Skip to main content

Advertisement

Log in

Reinstatement of cocaine seeking induced by drugs, cues, and stress in adolescent and adult rats

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

In human and animal studies, adolescence marks a period of increased vulnerability to the initiation and subsequent abuse of drugs. Adolescents may be especially vulnerable to relapse, and a critical aspect of drug abuse is that it is a chronically relapsing disorder. However, little is known of how vulnerability factors such as adolescence are related to conditions that induce relapse, triggered by the drug itself, drug-associated cues, or stress.

Objective

The purpose of this study was to compare adolescent and adult rats on drug-, cue-, and stress-induced reinstatement of cocaine-seeking behavior.

Methods

On postnatal days 23 (adolescents) and 90 (adults), rats were implanted with intravenous catheters and trained to lever press for i.v. infusions of cocaine (0.4 mg/kg) during two daily 2-h sessions. The rats then self-administered i.v. cocaine for ten additional sessions. Subsequently, visual and auditory stimuli that signaled drug delivery were unplugged, and rats were allowed to extinguish lever pressing for 20 sessions. Rats were then tested on cocaine-, cue-, and yohimbine (stress)-induced cocaine seeking using a within-subject multicomponent reinstatement procedure.

Results

Results indicated that adolescents had heightened cocaine seeking during maintenance and extinction compared to adults. During reinstatement, adolescents (vs adults) responded more following cocaine- and yohimbine injections, while adults (vs adolescents) showed greater responding following presentations of drug-associated cues.

Conclusion

These results demonstrated that adolescents and adults differed across several measures of drug-seeking behavior, and adolescents may be especially vulnerable to relapse precipitated by drugs and stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adriani W, Laviola G (2003) Elevated levels of impulsivity and reduced place conditioning with d-amphetamine: two behavioral features of adolescence in mice. Behav Neurosci 117:695–703

    Article  PubMed  CAS  Google Scholar 

  • Andersen SL, Dumont NL, Teicher MH (1997) Developmental differences in dopamine synthesis inhibition by (+/−)-7-OH-DPAT. Naunyn Schmiedebergs Arch Pharmacol 356:173–181

    Article  PubMed  CAS  Google Scholar 

  • Badanich KA, Adler KJ, Kirstein CL (2006) Adolescents differ from adults in cocaine conditioned place preference and cocaine-induced dopamine in the nucleus accumbens septi. Eur J Pharmacol 550:95–106

    Article  PubMed  CAS  Google Scholar 

  • Badanich KA, Maldonado AM, Kirstein CL (2008) Early adolescents show enhanced acute cocaine-induced locomotor activity in comparison to late adolescent and adult rats. Dev Psychobiol 50:127–133

    Article  PubMed  CAS  Google Scholar 

  • Baumeister SE, Tossmann P (2005) Association between early onset of cigarette, alcohol and cannabis use and later drug use patterns: an analysis of a survey in European metropolises. Eur Addict Res 11:92–98

    Article  PubMed  CAS  Google Scholar 

  • Belluzzi JD, Wang R, Leslie FM (2005) Acetaldehyde enhances acquisition of nicotine self-administration in adolescent rats. Neuropsychopharmacology 30:705–712

    Article  PubMed  CAS  Google Scholar 

  • Bolanos CA, Barrott M, Berton O, Wallace-Black D, Nestler EJ (2003) Methylphenidate treatement during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood. Biol Psychiatry 54:1317–1329

    Article  PubMed  CAS  Google Scholar 

  • Bongiovanni M, See RE (2008) A comparison of the effects of different operant training experiences and dietary restriction on the reinstatement of cocaine-seeking in rats. Pharmacol Biochem Behav 89:227–233

    Article  PubMed  CAS  Google Scholar 

  • Brenhouse HC, Andersen SL (2008) Delayed extinction and stronger reinstatement of cocaine conditioned place preference in adolescent rats, compared to adults. Behav Neurosci 122:460–465

    Article  PubMed  CAS  Google Scholar 

  • Brenhouse HC, Sonntag KC, Andersen SL (2008) Transient D1 dopamine receptor expression on prefrontal cortex projection neurons: relationship to enhanced motivational salience of drug cues in adolescence. J Neurosci 28:2375–2382

