Skip to main content

Advertisement

SpringerLink
Log in

Reduction of extinction and reinstatement of cocaine seeking by wheel running in female rats

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

Abstract

Rationale and objectives

Previous work has shown that wheel running reduced the maintenance of cocaine self-administration in rats. In the present study, the effect of wheel running on extinction and reinstatement of cocaine seeking was examined. Female rats were trained to run in a wheel during 6-h sessions, and they were then catheterized and placed in an operant conditioning chamber where they did not have access to the wheel but were allowed to self-administer iv cocaine. Subsequently, rats were divided into four groups and were tested on the extinction and reinstatement of cocaine seeking while they had varying access to a wheel in an adjoining compartment. The four groups were assigned to the following wheel access conditions: (1) wheel running during extinction and reinstatement (WER), (2) wheel running during extinction and a locked wheel during reinstatement (WE), (3) locked wheel during extinction and wheel running during reinstatement (WR), and (4) locked wheel during extinction and reinstatement (WL). WE and WR were retested later to examine the effect of one session of wheel access on cocaine-primed reinstatement.

Results

There were no group differences in wheel revolutions, in rate of acquisition of cocaine self-administration, or in responding during maintenance when there was no wheel access. However, during extinction, WE and WER responded less than WR and WL. WR and WER had lower cocaine-primed reinstatement than WE and WL. One session of wheel exposure in WE also suppressed cocaine-primed reinstatement.

Conclusions

Wheel running immediately and effectively reduced cocaine-seeking behavior, but concurrent access to running was necessary. Thus, exercise is a useful and self-sustaining intervention to reduce cocaine-seeking behavior.

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

Access this article

Log in via an institution

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahmad SO, Park JH, Stenho-Bittel L, Lau YS (2009) Effects of endurance exercise on ventral tegmental area neurons in the chronic 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine and probenecid-treated mice. Neurosci Lett 450:102–105

    Article  CAS  PubMed  Google Scholar 

  • Ahmadi J, Kampman K, Dackis C (2006) Outcome predictors in cocaine dependence treatment trials. Am J Addict 15:434–439

    Article  PubMed  Google Scholar 

  • Alaei H, Borjeian L, Azizi M, Orian S, Pourshanazari A, Hanninen O (2006) Treadmill running reverses retention deficit induced by morphine. Eur J Pharmacol 536:138–141

    Article  CAS  PubMed  Google Scholar 

  • Avena NM (2007) Examining the addictive-like properties of binge eating using an animal model of sugar dependence. Exp Clin Psychopharmacol 15:481–491

    Article  PubMed  Google Scholar 

  • Avena NM, Rada P, Hoebel BG (2008) Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32:20–39

    Article  CAS  PubMed  Google Scholar 

  • Bardo MT, Klebaur JE, Valone JM, Deaton C (2001) Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats. Psychopharmacology (Berl) 155:278–284

    Article  CAS  Google Scholar 

  • Belke TW, Wagner JP (2005) The reinforcing property and the rewarding aftereffect of wheel running in rats: a combination of two paradigms. Behav Processes 68:165–172

    Article  PubMed  Google Scholar 

  • Belke TW, Oldford AC, Forgie MY, Beye JA (2005) Responding for sucrose and wheel-running reinforcement: effect of D-amphetamine. Behav Pharmacol 16:219–225

    Article  CAS  PubMed  Google Scholar 

  • Berglind WJ, See RE, Fuchs RA, Ghee SM, Whitfield TW Jr, Miller SW, McGinty JF (2007) A BDNF infusion into the medial prefrontal cortex suppresses cocaine seeking in rats. Eur J Neurosci 26:757–766

    Article  PubMed  Google Scholar 

  • Boakes RA, Mills KJ, Single JP (1999) Sex differences in the relationship between activity and weight loss in the rat. Behav Neurosci 113:1080–1089

    Article  CAS  PubMed  Google Scholar 

  • Boecker H, Sprenger T, Spilker ME, Henriksen G, Koppenhowfer M, Wagner KJ, Valet M, Berthele A, Tolle TR (2008) The runner’s high: opioidergic mechanisms in the human brain. Cerebral Cortex 18:2523–2531

