Abstract
Adolescence is known for its high level of risk-taking, and neurobiological alterations during this period may predispose to psychoactive drug initiation and progression into more severe use patterns. Stress is a risk factor for drug consumption, and post-weaning social isolation increases drug self-administration in rodents. This review aimed to provide an overview of the effects of adolescent social isolation on cocaine, amphetamine and nicotine use-related behaviours, highlighting the specific period when animals were submitted to stress and these drugs. We wondered if there was a specific period during adolescence that isolation stress would increase drug use vulnerability. A total of 323 publications from the Scopus, Web of Science and PubMed (Medline) electronic databases were identified using the words “social isolation” and “adolescence” and “drug” or “cocaine” or “amphetamine” or “nicotine”, resulting in 24 articles after analyses criteria following the PRISMA statement. The main points raised were social isolation during adolescence increased cocaine self-administration, amphetamine and nicotine locomotor activity. We did not observe a pattern of a specific moment during the adolescent period that could lead to an increased vulnerability to drug use. The precise conditions under which adolescent social stress alters drug use parameters are complex and likely depend on several factors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The process of selecting the articles included in this systematic review is available upon request.
References
Adams E, Klug J, Quast M, Stairs DJ (2013) Effects of environmental enrichment on nicotine-induced sensitization and cross-sensitization to d-amphetamine in rats. Drug Alcohol Depend 129:247-253 doi:10.1016/j.drugalcdep.2013.02.019
Aguilar MA, Garcia-Pardo MP, Montagud-Romero S, Minarro J, Do Couto BR (2013) Impact of social stress in addiction to psychostimulants: what we know from animal models. Curr Pharm Des 19:7009–7025. https://doi.org/10.2174/138161281940131209124708
Andersen SL, Thompson AT, Rutstein M, Hostetter JC, Teicher MH (2000) Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37:167–169. https://doi.org/10.1002/1098-2396(200008)37:2<167::AID-SYN11>3.0.CO;2-B
Anker JJ, Carroll ME (2011) Females are more vulnerable to drug abuse than males: evidence from preclinical studies and the role of ovarian hormones. Curr Top Behav Neurosci 8:73–96. https://doi.org/10.1007/7854_2010_93
Baarendse PJ, Limpens JH, Vanderschuren LJ (2014) Disrupted social development enhances the motivation for cocaine in rats. Psychopharmacology (Berl) 231:1695–1704. https://doi.org/10.1007/s00213-013-3362-8
Belluzzi JD, Lee AG, Oliff HS, Leslie FM (2004) Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats. Psychopharmacology (Berl) 174:389–395. https://doi.org/10.1007/s00213-003-1758-6
Bielajew C, Konkle AT, Merali Z (2002) The effects of chronic mild stress on male Sprague-Dawley and Long Evans rats: I. Biochemical and physiological analyses. Behav Brain Res 136:583–592. https://doi.org/10.1016/s0166-4328(02)00222-x
Blanco-Gandia MC, Montagud-Romero S, Aguilar MA, Minarro J, Rodriguez-Arias M (2018) Housing conditions modulate the reinforcing properties of cocaine in adolescent mice that binge on fat. Physiol Behav 183:18–26. https://doi.org/10.1016/j.physbeh.2017.10.014
Bobzean SA, DeNobrega AK, Perrotti LI (2014) Sex differences in the neurobiology of drug addiction. Exp Neurol 259:64–74. https://doi.org/10.1016/j.expneurol.2014.01.022
Boero G et al (2018) Impaired glucocorticoid-mediated HPA axis negative feedback induced by juvenile social isolation in male rats. Neuropharmacology 133:242–253. https://doi.org/10.1016/j.neuropharm.2018.01.045
Bowling SL, Bardo MT (1994) Locomotor and rewarding effects of amphetamine in enriched, social, and isolate reared rats. Pharmacol Biochem Behav 48:459–464. https://doi.org/10.1016/0091-3057(94)90553-3
