Escalation of cocaine self-administration in adulthood after social defeat of adolescent rats: role of social experience and adaptive coping behavior (original) (raw)
Baarendse PJ, Limpens JH, Vanderschuren LJ (2014) Disrupted social development enhances the motivation for cocaine in rats. Psychopharmacology (Berl) 231:1695–1704 ArticleCAS 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 155:278–284 ArticleCASPubMed Google Scholar
Boyson CO, Holly EN, Shimamoto A, Albrechet-Souza L, Weiner LA, DeBold JF, Miczek KA (2014) Social stress and CRF-dopamine interactions in the VTA: role in long-term escalation of cocaine self-administration. J Neurosci 34:6659–6667 ArticleCASPubMed CentralPubMed Google Scholar
Boyson CO, Miguel TT, Quadros IM, Debold JF, Miczek KA (2011) Prevention of social stress-escalated cocaine self-administration by CRF-R1 antagonist in the rat VTA. Psychopharmacology 218:257–269
Broadwater M, Spear LP (2013) Age differences in fear retention and extinction in male Sprague–Dawley rats: effects of ethanol challenge during conditioning. Behav Brain Res 252:377–387 ArticleCASPubMed CentralPubMed Google Scholar
Burke AR, Forster GL, Novick AM, Roberts CL, Watt MJ (2013) Effects of adolescent social defeat on adult amphetamine-induced locomotion and corticoaccumbal dopamine release in male rats. Neuropharmacology 67:359–369 ArticleCASPubMed Google Scholar
Burke AR, Miczek KA (2014) Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis. Psychopharmacology (Berl) 231:1557–1580 ArticleCAS Google Scholar
Burke AR, Renner KJ, Forster GL, Watt MJ (2010) Adolescent social defeat alters neural, endocrine and behavioral responses to amphetamine in adult male rats. Brain Res 1352:147–156 ArticleCASPubMed CentralPubMed Google Scholar
Burke AR, Watt MJ, Forster GL (2011) Adolescent social defeat increases adult amphetamine conditioned place preference and alters D2 dopamine receptor expression. Neuroscience 197:269–279 ArticleCASPubMed CentralPubMed Google Scholar
Buwalda B, Kole MH, Veenema AH, Huininga M, de Boer SF, Korte SM, Koolhaas JM (2005) Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci Biobehav Rev 29:83–97 ArticlePubMed Google Scholar
Buwalda B, Scholte J, de Boer SF, Coppens CM, Koolhaas JM (2012) The acute glucocorticoid stress response does not differentiate between rewarding and aversive social stimuli in rats. Horm Behav 61:218–226 ArticleCASPubMed Google Scholar
Buwalda B, Stubbendorff C, Zickert N, Koolhaas JM (2013) Adolescent social stress does not necessarily lead to a compromised adaptive capacity during adulthood: a study on the consequences of social stress in rats. Neuroscience 26:258–270
Chappell AM, Carter E, McCool BA, Weiner JL (2013) Adolescent rearing conditions influence the relationship between initial anxiety-like behavior and ethanol drinking in male Long Evans rats. Alcohol Clin Exp Res 37(Suppl 1):E394–E403 ArticlePubMed CentralPubMed Google Scholar
Covington HE 3rd, Kikusui T, Goodhue J, Nikulina EM, Hammer RP Jr, Miczek KA (2005) Brief social defeat stress: long lasting effects on cocaine taking during a binge and zif268 mRNA expression in the amygdala and prefrontal cortex. Neuropsychopharmacology 30:310–321 ArticleCASPubMed Google Scholar
Covington HE 3rd, Miczek KA (2001) Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration “binges”. Psychopharmacology 158:388–398 ArticleCASPubMed Google Scholar
Covington HE 3rd, 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 ArticleCASPubMed Google Scholar
