Skip to main content

Advertisement

SpringerLink
Log in

Environmental modulation of cocaine self-administration in the rat

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

Abstract

Rationale

Previous studies have shown that environmental context can powerfully modulate the induction of psychomotor sensitization to cocaine in the rat. Rats that receive repeated administrations of cocaine in association with environmental novelty exhibit greater psychomotor sensitization than animals that receive the same treatments in their home cages.

Objectives

The goal of the present study was to investigate whether environmental context can exert its modulatory influence also on cocaine self-administration.

Materials and methods

Independent groups of rats with intravenous catheters were given the possibility to self-administer different doses of cocaine (0.0, 0.2, 0.4, and 0.8 mg/kg per infusion) under two environmental conditions. Some animals were housed in the self-administration cages (home groups), whereas other rats were transported to the self-administration cages only for the test sessions (novelty groups).

Results

Environmental “novelty” facilitated the acquisition of cocaine self-administration at the doses of 0.2 and 0.4 mg/kg per infusion. When rats were given access to a higher dose of cocaine (0.8 mg/kg per infusion), there were no significant group differences in drug taking. Environmental context had no effect on the self-administration of the vehicle. Thus, it appears that environmental “novelty” produced a shift to the left in the dose-effect curve for cocaine self-administration. Furthermore, “novelty” enhanced the motivation of the rats to work for cocaine, as indicated by the results of a progressive ratio procedure.

Conclusions

The present findings demonstrate for the first time that the environment surrounding drug taking can alter both the intake of and motivation for cocaine.

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

Access this article

Log in via an institution

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

  • Badiani A, Robinson TE (2004) Drug-induced neurobehavioral plasticity: the role of environmental context. Behav Pharmacol 15:327–339

    Article  PubMed  CAS  Google Scholar 

  • Badiani A, Anagnostaras SG, Robinson TE (1995a) The development of sensitization to the psychomotor stimulant effects of amphetamine is enhanced in a novel environment. Psychopharmacology (Berl) 117:443–452

    Article  CAS  Google Scholar 

  • Badiani A, Browman KE, Robinson TE (1995b) Influence of novel versus home environments on sensitization to the psychomotor stimulant effects of cocaine and amphetamine. Brain Res 674:291–298

    Article  PubMed  CAS  Google Scholar 

  • Badiani A, Morano I, Akil H, Robinson TE (1995c) Circulating adrenal hormones are not necessary for the development of sensitization to the psychomotor activating effects of amphetamine. Brain Res 673:13–24

    Article  PubMed  CAS  Google Scholar 

  • Badiani A, Camp DM, Robinson TE (1997) Enduring enhancement of amphetamine sensitization by drug-associated environmental stimuli. J Pharmacol Exp Ther 282:787–794

    PubMed  CAS  Google Scholar 

  • Badiani A, Oates MM, Day HEW, Watson SJ, Akil H, Robinson TE (1998) Amphetamine-induced behavior, dopamine release and c-fos mRNA expression: modulation by environmental novelty. J Neurosci 18:10579–10593

    PubMed  CAS  Google Scholar 

  • Badiani A, Oates MM, Day HEW, Watson SJ, Akil H, Robinson TE (1999) Environmental modulation of amphetamine-induced c-fos expression in D1 versus D2 striatal neurons. Behav Brain Res 103:203–209

    Article  PubMed  CAS  Google Scholar 

  • Badiani A, Oates MM, Fraioli S, Browman KE, Ostrander MM, Xue CJ, Wolf ME, Robinson TE (2000a) Environmental modulation of the response to amphetamine: dissociation between changes in behavior and changes in dopamine and glutamate overflow in the rat striatal complex. Psychopharmacology (Berl) 151:166–174

    Article  CAS  Google Scholar 

  • Badiani A, Oates MM, Robinson TE (2000b) Modulation of morphine sensitization in the rat by contextual stimuli. Psychopharmacology (Berl) 151:273–282

    Article  CAS  Google Scholar 

  • Bardo MT, Bowling SL, Rowlett JK, Manderscheid P, Buxton ST, Dwoskin LP (1995) Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine. Pharmacol Biochem Behav 51:397–405

    Article  PubMed  CAS  Google Scholar 

  • Browman KE, Badiani A, Robinson TE (1998a) Modulatory effect of environmental stimuli on the susceptibility to amphetamine sensitization: a dose-effect study in rats. J Pharmacol Exp Ther 287:1007–1014

    PubMed  CAS  Google Scholar 

  • Browman KE, Badiani A, Robinson TE (1998b) The influence of environment on the induction of sensitization to the psychomotor activating effects of intravenous cocaine in rats is dose-dependent. Psychopharmacology (Berl) 137:90–98

