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Modeling Relapse in Animals

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Book cover Behavioral Neurobiology of Alcohol Addiction

Part of the book series: Current Topics in Behavioral Neurosciences ((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.

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References

  • Aguilar MA, Rodríguez-Arias M, Miñarro J (2009) Neurobiological mechanisms of the reinstatement of drug-conditioned place preference. Brain Res Rev 59:253–277

    PubMed  Google Scholar 

  • Albus M, Zahn TP, Breier A (1992) Anxiogenic properties of yohimbine. I. Behavioral, physiological and biochemical measures. Eur Arch Psychiatry Clin Neurosci 241:337–344

    CAS  PubMed  Google Scholar 

  • American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th edn (Revised Version). American Psychiatric Association, Washington

    Google Scholar 

  • Anton RF (1999) What is craving? Models and implications for treatment. Alcohol Res Health 23:165–173

    CAS  PubMed  Google Scholar 

  • Banna KM, Back SE, Do P, See RE (2010) Yohimbine stress potentiates conditioned cue-induced reinstatement of heroin-seeking in rats. Behav Brain Res 208:144–148

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bardo MT, Bevins RA (2000) Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology (Berl) 153:31–43

    CAS  Google Scholar 

  • 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 28:1867–1874

    PubMed  Google Scholar 

  • 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 23:25–33

    Google Scholar 

  • 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 26:315–323

    Google Scholar 

  • Bienkowski P, Kostowski W, Koros E (1999a) Ethanol-reinforced behaviour in the rat: effects of naltrexone. Eur J Pharmacol 374:321–327

    CAS  PubMed  Google Scholar 

  • 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 374:315–319

    CAS  PubMed  Google Scholar 

  • 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 14:355–360

    CAS  PubMed  Google Scholar 

  • Blanchard RJ, Hori K, Tom P, Blanchard C (1987) Social structure and ethanol consumption in laboratory rats. Pharmacol Biochem Behav 28:437–442

    CAS  PubMed  Google Scholar 

  • Bouton ME (1988) Context and ambiguity in the extinction of emotional learning: implications for exposure therapy. Behav Res Ther 26:137–149

    CAS  PubMed  Google Scholar 

  • Bouton ME (2002) Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol Psychiatry 52:976–986

    PubMed  Google Scholar 

  • Bouton ME (2004) Context and behavioral processes in extinction. Learn Mem 11:485–494

    PubMed  Google Scholar 

  • 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 12:333–350

    Google Scholar 

  • 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: 2877503

    Google Scholar 

  • 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 105:12533–12538

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 108:887–894

    CAS  PubMed  Google Scholar 

  • Brooks DC (2000) Recent and remote extinction cues reduce spontaneous recovery. Q J Exp Psychol B 53:25–58

    CAS  PubMed  Google Scholar 

  • Brooks DC, Bouton ME (1993) A retrieval cue for extinction attenuates spontaneous recovery. J Exp Psychol Anim Behav Process 19:77–89

    CAS  PubMed  Google Scholar 

  • 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: 2998536

    Google Scholar 

  • Brown SA, Vik PW, Patterson TL, Grant I, Schuckit MA (1995) Stress, vulnerability and adult alcohol relapse. J Stud Alcohol 56:538–545

    CAS  PubMed  Google Scholar 

  • 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) 213:19–27

    CAS  Google Scholar 

  • Buller KM, Xu Y, Day TA (1998) Indomethacin attenuates oxytocin and hypothalamic-pituitary-adrenal axis responses to systemic interleukin-1 beta. J Neuroendocrinol 10:519–528

    CAS  PubMed  Google Scholar 

  • Burattini C, Gill TM, Aicardi G, Janak PH (2006) The ethanol self-administration context as a reinstatement cue: acute effects of naltrexone. Neuroscience 139:877–887

    CAS  PubMed  Google Scholar 

  • 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 42:1013–1020

    CAS  Google Scholar 

  • 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 3:205–221

    CAS  PubMed  Google Scholar 

  • 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 34:2125–2134

    CAS  PubMed  Google Scholar 

  • 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 26:321–352

    PubMed  Google Scholar 

  • 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 105:8114–8119

    CAS  PubMed Central  PubMed  Google Scholar 

  • Charney DS, Heninger GR, Redmond DE Jr (1983) Yohimbine induced anxiety and increased noradrenergic function in humans: effects of diazepam and clonidine. Life Sci 33:19–29