    Article  PubMed  Google Scholar 

  • Bossert JM, Ghitza UE, Lu L, Epstein DH, Shaham Y (2005) Neurobiology of relapse to heroin and cocaine seeking: an update and clinical implications. Eur J Pharmacol 526:36–50

    Article  CAS  PubMed  Google Scholar 

  • Caine SB, Koob GF (1994) Effects of dopamine depletion on responding maintained by cocaine and food. J Exp Anal Behav 61:213–221

    Google Scholar 

  • Campbell UC, Thompson SS, Carroll ME (1998) Acquisition of oral phencyclidine (PCP) self-administration in rhesus monkeys: effects of dose and an alternative nondrug reinforcer. Psychopharmacology 137:132–138

    Article  CAS  PubMed  Google Scholar 

  • Carroll ME (1985) Concurrent phencyclidine and saccharin access: presentation of an alternative reinforcer reduces drug intake. J Exp Anal Behav 43:131–144

    Article  CAS  PubMed  Google Scholar 

  • Carroll ME (1996) Reducing drug abuse by enriching the environment with alternative nondrug reinforcers. In: Green L, Kagel J (eds) Advances in behavioral economics, vol 3. Ablex, Norwood, pp 37–68

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Carroll ME, Campbell UC (2000) A behavioral economic analysis of the reinforcing effects of drugs: transition states of addiction. In: Bickel WK, Vuchinich R (eds) Reframing health behavior change with behavioral economics. Lawrence Erlbaum Associates, Mahwah, pp 63–87

    Google Scholar 

  • Carroll ME, Lac ST (1992) The effects of buprenorphine on self-administration of cocaine and a nondrug reinforcer in rats. Psychopharmacology 106:439–446

    Article  CAS  PubMed  Google Scholar 

  • Carroll ME, Lac ST, Nygaard SL (1989) A concurrently available nondrug reinforcer prevents the acquisition or decreases the maintenance of cocaine-reinforced behavior. Psychopharmacology 97:23–29

    Article  CAS  PubMed  Google Scholar 

  • Carroll ME, Bickel WK, Higgins ST (2001) Nondrug incentives to treat drug abuse: laboratory and clinical developments. In: Carroll ME, Overmier JB (eds) Animal research and human psychological health: advancing human welfare through behavioral science. American Psychological Association, Washington, pp 139–154

    Chapter  Google Scholar 

  • Carroll ME, Anker JJ, Perry JL (2009a) Modeling risk factors for nicotine and other drug abuse in the preclinical laboratory. Drug Alcohol Depend 104:S70–S78

    Article  CAS  PubMed  Google Scholar 

  • Carroll ME, Mach JL, LaNasa RM, Newman JL (2009b) Impulsivity as a measure of withdrawal of orally-delivered PCP and nondrug rewards in male and female monkeys. Psychopharmacology 207:85–98

    Article  CAS  PubMed  Google Scholar 

  • Charilaou M, Karekla M, Constantinou M, Price S (2009) Relationship between physical activity and type of smoking behavior among adolescents and young adults in Cyprus. Nicotine Tob Res 11:969–976

    Article  PubMed  Google Scholar 

  • Chen HI, Kuo YM, Liao CH, Jen CJ, Huang AM, Cherng CG, Su SW, Yu L (2008) Long-term compulsive exercise reduces the rewarding efficacy of 3, 4-methylenedioxymethamphetamine. Behav Brain Res 187:185–189

    Article  CAS  PubMed  Google Scholar 

  • Cleland BS, Foster TM, Temple W (2000) Resurgence: the role of extinction. Behav Processes 52:117–129

    Article  PubMed  Google Scholar 

  • Collingwood TR, Reynolds R, Kohl HW, Smith W, Sloan S (1991) Physical fitness effects on substance abuse risk factors and use patterns. J Drug Educ 21:73–84

    CAS  PubMed  Google Scholar 

  • Collingwood TR, Sunderlin J, Reynolds R, Kohl HW 3rd (2000) Physical training as a substance abuse prevention intervention for youth. J Drug Educ 30:435–451

