The Two Faces of Social Interaction Reward in Animal Models of Drug Dependence

Abstract

Drug dependence is a serious health and social problem. Social factors can modify vulnerability to developing drug dependence, acting as risk factors or protective factors. Whereas stress and peer environment that encourage substance use may increase drug taking, strong attachments between family members and peer environment that do not experience drug use may protect against drug taking and, ultimately, drug dependence. The rewarding effects of drug abuse and social interaction can be evaluated using animal models. In this review we focus on evaluating social interaction reward in the conditioned place preference paradigm. We give an overview of how social interaction, if made available within the drug context, may facilitate, promote and interact with the drug’s effects. However, social interaction, if offered alternatively outside the drug context, may have pronounced protective effects against drug abuse and relapse. We also address the importance of the weight difference parameter between the social partners in determining the positive or “agonistic” versus the hostile or “antagonistic” social interaction. We conclude that understanding social interaction reward and its subsequent effects on drug reward is sorely needed for therapeutic interventions against drug dependence.

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References

  1. 1.

    Kreek MJ, Nielsen DA, Butelman ER, LaForge KS (2005) Genetic influences on impulsivity, risk taking, stress responsivity and vulnerability to drug abuse and addiction. Nat Neurosci 8:1450–1457

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Enoch M-A (2006) Genetic and environmental influences on the development of alcoholism: resilience vs. risk. Ann N Y Acad Sci 1094:193–201

    Article  PubMed  Google Scholar 

  3. 3.

    Swadi H (1999) Individual risk factors for adolescent substance use. Drug Alcohol Depend 55:209–224

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Fergusson DM, Boden JM, Horwood LJ (2008) The developmental antecedents of illicit drug use: evidence from a 25-year longitudinal study. Drug Alcohol Depend 96:165–177

    Article  PubMed  Google Scholar 

  5. 5.

    Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology 158:343–359

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Haug S, Núñez CL, Becker J, Gmel G, Schaub MP (2014) Predictors of onset of cannabis and other drug use in male young adults: results from a longitudinal study. BMC Public Health 14:1202

    Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Iglesias EB, Fernández del Río E, Calafat A, Fernández-Hermida JR (2014) Attachment and substance use in adolescence: a review of conceptual and methodological aspects. Adicciones 26:77–86

    PubMed  Google Scholar 

  8. 8.

    Zernig G, Ahmed SH, Cardinal RN, Morgan D, Acquas E, Foltin RW, Vezina P, Negus SS, Crespo JA, Stöckl P, Grubinger P, Madlung E, Haring C, Kurz M, Saria A (2007) Explaining the escalation of drug use in substance dependence: models and appropriate animal laboratory tests. Pharmacology 80:65–119

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Bardo MT, Bevins RA (2000) Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology 153:31–43

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Tzschentke TM (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 56:613–672

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    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

    Article  PubMed  Google Scholar 

  13. 13.

    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 Depend 96:202–212

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Trezza V, Damsteegt R, Vanderschuren LJMJ (2009) Conditioned place preference induced by social play behavior: parametrics, extinction, reinstatement and disruption by methylphenidate. Eur Neuropsychopharmacol 19:659–669

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Calcagnetti DJ, Schechter MD (1992) Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav 51:667–672

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Van den Berg CL, Pijlman FT, Koning HA, 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 106:133–142

    Article  PubMed  Google Scholar 

  18. 18.

    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 33:2946–2956

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    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 5:80

    PubMed  PubMed Central  Google Scholar 

  20. 20.

    Peartree NA, Hood LE, Thiel KJ, Sanabria F, Pentkowski NS, Chandler KN, Neisewander JL (2012) Limited physical contact through a mesh barrier is sufficient for social reward-conditioned place preference in adolescent male rats. Physiol Behav 105:749–756

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Kummer KK, Hofhansel L, Barwitz CM, Schardl A, Prast JM, Salti A, El Rawas R, Zernig G (2014) Differences in social interaction-vs. cocaine reward in mouse vs. rat. Front. Behav Neurosci 8:363

    Google Scholar 

  22. 22.

    Panksepp JB, Lahvis GP (2007) Social reward among juvenile mice. Genes Brain Behav 6:661–671

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Kennedy BC, Panksepp JB, Runckel PA, Lahvis GP (2012) Social influences on morphine-conditioned place preference in adolescent BALB/cJ and C57BL/6J mice. Psychopharmacology 219:923–932

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    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 224:33–56

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    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

    Article  PubMed  Google Scholar 

  26. 26.

    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 19:409–419

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Chen H, Sharp BM, Matta SG, Wu Q (2011) Social interaction promotes nicotine self-administration with olfactogustatory cues in adolescent rats. Neuropsychopharmacology 36:2629–2638

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Newman JL, Perry JL, Carroll ME (2007) Social stimuli enhance phencyclidine (PCP) self-administration in rhesus monkeys. Pharmacol Biochem Behav 87:280–288

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Thiel KJ, Sanabria F, Neisewander JL (2009) Synergistic interaction between nicotine and social rewards in adolescent male rats. Psychopharmacology 204:391–402

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    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 231:3041–3053

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Watanabe S (2011) Drug-social interactions in the reinforcing property of methamphetamine in mice. Behav Pharmacol 22:203–206

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Gauvin DV, Briscoe RJ, Goulden KL, Holloway FA (1994) Aversive attributes of ethanol can be attenuated by dyadic social interaction in the rat. Alcohol 11:247–251

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Valente TW, Ritt-Olson A, Stacy A, Unger JB, Okamoto J, Sussman S (2007) Peer acceleration: effects of a social network tailored substance abuse prevention program among high-risk adolescents. Addiction 102:1804–1815

    Article  PubMed  Google Scholar 

  34. 34.