Covington HE 3rd, Tropea TF, Rajadhyaksha AM, Kosofsky BE, Miczek KA (2008) NMDA receptors in the rat VTA: a critical site for social stress to intensify cocaine taking. Psychopharmacology 197:203–216 ArticleCASPubMed CentralPubMed Google Scholar
de Jong JG, van der Vegt BJ, Buwalda B, Koolhaas JM (2005) Social environment determines the long-term effects of social defeat. Physiol Behav 84:87–95 ArticlePubMed Google Scholar
Ding YJ, Kang L, Li BM, Ma L (2005) Enhanced cocaine self-administration in adult rats with adolescent isolation experience. Pharmacol Biochem Behav 82:673–677 ArticleCAS Google Scholar
Douglas LA, Varlinskaya EI, Spear LP (2004) Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Dev Psychobiol 45:153–162 ArticlePubMed Google Scholar
Frank E, Salchner P, Aldag JM, Salome N, Singewald N, Landgraf R, Wigger A (2006) Genetic predisposition to anxiety-related behavior determines coping style, neuroendocrine responses, and neuronal activation during social defeat. Behav Neurosci 120:60–71 ArticlePubMed Google Scholar
Garcia-Pardo MP, Rodriguez-Arias M, Maldonado C, Manzanedo C, Minarro J, Aguilar MA (2014) Effects of acute social stress on the conditioned place preference induced by MDMA in adolescent and adult mice. Behav Pharmacol 25:532–546 CASPubMed Google Scholar
Goldman L, Winget C, Hollingshead GW, Levine S (1973) Postweaning development of negative feedback in the pituitary-adrenal system of the rat. Neuroendocrinology 12:199–211 ArticleCASPubMed Google Scholar
Grubbs FE (1969) Procedures for detecting outlying observations in samples. Technometrics 11:1 Article Google Scholar
Hall FS, Perona MT (2012) Have studies of the developmental regulation of behavioral phenotypes revealed the mechanisms of gene-environment interactions? Physiol Behav 107:623–640 ArticleCASPubMed CentralPubMed Google Scholar
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 ArticleCASPubMed Google Scholar
Hoffmann JP, Cerbone FG, Su SS (2000) A growth curve analysis of stress and adolescent drug use. Subst Use Misuse 35:687–716 ArticleCASPubMed Google Scholar
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 (Berl) 151:55–63 ArticleCAS Google Scholar
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 ArticleCASPubMed Google Scholar
Koolhaas JM, De Boer SF, De Rutter AJ, Meerlo P, Sgoifo A (1997) Social stress in rats and mice. Acta Physiol Scand 640:69–72 CAS Google Scholar
Koolhaas JM, Schuurman T, Wiepkema PR (1980) The organization of intraspecific agonistic behaviour in the rat. Prog Neurobiol 15:247–268 ArticleCASPubMed Google Scholar
Lapiz MD, Fulford A, Muchimapura S, Mason R, Parker T, Marsden CA (2003) Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neurosci Behav Physiol 33:13–29 ArticleCASPubMed Google Scholar
Levine JB, Youngs RM, MacDonald ML, Chu M, Leeder AD, Berthiaume F, Konradi C (2007) Isolation rearing and hyperlocomotion are associated with reduced immediate early gene expression levels in the medial prefrontal cortex. Neuroscience 145:42–55 ArticleCASPubMed Google Scholar
Lopez MF, Doremus-Fitzwater TL, Becker HC (2011) Chronic social isolation and chronic variable stress during early development induce later elevated ethanol intake in adult C57BL/6 J mice. Alcohol 45:355–364 ArticleCASPubMed CentralPubMed Google Scholar
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 ArticleCASPubMed Google Scholar
Lukkes J, Vuong S, Scholl J, Oliver H, Forster G (2009a) Corticotropin-releasing factor receptor antagonism within the dorsal raphe nucleus reduces social anxiety-like behavior after early-life social isolation. J Neurosci 29:9955–9960 ArticleCASPubMed CentralPubMed Google Scholar