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. https://doi.org/10.1007/s00213-013-3369-1
Burke AR, Miczek KA (2015) Escalation of cocaine self-administration in adulthood after social defeat of adolescent rats: role of social experience and adaptive coping behavior. Psychopharmacology (Berl) 232:3067–3079. https://doi.org/10.1007/s00213-015-3947-5
Burke AR, McCormick CM, Pellis SM, Lukkes JL (2017) Impact of adolescent social experiences on behavior and neural circuits implicated in mental illnesses. Neurosci Biobehav Rev 76:280–300. https://doi.org/10.1016/j.neubiorev.2017.01.018
Butler TR, Karkhanis AN, Jones SR, Weiner JL (2016) Adolescent social isolation as a model of heightened vulnerability to comorbid alcoholism and anxiety disorders. Alcohol Clin Exp Res 40:1202–1214. https://doi.org/10.1111/acer.13075
Cadoni C (2016) Fischer 344 and Lewis rat strains as a model of genetic vulnerability to drug addiction. Front Neurosci 10:13. https://doi.org/10.3389/fnins.2016.00013
Calipari ES, Juarez B, Morel C, Walker DM, Cahill ME, Ribeiro E, Roman-Ortiz C, Ramakrishnan C, Deisseroth K, Han MH, Nestler EJ (2017) Dopaminergic dynamics underlying sex-specific cocaine reward. Nat Commun 8:13877. https://doi.org/10.1038/ncomms13877
Caruso MJ, Reiss DE, Caulfield JI, Thomas JL, Baker AN, Cavigelli SA, Kamens HM (2018a) Adolescent chronic variable social stress influences exploratory behavior and nicotine responses in male, but not female. BALB/cJ mice Brain Res Bull 138:37–49. https://doi.org/10.1016/j.brainresbull.2017.08.001
Caruso MJ, Crowley NA, Reiss DE, Caulfield JI, Luscher B, Cavigelli SA, Kamens HM (2018b) Adolescent social stress increases anxiety-like behavior and alters synaptic transmission, without influencing nicotine responses, in a sex-dependent manner. Neuroscience 373:182–198. https://doi.org/10.1016/j.neuroscience.2018.01.006
Collins GT, Chen Y, Tschumi C, Rush EL, Mensah A, Koek W, France CP (2015) Effects of consuming a diet high in fat and/or sugar on the locomotor effects of acute and repeated cocaine in male and female C57BL/6J mice. Exp Clin Psychopharmacol 23:228–237. https://doi.org/10.1037/pha0000019
Crews F, He J, Hodge C (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86:189–199. https://doi.org/10.1016/j.pbb.2006.12.001
DePasque S, Galvan A (2017) Frontostriatal development and probabilistic reinforcement learning during adolescence. Neurobiol Learn Mem 143:1–7. https://doi.org/10.1016/j.nlm.2017.04.009
Diergaarde L, Pattij T, Poortvliet I, Hogenboom F, de Vries W, Schoffelmeer AN, De Vries TJ (2008) Impulsive choice and impulsive action predict vulnerability to distinct stages of nicotine seeking in rats Biol Psychiatry 63:301-308 doi:https://doi.org/10.1016/j.biopsych.2007.07.011
Douglas KR et al (2010) Adverse childhood events as risk factors for substance dependence: partial mediation by mood and anxiety disorders. Addict Behav 35:7–13. https://doi.org/10.1016/j.addbeh.2009.07.004
Dow-Edwards D, Iijima M, Stephenson S, Jackson A, Weedon J (2014) The effects of prenatal cocaine, post-weaning housing and sex on conditioned place preference in adolescent rats. Psychopharmacology (Berl) 231:1543–1555. https://doi.org/10.1007/s00213-013-3418-9
Einon DF, Morgan MJ (1978) Early isolation produces enduring hyperactivity in the rat, but no effect upon spontaneous alternation. Q J Exp Psychol 30:151–156. https://doi.org/10.1080/14640747808400663
Estelles J, Lluch J, Rodriguez-Arias M, Aguilar MA, Minarro J (2007) Cocaine exposure during adolescence affects anxiety in adult mice. Brain Res Bull 71:393–403. https://doi.org/10.1016/j.brainresbull.2006.10.008
Ferguson SA, Frisby NB, Ali SF (2000) Acute effects of cocaine on play behaviour of rats. Behav Pharmacol 11:175–179. https://doi.org/10.1097/00008877-200004000-00010