    Article  PubMed  CAS  Google Scholar 

  • Brielmaier JM, McDonald CG, Smith RF (2007) Immediate and long-term behavioral effects of a single nicotine injection in adolescent and adult rats. Neurotoxicol Teratol 29:74–80

    Article  PubMed  CAS  Google Scholar 

  • Brown SA, D’Amico EJ (2001) Outcomes of alcohol treatment for adolescents. Recent Dev Alcohol 15:307–327

    Article  PubMed  CAS  Google Scholar 

  • Carelli RM, Deadwyler SA (1994) A comparison of nucleus accumbens neuronal firing patterns during cocaine self-administration and water reinforcement in rats. J Neurosci 14:7735–7746

    PubMed  CAS  Google Scholar 

  • Carroll ME, Boe IN (1982) Increased intravenous drug self-administration during deprivation of other reinforcers. Pharmacol Biochem Behav 17:563–567

    Article  PubMed  CAS  Google Scholar 

  • Carroll ME, Morgan AD, Lynch WJ, Campbell UC, Dess NK (2002) Intravenous cocaine and heroin self-administration in rats selectively bred for differential saccharin intake: phenotype and sex differences. Psychopharmacology (Berl) 161:304–313

    Article  CAS  Google Scholar 

  • Carroll ME, Morgan AD, Anker JJ, Perry JL, Dess NK (2008) Selective breeding for differential saccharin intake as an animal model of drug abuse. Behav Pharmacol 19:435–460

    Article  PubMed  CAS  Google Scholar 

  • Carroll ME, Anker JJ, Perry JL (2009) Modeling risk factors for nicotine and other drug abuse in the preclinical laboratory. Drug Alcohol Depend 104:70–78

    Article  CAS  Google Scholar 

  • Casey BJ, Jones RM, Hare TA (2008) The adolescent brain. Ann N Y Acad Sci 1124:111–126

    Article  PubMed  CAS  Google Scholar 

  • Caster JM, Walker QD, Kuhn CM (2005) Enhanced behavioral response to repeated-dose cocaine in adolescent rats. Psychopharmacology (Berl) 183:218–225

    Article  CAS  Google Scholar 

  • Catalano RF, Hawkins JD, Wells EA, Miller J, Brewer D (1990) Evaluation of the effectiveness of adolescent drug abuse treatment, assessment of risks for relapse, and promising approaches for relapse prevention. Int J Addict 25:1085–1140

    PubMed  Google Scholar 

  • Catlow BJ, Kirstein CL (2007) Cocaine during adolescence enhances dopamine in response to a natural reinforcer. Neurotoxicol Teratol 29:57–65

    Article  PubMed  CAS  Google Scholar 

  • Chambers RA, Taylor JR, Potenza MN (2003) Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 160:1041–1052

    Article  PubMed  Google Scholar 

  • Chen H, Matta SG, Sharp BM (2007) Acquisition of nicotine self-administration in adolescent rats given prolonged access to the drug. Neuropsychopharmacology 32:700–709

    Article  PubMed  CAS  Google Scholar 

  • Chung T, Maisto SA (2006) Relapse to alcohol and other drug use in treated adolescents: review and reconsideration of relapse as a change point in clinical course. Clin Psychol Rev 26:149–161

    Article  PubMed  Google Scholar 

  • Colby CR, Whisler K, Steffen C, Nestler EJ, Self DW (2003) Striatal cell type-specific overexpression of DeltaFosB enhances incentive for cocaine. J Neurosci 23:2488–2493

    PubMed  CAS  Google Scholar 

  • Courtois R, Reveillere C, Paus A, Berton L, Jouint C (2007) Links between stress factors, mental health and initial consumption of tobacco and alcohol during pre-adolescence. Encephale 33:300–309

    Article  PubMed  CAS  Google Scholar 

  • Cunningham MG, Bhattacharyya S, Benes FM (2002) Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J Comp Neurol 453:116–130

    Article  PubMed  Google Scholar 

  • Deas D (2006) Adolescent substance abuse and psychiatric comorbidities. J Clin Psychiatry 67(Suppl 7):18–23

