, Volume 231, Issue 8, pp 1715–1729 | Cite as

On the interaction between drugs of abuse and adolescent social behavior

  • Viviana Trezza
  • Petra J. J. Baarendse
  • Louk J. M. J. Vanderschuren



Social factors influence drug abuse. Conversely, drugs of abuse alter social behavior. This is especially pertinent during post-weaning development, when there are profound changes in the social repertoire, and the sensitivity to the positive and negative effects of drugs of abuse is altered.


This study aimed to provide an overview of our current understanding of the interaction between drugs of abuse and juvenile/adolescent social behavior.


We first provide evidence that a characteristic form of juvenile and adolescent social behavior, i.e., social play behavior, has reinforcing properties and is affected by drugs of abuse. Next, social risk factors for drug use and addiction are described, including antisocial personality traits and early social insults. Last, we discuss research that investigates social influences on drug use, as well as the consequences of perinatal drug exposure on later social interactions.


Social play behavior is highly rewarding in laboratory animals, and it is affected by low doses of opioids, cannabinoids, ethanol, nicotine, and psychostimulants. In humans, antisocial personality traits, most prominently in the form of conduct disorder, are a prominent risk factor for drug addiction. Preclinical studies have consistently shown altered sensitivity to drugs as a result of social isolation during post-weaning development. The social environment of an individual has a profound, but complex, influence on drug use, and perinatal drug exposure markedly alters later social interactions.


The studies reviewed here provide a framework to understand the interaction between drugs of abuse and adolescent social interaction, at the preclinical and the clinical level.


Social behavior Drug addiction Adolescence Reward Risk factors Antisocial personality disorder 



Supported by National Institute on Drug Abuse Grant R01 DA022628 (L.J.M.J.V.).


  1. Achterberg EJM, Trezza V, Vanderschuren LJMJ (2012) Beta-adrenoreceptor stimulation mediates reconsolidation of social reward-related memories. PLos ONE 7:e39639PubMedCentralPubMedGoogle Scholar
  2. Achterberg EJM, Trezza V, Siviy SM, Schrama L, Schoffelmeer ANM, Vanderschuren LJMJ (2013) Amphetamine and cocaine suppress social play behavior in rats through distinct mechanisms. Psychopharmacol 2:1184. doi: 10.1007/s00213-013-3272-9 Google Scholar
  3. Alterman AI, Cacciola JS (1991) The antisocial personality disorder diagnosis in substance abusers: problems and issues. J Nerv Mental Dis 179:401–409Google Scholar
  4. Altman J, Everitt BJ, Glautier S, Markou A, Nutt D, Oretti R, Phillips GD, Robbins TW (1996) The biological, social and clinical bases of drug addiction: commentary and debate. Psychopharmacology 125:285–345PubMedGoogle Scholar
  5. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, Ed 4, Text Revision. American Psychiatric Association, WashingtonGoogle Scholar
  6. Andrews JA, Tildesley E, Hops H, Li F (2002) The influence of peers on young adult substance use. Health Psychol 21:349–457PubMedGoogle Scholar
  7. Anthony JC, Petronis KR (1995) Early-onset drug use and risk of later drug problems. Drug Alcohol Depend 40:9–15PubMedGoogle Scholar
  8. Baarendse PJJ, Limpens JHW, Vanderschuren LJMJ (2013) Disrupted social development enhances the motivation for cocaine in rats. Psychopharmacol. doi: 10.1007/s00213-013-3362-8 Google Scholar
  9. Bardo MT, Klebaur JE, Valone JM, Deaton C (2001) Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats. Psychopharmacology 155:278–284PubMedGoogle Scholar
  10. Bauman KE, Ennett ST (1996) On the importance of peer influence for adolescent drug use: commonly neglected considerations. Addiction 91:185–198PubMedGoogle Scholar
  11. Bean G, Lee T (1991) Social isolation and cohabitation with haloperidol-treated partners: effect on density of striatal dopamine D2 receptors in the developing rat brain. Psychiatry Res 36:307–317PubMedGoogle Scholar
  12. Beatty WW, Dodge AM, Dodge LJ, Panksepp J (1982) Psychomotor stimulants, social deprivation and play in juvenile rats. Pharmacol, Biochem Behav 16:417–422Google Scholar
  13. Beatty WW, Costello KB, Berry SL (1984) Suppression of play fighting by amphetamine: effects of catecholamine antagonists, agonists and synthesis inhibitors. Pharmacol, Biochem Behav 20:747–755Google Scholar
  14. Bechara A (2005) Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci 8:1458–1463PubMedGoogle Scholar
  15. Berridge KC (2009) 'Liking' and 'wanting' food rewards: brain substrates and roles in eating disorders. Physiol Behav 97:537–550PubMedCentralPubMedGoogle Scholar
  16. Biederman J, Monuteaux MC, Mick E, Spencer T, Wilens TE, Silva JM, Snyder LE, Faraone SV (2006) Young adult outcome of attention deficit hyperactivity disorder: a controlled 10-year follow-up study. Psychol Med 36:167–179PubMedGoogle Scholar