Fernandez-Fernandez R et al (2005) Effects of chronic hyperghrelinemia on puberty onset and pregnancy outcome in the rat. Endocrinology 146:3018–3025. https://doi.org/10.1210/en.2004-1622
Fone KC, Porkess MV (2008) Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32:1087–1102. https://doi.org/10.1016/j.neubiorev.2008.03.003
Fortenberry JD (2013) Puberty and adolescent sexuality. Horm Behav 64:280–287. https://doi.org/10.1016/j.yhbeh.2013.03.007
Fosnocht AQ, Lucerne KE, Ellis AS, Olimpo NA, Briand LA (2019) Adolescent social isolation increases cocaine seeking in male and female mice. Behav Brain Res 359:589–596. https://doi.org/10.1016/j.bbr.2018.10.007
Fulford AJ, Marsden CA (2007) An intact dopaminergic system is required for context-conditioned release of 5-HT in the nucleus accumbens of postweaning isolation-reared rats. Neuroscience 149:392–400. https://doi.org/10.1016/j.neuroscience.2007.08.002
Garcia EJ, Haddon TN, Saucier DA, Cain ME (2017) Differential housing and novelty response: protection and risk from locomotor sensitization. Pharmacol Biochem Behav 154:20–30. https://doi.org/10.1016/j.pbb.2017.01.004
Goosby BJ, Bellatorre A, Walsemann KM, Cheadle JE (2013) Adolescent loneliness and health in early adulthood. Sociol Inq 83:–536. https://doi.org/10.1111/soin.12018
Grace AA, Floresco SB, Goto Y, Lodge DJ (2007) Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30:220–227. https://doi.org/10.1016/j.tins.2007.03.003
Gray KM, Squeglia LM (2018) Research review: what have we learned about adolescent substance use? J Child Psychol Psychiatry 59:618–627. https://doi.org/10.1111/jcpp.12783
Green TA et al (2010) Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens. Biol Psychiatry 67:28–35. https://doi.org/10.1016/j.biopsych.2009.06.022
Green MR, Barnes B, McCormick CM (2013) Social instability stress in adolescence increases anxiety and reduces social interactions in adulthood in male Long-Evans rats. Dev Psychobiol 55:849–859. https://doi.org/10.1002/dev.21077
Grotewold SK, Wall VL, Goodell DJ, Hayter C, Bland ST (2014) Effects of cocaine combined with a social cue on conditioned place preference and nucleus accumbens monoamines after isolation rearing in rats. Psychopharmacology (Berl) 231:3041–3053. https://doi.org/10.1007/s00213-014-3470-0
Hall FS, Humby T, Wilkinson LS, Robbins TW (1997) The effects of isolation-rearing on sucrose consumption in rats. Physiol Behav 62:291–297. https://doi.org/10.1016/s0031-9384(97)00116-9
Hall FS, Wilkinson LS, Humby T, Inglis W, Kendall DA, Marsden CA, Robbins TW (1998) Isolation rearing in rats: pre- and postsynaptic changes in striatal dopaminergic systems. Pharmacol Biochem Behav 59:859–872. https://doi.org/10.1016/s0091-3057(97)00510-8
Harvey BH, Regenass W, Dreyer W, Moller M (2019) Social isolation rearing-induced anxiety and response to agomelatine in male and female rats: role of corticosterone, oxytocin, and vasopressin. J Psychopharmacol 33:640–646. https://doi.org/10.1177/0269881119826783
Heidbreder CA et al (2000) Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome. Neuroscience 100:749–768. https://doi.org/10.1016/s0306-4522(00)00336-5
Higgins JP et al (2011) The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343:d5928. https://doi.org/10.1136/bmj.d5928
Hikida T et al (2020) Adolescent psychosocial stress enhances sensitization to cocaine exposure in genetically vulnerable mice. Neurosci Res 151:38–45. https://doi.org/10.1016/j.neures.2019.02.007
Hofford RS, Prendergast MA, Bardo MT (2015) Pharmacological manipulation of glucocorticoid receptors differentially affects cocaine self-administration in environmentally enriched and isolated rats. Behav Brain Res 283:196–202. https://doi.org/10.1016/j.bbr.2015.01.049
Holder MK, Blaustein JD (2014) Puberty and adolescence as a time of vulnerability to stressors that alter neurobehavioral processes. Front Neuroendocrinol 35:89–110. https://doi.org/10.1016/j.yfrne.2013.10.004