    CAS  PubMed  Google Scholar 

  • 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):1739–1748

    Google Scholar 

  • 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 25:1414–1419

    CAS  PubMed  Google Scholar 

  • 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 27:391–399

    CAS  PubMed  Google Scholar 

  • 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) 172:170–178

    Google Scholar 

  • 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) 168:208–215

    CAS  Google Scholar 

  • 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 11:339–355

    PubMed Central  PubMed  Google Scholar 

  • Cooney NL, Gillespie RA, Baker LH, Kaplan RF (1987) Cognitive changes after alcohol cue exposure. J Consult Clin Psychol 55:150–155

    CAS  PubMed  Google Scholar 

  • 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 106:243–250

    CAS  PubMed  Google Scholar 

  • Corbit LH, Janak PH (2007) Ethanol-associated cues produce general pavlovian-instrumental transfer. Alcohol Clin Exp Res 31:766–774

    CAS  PubMed  Google Scholar 

  • Crombag HS, Shaham Y (2002) Renewal of drug seeking by contextual cues after prolonged extinction in rats. Behav Neurosci 116:169–173

    CAS  PubMed  Google Scholar 

  • 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 27:1006–1015

    CAS  PubMed  Google Scholar 

  • 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 363:3233–3243

    PubMed  Google Scholar 

  • Cunningham CL, Niehus JS, Noble D (1993) Species difference in sensitivity to ethanol’s hedonic effects. Alcohol 10:97–102

    CAS  PubMed  Google Scholar 

  • Cunningham CL, Gremel CM, Groblewski PA (2006) Drug-induced conditioned place preference and aversion in mice. Nat Protoc 1:1662–1670

    CAS  PubMed  Google Scholar 

  • Czachowski CL, Santini LA, Legg BH, Samson HH (2002) Separate measures of ethanol seeking and drinking in the rat: effects of remoxipride. Alcohol 28:39–46

    CAS  PubMed  Google Scholar 

  • Daglish MR, Nutt DJ (2003) Brain imaging studies in human addicts. Eur Neuropsychopharmacol 13:453–458

    CAS  PubMed  Google Scholar 

  • 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) 65:111–118

    CAS  Google Scholar 

  • 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 11:2312–2322

    CAS  PubMed  Google Scholar 

  • Dayas CV, Liu X, Simms JA, Weiss F (2007) Distinct patterns of neural activation associated with ethanol seeking: effects of naltrexone. Biol Psychiatry 61:979–989

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 4:153–159

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 189:1–16

    Google Scholar 

  • 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) 189:1–16

    CAS  Google Scholar 

  • 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 50:221–229

    CAS  PubMed  Google Scholar 

  • 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:RC35

    Google Scholar 

  • Eriksen L, Gotestam KG (1984) Conditioned abstinence in alcoholics: a controlled experiment. Int J Addict 19:287–294

    CAS  PubMed  Google Scholar 

  • Ettenberg A (1990) Haloperidol prevents the reinstatement of amphetamine-rewarded runway responding in rats. Pharmacol Biochem Behav 36:635–638

    CAS  PubMed  Google Scholar 

  • Ettenberg A (2009) The runway model of drug self-administration. Pharmacol Biochem Behav 91:271–277

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ettenberg A, MacConell LA, Geist TD (1996) Effects of haloperidol in a response-reinstatement model of heroin relapse. Psychopharmacology (Berl) 124:205–210

    CAS  Google Scholar 

  • Feltenstein MW, See RE (2006) Potentiation of cue-induced reinstatement of cocaine-seeking in rats by the anxiogenic drug yohimbine. Behav Brain Res 174:1–8

    CAS  PubMed  Google Scholar 

  • 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 30:880–891

    CAS  PubMed  Google Scholar 

  • 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 23:2809–2813

    PubMed  Google Scholar 

  • Gass JT, Olive MF (2007) Reinstatement of ethanol-seeking behavior following intravenous self-administration in Wistar rats. Alcohol Clin Exp Res 31:1441–1445

    CAS  PubMed  Google Scholar 

  • 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 58:345–352

    CAS  PubMed  Google Scholar 

  • Goldstein RZ, Volkow ND (2002) Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry 159:1642–1652