    Article  CAS  Google Scholar 

  • Covington HE III, Miczek KA (2005) Intense cocaine self-administration after episodic social defeat stress, but not after aggressive behavior: dissociation from corticosterone activation. Psychopharmacology (Berl) 183:331–340

    Article  CAS  Google Scholar 

  • Crombag HS, Badiani A, Robinson TE (1996) Signalled versus unsignalled intravenous amphetamine: large differences in the acute psychomotor response and sensitization. Brain Res 722:227–231

    Article  PubMed  CAS  Google Scholar 

  • Day HEW, Badiani A, Uslaner JM, Oates MM, Vittoz NM, Robinson TE, Watson SJ Jr, Akil H (2001) Environmental novelty differentially affects c-fos mRNA expression induced by amphetamine or cocaine in subregions of the bed nucleus of the stria terminalis and amygdala. J Neurosci 21:732–740

    PubMed  CAS  Google Scholar 

  • Erb S, Shaham Y, Stewart J (1998) The role of corticotropin-releasing factor and corticosterone in stress- and cocaine-induced relapse to cocaine seeking in rats. J Neurosci 18:5529–5536

    PubMed  CAS  Google Scholar 

  • Ferguson SM, Thomas MJ, Robinson TE (2004) Morphine-induced c-fos mRNA expression in striatofugal circuits: modulation by dose, environmental context, and drug history. Neuropsychopharmacology 29:1664–1674

    Article  PubMed  CAS  Google Scholar 

  • Fraioli S, Crombag HS, Badiani A, Robinson TE (1999) Susceptibility to amphetamine-induced locomotor sensitization is modulated by environmental stimuli. Neuropsychopharmacology 20:533–541

    Article  PubMed  CAS  Google Scholar 

  • Friedman SB, Ader R (1967) Adrenocortical response to novelty and noxious stimulation. Neuroendocrinology 2:209–212

    Google Scholar 

  • Goeders NE, Guerin GF (1994) Non-contingent electric footshock facilitates the acquisition of intravenous cocaine self-administration in rats. Psychopharmacology (Berl) 114:63–70

    Article  CAS  Google Scholar 

  • Goeders NE, Guerin G (1996) Role of corticosterone in intravenous cocaine self-administration in rats. Neuroendocrinology 64:337–348

    PubMed  CAS  Google Scholar 

  • Harlan RE, Garcia MM (1998) Drugs of abuse and immediate-early genes in the forebrain. Mol Neurobiol 16:221–267

    PubMed  CAS  Google Scholar 

  • Hennessy MB (1991) Sensitization of the plasma corticosterone response to novel environments. Physiol Behav 50:1175–1179

    Article  PubMed  CAS  Google Scholar 

  • Hennessy JW, Levin R, Levine S (1977) Influence of experiential factors and gonadal hormones on pituitary–adrenal response of the mouse to novelty and electric shock. J Comp Physiol Psychol 91:770–777

    Article  PubMed  CAS  Google Scholar 

  • Hope BT, Simmons DE, Mitchell TB, Kreuter JD, Mattson BJ (2006) Cocaine-induced locomotor activity and Fos expression in nucleus accumbens are sensitized for 6 months after repeated cocaine administration outside the home cage. Eur J Neurosci 24:867–875

    Article  PubMed  Google Scholar 

  • Hughes P, Dragunow M (1995) Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol Rev 47:133–178

    PubMed  CAS  Google Scholar 

  • Hyman SE, Malenka RC (2001) Addiction and the brain: the neurobiology of compulsion and its persistence. Nat Rev Neurosci 2:695–703

    Article  PubMed  CAS  Google Scholar 

  • King MG, Burrows GD, Stanley GV (1983) Measurement of stress and arousal: validation of the stress/arousal adjective checklist. Br J Psychol 74:473–479

    PubMed  Google Scholar 

  • Li Y, Acerbo MJ, Robinson TE (2004) The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur J Neurosci 20:1647–1654

    Article  PubMed  Google Scholar 

  • Mantsch JR, Katz ES (2007) Elevation of glucocorticoids is necessary but not sufficient for the escalation of cocaine self-administration by chronic electric footshock stress in rats. Neuropsychopharmacology 32(2):367–376

    Article  PubMed  CAS  Google Scholar 

  • Miczek KA, Mutschler NH (1996) Activational effects of social stress on IV cocaine self-administration in rats. Psychopharmacology (Berl) 128:256–264

    Article  CAS  Google Scholar 

  • Nestler EJ (2001) Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2:119–128

    Article  PubMed  CAS  Google Scholar 

  • Ostrander MM, Badiani A, Day HEW, Norton CS, Watson SJ, Akil H, Robinson TE (2003) Environmental context and drug history modulate amphetamine-induced c-fos mRNA expression in the basal ganglia, central extended amygdala, and associated limbic forebrain. Neuroscience 120:551–571