Hooijmans CR, Rovers MM, de Vries RB, Leenaars M, Ritskes-Hoitinga M, Langendam MW (2014) SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol 14:43. https://doi.org/10.1186/1471-2288-14-43
Johnston LDOM, P. M.; Bachman, J. G.; Schulenberg, J. E.; Miech, R. A. (2015) Monitoring the future national survey results on drug use, 1975–2014. College students and adults ages 19–55. Institute for Social Research, The University of Michigan, Ann Arbor, Michigan
Kar SK, Choudhury A, Singh AP (2015) Understanding normal development of adolescent sexuality: a bumpy ride. J Hum Reprod Sci 8:70–74. https://doi.org/10.4103/0974-1208.158594
Kokare DM, Dandekar MP, Singru PS, Gupta GL, Subhedar NK (2010) Involvement of alpha-MSH in the social isolation induced anxiety- and depression-like behaviors in rat. Neuropharmacology 58:1009–1018. https://doi.org/10.1016/j.neuropharm.2010.01.006
Lampert C et al (2017) Short post-weaning social isolation induces long-term changes in the dopaminergic system and increases susceptibility to psychostimulants in female rats. Int J Dev Neurosci 61:21–30. https://doi.org/10.1016/j.ijdevneu.2017.05.003
Lander SS, Linder-Shacham D, Gaisler-Salomon I (2017) Differential effects of social isolation in adolescent and adult mice on behavior and cortical gene expression. Behav Brain Res 316:245–254. https://doi.org/10.1016/j.bbr.2016.09.005
Larsen B, Luna B (2018) Adolescence as a neurobiological critical period for the development of higher-order cognition. Neurosci Biobehav Rev 94:179–195. https://doi.org/10.1016/j.neubiorev.2018.09.005
Laviola G, Macri S, Morley-Fletcher S, Adriani W (2003) Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci Biobehav Rev 27:19–31. https://doi.org/10.1016/s0149-7634(03)00006-x
Lewis EM, Barnett JF Jr, Freshwater L, Hoberman AM, Christian MS (2002) Sexual maturation data for Crl Sprague-Dawley rats: criteria and confounding factors. Drug Chem Toxicol 25:437–458. https://doi.org/10.1081/dct-120014794
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JPA, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700. https://doi.org/10.1136/bmj.b2700
Lisdahl KM et al (2018) Adolescent brain cognitive development (ABCD) study: overview of substance use assessment methods. Dev Cogn Neurosci 32:80–96. https://doi.org/10.1016/j.dcn.2018.02.007
Lu X et al (2012) The effects of rearing condition on methamphetamine self-administration and cue-induced drug seeking. Drug Alcohol Depend 124:288–298. https://doi.org/10.1016/j.drugalcdep.2012.01.022
Lukkes JL, Watt MJ, Lowry CA, Forster GL (2009) Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents. Front Behav Neurosci 3:18. https://doi.org/10.3389/neuro.08.018.2009
Lynch WJ, Nicholson KL, Dance ME, Morgan RW, Foley PL (2010) Animal models of substance abuse and addiction: implications for science, animal welfare, and society. Comp Med 60:177–188
Mastwal S, Ye Y, Ren M, Jimenez DV, Martinowich K, Gerfen CR, Wang KH (2014) Phasic dopamine neuron activity elicits unique mesofrontal plasticity in adolescence. J Neurosci 34:9484–9496. https://doi.org/10.1523/JNEUROSCI.1114-14.2014
McCormick CM, Ibrahim FN (2007) Locomotor activity to nicotine and Fos immunoreactivity in the paraventricular nucleus of the hypothalamus in adolescent socially-stressed rats. Pharmacol Biochem Behav 86:92–102. https://doi.org/10.1016/j.pbb.2006.12.012
McCormick CM, Mathews IZ (2007) HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 86:220–233. https://doi.org/10.1016/j.pbb.2006.07.012
McCormick CM, Robarts D, Kopeikina K, Kelsey JE (2005) Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats. Horm Behav 48:64–74. https://doi.org/10.1016/j.yhbeh.2005.01.008
McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904. https://doi.org/10.1152/physrev.00041.2006
Mills KL, Lalonde F, Clasen LS, Giedd JN, Blakemore SJ (2014) Developmental changes in the structure of the social brain in late childhood and adolescence. Soc Cogn Affect Neurosci 9:123–131. https://doi.org/10.1093/scan/nss113
