Abstract
Rationale
Drug addiction is a multifactorial disorder resulting from an interaction between genetic and environmental factors, and negative and positive environmental conditions may increase or reduce, respectively, vulnerability to drug addiction.
Objectives
The influence of different social experiences on the acquisition, extinction, and reinstatement of a cocaine-induced conditioned place preference (CPP) was evaluated.
Methods
In experiment 1, adolescent and adult male OF1 mice housed under four different conditions (grouped, isolated, crowded, and cohabitating with a female) were conditioned with 50, 12.5, or 3.125 mg/kg of cocaine. All mice underwent extinction sessions until the CPP was extinguished. The effects of cocaine priming injections on the reinstatement of CPP were then evaluated. In experiment 2, the effect of different social experiences on the maintenance and reinstatement of cocaine-CPP in adult mice was studied.
Results
Although housing conditions did not affect the acquisition of cocaine-CPP, it did modify reinstatement after extinction. Adolescent mice living in crowded conditions or cohabitating with a female did not present reinstatement after cocaine priming. Similarly, neither isolated adult mice nor adults cohabitating with a female presented reinstatement. In grouped adult mice, isolation after acquisition of the CPP and social defeat before reinstatement increased the vulnerability to reinstatement induced by cocaine priming. Conversely, both exposure to females and a brief social interaction undermined cocaine-induced reinstatement.
Conclusions
Social experiences modify vulnerability to reinstatement, acting as prevention or risk factors in the development of drug addiction.
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References
Ahmed SH, Koob GF (1997) Cocaine—but not food-seeking behavior is reinstated by stress after extinction. Psychopharmacology 132:289–295
Armario A, Castellanos JM, Balasch J (1984) Effect of crowding on emotional reactivity in male rats. Neuroendocrinology 39:330–333
Balda MA, Anderson KL, Itzhak Y (2006) Adolescent and adult responsiveness to the incentive value of cocaine reward in mice: role of neuronal nitric oxide synthase (nNOS) gene. Neuropharmacology 51:341–349
Boyle AE, Gill K, Smith BR, Amit Z (1991) Differential effects of an early housing manipulation on cocaine-induced activity and self-administration in laboratory rats. Pharmacol Biochem Behav 39:269–274
Bozarth MA, Murray A, Wise RA (1989) Influence of housing conditions on the acquisition of intravenous heroin and cocaine self-administration in rats. Pharmacol Biochem Behav 33:903–907
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
Broseta I, Rodríguez-Arias M, Aguilar MA, Miñarro J (2005) Isolation decreases physical and motivational aspects of morphine withdrawal. Behav Pharmacol 16:131–138
Brown KJ, Grunberg NE (1995) Effects of housing on male and female rats: crowding stresses male but calm females. Physiol Behav 58:1085–1089
Campbell JO, Wood RD, Spear LP (2000) Cocaine and morphine-induced place conditioning in adolescent and adult rats. Physiol Behav 68:487–493
Caprioli D, Celentano M, Paolone G, Badiani A (2007) Modeling the role of environment in addiction. Progress NeuroPsychopharmacol Biol Psychiatry 31:1639–1653
Covington HE, Miczek KA (2001) Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration “binges”. Psychopharmacology 158:388–398
Covington HE, Miczek KA (2005) Intense cocaine self-administration after episodic social defeat stress, but not after aggressive behavior: dissociation from corticosterone activation. Psychopharmacology 183:331–340
Ding Y, Kang L, Li ML (2005) Enhanced cocaine self-administration in adult rats with adolescent isolation experience. Pharmacol Biochem Behav 82:673–677
Doremus TL, Brunell SC, Rajendran P, Spear LP (2005) Factors influencing elevated ethanol consumption in adolescent relative to adult rats. Alcohol Clin Exp Res 29:1796–1808