    Article  CAS  PubMed  Google Scholar 

  • Comer SD, Lac ST, Wyvell CL, Curtis LK, Carroll ME (1995) Food deprivation affects extinction and reinstatement of responding in rats. Psychopharmacology 121:150–157

    Article  CAS  PubMed  Google Scholar 

  • Corwin RL, Wojnicki FH (2006) Binge eating in rats with limited access to vegetable shortening. Curr Protoc Neurosci Chapter 9: Unit9 23B

  • Cosgrove KP, Carroll ME (2003) Differential effects of a nondrug reinforcer, saccharin, on oral self-administration of phencyclidine (PCP) in male and female rhesus monkeys. Psychopharmacology 170:9–16

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove KP, Hunter R, Carroll ME (2002) Wheel-running attenuates intravenous cocaine self-administration in rats: sex differences. Pharm Biochem Behav 73:663–671

    Article  CAS  Google Scholar 

  • Daniel JZ, Cropley M, Fife-Schaw C (2007) Acute exercise effects on smoking withdrawal symptoms and desire to smoke are not related to expectation. Psychopharmacology (Berl) 195:125–129

    Article  CAS  Google Scholar 

  • Di Chiara V, Errico F, Musella A, Rossi S, Mataluni G, Sachetti L, Siracusano A, Castelli M, Cavasinni F, Bernardi G, Usiello A, Centonze D (2009) Voluntary exercise and sucrose consumption enhance cannabinoid CB1 receptor sensitivity in the striatum. Neuropsychopharmacology 35:374–387

    Article  Google Scholar 

  • Dishman RK (1997) Brain monoamines, exercise, and behavioral stress: animal models. Med Sci Sports Exerc 29:63–74

    CAS  PubMed  Google Scholar 

  • Eikelboom R, Mills R (1988) A microanalysis of wheel running in male and female rats. Physiol Behav 43:625–630

    Article  CAS  PubMed  Google Scholar 

  • Epstein R (1983) Resurgence of previously reinforced behavior during extinction. Behav Anal Lett 3:391–397

    Google Scholar 

  • Fisher BE, Petzinger GM, Nixon K, Hogg E, Bremmer S, Meshul CK, Jakowec MW (2004) Exercise-induced behavioral recovery and neuroplasticity in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-lesioned mouse basal ganglia. J Neurosci Res 77:378–390

    Article  CAS  PubMed  Google Scholar 

  • Fulk LJ, Stock HS, Lynn A, Marshall J, Wilson MA, Hand GA (2004) Chronic physical exercise reduces anxiety-like behavior in rats. Int J Sports Med 25:78–82

    Article  CAS  PubMed  Google Scholar 

  • Grimm JW, Osincup D, Wells B, Manaois M, Fyall A, Buse C, Harkness JH (2008) Environmental enrichment attenuates cue-induced reinstatement of surose seeking in rats. Behav Pharmacol 19:777–785

    Article  PubMed  Google Scholar 

  • Gyertyan I, Kiss B, Gal K, Laszlovszky I, Horvath A, Gemesi LI, Saghy K, Pasztor G, Zajer M, Kapas M, Csongor EA, Domany G, Tihanyi K, Szombathelyi Z (2007) Effects of RGH-237 [N-{4-[4-(3-aminocarbonyl-phenyl)-piperazin-1-yl]-butyl}-4-bromo-benzamide ], an orally active, selective dopamine D(3) receptor partial agonist in animal models of cocaine abuse. J Pharmacol Exp Ther 320:1268–1278

    Article  CAS  PubMed  Google Scholar 

  • Hattori S, Naoi M, Nishino H (1994) Striatal dopamine turnover during treadmill running in the rat: relation to the speed of running. Brain Res Bull 35:41–49

    Article  CAS  PubMed  Google Scholar 

  • Higgins ST (1997) The influence of alternative reinforcers on cocaine use and abuse: a brief review. Pharmacol Biochem Behav 57:419–427

    Article  CAS  PubMed  Google Scholar 

  • Jones LC, Bellingham WP, Ward LC (1990) Sex differences in voluntary locomotor activity of food-restricted and ad libitum-fed rats. Implications for the maintenance of a body weight set-point. Comp Biochem Physiol 96:287–290

