) The sigma1 (sigma1) receptor activation is a key step for the reactivation of cocaine conditioned place preference by drug priming. Psychopharmacology (Berl) 175:154–162Google Scholar
  162. Saghal A (1984) A critique of the vasopressin memory hypothesis. Psychopharmacology 83:215–228Google Scholar
  163. Salimov RM, Salimova NB (1993) The alcohol deprivation effect in hybrid mice. Drug Alcohol Dependence 32:187–191PubMedGoogle Scholar
  164. Samson HH, Chappell A (2002) Reinstatement of ethanol seeking responding after ethanol self-administration. Alcohol 26:95–101PubMedGoogle Scholar
  165. Samson HH, Slawecki CJ, Sharpe AL, Chappell A (1998) Appetitive and consummatory behaviors in the control of ethanol consumption: a measure of ethanol seeking behavior. Alcohol Clin Exp Res 22:1783–1787PubMedGoogle Scholar
  166. Samson HH, Sharpe AL, Denning C (1999) Initiation of ethanol self-administration in the rat using sucrose substitution in a sipper-tube procedure. Psychopharmacology (Berl) 147:274–279Google Scholar
  167. Samson HH, Czachowski CL, Slawecki CJ (2000) A new assessment of the ability of oral ethanol to function as a reinforcing stimulus. Alcohol Clin Exp Res 24:766–773PubMedGoogle Scholar
  168. Samson HH, Czachowski CL, Chappell A, Legg B (2003) Measuring the appetitive strength of ethanol: use of an extinction trial procedure. Alcohol 31:77–86PubMedGoogle Scholar
  169. Schechter MD, Calcagnetti DJ (1993) Trends in place preference conditioning with a cross-indexed bibliography; 1957–1991. Neurosci Biobehav Rev 17:21–41PubMedGoogle Scholar
  170. Schneider F, Habel U, Wagner M, Franke P, Salloum JB, Shah NJ, Toni I, Sulzbach C, Honig K, Maier W, Gaebel W, Zilles K (2001) Subcortical correlates of craving in recently abstinent alcoholic patients. Am J Psychiatry 158:1075–1083PubMedGoogle Scholar
  171. Schroeder JP, Overstreet DH, Hodge CW (2005) The mGluR5 antagonist MPEP decreases operant ethanol self-administration during maintenance and after repeated alcohol deprivations in alcohol-preferring (P) rats. Psychopharmacology (Berl) 179:262–270Google Scholar
  172. Schulteis G, Markou A, Cole M, Koob GF (1995) Decreased brain reward produced by ethanol withdrawal. Proc Natl Acad Sci 92:5880–5884PubMedGoogle Scholar
  173. See RE, Fuchs RA, Ledford CC, McLaughlin J (2003) Drug addiction, relapse, and the amygdala. Ann N Y Acad Sci 985:294–307PubMedGoogle Scholar
  174. Shaham Y, Erb S, Stewart J (2000) Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Brain Res Rev 33:13–33PubMedGoogle Scholar
  175. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168:3–20Google Scholar
  176. Shalev U, Grimm JW, Shaham (2002) Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacol Rev 54:1–42Google Scholar
  177. Sharpe AL, Samson HH (2001) Effect of naloxone on appetitive and consummatory phases of ethanol self-administration. Alcohol Clin Exp Res 25:1006–1011PubMedGoogle Scholar
  178. Shepard JD, Bossert JM, Liu SY, Shaham Y (2004) The anxiogenic drug yohimbine reinstates methamphetamine seeking in a rat model of drug relapse. Biol Psychiatry 55:1082–1089PubMedGoogle Scholar
  179. Sidhpura N, Weiss F, Martin-Fardon R (2010) 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 67:804–811PubMedCentralPubMedGoogle Scholar
  180. Simms JA, Steensland P, Medina B, Abernathy KE, Chandler LJ, Wise R, Bartlett SE (2008) Intermittent access to 20% ethanol induces high ethanol consumption in Long-Evans and Wistar rats. Alcohol Clin Exp Res 32:1816–1823. PMCID: 3151464Google Scholar
  181. Sinclair JD (1972) The alcohol-deprivation effect: Influence of various factors. Q Stud Alcohol 33:769–782Google Scholar
  182. Sinclair JD (1979) Alcohol-deprivation effect in rats genetically selected for their ethanol preference. Pharmacol Biochem Behav 10:597–602PubMedGoogle Scholar
  183. Sinclair JD, Li T-K (1989) Long and short alcohol deprivation: Effects on AA and P alcohol-preferring rats. Alcohol 6:505–509PubMedGoogle Scholar
  184. Sinclair JD, Senter RJ (1967) Increased preference for ethanol in rats following alcohol deprivation. Psychonomic Sci 8:11–12Google Scholar