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097. https://doi.org/10.1371/journal.pmed.1000097
Moncek F, Duncko R, Johansson BB, Jezova D (2004) Effect of environmental enrichment on stress related systems in rats. J Neuroendocrinol 16:423–431. https://doi.org/10.1111/j.1365-2826.2004.01173.x
Moreira PS, Almeida PR, Leite-Almeida H, Sousa N, Costa P (2016) Impact of chronic stress protocols in learning and memory in rodents: systematic review and meta-analysis. PLoS One 11:e0163245. https://doi.org/10.1371/journal.pone.0163245
Mormède P (2007) Strain differences in stress response in rodents. Encyclopedia of Stress (Second Edition):585-586 doi:https://doi.org/10.1016/B978-012373947-6.00654-1
Mueller DaDW H. (2011) Conditioned place preference in rodents and humans. . In: Neuromethods (ed). doi:https://doi.org/10.1007/978-1-60761-883-6_6
Pankevich DE, Bale TL (2008) Stress and sex influences on food-seeking behaviors. Obesity (Silver Spring) 16:1539–1544. https://doi.org/10.1038/oby.2008.221
Panksepp J, Beatty WW (1980) Social deprivation and play in rats. Behav Neural Biol 30:197–206. https://doi.org/10.1016/s0163-1047(80)91077-8
Perry JL, Carroll ME (2008) The role of impulsive behavior in drug abuse. Psychopharmacology (Berl) 200:1–26. https://doi.org/10.1007/s00213-008-1173-0
Piazza PV, Deroche-Gamonent V, Rouge-Pont F, Le Moal M (2000) Vertical shifts in self-administration dose-response functions predict a drug-vulnerable phenotype predisposed to addiction. J Neurosci 20:4226–4232
Prus AJ, James JR, Rosecrans JA (2009) Conditioned place preference. In: nd, Buccafusco JJ (eds) Methods of behavior analysis in neuroscience. Frontiers in Neuroscience. Boca Raton (FL)
Ravenelle R, Santolucito HB, Byrnes EM, Byrnes JJ, Donaldson ST (2014) Housing environment modulates physiological and behavioral responses to anxiogenic stimuli in trait anxiety male rats. Neuroscience 270:76–87. https://doi.org/10.1016/j.neuroscience.2014.03.060
Ribeiro Do Couto B, Aguilar MA, Lluch J, Rodriguez-Arias M, Minarro J (2009) Social experiences affect reinstatement of cocaine-induced place preference in mice. Psychopharmacology (Berl) 207:485–498. https://doi.org/10.1007/s00213-009-1678-1
Sanchez MM, Aguado F, Sanchez-Toscano F, Saphier D (1998) Neuroendocrine and immunocytochemical demonstrations of decreased hypothalamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 139:579–587. https://doi.org/10.1210/endo.139.2.5720
Schrijver NC, Bahr NI, Weiss IC, Wurbel H (2002) Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol Biochem Behav 73:209–224. https://doi.org/10.1016/s0091-3057(02)00790-6
Sisk CL, Foster DL (2004) The neural basis of puberty and adolescence. Nat Neurosci 7:1040–1047. https://doi.org/10.1038/nn1326
Smith MA, Iordanou JC, Cohen MB, Cole KT, Gergans SR, Lyle MA, Schmidt KT (2009) Effects of environmental enrichment on sensitivity to cocaine in female rats: importance of control rates of behavior. Behav Pharmacol 20:312–321. https://doi.org/10.1097/FBP.0b013e32832ec568
Smith LN, Penrod RD, Taniguchi M, Cowan CW (2016) Assessment of cocaine-induced behavioral sensitization and conditioned place preference in mice. J Vis Exp:53107 doi:https://doi.org/10.3791/53107
Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463. https://doi.org/10.1016/s0149-7634(00)00014-2
Tamnes CK et al (2017) Development of the cerebral cortex across adolescence: a multisample study of inter-related longitudinal changes in cortical volume, surface area, and thickness. J Neurosci 37:3402–3412. https://doi.org/10.1523/JNEUROSCI.3302-16.2017
Thomsen M, Caine SB (2011) Psychomotor stimulant effects of cocaine in rats and 15 mouse strains. Exp Clin Psychopharmacol 19:321–341. https://doi.org/10.1037/a0024798