    Google Scholar 

  • Kalivas PW, McFarland K (2003) Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology (Berl) 168:44–56

    Article  CAS  Google Scholar 

  • Kampman KM, Alterman AI, Volpicelli JR, Maany I, Muller ES, Luce DD, Mulholland EM, Jawad AF, Parikh GA, Mulvaney FD, Weinrieb RM, O’Brien CP (2001a) Cocaine withdrawal symptoms and initial urine toxicology results predict treatment attrition in outpatient cocaine dependence treatment. Psychol Addict Behav 15:52–59

    Article  CAS  PubMed  Google Scholar 

  • Kampman KM, Volpicelli JR, Mulvaney F, Alterman AI, Cornish J, Gariti P, Cnaan A, Poole S, Muller E, Acosta T, Luce D, O’Brien C (2001b) Effectiveness of propranolol for cocaine dependence treatment may depend on cocaine withdrawal symptom severity. Drug Alcohol Depend 63:69–78

    Article  CAS  PubMed  Google Scholar 

  • Kanarek RB, Marks-Kaufman R (1988) Animal models of appetitive behavior: interaction of nutritional factors and drug seeking behavior. Curr Concepts Nutr 16:1–25

    CAS  PubMed  Google Scholar 

  • Kanarek RB, Marks-Kaufman R, D’Anci KE, Przypek J (1995) Exercise attenuates oral intake of amphetamine in rats. Pharmacol Biochem Behav 51:725–729

    Article  CAS  PubMed  Google Scholar 

  • Kelamangalath L, Wagner JJ (2009) Effects of abstinence or extinction on cocaine seeking as a function of withdrawal duration. Behav Pharmacol 20:195–203

    Article  CAS  PubMed  Google Scholar 

  • Khabour OF, Alzoubi KH, Alomari MA, Alzubi MA (2009) Changes in spatial memory and BDNF expression to concurrent dietary restriction and voluntary exercise. Hippocampus. doi:10.1002/hipo.20657

  • Klebaur JE, Phillips SB, Kelly TH, Bardo MT (2001) Exposure to novel environmental stimuli decreases amphetamine self-administration in rats. Exp Clin Psychopharmacol 9:372–379

    Article  CAS  PubMed  Google Scholar 

  • Koob GF (2009) New dimensions in human laboratory models of addiction. Addict Biol 14:1–8

    Article  PubMed  Google Scholar 

  • Korhonen T, Kujala UM, Rose RJ, Kaprio J (2009) Physical activity in adolescence as a predictor of alcohol and illicit drug use in early adulthood: a longitudinal population-based twin study. Twin Res Hum Genet 12:261–268

    Article  PubMed  Google Scholar 

  • Kujala UM, Kaprio J, Rose RJ (2007) Physical activity in adolescence and smoking in young adulthood: a prospective twin cohort study. Addiction 102:1151–1157

    Article  PubMed  Google Scholar 

  • Lambert KG, Kinsley CH (1993) Sex differences and gonadal hormones influence susceptibility to the activity-stress paradigm. Physiol Behav 53:1085–1090

    Article  CAS  PubMed  Google Scholar 

  • Larson EB, Carroll ME (2007) Estrogen receptor beta, but not alpha, mediates estrogen's effect on cocaine-induced reinstatement of extinguished cocaineseeking behavior in ovariectomized female rats. Neuropsychopharmacology 32:1334–1345

    Google Scholar 

  • Lattanzio SB, Eikelboom R (2003) Wheel access duration in rats: I. Effects on feeding and running. Behav Neurosci 117:496–504

    Article  PubMed  Google Scholar 

  • Leitenberg H, Rawson RA, Bath K (1970) Reinforcement of competing behavior during extinction. Science 169:301–303

    Article  CAS  PubMed  Google Scholar 

  • Lett BT, Grant VL, Byrne MJ, Koh MT (2000) Pairings of a distinctive chamber with the aftereffect of wheel running produce conditioned place preference. Appetite 34:87–94