    PubMed  Google Scholar 

  • Dennis M, Godley SH, Diamond G, Tims FM, Babor T, Donaldson J, Liddle H, Titus JC, Kaminer Y, Webb C, Hamilton N, Funk R (2004) The Cannabis Youth Treatment (CYT) Study: main findings from two randomized trials. J Subst Abuse Treat 27:197–213

    Article  PubMed  Google Scholar 

  • Di Chiara G (1998) A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use. J Psychopharmacol 12:54–67

    Article  PubMed  Google Scholar 

  • Doherty J, Ogbomnwan Y, Williams B, Frantz K (2009) Age-dependent morphine intake and cue-induced reinstatement, but not escalation in intake, by adolescent and adult male rats. Pharmacol Biochem Behav 92:164–172

    Article  PubMed  CAS  Google Scholar 

  • Ehrlich ME, Sommer J, Canas E, Unterwald EM (2002) Periadolescent mice show enhanced DeltaFosB upregulation in response to cocaine and amphetamine. J Neurosci 22:9155–9159

    PubMed  CAS  Google Scholar 

  • Ernst M, Pine DS, Hardin M (2006) Triadic model of the neurobiology of motivated behavior in adolescence. Psychol Med 36:299–312

    Article  PubMed  Google Scholar 

  • Estroff TW, Schwartz RH, Hoffmann NG (1989) Adolescent cocaine abuse. Addictive potential, behavioral and psychiatric effects. Clin Pediatr (Phila) 28:550–555

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Fontaine RG (2006) Evaluative behavioral judgments and instrumental antisocial behaviors in children and adolescents. Clin Psychol Rev 26:956–967

    Article  PubMed  Google Scholar 

  • Frantz KJ, O’Dell LE, Parsons LH (2007) Behavioral and neurochemical responses to cocaine in periadolescent and adult rats. Neuropsychopharmacology 32:625–637

    Article  PubMed  CAS  Google Scholar 

  • Freeman MR (2006) Sculpting the nervous system: glial control of neuronal development. Curr Opin Neurobiol 16:119–125

    Article  PubMed  CAS  Google Scholar 

  • Fullgrabe MW, Vengeliene V, Spanagel R (2007) Influence of age at drinking onset on the alcohol deprivation effect and stress-induced drinking in female rats. Pharmacol Biochem Behav 86:320–326

    Article  PubMed  CAS  Google Scholar 

  • Galvan A, Hare TA, Parra CE, Penn J, Voss H, Glover G, Casey BJ (2006) Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J Neurosci 26:6885–6892

    Article  PubMed  CAS  Google Scholar 

  • Gullo MJ, Dawe S (2008) Impulsivity and adolescent substance use: rashly dismissed as “all-bad”? Neurosci Biobehav Rev 32:1507–1518

    Article  PubMed  Google Scholar 

  • Hayaki J, Stein MD, Lassor JA, Herman DS, Anderson BJ (2005) Adversity among drug users: relationship to impulsivity. Drug Alcohol Depend 78:65–71

    Article  PubMed  Google Scholar 

  • Hoffmann JP, Cerbone FG (2002) Parental substance use disorder and the risk of adolescent drug abuse: an event history analysis. Drug Alcohol Depend 66:255–264

    Article  PubMed  Google Scholar 

  • Ivanov I, Schulz KP, London ED, Newcorn JH (2008) Inhibitory control deficits in childhood and risk for substance use disorders: a review. Am J Drug Alcohol Abuse 34:239–258

    Article  PubMed  Google Scholar 

  • Jentsch JD, Taylor JR (1999) Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berl) 146:373–390

    Article  CAS  Google Scholar 

  • Kantak KM, Goodrich CM, Uribe V (2007) Influence of sex, estrous cycle, and drug-onset age on cocaine self-administration in rats (Rattus norvegicus). Exp Clin Psychopharmacol 15:37–47

    Article  PubMed  CAS  Google Scholar 

  • Keiflin R, Vouillac C, Cador M (2008) Level of operant training rather than cocaine intake predicts level of reinstatement. Psychopharmacology (Berl) 197:247–261

    Article  CAS  Google Scholar 

  • Kerstetter KA, Kantak KM (2007) Differential effects of self-administered cocaine in adolescent and adult rats on stimulus-reward learning. Psychopharmacology (Berl) 194:403–411

