Psychopharmacology

, Volume 214, Issue 2, pp 557–566 | Cite as

Effect of environmental enrichment on escalation of cocaine self-administration in rats

  • Cassandra D. Gipson
  • Joshua S. Beckmann
  • Shady El-Maraghi
  • Julie A. Marusich
  • Michael T. Bardo
Original Investigation

Abstract

Background

Previous studies found that environmental enrichment protects against the initiation of stimulant self-administration in rats, but it is unclear if enrichment also protects against the escalation of stimulant use with long-term exposure.

Objective

The current study examined the effects of environmental enrichment on escalation of cocaine self-administration using an extended access procedure.

Methods

Rats were raised from 21 days in an enriched condition (EC) with social cohorts and novel objects, a social condition with only social cohorts (SC), a novelty condition (NC) with novel objects in isolated cages, or an isolated condition (IC) without social cohorts or novel objects. In young adulthood, EC, SC, NC, and IC rats were separated into short access (ShA) or long access (LgA) groups that received either 1 or 6 h, respectively, of daily cocaine self-administration (0.1 mg/kg/infusion) for 14 days. In a second experiment, EC and IC rats were used to assess differences in acquisition and escalation of cocaine self-administration at a 0.5 mg/kg/infusion unit dose.

Results

With ShA sessions, EC rats acquired cocaine self-administration at a slower rate than IC rats at both unit doses; however, with extended training, both groups eventually reached similar rates. At the 0.1 mg/kg/infusion dose, only NC and IC rats escalated in amount of intake when switched to the LgA sessions. At the 0.5 mg/kg/infusion dose, rates of cocaine self-administration escalated in LgA groups over 14 days regardless of EC or IC rearing condition; however, EC rats escalated at a faster rate, eventually reaching the same level of intake observed in IC rats.

Conclusions

Although environmental enrichment protects against escalation of a low unit dose of cocaine, it may not protect against escalation with a higher unit dose. In addition, at a lower unit dose, this protective mechanism appears to be due to the presence of social cohorts rather than novel objects.