    PubMed Central  PubMed  Google Scholar 

  • Greeley JD, Swift W, Prescott J, Heather N (1993) Reactivity to alcohol-related cues in heavy and light drinkers. J Stud Alcohol 54:359–368

    CAS  PubMed  Google Scholar 

  • Gremel CM, Cunningham CL (2007) Role of test activity in ethanol-induced disruption of place preference expression in mice. Psychopharmacology (Berl) 191:195–202

    CAS  Google Scholar 

  • 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 28:1076–1084

    CAS  PubMed  Google Scholar 

  • Grimm JW, Hope BT, Wise RA, Shaham Y (2001) Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature 412:141–142

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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) 175:296–302

    Google Scholar 

  • Heilig M, Egli M, Crabbe JC, Becker HC (2010) Acute withdrawal, protracted abstinence and negative affect in alcoholism: are they linked? Addict Biol 15:169–184

    PubMed Central  PubMed  Google Scholar 

  • 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 162:1515–1520

    PubMed  Google Scholar 

  • 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 137–162

    Google Scholar 

  • 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:R70

    Google Scholar 

  • 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 21:784–791

    CAS  PubMed  Google Scholar 

  • 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 18:125–133

    CAS  PubMed  Google Scholar 

  • Heyser CJ, Moc K, Koob GF (2003) Effects of naltrexone alone and in combination with acamprosate on the alcohol deprivation effect in rats. Neuropsychopharmacology 28:1463–1471

    CAS  PubMed  Google Scholar 

  • 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 88:7261–7265

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 66:143–151

    CAS  PubMed  Google Scholar 

  • 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: 2997761

    Google Scholar 

  • Itzhak Y, Martin JL (2002) Cocaine-induced conditioned place preference in mice: induction, extinction and reinstatement by related psychostimulants. Neuropsychopharmacology 26:130–134

    CAS  PubMed  Google Scholar 

  • Jaffe JH, Cascella NG, Kumor KM, Sherer MA (1989) Cocaine-induced cocaine craving. Psychopharmacology 97:59–64

    CAS  PubMed  Google Scholar 

  • Janak PH, Chaudhri N (2010) The potent effect of environmental context on relapse to alcohol-seeking after extinction. Open Addict J 3:76–87

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kalivas PW, Volkow ND (2005) The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162:1403–1413

    PubMed  Google Scholar 

  • Kaplan RF, Meyer RE, Stroebel CF (1983) Alcohol dependence and responsivity to an ethanol stimulus as predictors of alcohol consumption. Br J Addict 78:259–267

    CAS  PubMed  Google Scholar 

  • 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 79:439–442

    CAS  PubMed  Google Scholar 

  • 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 46:267–272

    CAS  PubMed  Google Scholar 

  • 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 28:550–557

    PubMed  Google Scholar 

  • 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 23:1751–1760

    CAS  PubMed  Google Scholar 

  • Katner SN, Magalong JG, Weiss F (1999) Reinstatement of alcohol-seeking behavior by drug-associated discriminative stimuli after prolonged extinction in the rat. Neuropsychopharmacology 20:471–479

    CAS  PubMed  Google Scholar 

  • Katz JL, Higgins ST (2003) The validity of the reinstatement model of craving and relapse to drug use. Psychopharmacology (Berl) 168:21–30

    CAS  Google Scholar 

  • Kearns DN, Weiss SJ, Panlilio LV (2002) Conditioned suppression of behavior maintained by cocaine self-administration. Drug Alcohol Depend 65:253–261

    CAS  PubMed  Google Scholar 

  • Knackstedt LA, Ettenberg A (2005) Ethanol consumption reduces the adverse consequences of self-administered intravenous cocaine in rats. Psychopharmacology (Berl). 178:143–150

    CAS  PubMed  Google Scholar 

  • Knackstedt LA, Ben-Shahar O, Ettenberg A (2006) Alcohol consumption is preferred to water in rats pretreated with intravenous cocaine. Pharmacol Biochem Behav 85:281–286

    CAS  PubMed  Google Scholar 

  • Koob GF (2003) Alcoholism: allostasis and beyond. Alcohol Clin Exp Res 27:232–243

    CAS  PubMed  Google Scholar 

  • Koob GF, Le Moal M (2008) Review. Neurobiological mechanisms for opponent motivational processes in addiction. Philos Trans R Soc Lond B Biol Sci 363:3113–3123