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Grigson PS (2005) Brief access to sweets protect against relapse to cocaine-seeking. Brain Res 1049:128–131

    Article  CAS  PubMed  Google Scholar 

  • Lussier JP, Heil SH, Mongeon JA, Badger GJ, Higgins ST (2006) A meta-analysis of voucher-based reinforcement therapy for substance use disorders. Addiction 101:192–203

    Article  PubMed  Google Scholar 

  • Macias M, Dwornik A, Ziemlinska E, Fehr S, Schachner M, Czarkowska-Bauch J, Skup M (2007) Locomotor exercise alters expression of pro-brain-derived neurotrophic factor, brain-derived neurotrophic factor and its receptor TrkB in the spinal cord of adult rats. Eur J Neurosci 25:2425–2444

    Article  PubMed  Google Scholar 

  • Mantsch JR, Yuferov V, Mathieu-Kia AM, Ho A, Kreek MJ (2004) Effects of extended access to high versus low cocaine doses on self-administration, cocaine-induced reinstatement and brain mRNA levels in rats. Psychopharmacology (Berl) 175:26–36

    Article  CAS  Google Scholar 

  • Marlatt GA (1990) Cue exposure and relapse prevention in the treatment of addictive behaviors. Addict Behav 15:395–399

    Article  CAS  PubMed  Google Scholar 

  • McMillan DE, McClure GY, Hardwick WC (1995) Effects of access to a running wheel on food, water and ethanol intake in rats bred to accept ethanol. Drug Alcohol Depend 40:1–7

    Article  CAS  PubMed  Google Scholar 

  • Meeusen R (2005) Exercise and the brain: insight in new therapeutic modalities. Ann Transplant 10:49–51

    PubMed  Google Scholar 

  • Micheli F, Bonanomi G, Blaney FE, Braggio S, Capelli AM, Checchia A, Curcuruto O, Damiani F, Fabio RD, Donati D, Gentile G, Gribble A, Hamprecht D, Tedesco G, Terreni S, Tarsi L, Lightfoot A, Stemp G, Macdonald G, Smith A, Pecoraro M, Petrone M, Perini O, Piner J, Rossi T, Worby A, Pilla M, Valerio E, Griffante C, Mugnaini M, Wood M, Scott C, Andreoli M, Lacroix L, Schwarz A, Gozzi A, Bifone A, Ashby CR Jr, Hagan JJ, Heidbreder C (2007) 1, 2, 4-Triazol-3-yl-thiopropyl-tetrahydrobenzazepines: a series of potent and selective dopamine D(3) receptor antagonists. J Med Chem 50:5076–5089

    Article  CAS  PubMed  Google Scholar 

  • Mulick JA, Leitenberg H, Rawson RA (1976) Alternative response training, differential reinforcement of other behavior, and extinction in squirrel monkeys (Saimiri sciureus). J Exp Anal Behav 25:311–320

    Article  PubMed  Google Scholar 

  • National Research Council (2003) Guide for the care and use of mammals in neuroscience and behavioral research. National Academies, Washington

    Google Scholar 

  • Neeper SA, Gomez-Pinilla F, Choi J, Cotman CW (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726:49–56

    Article  CAS  PubMed  Google Scholar 

  • O’Dell LE, Chen SA, Smith RT, Specio SE, Balster RL, Paterson NE, Markou A, Zorrilla EP, Koob GF (2007) Extended access to nicotine self-administration leads to dependence: circadian measures, withdrawal measures, and extinction behavior in rats. J Pharmacol Exp Ther 320:180–193

    Article  PubMed  Google Scholar 

  • Olmstead TA, Petry NM (2009) The cost-effectiveness of prize-based and voucher-based contingency management in a population of cocaine-or opioid-dependent outpatients. Drug Alcohol Depend 102:108–115

    Article  PubMed  Google Scholar 

  • Palmer J, Vacc N, Epstein J (1988) Adult inpatient alcoholics: physical exercise as a treatment intervention. J Stud Alcohol 49:418–421