    Article  CAS  Google Scholar 

  • Koob GF (2009) Brain stress systems in the amygdala and addiction. Brain Res 1293:61–75

    Article  PubMed  CAS  Google Scholar 

  • Kota D, Martin BR, Robinson SE, Damaj MI (2007) Nicotine dependence and reward differ between adolescent and adult male mice. J Pharmacol Exp Ther 322:399–407

    Article  PubMed  CAS  Google Scholar 

  • Laviola G, Adriani W, Terranova ML, Gerra G (1999) Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neurosci Biobehav Rev 23:993–1010

    Article  PubMed  CAS  Google Scholar 

  • Leri F, Stewart J (2001) Drug-induced reinstatement to heroin and cocaine seeking: a rodent model of relapse in polydrug use. Exp Clin Psychopharmacol 9:297–306

    Article  PubMed  CAS  Google Scholar 

  • Levesque J, Joanette Y, Mensour B, Beaudoin G, Leroux JM, Bourgouin P, Beauregard M (2004) Neural basis of emotional self-regulation in childhood. Neuroscience 129:361–369

    Article  PubMed  CAS  Google Scholar 

  • Levin ED, Rezvani AH, Montoya D, Rose JE, Swartzwelder HS (2003) Adolescent-onset nicotine self-administration modeled in female rats. Psychopharmacology (Berl) 169:141–149

    Article  CAS  Google Scholar 

  • Levin ED, Lawrence SS, Petro A, Horton K, Rezvani AH, Seidler FJ, Slotkin TA (2007) Adolescent vs. adult-onset nicotine self-administration in male rats: duration of effect and differential nicotinic receptor correlates. Neurotoxicol Teratol 29:458–465

    Article  PubMed  CAS  Google Scholar 

  • Li C, Frantz KJ (2009) Attenuated incubation of cocaine seeking in male rats trained to self-administer cocaine during periadolescence. Psychopharmacology (Berl) 204:725–733

    Article  CAS  Google Scholar 

  • Lopez B, Turner RJ, Saavedra LM (2005) Anxiety and risk for substance dependence among late adolescents/young adults. J Anxiety Disord 19:275–294

    Article  PubMed  Google Scholar 

  • Lynch WJ, Carroll ME (1999) Sex differences in the acquisition of intravenously self-administered cocaine and heroin in rats. Psychopharmacology (Berl) 144:77–82

    Article  CAS  Google Scholar 

  • Maldonado AM, Kirstein CL (2005a) Cocaine-induced locomotor activity is increased by prior handling in adolescent but not adult female rats. Physiol Behav 86:568–572

    Article  PubMed  CAS  Google Scholar 

  • Maldonado AM, Kirstein CL (2005b) Handling alters cocaine-induced activity in adolescent but not adult male rats. Physiol Behav 84:321–326

    Article  PubMed  CAS  Google Scholar 

  • McCambridge J, Strang J (2005) Age of first use and ongoing patterns of legal and illegal drug use in a sample of young Londoners. Subst Use Misuse 40:313–319

    Article  PubMed  Google Scholar 

  • McCormick CM, Mathews IZ (2007) HPA function in adolescence: role of sex hormones in its regulation and the enduring consequence of exposure to stressors. Pharmacol Biochem Behav 86:220–233

    Article  PubMed  CAS  Google Scholar 

  • Montague DM, Lawler CP, Mailman RB, Gilmore JH (1999) Developmental regulation of the dopamine D1 receptor in human caudate and putamen. Neuropsychopharmacology 21:641–649

    Article  PubMed  CAS  Google Scholar 

  • National Research Council (2003) Guidelines for the care and use of mammals in neuroscience and behavioral research. The National Academies, Washington D.C., p 209

    Google Scholar 

  • Nestler EJ (2008) Review. Transcriptional mechanisms of addiction: role of DeltaFosB. Philos Trans R Soc Lond B Biol Sci 363:3245–3255

    Article  PubMed  CAS  Google Scholar 

  • Nestler EJ, Barrot M, Self DW (2001) DeltaFosB: a sustained molecular switch for addiction. Proc Natl Acad Sci U S A 98:11042–11046