  17. Blakemore S-J (2008) The social brain in adolescence. Nat Rev Neurosci 9:267–277PubMedGoogle Scholar
  18. Blanchard RJ, Hori K, Tom P, Blanchard DC (1987) Social structure and ethanol consumption in the laboratory rat. Pharmacol, Biochem Behav 28:437–442Google Scholar
  19. 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 39:269–274Google Scholar
  20. Braun K, Bock J (2011) The experience-dependent maturation of prefronto-limbic circuits and the origin of developmental psychopathology: implications for the pathogenesis and therapy of behavioural disorders. Dev Med Child Neurol 53(Suppl 4):14–18PubMedGoogle Scholar
  21. Burkett JP, Young LJ (2012) The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction. Psychopharmacology 224:1–2PubMedCentralPubMedGoogle Scholar
  22. Cacioppo JT, Hawkley LC (2009) Perceived social isolation and cognition. Trends Cogn Sci 13:447–454PubMedCentralPubMedGoogle Scholar
  23. Calcagnetti DJ, Schechter MD (1992) Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav 51:667–672PubMedGoogle Scholar
  24. Carmichael-Olson H, Streissguth AP, Sampson PD, Barr HM, Bookstein FL, Thiede K (1997) Association of prenatal alcohol exposure with behavioral and learning problems in early adolescence. J Am Acad Child Adolesc Psychiatry 36:1187–1194Google Scholar
  25. Carroll KM, Powers MD, Bryant K, Rounsaville BJ (1993) One year follow up status of treatment seeking cocaine abusers: psychopathology and dependence severity as predictors of outcome. J Nerv Ment Dis 181:71–79PubMedGoogle Scholar
  26. Chasnoff IJ, Lewis DE, Squires L (1987) Cocaine intoxication in a breast-fed infant. Pediatrics 80:836–838PubMedGoogle Scholar
  27. Chen H, Sharp BM, Matta SG, Wu Q (2011) Social interaction promotes nicotine self-administration with olfactogustatory cues in adolescent rats. Neuropsychopharmacology 36:2629–2638PubMedCentralPubMedGoogle Scholar
  28. Cloninger CR, Christiansen RC, Reich T, Gottesman II (1978) Implications of sex differences in the prevalences of antisocial personality, alcoholism, and criminality for familial transmission. Arch Gen Psychiatry 35:941–951PubMedGoogle Scholar
  29. Compton WM, ThomasYF SFS, Grant BF (2007) Prevalence, correlates, disability, and comorbidity of DSM-IV drug abuse and dependence in the United States: results from the national epidemiologic survey on alcohol and related conditions. Arch Gen Psychiatry 64:566–576PubMedGoogle Scholar
  30. Cooper A, Barnea-Ygael N, Levy D, Shaham Y, Zangen A (2007) A conflict rat model of cue-induced relapse to cocaine seeking. Psychopharmacology 194:117–125PubMedGoogle Scholar
  31. Costello EJ, Mustillo S, Erkanli A, Keeler G, Angold A (2003) Prevalence and development of psychiatric disorders in childhood and adolescence. Arch Gen Psychiatry 60:837–844PubMedGoogle Scholar
  32. Counotte DS, Smit AB, Pattij T, Spijker S (2011) Development of the motivational system during adolescence, and its sensitivity to disruption by nicotine. Dev Cogn Neurosci 1:430–443PubMedGoogle Scholar
  33. Crone EA, Dahl RE (2012) Understanding adolescence as a period of social-affective engagement and goal flexibility. Nat Rev Neurosci 13:636–650PubMedGoogle Scholar
  34. Crowder WF, Hutto CW Jr (1992) Operant place conditioning measures examined using two nondrug reinforcers. Pharmacol, Biochem Behav 41:817–824Google Scholar
  35. Curley JP, Jensen CL, Mashoodh R, Champagne FA (2011) Social influences on neurobiology and behavior: epigenetic effects during development. Psychoneuroendoccrinology 36:352–371Google Scholar
  36. Czoty PW, Morgan D, Shannon EE, Gage HD, Nader MA (2004) Characterization of dopamine D1 and D2 receptor function in socially housed cynomolgus monkeys self-administering cocaine. Psychopharmacology 174:381–388PubMedGoogle Scholar
  37. Czoty PW, McCabe C, Nader MA (2005) Assessment of the relative reinforcing strength of cocaine in socially housed monkeys using a choice procedure. J Pharmacol Exp Ther 312:96–102PubMedGoogle Scholar
  38. Dalley JW, Everitt BJ, Robbins TW (2011) Impulsivity, compulsivity, and top-down cognitive control. Neuron 69:680–694PubMedGoogle Scholar
  39. D’Amato FR, Pavone F (2012) Modulation of nociception by social factors in rodents: contribution of the opioid system. Psychopharmacology 224:189–200PubMedGoogle Scholar
  40. DeLeon KR, Grimes JM, Connor DF, Melloni RH Jr (2002) Adolescent cocaine exposure and offensive aggression: involvement of serotonin neural signaling and innervation in male Syrian hamsters. Behav Brain Res 133:211–220PubMedGoogle Scholar
  41. Delfs JM, Schreiber L, Kelley AE (1990) Microinjection of cocaine into the nucleus accumbens elicits locomotor activation in the rat. J Neurosci 10:303–310PubMedGoogle Scholar
  42. Deroche-Gamonet V, Belin D, Piazza PV (2004) Evidence for addiction-like behavior in the rat. Science 305:1014–1017PubMedGoogle Scholar
  43. Di Marzo V, Bifulco M, De Petrocellis L (2004) The endocannabinoid system and its therapeutic exploitation. Nat Rev Drug Disc 3:771–784Google Scholar