Lukkes JL, Mokin MV, Scholl JL, Forster GL (2009b) Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm Behav 55:248–256 ArticleCASPubMed Google Scholar
Lukkes JL, Watt MJ, Lowry CA, Forster GL (2009c) Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents. Front Behav Neurosci 3:18 ArticlePubMed CentralPubMed Google Scholar
Meng Q, Li N, Han X, Shao F, Wang W (2010) Peri-adolescence isolation rearing alters social behavior and nociception in rats. Neurosci Lett 480:25–29 ArticleCASPubMed Google Scholar
Miczek KA, Nikulina EM, Shimamoto A, Covington HE 3rd (2011) Escalated or suppressed cocaine reward, tegmental BDNF, and accumbal dopamine caused by episodic versus continuous social stress in rats. J Neurosci 31:9848–9857 ArticleCASPubMed CentralPubMed Google Scholar
Miczek KA, Thompson ML, Tornatzky W (1991) Subordinate animals: behavioral and physiological adaptations and opioid tolerance. In: Brown MR, Koob GF, Rivier C (eds) Stress neurobiology and neuroendocrinology. Marcel Dekker Inc., pp 323–357
Miczek KA, Yap JJ, Covington HE 3rd (2008) Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake. Pharmacol Ther 120:102–128 ArticleCASPubMed CentralPubMed Google Scholar
Nakayasu T, Ishii K (2008) Effects of pair-housing after social defeat experience on elevated plus-maze behavior in rats. Behav Processes 78:477–480 ArticlePubMed Google Scholar
Nansel TR, Overpeck M, Pilla RS, Ruan WJ, Simons-Morton B, Scheidt P (2001) Bullying behaviors among US youth: prevalence and association with psychosocial adjustment. JAMA 285:2094–2100 ArticleCASPubMed CentralPubMed Google Scholar
National Research Council (U.S.). Committee for the Update of the Guide for the Care and Use of Laboratory Animals., Institute for Laboratory Animal Research (U.S.), National Academies Press (U.S.) (2011) Guide for the care and use of laboratory animals, 8th edn. National Academies Press, Washington, D.C Google Scholar
Nelson DE, Higginson GK, Grant-Worley JA (1995) Physical abuse among high school students. Prevalence and correlation with other health behaviors. Arch Pediatr Adolesc Med 149:1254–1258 ArticleCASPubMed Google Scholar
Newman ML, Holden GW, Delville Y (2005) Isolation and the stress of being bullied. J Adolesc 28:343–357 ArticlePubMed Google Scholar
Nocjar C, Zhang J, Feng P, Panksepp J (2012) The social defeat animal model of depression shows diminished levels of orexin in mesocortical regions of the dopamine system, and of dynorphin and orexin in the hypothalamus. Neuroscience 218:138–153 ArticleCASPubMed Google Scholar
Panksepp J, Siviy S, Normansell L (1984) The psychobiology of play: theoretical and methodological perspectives. Neurosci Biobehav Rev 8:465–492 ArticleCASPubMed Google Scholar
Paul ED, Hale MW, Lukkes JL, Valentine MJ, Sarchet DM, Lowry CA (2011) Repeated social defeat increases reactive emotional coping behavior and alters functional responses in serotonergic neurons in the rat dorsal raphe nucleus. Physiol Behav 104:272–282 ArticleCASPubMed CentralPubMed Google Scholar
Plyusnina IZ, Solov'eva MY, Oskina IN (2011) Effect of domestication on aggression in gray Norway rats. Behav Genet 41:583–592 ArticlePubMed Google Scholar
Powell SB, Swerdlow NR, Pitcher LK, Geyer MA (2002) Isolation rearing-induced deficits in prepulse inhibition and locomotor habituation are not potentiated by water deprivation. Physiol Behav 77:55–64 ArticleCASPubMed Google Scholar
Prut L, Belzung C (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463:3–33 ArticleCASPubMed Google Scholar