    PubMed  Google Scholar 

  • Kornet M, Goosen C, Van Ree JM (1990) The effect of interrupted alcohol supply on spontaneous alcohol consumption by rhesus monkeys. Alcohol Alcoholism 25:407–412

    CAS  PubMed  Google Scholar 

  • 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 104:367–376

    CAS  Google Scholar 

  • Kreek MJ, Koob GF (1998) Drug dependence: stress and dysregulation of brain reward pathways. Drug Alcohol Depend 51:23–47

    CAS  PubMed  Google Scholar 

  • 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):2762–2773

    Google Scholar 

  • 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 304:310–318

    CAS  PubMed  Google Scholar 

  • Laberg JC (1986) Alcohol and expectancy: subjective, psychophysiological and behavioral responses to alcohol stimuli in severely, moderately and non-dependent drinkers. Br J Addict 81:797–808

    CAS  PubMed  Google Scholar 

  • 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 142:457–472

    CAS  PubMed  Google Scholar 

  • Lauener H (1963) Conditioned suppression in rats and the effect of pharmacological agents thereon. Psychopharmacologia 4:311–325

    CAS  PubMed  Google Scholar 

  • Le A, Shaham Y (2002) Neurobiology of relapse to alcohol in rats. Pharmacol Ther 94:137–156

    CAS  PubMed  Google Scholar 

  • 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) 135:169–174

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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) 150:317–324

    CAS  Google Scholar 

  • Le AD, Wang A, Harding S, Juzytsch W, Shaham Y (2003) Nicotine increases alcohol self-administration and reinstates alcohol seeking in rats. Psychopharmacology (Berl) 168:216–221

    CAS  Google Scholar 

  • 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) 179:366–373

    CAS  Google Scholar 

  • 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 Biol

    Google Scholar 

  • 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) 218:89–99

    CAS  Google Scholar 

  • Lee B, Tiefenbacher S, Platt DM, Spealman RD (2004) Pharmacological blockade of alpha2-adrenoceptors induces reinstatement of cocaine-seeking behavior in squirrel monkeys. Neuropsychopharmacology 29:686–693

    CAS  PubMed  Google Scholar 

  • Li TK, Lumeng L, McBride WJ, Waller MB (1979) Progress towards a voluntary oral consumption model of alcoholism. Drug Alcohol Depend 4:45–60

    CAS  PubMed  Google Scholar 

  • 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 22:7856–7861

    CAS  PubMed  Google Scholar 

  • 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 300:882–889

    CAS  PubMed  Google Scholar 

  • Liu X, Weiss F (2003) Stimulus conditioned to foot-shock stress reinstates alcohol-seeking behavior in an animal model of relapse. Psychopharmacology (Berl) 168:184–191

    CAS  Google Scholar 

  • 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 8:1228–1245

    Google Scholar 

  • Ludwig AM, Wikler A (1974) “Craving” and relapse to drink. Q J Stud Alcohol 35:108–130

    Google Scholar 

  • Ludwig AM, Wikler A, Stark LH (1974) The first drink: psychobiological aspects of craving. Arch Gen Psychiatry 30:539–547

    CAS  PubMed  Google Scholar 

  • 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 155:124–126

    CAS  PubMed  Google Scholar 

  • Majchrowicz E (1989) Reversal in central nervous system function during ethanol withdrawal in humans and experimental animals. Fed Proc 40:2065–2072

    Google Scholar 

  • 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) 195:345–355

    CAS  Google Scholar 

  • 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 3–70

    Google Scholar 

  • Martin-Fardon R, Ciccocioppo R, Massi M, Weiss F (2000) Nociceptin prevents stress-induced ethanol- but not cocaine-seeking behavior in rats. Neuroreport 11:1939–1943

    CAS  PubMed  Google Scholar 

  • 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 43:271–284

    CAS  PubMed  Google Scholar 

  • 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 74:869–876

    CAS  PubMed  Google Scholar 

  • McBride WJ, Li TK (1998) Animal models of alcoholism: neurobiology of high alcohol-drinking behavior in rodents. Crit Rev Neurobiol 12:339–369

    CAS  PubMed  Google Scholar 

  • McBride WJ, Le AD, Noronha A (2002) Central nervous system mechanisms in alcohol relapse. Alcohol Clin Exp Res 26:280–286