    Article  PubMed  CAS  Google Scholar 

  • Paolone G, Burdino R, Badiani A (2003) Dissociation in the modulatory effects of environmental novelty on the locomotor, analgesic, and eating response to acute and repeated morphine in the rat. Psychopharmacology (Berl) 166:146–155

    CAS  Google Scholar 

  • Paolone G, Palopoli M, Marrone MC, Nencini P, Badiani A (2004) Environmental modulation of the interoceptive effects of amphetamine in the rat. Behav Brain Res 152:149–155

    PubMed  CAS  Google Scholar 

  • Paolone G, Conversi D, Caprioli D, Del Bianco P, Nencini P, Cabib S, Badiani A (2007) Modulatory effect of environmental context and drug history on heroin-induced psychomotor activity and Fos protein expression in the rat brain. Neuropsychopharmacology (in press)

  • Piazza PV, Marinelli M, Jodogne C, Deroche V, Rouge-Pont F, Maccari S, Le Moal M, Simon H (1994) Inhibition of corticosterone synthesis by Metyrapone decreases cocaine-induced locomotion and relapse of cocaine self-administration. Brain Res 658:259–264

    Article  PubMed  CAS  Google Scholar 

  • Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ (1987) Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237:1219–1223

    Article  PubMed  CAS  Google Scholar 

  • Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18:247–291

    Article  PubMed  CAS  Google Scholar 

  • Segal DS, Kuczenski R (1994) Behavioral pharmacology of amphetamine. In: Cho AK, Segal DS (eds) Amphetamine and its analogs: psychopharmacology, toxicology, and abuse. Academic, San Diego, pp 115–150

    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

    Article  PubMed  CAS  Google Scholar 

  • Shalev U, Marinelli M, Baumann MH, Piazza PV, Shaham Y (2003) The role of corticosterone in food deprivation-induced reinstatement of cocaine seeking in the rat. Psychopharmacology (Berl) 168(1–2):170–176, (Jul)

    Article  CAS  Google Scholar 

  • Ujike H, Takaki M, Kodama M, Kuroda S (2002) Gene expression related to synaptogenesis, neuritogenesis, and MAP kinase in behavioral sensitization to psychostimulants. Ann NY Acad Sci 965:55–67

    Article  PubMed  CAS  Google Scholar 

  • Uslaner J, Badiani A, Day HEW, Watson SJ, Akil H, Robinson TE (2001a) Environmental context modulates the ability of cocaine and amphetamine to induce c-fos mRNA expression in the neocortex, caudate nucleus, and nucleus accumbens. Brain Res 920:106–116

    Article  PubMed  CAS  Google Scholar 

  • Uslaner J, Badiani A, Norton CS, Day HEW, Watson SJ, Akil H, Robinson TE (2001b) Amphetamine and cocaine induce different patterns of c-fos mRNA expression in the striatum and subthalamic nucleus depending on environmental context. Eur J Neurosci 13:1977–1983

    Article  PubMed  CAS  Google Scholar 

  • Vezina P (2004) Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs. Neurosci Biobehav Rev 27:827–839

    Article  PubMed  CAS  Google Scholar 

  • White FJ, Kalivas PW (1998) Neuroadaptations involved in amphetamine and cocaine addiction. Drug Alcohol Depend 51:141–153

    Article  PubMed  CAS  Google Scholar 

  • Woodson JC, Macintosh D, Fleshner M, Diamond DM (2003) Emotion-induced amnesia in rats: working memory-specific impairment, corticosterone-memory correlation, and fear versus arousal effects on memory. Learn Mem 10:326–336

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

This work was supported by grants from the University of Rome La Sapienza (Fondi di Ateneo e Fondi di Facoltà) and from the Italian Ministry for University and Research (PRIN).

Author information

Authors and Affiliations

  1. Department of Human Physiology and Pharmacology, University of Rome Sapienza, 5 Piazzale Aldo Moro, 00185, Rome, Italy

    Daniele Caprioli, Giovanna Paolone, Michele Celentano, Arianna Testa, Paolo Nencini & Aldo Badiani

  2. Center for Research in Neurobiology (CRiN), University of Rome Sapienza, Rome, Italy

    Paolo Nencini & Aldo Badiani

Authors
  1. Daniele Caprioli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giovanna Paolone
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michele Celentano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arianna Testa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paolo Nencini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aldo Badiani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aldo Badiani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caprioli, D., Paolone, G., Celentano, M. et al. Environmental modulation of cocaine self-administration in the rat. Psychopharmacology 192, 397–406 (2007). https://doi.org/10.1007/s00213-007-0717-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-007-0717-z

Keywords

Search

Navigation