  44. Ding Y, Kang L, Li B, Ma L (2005) Enhanced cocaine self-administration in adult rats with adolescent isolation experience. Pharmacol, Biochem Behav 82:673–677Google Scholar
  45. Disney ER, Elkins IJ, McGue M, Iacono WG (1999) Effects of ADHD, conduct disorder, and gender on substance use and abuse in adolescence. Am J Psychiatry 156:1515–1521PubMedGoogle Scholar
  46. Disney ER, Iacono W, McGue M, Tully E, Legrand L (2008) Strengthening the case: prenatal alcohol exposure is associated with increased risk for conduct disorder. Pediatr 122:e1225–e1230Google Scholar
  47. D’Onofrio B, Van Hulle C, Waldman I, Rodgers J, Rathouz P, Lahey B (2007) Causal inferences regarding prenatal alcohol exposure and childhood externalizing problems. Arch Gen Psychiatry 64:1296–1304PubMedGoogle Scholar
  48. 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 45:153–162PubMedGoogle Scholar
  49. Ellison GD (1981) A novel animal model of alcohol consumption based on the development of extremes of ethanol preference in colony-housed but not isolated rats. Behav Neural Biol 31:324–330PubMedGoogle Scholar
  50. Ersche KD (2013) Neurobiological correlates of the familial risk for stimulant drug dependence. Neuropsychopharmacol 38:238–239Google Scholar
  51. Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481–1489PubMedGoogle Scholar
  52. Fagen R (1981) Animal play behavior. Oxford University Press, OxfordGoogle Scholar
  53. Fairchild G, van Goozen SHM, Stollery SJ, Aitken MRF, Savage J, Moore SC, Goodyer IM (2009) Decision making and executive function in male adolescents with early-onset or adolescence-onset conduct disorder and control subjects. Biol Psychiatry 66:162–168PubMedCentralPubMedGoogle Scholar
  54. Farde L, Gustavsson JP, Jonsson E (1997) D2 dopamine receptors and personality traits. Nature 385:590PubMedGoogle Scholar
  55. Ferguson SA, Frisby NB, Ali SF (2000) Acute effects of cocaine on play behaviour of rats. Behav Pharmacol 11:175–179PubMedGoogle Scholar
  56. Fergusson DM, Horwood LJ, Ridder EM (2007) Conduct and attentional problems in childhood and adolescence and later substance use, abuse and dependence: results of a 25-year longitudinal study. Drug Alcohol Depend 88(suppl 1):S14–S26PubMedGoogle Scholar
  57. Finn PR, Mazas CA, Justus AN, Steinmetz J (2002) Early-onset alcoholism with conduct disorder: go/no go learning deficits, working memory capacity, and personality. Alcohol Clin Exp Res 26:186–206PubMedGoogle Scholar
  58. Fone KCF, Porkess MV (2008) Behavioural and neurochemical effects of post-weaning social isolation in rodents—relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32:1087–1102PubMedGoogle Scholar
  59. Fried PA (2002) Conceptual issues in behavioral teratology and their application in determining long-term sequelae of prenatal marihuana exposure. J Child Psychol Psychiatr 43:81–102Google Scholar
  60. Fritz M, El Rawas R, Klement S, Kummer K, Mayr MJ, Eggart V, Salti A, Bardo MT, Saria A, Zernig G (2011a) Differential effects of accumbens core vs. shell lesions in a rat concurrent conditioned place preference paradigm for cocaine vs. social interaction. PLoS One 6(10):e26761PubMedCentralPubMedGoogle Scholar
  61. Fritz M, El Rawas R, Salti A, Klement S, Bardo MT, Kemmler G, Dechant G, Saria A, Zernig G (2011b) Reversal of cocaine-conditioned place preference and mesocorticolimbic Zif268 expression by social interaction in rats. Addict Biol 16:273–284PubMedGoogle Scholar
  62. Fritz M, Klement S, El Rawas R, Saria A, Zernig G (2011c) Sigma1 receptor antagonist BD1047 enhances reversal of conditioned place preference from cocaine to social interaction. Pharmacology 87:45–48PubMedGoogle Scholar
  63. Galli G, Wolffgramm J (2004) Long-term voluntary D-amphetamine consumption and behavioral predictors for subsequent D-amphetamine addiction in rats. Drug Alcohol Dep 73:51–60Google Scholar
  64. Gipson CD, Yates JR, Beckmann JS, Marusich JA, Zentall TR, Bardo MT (2011) Social facilitation of d-amphetamine self-administration in rats. Exp Clin Psychopharmacol 19:409–419PubMedCentralPubMedGoogle Scholar
  65. Gobrogge KL, Wang ZW (2011) Genetics of aggression in voles. Adv Genet 75:121–150PubMedGoogle Scholar
  66. Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12:652–669PubMedCentralPubMedGoogle Scholar
  67. Graham KL, Burghardt GM (2010) Current perspectives on the biological study of play: signs of progress. Q Rev Biol 85(4):393–418PubMedGoogle Scholar
  68. Grant BF, Dawson DA (1997) Age at onset of alcohol use and its association with DSM-IV alcohol abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse 9:103–110PubMedGoogle Scholar
  69. Grant BF, Dawson DA (1998) Age of onset of drug use and its association with DSM-IV drug abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse 10:163–173PubMedGoogle Scholar
  70. Harpur TJ, Hare RD (1994) Assessment of psychopathy as a function of age. J Abnorm Psychol 103:604–609PubMedGoogle Scholar
  71. Harrison RJ, Connor DF, Nowak C, Melloni RH Jr (2000) Chronic low-dose cocaine treatment during adolescence facilitates aggression in hamsters. Physiol Behav 69:555–562PubMedGoogle Scholar