    Fritz M, El Rawas R, Salti A, Klement S, Bardo MT, Kemmler G, Dechant G, Saria A, Zernig G (2011) Reversal of cocaine-conditioned place preference and mesocorticolimbic Zif268 expression by social interaction in rats. Addict Biol 16:273–284

    Article  PubMed  Google Scholar 

  35. 35.

    Fritz M, Klement S, El Rawas R, Saria A, Zernig G (2011) Sigma1 receptor antagonist BD1047 enhances reversal of conditioned place preference from cocaine to social interaction. Pharmacology 87:45–48

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Prast JM, Schardl A, Schwarzer C, Dechant G, Saria A, Zernig G (2014) Reacquisition of cocaine conditioned place preference and its inhibition by previous social interaction preferentially affect D1-medium spiny neurons in the accumbens corridor. Front Behav Neurosci 8:317

    PubMed  PubMed Central  Google Scholar 

  37. 37.

    El Rawas R, Klement S, Salti A, Fritz M, Dechant G, Saria A, Zernig G (2012) Preventive role of social interaction for cocaine conditioned place preference: correlation with FosB/DeltaFosB and pCREB expression in rat mesocorticolimbic areas. Front Behav Neurosci 6:8

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Ribeiro Do Couto B, Aguilar MA, Lluch J, Rodríguez-Arias M, Miñarro J (2009) Social experiences affect reinstatement of cocaine-induced place preference in mice. Psychopharmacology 207:485–498

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Solinas M, Chauvet C, Thiriet N, El Rawas R, Jaber M (2008) Reversal of cocaine addiction by environmental enrichment. Proc Natl Acad Sci USA 105:17145–17150

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Bardo MT, Rowlett JK, Harris MJ (1995) Conditioned place preference using opiate and stimulant drugs: a meta-analysis. Neurosci Biobehav Rev 19:39–51

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Reichel CM, Wilkinson JL, Bevins RA (2010) Reference place conditioning procedure with cocaine: increased sensitivity for measuring associatively motivated choice behavior in rats. Behav Pharmacol 21:323–331

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Fritz M, El Rawas R, Klement S, Kummer K, Mayr MJ, Eggart V, Salti A, Bardo MT, Saria A, Zernig G (2011) Differential effects of accumbens core vs. shell lesions in a rat concurrent conditioned place preference paradigm for cocaine vs. social interaction. PLoS One 6:e26761

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Lenoir M, Serre F, Cantin L, Ahmed SH (2007) Intense sweetness surpasses cocaine reward. PLoS One 2:e698

    Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    El Rawas R, Klement S, Kummer KK, Fritz M, Dechant G, Saria A, Zernig G (2012) Brain regions associated with the acquisition of conditioned place preference for cocaine vs. social interaction. Front Behav Neurosci 6:63

    PubMed  PubMed Central  Google Scholar 

  46. 46.

    Kummer KK, El Rawas R, Kress M, Saria A, Zernig G (2015) Social interaction and cocaine conditioning in mice increase spontaneous spike frequency in the nucleus accumbens or septal nuclei as revealed by multielectrode array recordings. Pharmacology 95:42–49

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Raz S, Berger BD (2010) Social isolation increases morphine intake: behavioral and psychopharmacological aspects. Behav Pharmacol 21:39–46

    Article  PubMed  Google Scholar 

  48. 48.

    Aguilar MA, García-Pardo MP, Montagud-Romero S, Miñarro 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

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Tornatzky W, Miczek KA (1993) Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol Behav 53:983–993

    CAS  Article  PubMed  Google Scholar 

  50. 50.

    Covington HE, Kikusui T, Goodhue J, Nikulina EM, Hammer RP, 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

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Covington HE, 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Gil M, Nguyen N-T, McDonald M, Albers HE (2013) Social reward: interactions with social status, social communication, aggression, and associated neural activation in the ventral tegmental area. Eur J Neurosci 38:2308–2318

    Article  PubMed  Google Scholar 

  53. 53.

    Drickamer LC, Vandenbergh JG, Colby DR (1973) Predictors of dominance in the male golden hamster (Mesocricetus auratus). Anim Behav 21:557–563

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Carelli RM, Ijames SG, Crumling AJ (2000) Evidence that separate neural circuits in the nucleus accumbens encode cocaine versus “natural” (water and food) reward. J Neurosci 20:4255–4266

    CAS  PubMed  Google Scholar 

  55. 55.

    Frohmader KS, Wiskerke J, Wise RA, Lehman MN, Coolen LM (2010) Methamphetamine acts on subpopulations of neurons regulating sexual behavior in male rats. Neuroscience 166:771–784

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to Alois Saria.

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Special Issue: In honor of Dr. Philip Beart.

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El Rawas, R., Saria, A. The Two Faces of Social Interaction Reward in Animal Models of Drug Dependence. Neurochem Res 41, 492–499 (2016). https://doi.org/10.1007/s11064-015-1637-7

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Keywords

  • Drug dependence
  • Reward
  • Social interaction
  • Animal model
  • Conditioned place preference
  • Drug context