    Article  PubMed  CAS  Google Scholar 

  • Niculescu M, Ehrlich ME, Unterwald EM (2005) Age-specific behavioral responses to psychostimulants in mice. Pharmacol Biochem Behav 82:280–288

    Article  PubMed  CAS  Google Scholar 

  • Obot IS, Wagner FA, Anthony JC (2001) Early onset and recent drug use among children of parents with alcohol problems: data from a national epidemiologic survey. Drug Alcohol Depend 65:1–8

    Article  PubMed  CAS  Google Scholar 

  • Ojeda SR, Andrews WW, Advis JP, White SS (1980) Recent advances in the endocrinology of puberty. Endocr Rev 1:228–257

    Article  PubMed  CAS  Google Scholar 

  • Palmer RH, Young SE, Hopfer CJ, Corley RP, Stallings MC, Crowley TJ, Hewitt JK (2009) Developmental epidemiology of drug use and abuse in adolescence and young adulthood: evidence of generalized risk. Drug Alcohol Depend 102:78–87

    Article  PubMed  CAS  Google Scholar 

  • Parylak SL, Caster JM, Walker QD, Kuhn CM (2008) Gonadal steroids mediate the opposite changes in cocaine-induced locomotion across adolescence in male and female rats. Pharmacol Biochem Behav 89:314–323

    Article  PubMed  CAS  Google Scholar 

  • Perepletchikova F, Krystal JH, Kaufman J (2008) Practitioner review: adolescent alcohol use disorders: assessment and treatment issues. J Child Psychol Psychiatry 49:1131–1154

    PubMed  Google Scholar 

  • Perry JL, Anderson MM, Nelson SE, Carroll ME (2007) Acquisition of i.v. cocaine self-administration in adolescent and adult male rats selectively bred for high and low saccharin intake. Physiol Behav 91:126–133

    Article  PubMed  CAS  Google Scholar 

  • Rao U, Ryan ND, Dahl RE, Birmaher B, Rao R, Williamson DE, Perel JM (1999) Factors associated with the development of substance use disorder in depressed adolescents. J Am Acad Child Adolesc Psychiatry 38:1109–1117

    Article  PubMed  CAS  Google Scholar 

  • Roth ME, Cosgrove KP, Carroll ME (2004) Sex differences in the vulnerability to drug abuse: a review of preclinical studies. Neurosci Biobehav Rev 28:533–546

    Article  PubMed  CAS  Google Scholar 

  • Rubinow MJ, Juraska JM (2009) Neuron and glia numbers in the basolateral nucleus of the amygdala from preweaning through old age in male and female rats: a stereological study. J Comp Neurol 512:717–725

    Article  PubMed  Google Scholar 

  • Rubinow MJ, Hagerbaumer DA, Juraska JM (2009) The food-conditioned place preference task in adolescent, adult and aged rats of both sexes. Behav Brain Res 198:263–266

    Article  PubMed  Google Scholar 

  • Schepis TS, Adinoff B, Rao U (2008) Neurobiological processes in adolescent addictive disorders. Am J Addict 17:6–23

    Article  PubMed  Google Scholar 

  • Schramm-Sapyta NL, Walker QD, Caster JM, Levin ED, Kuhn CM (2009) Are adolescents more vulnerable to drug addiction than adults? Evidence from animal models. Psychopharmacology (Berl) 206:1–21

    Article  CAS  Google Scholar 

  • Schultz W, Apicella P, Ljungberg T (1993) Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 13:900–913

    PubMed  CAS  Google Scholar 

  • Schweinsburg AD, Paulus MP, Barlett VC, Killeen LA, Caldwell LC, Pulido C, Brown SA, Tapert SF (2004) An FMRI study of response inhibition in youths with a family history of alcoholism. Ann N Y Acad Sci 1021:391–394

    Article  PubMed  Google Scholar 

  • See RE (2005) Neural substrates of cocaine-cue associations that trigger relapse. European Journal of Pharmacology 526:140–146

    Article  PubMed  CAS  Google Scholar 

  • Shahbazi M, Moffett AM, Williams BF, Frantz KJ (2008) Age- and sex-dependent amphetamine self-administration in rats. Psychopharmacology (Berl) 196:71–81