Ellenbroek BA, van der Kam EL, van der Elst MC, Cools AR (2005) Individual differences in drug dependence in rats: the role of genetic factors and life events. Eur J Pharmacol 526:251–258
Enoch MA (2006) Genetic and environmental influences on the development of alcoholism: resilience vs. risk. Ann N Y Acad Sci 1094:193–201
Erb S, Shaham Y, Stewart J (1996) Stress reinstates cocaine-seeking behavior after prolonged extinction and a drug-free period. Psychopharmacology 128:408–412
Flynn HA, Walton MA, Curran GM, Blow FC, Knutzen S (2004) Psychological distress and return to substance use two years following treatment. Subst Use Misuse 39:885–910
Gawin FH (1991) Cocaine addiction: psychology and neurophysiology. Science 251:1580–1586
Hall FS (1998) Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit Rev Neurobiol 12:129–162
Haney M, Maccari S, Le Moal M, Simon H, Piazza PV (1995) Social stress increases the acquisition of cocaine self-administration in male and female rats. Brain Res 698:46–52
Higgins ST (1997) The influence of alternative reinforcers on cocaine use and abuse: a brief review. Pharmacol Biochem Behav 57:419–427
Hill SY, Powell BJ (1976) Cocaine and morphine self-administration: effects of differential rearing. Pharmacol Biochem Behav 5:701–704
Howes SR, Dalley JW, Morrison CH, Robbins TW, Everitt BJ (2000) Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala-striatal FOS expression. Psychopharmacology 151:55–63
Kabbaj M, Norton CS, Kollack-Walker S, Watson SJ, Robinson TE, Akil H (2001) Social defeat alters the acquisition of cocaine self-administration in rats: role of individual differences in cocaine-taking behavior. Psychopharmacology 158:382–387
Kosten TA, Miserendino MJ, Kehoe P (2000) Enhanced acquisition of cocaine self-administration in adult rats with neonatal isolation stress experience. Brain Res 875:44–50
Laviola G, Adriani W, Morley-Fletcher S, Terranova ML (2002) Peculiar response of adolescent mice to acute and chronic stress and to amphetamine: evidence of sex differences. Behav Brain Res 130:117–125
Lu L, Shepard JD, Hall FS, Shaham Y (2003) Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 27:457–491
Lynch WJ, Mangini LD, Taylor JR (2005) Neonatal isolation stress potentiates cocaine seeking behavior in adult male and female rats. Neuropsychopharmacology 30:322–329
Maldonado C, Rodríguez-Arias M, Castillo A, Aguilar MA, Miñarro J (2006) Gamma-hydroxybutyric acid affects the acquisition and reinstatement of cocaine-induced conditioned place preference in mice. Behav Pharmacol 17:119–131
Maldonado C, Rodríguez-Arias M, Castillo A, Aguilar MA, Miñarro J (2007) Effect of memantine and CNQX in the acquisition, expression and reinstatement of cocaine-induced conditioned place preference. Prog Neuropsychopharmacol Biol Psychiatry 31:932–939
Manzanedo C, Aguilar MA, Rodríguez-Arias M, Miñarro J (2001) Effects of dopamine antagonists with different receptor blockade profiles on morphine-induced place preference in male mice. Behav Brain Res 121:189–197
Miczek KA, Mutschler NH (1996) Activational effects of social stress on IV cocaine self-administration in rats. Psychopharmacology 128:256–264
Miczek KA, Thompson ML, Shuster L (1982) Opioid-like analgesia in defeated mice. Science 215:1520–1522
Morse AC, Erwin VG, Jones BC (1993) Strain and housing affect cocaine self-selection and open-field locomotor activity in mice. Pharmacol Biochem Behav 45:905–912
Nagaraja HS, Jeganathan PS (2003) Effect of acute and chronic conditions of over-crowding on free choice ethanol intake in rats. Indian J Physiol Pharmacol 47:325–331
Ortiz R, Armario A, Castellanos JM, Balasch J (1985) Post-weaning crowding induces corticoadrenal hyperreactivity in male mice. Physiol Behav 34:857–860
Panksepp JB, Lahvis GP (2007) Social reward among juvenile mice. Genes Brain Behav 6:661–671
Phillips GD, Howes SR, Whitelaw RB, Robbins TW, Everitt BJ (1994a) Isolation rearing impairs the reinforcing efficacy of intravenous cocaine or intra-accumbens d-amphetamine: impaired response to intra-accumbens D1 and D2/D3 dopamine receptor antagonists. Psychopharmacology 115:419–429