  72. Hawkins JD, Catalano RF, Miller JY (1992) Risk and protective factors for alcohol and other drug problems in adolescence and early adulthood: implications for substance abuse prevention. Psychol Bull 112:64–105PubMedGoogle Scholar
  73. Heidbreder CA, Weiss IC, Domeney AM, Pryce C, Homberg J, Hedou G, Feldon J, Moran MC, Nelson P (2000) Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome. Neuroscience 100:749–768PubMedGoogle Scholar
  74. Helzer J, Pryzbeck T (1998) The co-occurrence of alcoholism with other psychiatric disorders in the general population and its impact on treatment. J Stud Alcohol 49:219–224Google Scholar
  75. Hesselbrock MN (1986) Alcoholic typologies. A review of empirical evaluations of common classification schemes. Recent Dev Alcohol 4:191–206PubMedGoogle Scholar
  76. Hesselbrock VM, Hesselbrock MN (2006) Are there empirically supported and clinically useful subtypes of alcohol dependence? Addiction 101:97–103PubMedGoogle Scholar
  77. Heyne A (1996) The development of opiate addiction in the rat. Pharmacol, Biochem Behav 53:11.25Google Scholar
  78. Heyne A, Wolffgramm J (1998) The development of addiction to d-amphetamine in an animal model: same principles as for alcohol and opiate. Psychopharmacology 140:510–518PubMedGoogle Scholar
  79. Hicks BM, Krueger RF, Iacono WG, McGue M, Patrick CJ (2004) Family transmission and heritability of externalizing disorders: a twin-family study. Arch Gen Psychiatr 61:922–928PubMedGoogle Scholar
  80. Hol T, Niesink RJM, van Ree JM, Spruijt BM (1996) Prenatal exposure to morphine affects juvenile play behavior and adult social behavior in rats. Pharmacol, Biochem Behav 55:615–618Google Scholar
  81. Homberg JR, Schiepers OJG, Schoffelmeer ANM, Cuppen E, Vanderschuren LJMJ (2007) Acute and constitutive increases in central serotonin levels reduce social play behaviour in peri-adolescent rats. Psychopharmacology 195:175–182PubMedCentralPubMedGoogle Scholar
  82. Hopf FW, Chang SJ, Sparta DR, Bowers MS, Bonci A (2010) Motivation for alcohol becomes resistant to quinine adulteration after 3 to 4 months of intermittent alcohol self-administration. Alcohol Clin Exp Res 34:1565–1573PubMedCentralPubMedGoogle Scholar
  83. Hostetler CM, Anacker AM, Loftis JM, Ryabinin AE (2012) Social housing and alcohol drinking in male–female pairs of prairie voles (Microtus ochrogaster). Psychopharmacology 224:121–132. doi: 10.1007/s00213-012-2836-4: PubMedGoogle Scholar
  84. 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 151:55–63PubMedGoogle Scholar
  85. Humphreys AP, Einon DF (1981) Play as a reinforcer for maze-learning in juvenile rats. Anim Behav 29:259–270Google Scholar
  86. Ikemoto S, Panksepp J (1992) The effects of early social isolation on the motivation for social play. Dev Psychobiol 25:261–274PubMedGoogle Scholar
  87. Karelina K, DeVries AC (2011) Modeling social influences on human health. Psychosom Med 73:67–74PubMedCentralPubMedGoogle Scholar
  88. Kelley AE (2004) Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27:765–776PubMedGoogle Scholar
  89. Kelly PH, Seviour PW, Iversen SD (1975) Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Res 94:507–522PubMedGoogle Scholar
  90. Kessler RC, Nelson CB, McGonagle KA, Edlund MJ, Frank RG, Leaf PJ (1996) The epidemiology of co-occurring addictive and mental disorders: implications for prevention and service utilization. Am J Orthopsychiatry 66:17–31PubMedGoogle Scholar
  91. Kim-Cohen J, Caspi A, Moffitt TE, Harrington H, Milne BJ, Poulton R (2003) Prior juvenile diagnoses in adults with mental disorder: developmental follow-back of a prospective-longitudinal cohort. Arch Gen Psychiatry 60:709–717PubMedGoogle Scholar
  92. Kofoed L, MacMillan J (1986) Alcoholism and antisocial personality. The sociobiology of an addiction. J Nerv Ment Dis 174:332–335PubMedGoogle Scholar
  93. Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238PubMedCentralPubMedGoogle Scholar
  94. Kummer K, Klement S, Eggart V, Mayr MJ, Saria A, Zernig G (2011) Conditioned place preference for social interaction in rats: contribution of sensory components. Front Behav Neurosci 5:80PubMedCentralPubMedGoogle Scholar
  95. Lawrence RC, Cale Bonner H, Newsom RJ, Kelly SJ (2008) Effects of alcohol exposure during development on play behavior and c-Fos expression in response to play behavior. Behav Brain Res 188:209–218PubMedCentralGoogle Scholar
  96. Lesscher HMB, Vanderschuren LJMJ (2012) Compulsive drug use and its neural substrates. Rev Neurosci 23:731–745PubMedGoogle Scholar
  97. Lesscher HMB, Van Kerkhof LWM, Vanderschuren LJMJ (2010) Inflexible and indifferent ethanol drinking in mice. Alcohol Clin Exp Res 34:1219–1225PubMedGoogle Scholar
  98. Lewis CF (2011) Substance use and violent behavior in women with antisocial personality disorder. Behav Sci Law 29:667–676PubMedGoogle Scholar
  99. Liu Y, Aragona BJ, Young KA, Dietz DM, Kabbaj M, Mazei-Robison M, Nestler EJ, Wang Z (2010) Nucleus accumbens dopamine mediates amphetamine-induced impairment of social bonding in a monogamous rodent species. Proc Natl Acad Sci U S A 107:1217–1222PubMedCentralPubMedGoogle Scholar