    CAS  PubMed  Google Scholar 

  • Parsons LH, Koob GF, Weiss F (1995) Serotonin dysfunction in the nucleus accumbens of rats during withdrawal after unlimited access to intravenous cocaine. J Pharmacol Exp Ther 274:1182–1191

    CAS  PubMed  Google Scholar 

  • Pendergast DR, Lindholm P, Wylegala J, Warkander D, Lundgren CE (2006) Effects of respiratory muscle training on respiratory CO2 sensitivity in SCUBA divers. Undersea Hyperb Med 33:447–453

    CAS  PubMed  Google Scholar 

  • Petzinger GM, Walsh JP, Akopian G, Hogg E, Abernathy A, Arevalo P, Turnquist P, Vuckovic M, Fisher BE, Togasaki DM, Jakowec MW (2007) Effects of treadmill exercise on dopaminergic transmission in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-lesioned mouse model of basal ganglia injury. J Neurosci 27:5291–5300

    Article  CAS  PubMed  Google Scholar 

  • Pich EM, Pagliusi SR, Tessari M, Talabot-Ayer D, Hooft van Huijsduijnen R, Chiamulera C (1997) Common neural substrates for the addictive properties of nicotine and cocaine. Science 275:83–86

    Article  CAS  PubMed  Google Scholar 

  • Ping A, Kruzich PJ (2008) Concurrent access to sucrose pellets decreases methamphetamine-seeking behavior in Lewis rats. Pharmacol Biochem Behav 90:492–496

    Article  CAS  PubMed  Google Scholar 

  • Podlesnik CA, Jimenez-Gomez STA (2006) Resurgence of alcohol seeking produced by discontinuing non-drug reinforcement as an animal model of drug relapse. Behav Pharmacol 17:369–374

    Article  CAS  PubMed  Google Scholar 

  • Rodefer JS, Carroll ME (1997) A comparison of progressive ratio schedules vs behavioral economic measures: effect of an alternative reinforcer on the reinforcing efficacy of phencyclidine. Psychopharmacology 132:95–103

    Article  CAS  PubMed  Google Scholar 

  • Rossetti ZL, Melis F, Carboni S, Gessa GL (1992) Dramatic depletion of mesolimbic extracellular dopamine after withdrawal from morphine, alcohol or cocaine: a common neurochemical substrate for drug dependence. Ann N Y Acad Sci 654:513–516

    Article  CAS  PubMed  Google Scholar 

  • Sarbadhikari SN, Saha AK (2006) Moderate exercise and chronic stress produce counteractive effects on different areas of the brain by acting through various neurotransmitter receptor subtypes: a hypothesis. Theor Biol Med Model 3:33

    Article  PubMed  Google Scholar 

  • Schenk S, Lacelle G, Gorman K, Amit Z (1987) Cocaine self-administration in rats influenced by environmental conditions: implications for the etiology of drug abuse. Neurosci Lett 81:227–231

    CAS  PubMed  Google Scholar 

  • Schmidt HD, Pierce RC (2006) Systemic administration of a dopamine, but not a serotonin or norepinephrine, transporter inhibitor reinstates cocaine seeking in the rat. Behav Brain Res 175:189–194

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sindelar JL, Olmstead TA, Peirce JM (2007) Cost-effectiveness of prize-based contingency management in methadone maintenance treatment programs. Addiction 102:1463–1471

    Article  PubMed  Google Scholar 

  • Sinyor D, Brown T, Rostant L, Seraganian P (1982) The role of a physical fitness program in the treatment of alcoholism. J Stud Alcohol 43:380–386

    CAS  PubMed  Google Scholar 

  • Smith MA, Schmidt KT, Iordanou JC, Mustroph ML (2008) Aerobic exercise decreases the positive-reinforcing effects of cocaine. Drug Alcohol Depend 98:129–135

    Article  CAS  PubMed  Google Scholar 

  • Solinas M, Chauvet C, Thiriet N, El Rawas R, Jaber M (2008) Reversal of cocaine addiction by environmental enrichment. Proc Natl Acad Sci U S A 105:17145–17150

    Article  CAS  PubMed  Google Scholar 

  • Stairs DJ, Klein ED, Bardo MT (2006) Effects of environmental enrichment on extinction and reinstatement of amphetamine self-administration and sucrose-maintained responding. Behav Pharmacol 17:597–604