Richardson NR, Roberts DCS (1996) Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J Neurosci Methods 66:1–11 ArticleCASPubMed Google Scholar
Robbins TW, Jones GH, Wilkinson LS (1996) Behavioural and neurochemical effects of early social deprivation in the rat. J Psychopharmacol (Oxford, England) 10:39–47 ArticleCAS Google Scholar
Romeo RD (2010) Adolescence: a central event in shaping stress reactivity. Dev Psychobiol 52:244–253 PubMed Google Scholar
Ruis MA, te Brake JH, Buwalda B, De Boer SF, Meerlo P, Korte SM, Blokhuis HJ, Koolhaas JM (1999) Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat. Psychoneuroendocrinology 24:285–300 ArticleCASPubMed Google Scholar
Schenk S, Gorman K, Amit Z (1990) Age-dependent effects of isolation housing on the self-administration of ethanol in laboratory rats. Alcohol 7:321–326 ArticleCASPubMed Google Scholar
Tharp-Taylor S, Haviland A, D'Amico EJ (2009) Victimization from mental and physical bullying and substance use in early adolescence. Addict Behav 34:561–567 ArticlePubMed CentralPubMed Google Scholar
Tidey JW, Miczek KA (1997) Acquisition of cocaine self-administration after social stress: role of accumbens dopamine. Psychopharmacology 130:203–212 ArticleCASPubMed Google Scholar
Trezza V, Baarendse PJ, Vanderschuren LJ (2010) The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol Sci 31:463–469 ArticleCASPubMed CentralPubMed Google Scholar
van den Berg CL, Hol T, Van Ree JM, Spruijt BM, Everts H, Koolhaas JM (1999) Play is indispensable for an adequate development of coping with social challenges in the rat. Dev Psychobiol 34:129–138 ArticlePubMed Google Scholar
Varlinskaya EI, Spear LP (2008) Social interactions in adolescent and adult Sprague–Dawley rats: impact of social deprivation and test context familiarity. Behav Brain Res 188:398–405 ArticlePubMed CentralPubMed Google Scholar
Varlinskaya EI, Spear LP, Spear NE (1999) Social behavior and social motivation in adolescent rats: role of housing conditions and partner’s activity. Physiol Behav 67:475–482 ArticleCASPubMed Google Scholar
Ver Hoeve ES, Kelly G, Luz S, Ghanshani S, Bhatnagar S (2013) Short-term and long-term effects of repeated social defeat during adolescence or adulthood in female rats. Neuroscience 249:63–73 ArticleCASPubMed CentralPubMed Google Scholar
Von Frijtag JC, Reijmers LG, Van der Harst JE, Leus IE, Van den Bos R, Spruijt BM (2000) Defeat followed by individual housing results in long-term impaired reward- and cognition-related behaviours in rats. Behav Brain Res 117:137–146 Article Google Scholar
Watt MJ, Burke AR, Renner KJ, Forster GL (2009) Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults. Behav Neurosci 123:564–576 ArticleCASPubMed CentralPubMed Google Scholar
Whitaker LR, Degoulet M, Morikawa H (2013) Social deprivation enhances VTA synaptic plasticity and drug-induced contextual learning. Neuron 77:335–345 ArticleCASPubMed CentralPubMed Google Scholar
Wright IK, Upton N, Marsden CA (1991) Resocialisation of isolation-reared rats does not alter their anxiogenic profile on the elevated X-maze model of anxiety. Physiol Behav 50:1129–1132 ArticleCASPubMed Google Scholar
Yates JR, Beckmann JS, Meyer AC, Bardo MT (2013) Concurrent choice for social interaction and amphetamine using conditioned place preference in rats: effects of age and housing condition. Drug Alcohol Depend 129:240–246 ArticleCASPubMed CentralPubMed Google Scholar
Zou S, Funk D, Shram MJ, Le AD (2014) Effects of stressors on the reinforcing efficacy of nicotine in adolescent and adult rats. Psychopharmacology (Berl) 231:1601–1614 ArticleCAS Google Scholar