Keywords

Environmental enrichment Escalation Cocaine Addiction 

References

  1. Adams J, Bowman K, Burke B, Casson L, Caviness L, Coffey LE (1999) National household survey on drug abuse data collection. Final reportGoogle Scholar
  2. Ahmed SH (2009) Escalation of drug use. In: Olmstead MC (ed) Neuromethods: animal models of drug addiction. Humana, TotowaGoogle Scholar
  3. Ahmed SH, Koob GF (1998) Transition from moderate to excessive drug intake: change in hedonic set point. Science 282(5387):298–300PubMedCrossRefGoogle Scholar
  4. Ahmed SH, Koob GF (1999) Long-lasting increase in the set point for cocaine self administration after escalation in rats. Psychopharmacology 146(3):303–312PubMedCrossRefGoogle Scholar
  5. Ahmed SH, Koob GF (2004) Changes in response to a dopamine receptor antagonist in rats with escalating cocaine intake. Psychopharmacology 172(4):450–454PubMedCrossRefGoogle Scholar
  6. Ahmed SH, Lin D, Koob GF, Parsons LH (2003) Escalation of cocaine self-administration does not depend on altered cocaine-induced nucleus accumbens dopamine levels. J Neurochem 86:102–113PubMedCrossRefGoogle Scholar
  7. Ahmed SH, Stinus L, Le Moal M, Cador M (1995) Social deprivation enhances the vulnerability of male Wistar rats to stressor- and amphetamine-induced behavioral sensitization. Psychopharmacology 117(1):116–124PubMedCrossRefGoogle Scholar
  8. Bardo MT, Bowling SL, Rowlett JK, Manderscheid P (1995) Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine. Pharmacol Biochem Behav 51(2–3):397–405PubMedCrossRefGoogle Scholar
  9. Bardo MT, Valone JM, Robinet PM, Shaw WB, Dwoskin LP (1999) Environmental enrichment enhances the stimulant effect of intravenous amphetamine: search for a cellular mechanism in the nucleus accumbens. Psychobiology 27(2):292–299Google Scholar
  10. Bardo MT, Valone KJE, JM DC (2001) Environmental enrichment decreases intravenous self administration of amphetamine in female and male rats. Psychopharmacology 155(3):278–284PubMedCrossRefGoogle Scholar
  11. Bowling SL, Rowlett JK, Bardo MT (1993) The effect of environmental enrichment on amphetamine-stimulated locomotor activity, dopamine synthesis and dopamine release. Neuropharmacology 32(9):885–893PubMedCrossRefGoogle Scholar
  12. Carroll ME (1996) Reducing drug abuse by enriching the environment with alternative nondrug reinforcers. In: Green L, Kagel J (eds) Advances in behavioral economics. Ablex, Norwood, p 3Google Scholar
  13. Carroll ME, Meisch RA (1984) Increased drug-reinforced behavior due to food deprivation. In: Thompson T, Barrett JE (eds) Advances in behavioral pharmacology, 4th edn. Academic, New York, pp 47–88Google Scholar
  14. Carroll ME, Lac ST (1993) Autoshaping i.v. cocaine self-administration in rats: effects of nondrug alternative reinforcers on acquisition. Psychopharmacology 110(1–2):5–12PubMedCrossRefGoogle Scholar
  15. Fritz M, El Rawas R, Ahmad S, Klement S, Bardo MT, Kemmler G, Dechant G, Saria A, Zernig G (2010) Reversal of cocaine-conditioned place preference and mesocorticolimbic Zif268 expression by social interaction in rats. Addict Biol (in press)Google Scholar
  16. Gipson CD, Bardo MT (2009) Extended access to d-amphetamine self-administration increases impulsive choice in a delay discounting task in rats. Psychopharmacology 207:391–400PubMedCrossRefGoogle Scholar
  17. Green T, Gehrke B, Bardo MT (2002) Environmental enrichment decreases intravenous amphetamine self-administration in rats: dose-response functions for fixed- and progressive-ratio schedules. Psychopharmacology 162:373–378PubMedCrossRefGoogle Scholar
  18. Green TA, Alibhai IN, Roybal N, Winstanley CA, Theobald DEH, Birnbaum SG, Graham AR, Unterberg S, Graham DL, Vialou V, Bass CE, Terwilliger EF, Bardo MT, Nestler EJ (2010) Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens. Biol Psychiatry 67:28–35PubMedCrossRefGoogle Scholar
  19. Hopfer CJ, Crowley TJ, Hewitt JK (2003) Review of twin and adoption studies of adolescent substance abuse. J Am Acad Child Adolesc Psych 42(6):710–719CrossRefGoogle Scholar
  20. Kanarek RB, Marks-Kaufman R (1988) Dietary modulation of oral amphetamine intake in rats. Physio & Beh 44(4–5):501–505CrossRefGoogle Scholar
  21. Kitamura O, Wee S, Specio SE, Koob GF, Pulvirenti L (2006) Escalation of methamphetamine self administration in rats: a dose effect function. Psychopharmacology 186(1):48–53PubMedCrossRefGoogle Scholar
  22. Koob GF, Kreek MJ (2007) Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am J Psychiatry 164:1149–1159PubMedCrossRefGoogle Scholar
  23. Landau D (1986) The effects of changes and constraints on access to video game playing on alcohol consumption. Diss Abstr Int 48:1174BGoogle Scholar
  24. Marusich JA, Beckmann JS, Gipson CD, Bardo MT (2010) Methylphenidate as a reinforcer for rats: contingent delivery and intake escalation. Exp Clin Psychopharmacol 18(3):257–266PubMedCrossRefGoogle Scholar
  25. McGue M, Sharma A, Benson P (1996) Parent and sibling influences on adolescent alcohol use and misuse: evidence from a U.S. adoption cohort. J Stud Alcohol 57(1):8–18PubMedGoogle Scholar
  26. Montgomery DC, Peck A, Vining GG (2006) Introduction to linear regression analysis, 4th edn. Wiley, New YorkGoogle Scholar
  27. Olmstead MC (2006) Animal models of drug addiction: where do we go from here? Q J Exp Psychol 59(4):625–653CrossRefGoogle Scholar
  28. Renner MJ, Rosenzweig MR (1987) Enriched and impoverished environments: effects on brain and behavior. Springer, New YorkGoogle Scholar
  29. Rosenzweig MR, Bennet EL, Hebert M, Morimoto H (1978) Social grouping cannot account for cerebral effects of enriched environments. Brain Res 153(3):563–576PubMedCrossRefGoogle Scholar
  30. Solinas M, Chauvet C, Thiriet N, El Rawas R, Jaber M (2008) Reversal of cocaine addiction by environmental enrichment. Proc Natl Acad Sci 105(44):17145–17150PubMedCrossRefGoogle Scholar
  31. Solinas M, Thiriet N, El Rawas R, Lardeux V, Jaber M (2009) Environmental enrichment during early states of life reduces the behavioral, neurochemical, and molecular effects of cocaine. Neuropsychopharmacology 34:1102–1111PubMedCrossRefGoogle Scholar
  32. Schwendt M, Rocha A, See RE, Pacchioni AM, McGinty JF, Kalivas PW (2009) Extended methamphetamine self-administration in rats results in a selective reduction of dopamine transporter levels in the prefrontal cortex and dorsal striatum not accompanied by marked monoaminergic depletion. J Pharmacol Exp Ther 331(2):555–562PubMedCrossRefGoogle Scholar
  33. Thiel KJ, Sanabria F, Pentkowski NS, Neisewander JL (2009) Anti-craving effects of environmental enrichment. Int J Neuropsychopharmacol 12(9):1151–1156PubMedCrossRefGoogle Scholar
  34. Vuchinich RE, Tucker JA (1983) Behavioral theories of choice as a framework for studying drinking behavior. J Abnormal Psy 92(4):408–416CrossRefGoogle Scholar
  35. Wagner FA, Anthony JC (2002) From first drug use to drug dependence: developmental periods of risk for dependence upon marijuana, cocaine and alcohol. Neuropsychopharmacol 26:479–488CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Cassandra D. Gipson
    • 1
  • Joshua S. Beckmann
    • 1
  • Shady El-Maraghi
    • 1
  • Julie A. Marusich
    • 2
  • Michael T. Bardo
    • 1
  1. 1.Center for Drug Abuse Research Translation (CDART)University of KentuckyLexingtonUSA
  2. 2.Discovery & Analytical SciencesRTI InternationalResearch Triangle ParkUSA

Personalised recommendations