Tirelli E, Laviola G, Adriani W (2003) Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci Biobehav Rev 27:163–178. https://doi.org/10.1016/s0149-7634(03)00018-6
Tomie A, Uveges JM, Burger KM, Patterson-Buckendahl P, Pohorecky LA (2004) Effects of ethanol sipper and social opportunity on ethanol drinking in rats. Alcohol Alcohol 39:197–202. https://doi.org/10.1093/alcalc/agh055
Trainor BC (2011) Stress responses and the mesolimbic dopamine system: social contexts and sex differences. Horm Behav 60:457–469. https://doi.org/10.1016/j.yhbeh.2011.08.013
Trezza V, Campolongo P, Vanderschuren LJ (2011) Evaluating the rewarding nature of social interactions in laboratory animals. Dev Cogn Neurosci 1:444–458. https://doi.org/10.1016/j.dcn.2011.05.007
Trezza V, Baarendse PJ, Vanderschuren LJ (2014) On the interaction between drugs of abuse and adolescent social behavior. Psychopharmacology (Berl) 231:1715–1729. https://doi.org/10.1007/s00213-014-3471-z
Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462. https://doi.org/10.1111/j.1369-1600.2007.00070.x
Varlinskaya EI, Spear LP (2006) Differences in the social consequences of ethanol emerge during the course of adolescence in rats: social facilitation, social inhibition, and anxiolysis. Dev Psychobiol 48:146–161. https://doi.org/10.1002/dev.20124
Vetter-O'Hagen CS, Spear LP (2012) Hormonal and physical markers of puberty and their relationship to adolescent-typical novelty-directed behavior. Dev Psychobiol 54:523–535. https://doi.org/10.1002/dev.20610
Wahlstrom D, Collins P, White T, Luciana M (2010) Developmental changes in dopamine neurotransmission in adolescence: behavioral implications and issues in assessment. Brain Cogn 72:146–159. https://doi.org/10.1016/j.bandc.2009.10.013
Watt MJ, Weber MA, Davies SR, Forster GL (2017) Impact of juvenile chronic stress on adult cortico-accumbal function: implications for cognition and addiction. Prog Neuropsychopharmacol Biol Psychiatry 79:136–154. https://doi.org/10.1016/j.pnpbp.2017.06.015
Westenbroek C, Perry AN, Becker JB (2013) Pair housing differentially affects motivation to self-administer cocaine in male and female rats. Behav Brain Res 252:68–71. https://doi.org/10.1016/j.bbr.2013.05.040
Whitaker LR, Degoulet M, Morikawa H (2013) Social deprivation enhances VTA synaptic plasticity and drug-induced contextual learning. Neuron 77:335–345. https://doi.org/10.1016/j.neuron.2012.11.022
Yajie D, Lin K, Baoming L, Lan M (2005) Enhanced cocaine self-administration in adult rats with adolescent isolation experience. Pharmacol Biochem Behav 82:673–677. https://doi.org/10.1016/j.pbb.2005.11.007
Zakharova E, Miller J, Unterwald E, Wade D, Izenwasser S (2009) Social and physical environment alter cocaine conditioned place preference and dopaminergic markers in adolescent male rats. Neuroscience 163:890–897. https://doi.org/10.1016/j.neuroscience.2009.06.068
Zakharova E, Starosciak A, Wade D, Izenwasser S (2012) Sex differences in the effects of social and physical environment on novelty-induced exploratory behavior and cocaine-stimulated locomotor activity in adolescent rats. Behav Brain Res 230:92–99. https://doi.org/10.1016/j.bbr.2012.01.052
Zoratto F, Altabella L, Tistarelli N, Laviola G, Adriani W, Canese R (2018) Inside the developing brain to understand teen behavior from rat models: metabolic, structural, and functional-connectivity alterations among limbic structures across three pre-adolescent stages. Front Behav Neurosci 12:208. https://doi.org/10.3389/fnbeh.2018.00208
Funding
We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for CN and CL fellowships.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Noschang, C., Lampert, C., Krolow, R. et al. Social isolation at adolescence: a systematic review on behaviour related to cocaine, amphetamine and nicotine use in rats and mice. Psychopharmacology 238, 927–947 (2021). https://doi.org/10.1007/s00213-021-05777-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00213-021-05777-z