    CAS  PubMed  Google Scholar 

  • McKay JR, Rutherford MJ, Alterman AI, Cacciola JS, Kaplan MR (1995) An examination of the cocaine relapse process. Drug Alcohol Dep 38:35–43

    CAS  Google Scholar 

  • 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):1689–1695

    Google Scholar 

  • 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 15:5439–5447

    Google Scholar 

  • Meyer RE (1996) The disease called addiction: emerging evidence in a 200 year debate. Lancet 347:162–166

    Google Scholar 

  • Miller NS, Goldsmith RJ (2001) Craving for alcohol and drugs in animals and humans: biology and behavior. J Addict Dis 20:87–104

    CAS  PubMed  Google Scholar 

  • 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 46:35–38

    CAS  PubMed  Google Scholar 

  • Monti PM, Binkoff JA, Abrams DB, Zwick WR, Nirenberg TD, Liepman MR (1987) Reactivity of alcoholics and nonalcoholics to drinking cues. J Abnorm Psychol 96:122–126

    CAS  PubMed  Google Scholar 

  • 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 54:235–245

    CAS  PubMed  Google Scholar 

  • 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 23:1386–1394

    CAS  PubMed  Google Scholar 

  • Mueller D, Stewart J (2000) Cocaine-induced conditioned place preference: reinstatement by priming injections of cocaine after extinction. Behav Brain Res 115:39–47

    CAS  PubMed  Google Scholar 

  • 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 29:393–402

    CAS  PubMed  Google Scholar 

  • Nair SG, Gray SM, Ghitza UE (2006) Role of food type in yohimbine- and pellet-priming-induced reinstatement of food seeking. Physiol Behav 88:559–566

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 12:653–671

    CAS  PubMed  Google Scholar 

  • 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 15:81–87

    Google Scholar 

  • O’Brien CP, McLellan AT (1996) Myths about the treatment of addiction. Lancet 347:237–240

    PubMed  Google Scholar 

  • O’Brien CP, Volpicelli LA, Volpicelli JR (1996) Naltrexone in the treatment of alcoholism: a clinical review. Alcohol 13:35–39

    PubMed  Google Scholar 

  • O’Brien CP, Childress AR, Ehrman R, Robbins SJ (1998) Conditioning factors in drug abuse: can they explain compulsion? J Psychopharmacol 12:15–22

    PubMed  Google Scholar 

  • O’Donnel PJ (1984) The abstinence violation effect and circumstances surrounding relapse as a predictor of outcome status in male alcoholic outposts. J Psychol 117:257–262

    Google Scholar 

  • 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 72:213–220

    CAS  PubMed  Google Scholar 

  • Pavlov IP (1927) Conditioned reflexes (GV Anrep trans). Oxford University Press, London

    Google Scholar 

  • Pelloux Y, Everitt BJ, Dickinson A (2007) Compulsive drug seeking by rats under punishment: effects of drug taking history. Psychopharmacology (Berl) 194:127–137

    CAS  Google Scholar 

  • 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 33:1835–1846

    CAS  PubMed  Google Scholar 

  • Rankin HR, Hogson R, Stockwell T (1979) The concept of craving and its measurement. Behav Res Ther 17:389–396

    CAS  PubMed  Google Scholar 

  • 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) 199:109–117

    CAS  Google Scholar 

  • Rodd ZA, Bell RL, Sable HJ, Murphy JM, McBride WJ (2004) Recent advances in animal models of alcohol craving and relapse. Pharmacol Biochem Behav 79:439–450

    CAS  PubMed  Google Scholar 

  • 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 171:207–215

    CAS  PubMed  Google Scholar 

  • 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 26:1632–1641

    CAS  PubMed  Google Scholar 

  • 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 26:1642–1652

    CAS  PubMed  Google Scholar 

  • 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 109:738–742

    CAS  PubMed  Google Scholar 

  • 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) 175:154–162

    CAS  Google Scholar 

  • Saghal A (1984) A critique of the vasopressin memory hypothesis. Psychopharmacology 83:215–228

    Google Scholar 

  • Salimov RM, Salimova NB (1993) The alcohol deprivation effect in hybrid mice. Drug Alcohol Dependence 32:187–191