    Article  CAS  Google Scholar 

  • Shram MJ, Funk D, Li Z, Le AD (2006) Periadolescent and adult rats respond differently in tests measuring the rewarding and aversive effects of nicotine. Psychopharmacology (Berl) 186:201–208

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Snyder KJ, Katovic NM, Spear LP (1998) Longevity of the expression of behavioral sensitization to cocaine in preweanling rats. Pharmacol Biochem Behav 60:909–914

    Article  PubMed  CAS  Google Scholar 

  • Spear L (2000a) Modeling adolescent development and alcohol use in animals. Alcohol Res Health 24:115–123

    PubMed  CAS  Google Scholar 

  • Spear LP (2000b) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463

    Article  PubMed  CAS  Google Scholar 

  • Spear LP (2009) Heightened stress responsivity and emotional reactivity during pubertal maturation: implications for psychopathology. Dev Psychopathol 21:87–97

    Article  PubMed  Google Scholar 

  • Spencer TJ, Biederman J, Mick E (2007) Attention-deficit/hyperactivity disorder: diagnosis, lifespan, comorbidities, and neurobiology. J Pediatr Psychol 32:631–642

    Article  PubMed  Google Scholar 

  • Stansfield KH, Kirstein CL (2007) Chronic cocaine or ethanol exposure during adolescence alters novely-related behaviors in adulthood. Pharmacol Biochem Behav 86:637–642

    Article  PubMed  CAS  Google Scholar 

  • Tarazi FI, Tomasini EC, Baldessarini RJ (1999) Postnatal development of dopamine D1-like receptors in rat cortical and striatolimbic brain regions: an autoradiographic study. Dev Neurosci 21:43–49

    Article  PubMed  CAS  Google Scholar 

  • Torres OV, Tejeda HA, Natividad LA, O’Dell LE (2008) Enhanced vulnerability to the rewarding effects of nicotine during the adolescent period of development. Pharmacol Biochem Behav 90:658–663

    Article  PubMed  CAS  Google Scholar 

  • Underwood MD, Mann JJ, Huang YY, Arango V (2008) Family history of alcoholism is associated with lower 5-HT2A receptor binding in the prefrontal cortex. Alcohol Clin Exp Res 32:593–599

    Article  PubMed  CAS  Google Scholar 

  • Vetter CS, Doremus-Fitzwater TL, Spear LP (2007) Time course of elevated ethanol intake in adolescent relative to adult rats under continuous, voluntary-access conditions. Alcohol Clin Exp Res 31:1159–1168

    Article  PubMed  CAS  Google Scholar 

  • Winters KC, Lee CY (2008) Likelihood of developing an alcohol and cannabis use disorder during youth: association with recent use and age. Drug Alcohol Depend 92:239–247

    Article  PubMed  Google Scholar 

  • Winters KC, Stinchfield RD, Opland E, Weller C, Latimer WW (2000) The effectiveness of the Minnesota Model approach in the treatment of adolescent drug abusers. Addiction 95:601–612

    Article  PubMed  CAS  Google Scholar 

  • Zakharova E, Leoni G, Kichko I, Izenwasser S (2009a) Differential effects of methamphetamine and cocaine on conditioned place preference and locomotor activity in adult and adolescent male rats. Behav Brain Res 198:45–50

    Article  PubMed  CAS  Google Scholar 

  • Zakharova E, Wade D, Izenwasser S (2009b) Sensitivity to cocaine conditioned reward depends on sex and age. Pharmacol Biochem Behav 92:131–134

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Institute on Drug Abuse grants, R01 DA 003240-25, R01 DA019942-2, K05 015267-07 (MEC), and F31 DA 023301-02 (JJA). The authors would like to thank Luke Gliddon, Nathan Holtz, Emily Kidd, Paul Regier, Amy Saykao, Matthew Starr, Rachel Turner, and Natalie Zlebnik for their technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Justin J. Anker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anker, J.J., Carroll, M.E. Reinstatement of cocaine seeking induced by drugs, cues, and stress in adolescent and adult rats. Psychopharmacology 208, 211–222 (2010). https://doi.org/10.1007/s00213-009-1721-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-009-1721-2

Keywords

Navigation