  100. Mariani JJ, Horey J, Bisaga A, Aharonovich E, Raby W, Cheng WY, Nunes E, Levin FR (2008) Antisocial behavioral syndromes in cocaine and cannabis dependence. Am J Drug Alcohol Abuse 34:405–414PubMedCentralPubMedGoogle Scholar
  101. Marks-Kaufman R, Lewis MJ (1984) Early housing experience modifies morphine self-administration and physical dependence in adult rats. Addict Behav 9:235–243PubMedGoogle Scholar
  102. Martinez D, Orlowska D, Narendran R, Slifstein M, Liu F, Kumar D, Broft A, Van Heertum R, Kleber HD (2010) Dopamine type 2/3 receptor availability in the striatum and social status in human volunteers. Biol Psychiatry 67:275–278PubMedCentralPubMedGoogle Scholar
  103. Mason WA, Hollis JH, Sharpe LG (1962) Differential responses of chimpanzees to social stimulation. J Comp Physiol Psychol 55:1105–1110Google Scholar
  104. Mason WM, Saxon SV, Sharpe LG (1963) Preferential responses of young chimpanzees to food and social rewards. Psychol Rec 13:341–345Google Scholar
  105. Matthys W, Lochman JE (2010) Oppositional defiant disorder and conduct disorder in childhood. Wiley Blackwell, ChichesterGoogle Scholar
  106. Matthys W, Vanderschuren LJMJ, Schutter DJLG, Lochman JE (2012) Impaired neurocognitive functions affect social learning processes in oppositional defiant disorder and conduct disorder: implications for interventions. Clin Child Fam Psychol Rev 15:234–246PubMedGoogle Scholar
  107. Matthys W, Vanderschuren LJMJ, Schutter DJLG (2013) The neurobiology of oppositional defiant disorder and conduct disorder: altered functioning in three mental domains. Dev Psychopathol 25:193–207PubMedGoogle Scholar
  108. McKenzie-Quirk SD, Miczek KA (2008) Social rank and social separation as determinants of alcohol drinking in squirrel monkeys. Psychopharmacology 201:137–145PubMedGoogle Scholar
  109. Melloni RH Jr, Connor DF, Todtenkopf MS, DeLeon KR, Sanyal P, Harrison RJ (2001) Repeated cocaine treatment activates flank marking in adolescent female hamsters. Physiol Behav 73:561–570PubMedGoogle Scholar
  110. Merikangas KR, Avenevoli S (2000) Implications of genetic epidemiology for the prevention of substance use disorders. Addict Behav 25:807–820PubMedGoogle Scholar
  111. Miczek KA, Yap JJ, Covington HE III (2008) Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake. Pharmacol Ther 120:102–128PubMedCentralPubMedGoogle Scholar
  112. Mooney SM, Varlinskaya EI (2011) Acute prenatal exposure to ethanol and social behavior: effects of age, sex, and timing of exposure. Behav Brain Res 216:358–364PubMedCentralPubMedGoogle Scholar
  113. Morgan D, Grant KA, Gage HD, Mach RH, Kaplan JR, Prioleau O, Nader SH, Buchheimer N, Ehrenkaufer RL, Nader MA (2002) Social dominance in monkeys: dopamine D2 receptors and cocaine self-administration. Nat Neurosci 5:169–174PubMedGoogle Scholar
  114. Nader MA, Czoty PW, Nader SH, Morgan D (2012a) Nonhuman primate models of social behavior and cocaine abuse. Psychopharmacology 224:57–67PubMedCentralPubMedGoogle Scholar
  115. Nader MA, Nader SH, Czoty PW, Riddick NV, Gage HD, Gould RW, Blaylock BL, Kaplan JR, Garg PK, Davies HM, Morton D, Garg S, Reboussin BA (2012b) Social dominance in female monkeys: dopamine receptor function and cocaine reinforcement. Biol Psychiatry 72:414–421PubMedCentralPubMedGoogle Scholar
  116. National Collaborating Centre for Mental Health (2009) Antisocial personality disorder: treatment, management and prevention. The British Psychological Society and the Royal College of Psychiatrists, LeicesterGoogle Scholar
  117. Neisewander JL, Peartree NA, Pentkowski NS (2012) Emotional valence and context of social influences on drug abuse-related behavior in animal models of social stress and prosocial interaction. Psychopharmacology 224:33–56PubMedGoogle Scholar
  118. Nelson EE, Leibenluft E, McClure EB, Pine DS (2005) The socialre-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology. Psychol Med 35:163–174PubMedGoogle Scholar
  119. Nemeroff CB (2004) Neurobiological consequences of childhood trauma. J Clin Psychiatry 65(Suppl 1):18–28PubMedGoogle Scholar
  120. Nesse RM, Berridge KC (1997) Psychoactive drug use in evolutionary perspective. Science 278:63–66PubMedGoogle Scholar
  121. Niesink RJM, Van Ree JM (1989) Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats. Neuropharmacology 28:411–418PubMedGoogle Scholar
  122. Niesink RJM, Vanderschuren LJMJ, van Ree JM (1996) Social play in juvenile rats after in utero exposure to morphine. Neurotoxicology 17:905–912PubMedGoogle Scholar
  123. Niesink RJM, van Buren-van DL, van Ree JM (1999) Social behavior of juvenile rats after in utero exposure to morphine: dose–time–effect relationship. Neuropharmacology 38:1207–1223PubMedGoogle Scholar
  124. Normansell L, Panksepp J (1990) Effects of morphine and naloxone on play-rewarded spatial discrimination in juvenile rats. Dev Psychobiol 23:75–83PubMedGoogle Scholar