  185. Sinclair JD, Senter RJ (1968) Development of an alcohol deprivation effect in rats. Q J Stud Alcohol 29:863–867PubMedGoogle Scholar
  186. Sinha R (2000) Stress, craving, and relapse to drug use National Institute on Drug Abuse (NIDA) Symposium: The Intersection of Stress, Drug Abuse, and Development, BethesdaGoogle Scholar
  187. Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158:343–359Google Scholar
  188. Sinha R (2009) Modeling stress and drug craving in the laboratory: implications for addiction treatment development. Addict Biol 14:84–98PubMedCentralPubMedGoogle Scholar
  189. Sinha R, Catapano D, O’Malley S (1999) Stress-induced craving and stress response in cocaine dependent individuals. Psychopharmacology (Berl) 142:343–351Google Scholar
  190. Sinha R, Fuse T, Aubin LR, O’Malley SS (2000) Psychological stress, drug-related cues and cocaine craving. Psychopharmacology (Berl) 152:140–148Google Scholar
  191. Sinha R, Talih M, Malison R, Cooney N, Anderson GM, Kreek MJ (2003) Hypothalamic-pituitary-adrenal axis and sympatho-adreno-medullary responses during stress-induced and drug cue-induced cocaine craving states. Psychopharmacology (Berl) 170:62–72Google Scholar
  192. Sinha R, Garcia M, Paliwal P, Kreek MJ, Rounsaville BJ (2006) Stress-induced cocaine craving and hypothalamic-pituitary-adrenal responses are predictive of cocaine relapse outcomes. Arch Gen Psychiatry 63:324–331PubMedGoogle Scholar
  193. Sinha R, Fox HC, Hong KA, Bergquist K, Bhagwagar Z, Siedlarz KM (2009) Enhanced negative emotion and alcohol craving, and altered physiological responses following stress and cue exposure in alcohol dependent individuals. Neuropsychopharmacology 34:1198–1208. PMCID: 2734452Google Scholar
  194. Spanagel R, Holter SM (2000) Pharmacological validation of a new animal model of alcoholism. J Neural Transm 107:669–680PubMedGoogle Scholar
  195. Spanagel R, Kiefer F (2008) Drugs for relapse prevention of alcoholism: ten years of progress. Trends Pharmacol Sci 29:109–115PubMedGoogle Scholar
  196. Spanagel R, Hölter SM, Allingham K, Landgraf R, Zieglgänsberger W (1996) Acamprosate and alcohol: I. Effects on alcohol intake following alcohol deprivation in the rat. Eur J Pharmacol 305:39–44PubMedGoogle Scholar
  197. Steketee JD, Kalivas PW (2011) Drug wanting: behavioral sensitization and relapse to drug-seeking behavior. Pharmacol Rev 63:348–365Google Scholar
  198. Stine SM, Southwick SM, Petrakis IL, Kosten TR, Charney DS, Krystal JH (2002) Yohimbine-induced withdrawal and anxiety symptoms in opioid-dependent patients. Biol Psychiatry 51:642–651PubMedGoogle Scholar
  199. Stopponi S, Somaini L, Cippitelli A, Cannella N, Braconi S, Kallupi M, Ruggeri B, Heilig M, Demopulos G, Gaitanaris G, Massi M, Ciccocioppo R (2011a) Activation of nuclear PPARgamma receptors by the antidiabetic agent pioglitazone suppresses alcohol drinking and relapse to alcohol seeking. Biol Psychiatry 69:642–649PubMedGoogle Scholar
  200. Stopponi S, Somaini L, Cippitelli A, de Guglielmo G, Kallupi M, Cannella N, Gerra G, Massi M, Ciccocioppo R (2011b) Pregabalin reduces alcohol drinking and relapse to alcohol seeking in the rat. Psychopharmacology (Berl) 17(8):E113–E115Google Scholar
  201. Stormark KM, Laberg JC, Bjerland T, Nordby H, Hugdahl K (1995) Autonomic cued reactivity in alcoholics: the effect of olfactory stimuli. Addict Behav 20:571–584PubMedGoogle Scholar
  202. Streeter CC, Gulliver SB, Baker E, Blank SR, Meyer AA, Ciraulo DA, Renshaw PF (2002) Videotaped cue for urge to drink alcohol. Alcohol Clin Exp Res 26:627–634PubMedGoogle Scholar
  203. Suemaru S, Dallman MF, Darlington DN, Cascio CS, Shinsako J (1989) Role of alpha-adrenergic mechanism in effects of morphine on the hypothalamo-pituitary-adrenocortical and cardiovascular systems in the rat. Neuroendocrinology 49:181–190PubMedGoogle Scholar
  204. Szumlinski KK, Price KL, Frys KA, Middaugh LD (2002) Unconditioned and conditioned factors contribute to the ‘reinstatement’ of cocaine place conditioning following extinction in C57BL/6 mice. Behav Brain Res 136:151–160PubMedGoogle Scholar