    Article  CAS  PubMed  Google Scholar 

  • Taylor A, Katomeri M (2007) Walking reduces cue-elicited cigarette cravings and withdrawal symptoms, and delays ad libitum smoking. Nicotine Tob Res 9:1183–1190

    Article  PubMed  Google Scholar 

  • Taylor AH, Ussher MH, Faulkner G (2007) The acute effects of exercise on cigarette cravings, withdrawal symptoms, affect and smoking behaviour: a systematic review. Addiction 102:534–543

    Article  PubMed  Google Scholar 

  • Ussher M, Nunziata P, Cropley M, West R (2001) Effect of a short bout of exercise on tobacco withdrawal symptoms and desire to smoke. Psychopharmacology (Berl) 158:66–72

    Article  CAS  Google Scholar 

  • Ussher M, West R, Doshi R, Sampuran AK (2006) Acute effect of isometric exercise on desire to smoke and tobacco withdrawal symptoms. Hum Psychopharmacol 21:39–46

    Article  PubMed  Google Scholar 

  • Ussher MH, Owen CG, Cook DG, Whincup PH (2007) The relationship between physical activity, sedentary behaviour and psychological wellbeing among adolescents. Soc Psychiatry Psychiatri Epidemiol 42:851–856

    Article  Google Scholar 

  • Ussher M, Cropley M, Playle S, Mohidin R, West R (2009) Effect of isometric exercise and body scanning on cigarette cravings and withdrawal symptoms. Addiction 104:1251–1257

    Article  PubMed  Google Scholar 

  • Weinstock J, Barry D, Petry NM (2008) Exercise-related activities are associated with positive outcome in contingency management treatment for substance use disorders. Addict Behav 33:1072–1075

    Article  PubMed  Google Scholar 

  • Werme M, Thoren P, Olson L, Brene S (2000) Running and cocaine both upregulate dynorphin mRNA in medial caudate putamen. Eur J Neurosci 12:2967–2974

    Article  CAS  PubMed  Google Scholar 

  • Werme M, Messer C, Olson L, Gilden L, Thoren P, Nestler EJ, Brene S (2002) Delta FosB regulates wheel running. J Neurosci 22:8133–8138

    CAS  PubMed  Google Scholar 

  • Widenfalk J, Olson L, Thoren P (1999) Deprived of habitual running, rats downregulate BDNF and TrkB messages in the brain. Neurosci Res 34:125–132

    Article  CAS  PubMed  Google Scholar 

  • Wilson KG, Hayes SC (1996) Resurgence of derived stimulus relations. J Exp Anal Behav 66:267–281

    Article  CAS  PubMed  Google Scholar 

  • Wise RA, Newton P, Leeb K, Burnette B, Pocock D, Justice JB Jr (1995) Fluctuations in nucleus accumbens dopamine concentration during intravenous cocaine self-administration in rats. Psychopharmacology (Berl) 120:10–20

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Institute on Drug Abuse, R01 DA 003240-25, K05 015267-07 (MEC), and F31 DA 023301-02 (JJA). The authors would like to thank Nathan Holtz, Emily Kidd, Brandon Knight, Kinner Patel, Amy Saykao, Matthew Starr, Rachael Turner, Troy Velie, and Jeremy Williams for their technical assistance.

Author information

Authors and Affiliations

  1. Department of Psychiatry, University of Minnesota, MMC 392, Minneapolis, MN, 55455, USA

    Natalie E. Zlebnik, Justin J. Anker, Luke A. Gliddon & Marilyn E. Carroll

Authors
  1. Natalie E. Zlebnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Justin J. Anker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luke A. Gliddon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marilyn E. Carroll
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marilyn E. Carroll.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zlebnik, N.E., Anker, J.J., Gliddon, L.A. et al. Reduction of extinction and reinstatement of cocaine seeking by wheel running in female rats. Psychopharmacology 209, 113–125 (2010). https://doi.org/10.1007/s00213-010-1776-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-010-1776-0

Keywords

Search

Navigation