  125. O’Shea M, McGregor IS, Mallet PE (2006) Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar long-lasting deficits in object recognition and reduced social interaction in rats. J Psychopharmacol 20:611–621PubMedGoogle Scholar
  126. O’Brien CP (1996) Drug addiction and drug abuse. In: Hardman JG, Limbird LE, Molinoff PB, Ruddon RW, Goodman Gilman A (eds) Goodman & Gilman’s The pharmacological basis of therapeutics. McGraw-Hill, New York, pp 557–577Google Scholar
  127. Olson HC, Streissguth AP, Sampson PD, Barr HM, Bookstein FL, Thiede K (1997) Association of prenatal alcohol exposure with behavioral and learning problems in early adolescence. J Am Acad Child Adolesc Psychiatry 36:1187–1194PubMedGoogle Scholar
  128. Ong TH (1989) Peers as perceived by drug abusers in their drug-seeking behaviour. Br J Addict 84:631–637PubMedGoogle Scholar
  129. Oro AS, Dixon SD (1987) Perinatal cocaine and methamphetamine exposure: maternal and neonatal correlates. J Pediatr 111:571–578PubMedGoogle Scholar
  130. Panksepp J, Herman BH, Vilberg T, Bishop P, DeEskinazi FG (1980) Endogenous opioids and social behavior. Neurosci Biobehav Rev 4:473–487PubMedGoogle Scholar
  131. Panksepp J, Siviy SM, Normansell L (1984) The psychobiology of play: theoretical and methodological perspectives. Neurosci Biobehav Rev 8:465–492PubMedGoogle Scholar
  132. Panksepp J, Jalowiec JE, DeEskenazi FG, Bishop P (1985) Opiates and play dominance in juvenile rats. Behav Neurosci 99:441–453PubMedGoogle Scholar
  133. Peartree NA, Hood LE, Thiel KJ, Sanabria F, Pentkowski NS, Chandler KL, Neisewander JL (2012) Limited physical contact through a mesh barrier is sufficient for social reward-conditioned place preference in adolescent male rats. Physiol Behav 105:749–756PubMedPubMedCentralGoogle Scholar
  134. Peitz GW, Strickland JC, Pitts EG, Foley M, Tonidandel S, Smith MA (2013) Peer influences on drug self-administration: an econometric analysis in socially housed rats. Behav Pharmacol 24:114–123PubMedCentralPubMedGoogle Scholar
  135. Pellis SM, Pellis VC (2009) The playful brain: venturing to the limits of neuroscience. Oneworld Publications, OxfordGoogle Scholar
  136. Pelloux Y, Everitt BJ, Dickinson A (2007) Compulsive drug seeking by rats under punishment: effects of drug taking history. Psychopharmacology 194:127–137PubMedGoogle Scholar
  137. Perry JL, Carroll ME (2008) The role of impulsive behavior in drug abuse. Psychopharmacology 200:1–26PubMedGoogle Scholar
  138. 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 115:419–429PubMedGoogle Scholar
  139. 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 115:407–418PubMedGoogle Scholar
  140. Pijnenburg AJJ, Honig WMM, Van Rossum JM (1975) Inhibition of d-amphetamine-induced locomotor activity by injection of haloperidol into the nucleus accumbens of the rat. Psychopharmacologia 41:87–95PubMedGoogle Scholar
  141. Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873–884PubMedGoogle Scholar
  142. Randolph MJ, Yates WR (1993) Antisocial personality disorder in alcohol- and drug-dependent individuals: a study of gender effects. Am J Addict 2:9–17Google Scholar
  143. Regier DA, Farmer ME, Rae DS, Locke BZ, Keith SJ, Judd LL, Goodwin FK (1990) Comorbidity of mental disorders with alcohol and other drug abuse. Results from the Epidemiologic Catchment Area (ECA) Study. JAMA 264:2511–2518PubMedGoogle Scholar
  144. Riley EP, McGee CL (2007) Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Exp Biol Med 230:357–365Google Scholar
  145. Rilke O, May T, Oehler J, Wolffgramm J (1995) Influences of housing conditions and ethanol intake on binding characteristics of D2, 5-HT1A, and benzodiazepine receptors of rats. Pharmacol, Biochem Behav 52:23–28Google Scholar
  146. Robbins TW, Jones GH, Wilkinson LS (1996) Behavioural and neurochemical effects of early social deprivation in the rat. J Psychopharmacol 10:39–47PubMedGoogle Scholar
  147. Rodning C, Beckwith L, Howard J (1989) Prenatal exposure to drugs: behavioral distortions reflecting CNS impairment? Neurotoxicology 10:629–634PubMedGoogle Scholar
  148. Rutter M, Kim-Cohen J, Maughan B (2006) Continuities and discontinuities in psychopathology between childhood and adult life. J Child Psychol Psychiatry 47:276–295PubMedGoogle Scholar
  149. 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 81:227–231PubMedGoogle Scholar
  150. Schenk S, Gorman K, Amit Z (1990) Age-dependent effects of isolation housing on the self-administration of ethanol in laboratory rats. Alcohol 7:321–326PubMedGoogle Scholar
  151. Schramm-Sapyta NL, Walker QD, Caster JM, Levin ED, Kuhn CM (2009) Are adolescents more vulnerable to drug addiction than adults? Evidence from animal models. Psychopharmacology 206:1–21PubMedCentralPubMedGoogle Scholar
  152. Schutter DJLG, van Bokhoven I, Vanderschuren LJMJ, Lochman JE, Matthys W (2011) Risky decision making in substance dependent adolescents with a disruptive behavior disorder. J Abnorm Child Psychol 39:333–339PubMedCentralPubMedGoogle Scholar
  153. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology 168:3–20PubMedGoogle Scholar