    CAS  PubMed  Google Scholar 

  • Samson HH, Chappell A (2002) Reinstatement of ethanol seeking responding after ethanol self-administration. Alcohol 26:95–101

    CAS  PubMed  Google Scholar 

  • 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 22:1783–1787

    CAS  PubMed  Google Scholar 

  • 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) 147:274–279

    CAS  Google Scholar 

  • 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 24:766–773

    CAS  PubMed  Google Scholar 

  • Samson HH, Czachowski CL, Chappell A, Legg B (2003) Measuring the appetitive strength of ethanol: use of an extinction trial procedure. Alcohol 31:77–86

    CAS  PubMed  Google Scholar 

  • Schechter MD, Calcagnetti DJ (1993) Trends in place preference conditioning with a cross-indexed bibliography; 1957–1991. Neurosci Biobehav Rev 17:21–41

    CAS  PubMed  Google Scholar 

  • 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 158:1075–1083

    CAS  PubMed  Google Scholar 

  • 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) 179:262–270

    CAS  Google Scholar 

  • Schulteis G, Markou A, Cole M, Koob GF (1995) Decreased brain reward produced by ethanol withdrawal. Proc Natl Acad Sci 92:5880–5884

    CAS  PubMed  Google Scholar 

  • See RE, Fuchs RA, Ledford CC, McLaughlin J (2003) Drug addiction, relapse, and the amygdala. Ann N Y Acad Sci 985:294–307

    CAS  PubMed  Google Scholar 

  • Shaham Y, Erb S, Stewart J (2000) Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Brain Res Rev 33:13–33

    CAS  PubMed  Google Scholar 

  • 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) 168:3–20

    CAS  Google Scholar 

  • Shalev U, Grimm JW, Shaham (2002) Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacol Rev 54:1–42

    Google Scholar 

  • Sharpe AL, Samson HH (2001) Effect of naloxone on appetitive and consummatory phases of ethanol self-administration. Alcohol Clin Exp Res 25:1006–1011

    CAS  PubMed  Google Scholar 

  • 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 55:1082–1089

    CAS  PubMed  Google Scholar 

  • 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 67:804–811

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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: 3151464

    Google Scholar 

  • Sinclair JD (1972) The alcohol-deprivation effect: Influence of various factors. Q Stud Alcohol 33:769–782

    CAS  Google Scholar 

  • Sinclair JD (1979) Alcohol-deprivation effect in rats genetically selected for their ethanol preference. Pharmacol Biochem Behav 10:597–602

    CAS  PubMed  Google Scholar 

  • Sinclair JD, Li T-K (1989) Long and short alcohol deprivation: Effects on AA and P alcohol-preferring rats. Alcohol 6:505–509

    CAS  PubMed  Google Scholar 

  • Sinclair JD, Senter RJ (1967) Increased preference for ethanol in rats following alcohol deprivation. Psychonomic Sci 8:11–12

    Google Scholar 

  • Sinclair JD, Senter RJ (1968) Development of an alcohol deprivation effect in rats. Q J Stud Alcohol 29:863–867

    CAS  PubMed  Google Scholar 

  • 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, Bethesda

    Google Scholar 

  • Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158:343–359

    CAS  Google Scholar 

  • Sinha R (2009) Modeling stress and drug craving in the laboratory: implications for addiction treatment development. Addict Biol 14:84–98

    PubMed Central  PubMed  Google Scholar 

  • Sinha R, Catapano D, O’Malley S (1999) Stress-induced craving and stress response in cocaine dependent individuals. Psychopharmacology (Berl) 142:343–351

    CAS  Google Scholar 

  • Sinha R, Fuse T, Aubin LR, O’Malley SS (2000) Psychological stress, drug-related cues and cocaine craving. Psychopharmacology (Berl) 152:140–148

    CAS  Google Scholar 

  • 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) 170:62–72

    CAS  Google Scholar 

  • 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 63:324–331

    PubMed  Google Scholar 

  • 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: 2734452

    Google Scholar 

  • Spanagel R, Holter SM (2000) Pharmacological validation of a new animal model of alcoholism. J Neural Transm 107:669–680

    CAS  PubMed  Google Scholar 

  • Spanagel R, Kiefer F (2008) Drugs for relapse prevention of alcoholism: ten years of progress. Trends Pharmacol Sci 29:109–115