  205. Thanos PK, Bermeo C, Wang GJ, Volkow ND (2009) D-cycloserine accelerates the extinction of cocaine-induced conditioned place preference in C57bL/c mice. Behav Brain Res 199:345–349PubMedCentralPubMedGoogle Scholar
  206. Topple AN, Hunt GE, McGregor IS (1998) Possible neural substrates of beer-craving in rats. Neurosci Lett 252:99–102PubMedGoogle Scholar
  207. Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462PubMedGoogle Scholar
  208. Tzschentke TM, Schmidt WJ (2000) Functional relationship among medial prefrontal cortex, nucleus accumbens, and ventral tegmental area in locomotion and reward. Crit Rev Neurobiol 14:131–142PubMedGoogle Scholar
  209. Valdez GR, Roberts AJ, Chan K, Davis H, Brennan M, Zorrilla EP, Koob GF (2002) Increased ethanol self-administration and anxiety-like behavior during acute ethanol withdrawal and protracted abstinence: regulation by corticotropin-releasing factor. Alcohol Clin Exp Res 26:1494–1501PubMedGoogle Scholar
  210. Vanderschuren LJ, Everitt BJ (2004) Drug seeking becomes compulsive after prolonged cocaine self-administration. Science 305:1017–1019PubMedGoogle Scholar
  211. Vengeliene V, Celerier E, Chaskiel L, Penzo F, Spanagel R (2009) Compulsive alcohol drinking in rodents. Addict Biol 14:384–396PubMedGoogle Scholar
  212. Vollstadt-Klein S, Loeber S, Kirsch M, Bach P, Richter A, Buhler M, von der Goltz C, Hermann D, Mann K, Kiefer F (2011) Effects of cue-exposure treatment on neural cue reactivity in alcohol dependence: a randomized trial. Biol Psychiatry 69:1060–1066PubMedGoogle Scholar
  213. Volpicelli JR, Alterman AI, Hayashida M, O’Brien CP (1992) Naltrexone in the treatment of alcohol dependence. Arch Gen Psychiatry 49:876–880PubMedGoogle Scholar
  214. Walker BM, Ehlers CL (2009) Appetitive motivational experience during adolescence results in enhanced alcohol consumption during adulthood. Behav Neurosci 123:926–935. PMCID: 2787447Google Scholar
  215. Wallace BC (1989) Psychological and environmental determinants of relapse in crack cocaine smokers. J Subst Abuse Treat 6:95–106PubMedGoogle Scholar
  216. Wang B, Shaham Y, Zitzman D, Azari S, Wise RA, You ZB (2005) Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin-releasing factor: a role in stress-induced relapse to drug seeking. J Neurosci 25:5389–5396PubMedGoogle Scholar
  217. Wang J, Fang Q, Liu Z, Lu L (2006) Region-specific effects of brain corticotropin-releasing factor receptor type 1 blockade on footshock-stress- or drug-priming-induced reinstatement of morphine conditioned place preference in rats. Psychopharmacology (Berl) 185:19–28Google Scholar
  218. Wang B, You ZB, Rice KC, Wise RA (2007) Stress-induced relapse to cocaine seeking: roles for the CRF(2) receptor and CRF-binding protein in the ventral tegmental area of the rat. Psychopharmacology (Berl) 193:283–294Google Scholar
  219. Weiss F, Martin-Fardon R, Ciccocioppo R, Kerr TM, Smith DL, Ben-Shahar O (2001) Enduring resistance to extinction of cocaine-seeking behavior induced by drug-related cues. Neuropsychopharmacology 25:361–372PubMedGoogle Scholar
  220. Wolffgramm J, Heyne A (1995) From controlled drug intake to loss of control: the irreversible development of drug addiction in the rat. Behav Brain Res 70:77–94PubMedGoogle Scholar
  221. Zhao Y, Dayas CV, Aujla H, Baptista MA, Martin-Fardon R, Weiss F (2006) 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 26:9967–9974PubMedGoogle Scholar
  222. Zhao Y, Weiss F, Zorrilla EP (2007) Remission and resurgence of anxiety-like behavior across protracted withdrawal stages in ethanol-dependent rats. Alcohol Clin Exp Res 31:1505–1515PubMedGoogle Scholar
  223. Zironi I, Burattini C, Aicardi G, Janak PH (2006) Context is a trigger for relapse to alcohol. Behav Brain Res 167:150–155PubMedGoogle Scholar
  224. Zorrilla EP, Valdez GR, Weiss F (2001) Changes in levels of regional CRF-like-immunoreactivity and plasma corticosterone during protracted drug withdrawal in dependent rats. Psychopharmacology (Berl) 158:374–381Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Molecular and Integrative Neurosciences DepartmentThe Scripps Research InstituteLa JollaUSA

Personalised recommendations