  154. Smith MA (2012) Peer influences on drug self-administration: social facilitation and social inhibition of cocaine intake in male rats. Psychopharmacology. doi: 10.1007/s00213-012-2737-6 Google Scholar
  155. Sobrian SK, Holson RR (2011) Social behavior of offspring following prenatal cocaine exposure in rodents: a comparison with prenatal alcohol. Front Psychiatry 66:1–17Google Scholar
  156. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463PubMedGoogle Scholar
  157. Špinka M, Newberry RC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76:141–168PubMedGoogle Scholar
  158. Sutton ME, Raskin LA (1986) A behavioral analysis of the effects of amphetamine on play and locomotor activity in the post-weaning rat. Pharmacol, Biochem Behav 24:455–461Google Scholar
  159. Swadi HS (1988) Adolescent drug taking: role of family and peers. Drug Alcohol Depend 21:157–160PubMedGoogle Scholar
  160. Thiel KJ, Okun AC, Neisewander JL (2008) Social reward-conditioned place preference: a model revealing an interaction between cocaine and social context rewards in rats. Drug Alcohol Dep 96:202–212Google Scholar
  161. Thiel KJ, Sanabria F, Neisewander JL (2009) Synergistic interaction between nicotine and social rewards in adolescent male rats. Psychopharmacology 204:391–402PubMedCentralPubMedGoogle Scholar
  162. Thor DH, Holloway WR Jr (1983) Play soliciting in juvenile male rats: effects of caffeine, amphetamine and methylphenidate. Pharmacol, Biochem Behav 19:725–727Google Scholar
  163. Trezza V, Vanderschuren LJMJ (2008a) Bidirectional cannabinoid modulation of social behavior in adolescent rats. Psychopharmacology 197:217–227PubMedGoogle Scholar
  164. Trezza V, Vanderschuren LJMJ (2008b) Cannabinoid and opioid modulation of social play behavior in adolescent rats: differential behavioral mechanisms. Eur Neuropsychopharmacol 18:519–530PubMedCentralPubMedGoogle Scholar
  165. Trezza V, Vanderschuren LJMJ (2009) Divergent effects of anandamide transporter inhibitors with different target selectivity on social play behavior in adolescent rats. J Pharmacol Exp Ther 328:343–350PubMedCentralPubMedGoogle Scholar
  166. Trezza V, Campolongo P, Cassano T, Macheda T, Dipasquale P, Carratù MR, Gaetani S, Cuomo V (2008) Effects of perinatal exposure to Delta-9-tetrahydrocannabinol on the emotional reactivity of the offspring: a longitudinal behavioral study in Wistar rats. Psychopharmacology 198:529–537PubMedGoogle Scholar
  167. Trezza V, Baarendse PJJ, Vanderschuren LJMJ (2009a) Prosocial effects of nicotine and ethanol in adolescent rats through partially dissociable neurobehavioral mechanisms. Neuropsychopharmacology 34:2560–2573PubMedCentralPubMedGoogle Scholar
  168. Trezza V, Damsteegt R, Vanderschuren LJMJ (2009b) Conditioned place preference induced by social play behavior: parametrics, extinction, reinstatement and disruption by methylphenidate. Eur Neuropsychopharmacol 19:659–669PubMedCentralPubMedGoogle Scholar
  169. Trezza V, Baarendse PJJ, Vanderschuren LJMJ (2010) The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol Sci 31:463–469PubMedCentralPubMedGoogle Scholar
  170. Trezza V, Campolongo P, Vanderschuren LJMJ (2011a) Evaluating the rewarding nature of social interactions in laboratory animals. Dev Cogn Neurosci 1:444–457PubMedGoogle Scholar
  171. Trezza V, Damsteegt R, Achterberg EJM, Vanderschuren LJMJ (2011b) Nucleus accumbens μ-opioid receptors mediate social reward. J Neurosci 31:6362–6370PubMedCentralPubMedGoogle Scholar
  172. Trezza V, Damsteegt R, Manduca A, Petrosino S, Van Kerkhof LWM, Pasterkamp RJ, Zhou YP, Campolongo P, Cuomo V, Di Marzo V, Vanderschuren LJMJ (2012) Endocannabinoids in amygdala and nucleus accumbens mediate social play reward in adolescent rats. J Neurosci 32:14899–14908PubMedCentralPubMedGoogle Scholar
  173. Van den Berg CL, Pijlman FTA, Koning HAM, Diergaarde L, Van Ree JM, Spruijt BM (1999) Isolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats. Behav Brain Res 106:133–142PubMedGoogle Scholar
  174. Van Kerkhof LWM, Achterberg EJM, Lesscher HMB, Trezza V, Vanderschuren LJMJ (2012) Dissociating the rewarding and motivational properties of social play behavior in adolescent rats: the role of dopamine, opioids and endocannabinoids. Soc Neurosci Abs 295:06Google Scholar
  175. Van Kerkhof LWM, Damsteegt R, Trezza V, Voorn P, Vanderschuren LJMJ (2013) Social play behavior in adolescent rats is mediated by functional activity in medial prefrontal cortex and striatum. Neuropsychopharmacology 38:1899–1909PubMedGoogle Scholar
  176. Vanderschuren LJMJ (2010) How the brain makes play fun. Am J Play 2:315–337Google Scholar
  177. Vanderschuren LJMJ, Ahmed SH (2013) Animals studies of addictive behavior. Cold Spring Harb Perspect Med 3(4):a011932PubMedGoogle Scholar
  178. Vanderschuren LJMJ, Everitt BJ (2004) Drug seeking becomes compulsive after prolonged cocaine self-administration. Science 305:1017–1019PubMedGoogle Scholar
