Abstract
Rationale
The circumstances of drug taking are thought to play a role in drug abuse but the evidence of it is anecdotal. Previous studies have shown that the intravenous self-administration of cocaine is facilitated in rats non-residing in the test chambers relative to rats that live in the test chambers at all times. We investigated here whether environmental context could exert its modulatory influence on heroin and amphetamine self-administration as well.
Materials and methods
Independent groups of rats were given the possibility to self-administer different doses of heroin or amphetamine (12.5, 25.0, or 50.0 μg/kg). Some animals were housed in the self-administration chambers (resident groups) whereas other rats were transported to the self-administration chambers only for the test sessions (non-resident groups).
Results
Amphetamine-reinforcing effects were more pronounced in non-resident rats than in resident rats, as previously reported for cocaine. Quite unexpectedly, the opposite was found for heroin. Because of this surprising dissociation, some of the rats trained to self-administer amphetamine were later given the opportunity to self-administer heroin. Also in this case, resident rats took more heroin than non-resident rats.
Conclusions
These findings suggest an unforeseen dissociation between opioid and psychostimulant reward and demonstrate that even in the laboratory rat some contexts are associated with the propensity to self-administer more opioid than psychostimulant drugs and vice versa, thus indicating that drug taking is influenced not only by economical or cultural factors but also can be modulated at a much more basic level by the setting in which drugs are experienced.
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References
Anthony JC, Chen YC (2004) Epidemiology of drug dependence. In: Galanter M, Kleber HD (eds) Textbook of substance abuse treatment. American Psychiatric, Washington, DC, pp 55–72
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
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
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
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
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
Badiani A, Oates MM, Robinson TE (2000a) Modulation of morphine sensitization in the rat by contextual stimuli. Psychopharmacology (Berl) 151:273–282
Badiani A, Oates MM, Fraioli S, Browman KE, Ostrander MM, Xue CJ et al (2000b) 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
Browman KE, Badiani A, Robinson TE (1998) 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
Caprioli D, Paolone G, Celentano M, Testa A, Nencini P, Badiani A (2007a) Environmental modulation of cocaine self-administration in the rat. Psychopharmacology (Berl) 192:397–406
Caprioli D, Celentano M, Paolone G, Badiani A (2007b) Modeling the role of environment in addiction. Prog Neuropsychopharmacol Biol Psychiatry 31:1639–1653
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
Devine DP, Leone P, Pocock D, Wise RA (1993) Differential involvement of ventral tegmental mu, delta and kappa opioid receptors in modulation of basal mesolimbic dopamine release: in vivo microdialysis studies. J Pharmacol Exp Ther 266:1236–1246
Di Chiara G, Imperato A (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85:5274–5278
Falk JL, Feingold DA (1987) Environmental and cultural factors in the behavioral actions of drugs. In: Meltzer HY (ed) Psychopharmacology: the third generation of progress. Raven, New York, pp 1503–1510
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
Friedman SB, Ader R (1967) Adrenocortical response to novelty and noxious stimulation. Neuroendocrinology 2:209–212
Gysling K, Wang RY (1983) Morphine-induced activation of A10 dopamine neurons in the rat. Brain Res 277:119–127
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
Hinson RE, Poulous CX (1981) Sensitization to the behavioral effects of cocaine: modification by Pavlovian conditioning. Pharmacol Biochem Behav 15:559–562
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
Ikemoto S (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56:27–78
Johanson CE, Fischman MW (1989) The pharmacology of cocaine related to its abuse. Pharmacol Rev 41:3–52
Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483–488
Kuczenski R, Segal DS (1994) Neurochemistry of amphetamine. In: Cho AK, Segal DS (eds) Amphetamine and its analogs: psychopharmacology, toxicology and abuse. Academic, San Diego, pp 81–113
Matthews RT, German DC (1984) Electrophysiological evidence for excitation of rat ventral tegmental area dopamine neurons by morphine. Neuroscience 11:617–625
Nestler EJ (2005) Historical review: molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol Sci 25:210–218
Ostrander MM, Badiani A, Day HE, 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
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
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
Paolone G, Conversi D, Caprioli D, Del Bianco P, Nencini P, Cabib S et al (2007) Modulatory effect of environmental context and drug history on heroin-induced psychomotor activity and Fos protein expression in the rat brain. Neuropsychopharmacology 32:2611–2623
Piazza PV, Le Moal M (1998) The role of stress in drug self-administration. Trends Pharmacol Sci 19:67–74
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
Tilson HA, Rech RH (1973) Conditioned drug effects and absence of tolerance to d-amphetamine induced motor activity. Pharmacol Biochem Behav 1:149–153
Trujillo KA, Zamora JJ, Warmoth KP (2008) Increased response to ketamine following treatment at long intervals: implications for intermittent use. Biol Psychiatry 63(2):178–183
Uslaner J, Badiani A, Norton CS, Day HEW, Watson SJ, Akil H, Robinson TE (2001) 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
Vezina P, Stewart J (1984) Conditioning and place-specific sensitization of increases in activity induced by morphine in the VTA. Pharmacol Biochem Behav 20:925–934
Wang H, Gracy KN, Pickel VM (1999) Mu-opioid and NMDA-type glutamate receptors are often colocalized in spiny neurons within patches of the caudate–putamen nucleus. J Comp Neurol 412:132–146
Westermeyer J (2004) Cross-cultural aspects of substance abuse. In: Galanter M, Kleber HD (eds) Textbook of substance abuse treatment. American Psychiatric, Washington, DC, pp 55–72
Wise RA (2004) Dopamine, learning and motivation. Nature Reviews Neuroscience 5:483–494
Wise RA, Bozarth MA (1987) A psychomotor stimulant theory of addiction. Psychol Rev 94:469–492
Zinberg NE (1984) Drug, set, and setting: the basis for controlled intoxicant use. Yale University Press, New Haven
Acknowledgments
The authors wish to thank Jane Stewart and Yavin Shaham for their helpful comments on previous versions of this manuscript. This work was supported by grants from the University of Rome Sapienza (Fondi di Ateneo 2006, C26A06LHXL, and Fondi di Facoltà 2006, C26F06Y9LL) and from the Italian Ministry for University and Research (PRIN, 2005050334_004).
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The authors of the present manuscript do not have any conflicts of interest, financial or otherwise, including direct or indirect financial or personal relationships, interests, and affiliations relevant to the subject matter of the manuscript, that have occurred in the past or that are expected in the foreseeable future. This disclosure includes, but is not limited to, grants or funding, employment, affiliations, patents (in preparation, filed, or granted), inventions, honoraria, consultancies, royalties, stock options/ownership, or expert testimony.
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Daniele Caprioli and Michele Celentano equally contributed to the study.
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Caprioli, D., Celentano, M., Paolone, G. et al. Opposite environmental regulation of heroin and amphetamine self-administration in the rat. Psychopharmacology 198, 395–404 (2008). https://doi.org/10.1007/s00213-008-1154-3
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DOI: https://doi.org/10.1007/s00213-008-1154-3