Phillips GD, Howes SR, Whitelaw RB, Wilkinson LS, Robbins TW, Everitt BJ (1994b) Isolation rearing enhances the locomotor response to cocaine and a novel environment, but impairs the intravenous self-administration of cocaine. Psychopharmacology 115:407–418
Ribeiro Do Couto B, Aguilar MA, Manzanedo C, Rodríguez-Arias M, Armario A, Miñarro J (2006) Social stress is as effective as physical stress in reinstating morphine-induced place preference in mice. Psychopharmacology 185:459–470
Rodríguez-Arias M, Miñarro J, Aguilar MA, Pinazo J, Simon VM (1998) Effects of risperidone and SCH23390 on isolation-induced aggression in male mice. Eur Neuropsychopharmacol 8:95–103
Schenk S, Hunt T, Malovechko R, Robertson A, Klukowski G, Amit Z (1986) Differential effects of isolation housing on the conditioned place preference produced by cocaine and amphetamine. Pharmacol Biochem Behav 24:1793–1796
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
Schramm-Sapyta NL, Pratt AR, Winder DG (2004) Effects of periadolescent versus adult cocaine exposure on cocaine conditioned place preference and motor sensitization in mice. Psychopharmacology 173:41–48
Shaham Y, Puddicombe J, Stewart J (1997) Sexually arousing events and relapse to heroin-seeking in sexually experienced male rats. Physiol Behav 61:337–341
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 168:170–176
Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology 158:343–359
Sinha R, Garcia M, Paliwal P, Kreek MJ, Rounsaville BJ (2006) Stress-induced cocaine craving and hypothalamic-pituitary-adrenal responses are predictive of cocaine relapse outcomes. Arch Gen Psychiatry 63:324–331
Smith JK, Neill JC, Costall B (1997) Post-weaning housing conditions influence the behavioural effects of cocaine and d-amphetamine. Psychopharmacology 131:23–33
Smoothy R, Brain PF, Berry MS, Haug M (1986) Alcohol and social behaviour in group-housed female mice. Physiol Behav 37:689–694
Solinas M, Thiriet N, Rawas RE, Lardeux V, Jaber M (2009) Environmental enrichment during early stages of life reduces the behavioral, neurochemical, and molecular effects of cocaine. Neuropsychopharmacology 34:1102–1111
Tidey JW, Miczek KA (1997) Acquisition of cocaine self-administration after social stress: role of accumbens dopamine. Psychopharmacology 130:203–212
Tornatzky W, Miczek KA (1993) Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol Behav 53:983–993
Van der Veen R, Piazza PV, Deroche-Gamonet V (2007) Gene-environment interactions in vulnerability to cocaine intravenous self-administration: a brief social experience affects intake in DBA/2J but not in C57BL/6 J mice. Psychopharmacology 193:179–186
Xigeng Z, Yonghui L, Xiaojing L, Lin X, Dongmei W, Jie L, Xiaoyan Y, Nan S (2004) Social crowding sensitizes high-responding rats to psychomotor-stimulant effects of morphine. Pharmacol Biochem Behav 79:213–218
Zhang XY, Sanchez H, Kehoe P, Kosten TA (2005) Neonatal isolation enhances maintenance but not reinstatement of cocaine self-administration in adult male rats. Psychopharmacology 177:391–399
Acknowledgments
This work was supported by the following grants: Ministerio de Ciencia e Innovación, Dirección General de Investigación (PSI2008-00101/PSIC), Instituto de Salud “Carlos III” (FIS), RETICS, Red de Trastornos Adictivos (RD06/001/0016), Generalitat Valenciana, Conselleria de Educación (PROMETEO/2009/072), and Agencia Valenciana de Salud, Dirección General de Drogodependencias (FEPAD), Spain.
We wish to thank Mr. Brian Normanly for the English language revision of the manuscript and Ana Diaz for her careful supervision of the animals.
All experiments complied with current Spanish law.
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Ribeiro Do Couto, B., Aguilar, M.A., Lluch, J. et al. Social experiences affect reinstatement of cocaine-induced place preference in mice. Psychopharmacology 207, 485–498 (2009). https://doi.org/10.1007/s00213-009-1678-1
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DOI: https://doi.org/10.1007/s00213-009-1678-1