  179. Vanderschuren LJMJ, Trezza V (2013) What the laboratory rat has taught us about social play behavior: role in behavioral development and neural mechanisms. In: Andersen SL, Pine D (eds) The neurobiology of childhood, current topics in behavioral neuroscience. Springer, New York. doi: 10.1007/7854_2013_268 Google Scholar
  180. Vanderschuren LJMJ, Niesink RJM, Spruijt BM, Van Ree JM (1995a) Effects of morphine on different aspects of social play in juvenile rats. Psychopharmacology 117:225–231PubMedGoogle Scholar
  181. Vanderschuren LJMJ, Niesink RJM, Spruijt BM, Van Ree JM (1995b) μ- and κ-opioid receptor-mediated opioid effects on social play in juvenile rats. Eur J Pharmacol 276:257–266PubMedGoogle Scholar
  182. Vanderschuren LJMJ, Spruijt BM, Hol T, Niesink RJM, Van Ree JM (1995c) Sequential analysis of social play behavior in juvenile rats: effects of morphine. Behav Brain Res 72:89–95PubMedGoogle Scholar
  183. Vanderschuren LJMJ, Niesink RJM, Van Ree JM (1997) The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 21:309–326PubMedGoogle Scholar
  184. Vanderschuren LJMJ, Trezza V, Griffioen-Roose S, Schiepers OJG, Van Leeuwen N, De Vries TJ, Schoffelmeer ANM (2008) Methylphenidate disrupts social play behavior in adolescent rats. Neuropsychopharmacology 33:2946–2956PubMedCentralPubMedGoogle Scholar
  185. Varlinskaya EI, Spear LP (2002) Acute effects of ethanol on social behavior of adolescent and adult rats: role of familiarity of the test situation. Alcohol Clin Exp Res 26:1502–1511PubMedGoogle Scholar
  186. 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 48:146–161PubMedGoogle Scholar
  187. Varlinskaya EI, Spear LP (2009) Ethanol-induced social facilitation in adolescent rats: role of endogenous activity at mu opioid receptors. Alcohol Clin Exp Res 33:991–1000PubMedCentralPubMedGoogle Scholar
  188. Varlinskaya EI, Spear LP, Spear NE (2001) Acute effects of ethanol on behavior of adolescent rats: role of social context. Alcohol Clin Exp Res 25:377–385PubMedGoogle Scholar
  189. Varlinskaya EI, Doremus-Fitzwater TL, Spear LP (2010) Repeated restraint stress alters sensitivity to the social consequences of ethanol in adolescent and adult rats. Pharmacol, Biochem Behav 96:228–235Google Scholar
  190. Verdejo-García A, Lawrence AJ, Clark L (2008) Impulsivity as a vulnerability marker for substance-use disorders: review of findings from high-risk research, problem gamblers and genetic association studies. Neurosci Biobehav Rev 32:777–810PubMedGoogle Scholar
  191. Vetter-O’Hagen C, Varlinskaya E, Spear L (2009) Sex differences in ethanol intake and sensitivity to aversive effects during adolescence and adulthood. Alcohol Alcohol 44:547–554PubMedCentralPubMedGoogle Scholar
  192. Whitaker LR, Degoulet M, Morikawa H (2013) Social deprivation enhances VTA synaptic plasticity and drug-induced contextual learning. Neuron 77:335–345PubMedCentralPubMedGoogle Scholar
  193. Wilens TE, Biederman J (1993) Psychopathology in preadolescent children at high risk for substance abuse: a review of the literature. Harv Rev Psychiatry 1:207–218PubMedGoogle Scholar
  194. Willford JA, Segar TM, Hansen-Trench LS, Barron S (1999) The effects of neonatal cocaine exposure on a play-rewarded spatial discrimination task in juvenile rats. Pharmacol, Biochem Behav 62:137–143Google Scholar
  195. Wolffgramm J, Heyne A (1991) Social behavior, dominance, and social deprivation of rats determine drug choice. Pharmacol, Biochem Behav 38:389.399Google Scholar
  196. Wolffgramm J, Heyne A (1995) From controlled drug intake to loss of control: the irreversible development of drug addiction in the rat. Behav Brain Res 70:77–94Google Scholar
  197. Wood RD, Bannoura MD, Johanson IB (1994) Prenatal cocaine exposure: effects on play behavior in the juvenile rat. Neurotoxicol Teratol 16:139–144PubMedGoogle Scholar
  198. Wood RD, Molina VA, Wagner JM, Spear LP (1995) Play behavior and stress responsivity in periadolescent offspring exposed prenatally to cocaine. Pharmacol, Biochem Behav 52:367–374Google Scholar
  199. 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 129:240–246PubMedGoogle Scholar
  200. Young SE, Mikulich SK, Goodwin MB, Hardy J, Martin CL, Zoccolillo MS, Crowley TJ (1995) Treated delinquent boys’ substance use: onset, pattern, relationship to conduct and mood disorders. Drug Alcohol Dep 37:149–162Google Scholar
  201. Young KA, Gobrogge KL, Wang Z (2011) The role of mesocorticolimbic dopamine in regulating interactions between drugs of abuse and social behavior. Neurosci Biobehav Rev 35:498–515PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Viviana Trezza
    • 1
  • Petra J. J. Baarendse
    • 2
  • Louk J. M. J. Vanderschuren
    • 2
    • 3
  1. 1.Department of Science, Section of Biomedical Science and TechnologiesUniversity “Roma Tre”RomeItaly
  2. 2.Department of Translational Neuroscience, Brain Center Rudolf MagnusUniversity Medical Center UtrechtUtrechtThe Netherlands
  3. 3.Department of Animals in Science and Society, Division of Behavioural Neuroscience, Faculty of Veterinary MedicineUtrecht UniversityUtrechtThe Netherlands

Personalised recommendations