    CAS  PubMed  Google Scholar 

  • 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 305:39–44

    CAS  PubMed  Google Scholar 

  • Steketee JD, Kalivas PW (2011) Drug wanting: behavioral sensitization and relapse to drug-seeking behavior. Pharmacol Rev 63:348–365

    Google Scholar 

  • 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 51:642–651

    CAS  PubMed  Google Scholar 

  • 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 69:642–649

    CAS  PubMed  Google Scholar 

  • 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–E115

    Google Scholar 

  • Stormark KM, Laberg JC, Bjerland T, Nordby H, Hugdahl K (1995) Autonomic cued reactivity in alcoholics: the effect of olfactory stimuli. Addict Behav 20:571–584

    CAS  PubMed  Google Scholar 

  • 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 26:627–634

    PubMed  Google Scholar 

  • 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 49:181–190

    CAS  PubMed  Google Scholar 

  • 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 136:151–160

    CAS  PubMed  Google Scholar 

  • 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 199:345–349

    CAS  PubMed Central  PubMed  Google Scholar 

  • Topple AN, Hunt GE, McGregor IS (1998) Possible neural substrates of beer-craving in rats. Neurosci Lett 252:99–102

    CAS  PubMed  Google Scholar 

  • Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462

    CAS  PubMed  Google Scholar 

  • Tzschentke TM, Schmidt WJ (2000) Functional relationship among medial prefrontal cortex, nucleus accumbens, and ventral tegmental area in locomotion and reward. Crit Rev Neurobiol 14:131–142

    CAS  PubMed  Google Scholar 

  • 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 26:1494–1501

    CAS  PubMed  Google Scholar 

  • Vanderschuren LJ, Everitt BJ (2004) Drug seeking becomes compulsive after prolonged cocaine self-administration. Science 305:1017–1019

    CAS  PubMed  Google Scholar 

  • Vengeliene V, Celerier E, Chaskiel L, Penzo F, Spanagel R (2009) Compulsive alcohol drinking in rodents. Addict Biol 14:384–396

    CAS  PubMed  Google Scholar 

  • 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 69:1060–1066

    PubMed  Google Scholar 

  • Volpicelli JR, Alterman AI, Hayashida M, O’Brien CP (1992) Naltrexone in the treatment of alcohol dependence. Arch Gen Psychiatry 49:876–880

    CAS  PubMed  Google Scholar 

  • Walker BM, Ehlers CL (2009) Appetitive motivational experience during adolescence results in enhanced alcohol consumption during adulthood. Behav Neurosci 123:926–935. PMCID: 2787447

    Google Scholar 

  • Wallace BC (1989) Psychological and environmental determinants of relapse in crack cocaine smokers. J Subst Abuse Treat 6:95–106

    CAS  PubMed  Google Scholar 

  • 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 25:5389–5396

    CAS  PubMed  Google Scholar 

  • 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) 185:19–28

    CAS  Google Scholar 

  • 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) 193:283–294

    CAS  Google Scholar 

  • 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 25:361–372

    CAS  PubMed  Google Scholar 

  • 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 70:77–94

    CAS  PubMed  Google Scholar 

  • 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 26:9967–9974

    CAS  PubMed  Google Scholar 

  • 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 31:1505–1515

    PubMed  Google Scholar 

  • Zironi I, Burattini C, Aicardi G, Janak PH (2006) Context is a trigger for relapse to alcohol. Behav Brain Res 167:150–155

    CAS  PubMed  Google Scholar 

  • 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) 158:374–381

    CAS  Google Scholar 

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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.

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  1. Molecular and Integrative Neurosciences Department, The Scripps Research Institute, La Jolla, CA, 92037, USA

    Rémi Martin-Fardon & Friedbert Weiss

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Correspondence to Friedbert Weiss .

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  1. Abt. Psychopharmakologie, Zentralinstitut für Seelische Gesundheit, J 5, Mannheim, 68159, Germany

    Wolfgang H. Sommer

  2. Abt. Psychopharmakologie, Zentralinstitut für Seelische Gesundheit, J 5, Mannheim, 68159, Germany

    Rainer Spanagel

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Martin-Fardon, R., Weiss, F. (2012). Modeling Relapse in Animals. In: Sommer, W., Spanagel, R. (eds) Behavioral Neurobiology of Alcohol Addiction. Current Topics in Behavioral Neurosciences, vol 13. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-28720-6_202

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