Psychopharmacology

, Volume 195, Issue 1, pp 117–124 | Cite as

Gestational exposure to nicotine and monoamine oxidase inhibitors influences cocaine-induced locomotion in adolescent rats

  • Ryan M. Franke
  • James D. Belluzzi
  • Frances M. Leslie
Original Investigation

Abstract

Rationale

Many pregnant women continue to smoke, despite a strong association between maternal smoking and neurobehavioral deficits in the offspring. Although gestational nicotine (GN) treatment in rodents is used as the primary animal model of maternal smoking, tobacco smoke contains more than 4,000 constituents, including monoamine oxidase inhibitors (MAOIs).

Objectives

The aim of this study was to determine whether there are interactions between the effects of gestational exposure to nicotine and MAOIs on cocaine-induced locomotor sensitization in adolescent rats.

Materials and methods

Pregnant rats were implanted on day 4 of gestation with osmotic minipumps delivering saline, nicotine (3 mg/kg per day), the MAOIs clorgyline and deprenyl (1 and 0.25 mg/kg per day, respectively), or nicotine/clorgyline/deprenyl (GMN). Adolescent female offspring were tested for cocaine-induced locomotor sensitization. Animals were treated with saline or cocaine (5 or 15 mg/kg, intraperitoneally) daily from postnatal (P) days 32–36 and challenged with cocaine (15 mg/kg) on P51 (day 20).

Results

Group differences were observed in chronic but not acute effects of cocaine. Whereas gestational MAOI treatment, with or without nicotine, increased ambulatory response to cocaine on day 5, the opposite was found for vertical activity. Different adaptive responses were observed on cocaine challenge day. GNM animals exhibited enhanced locomotor activity in the cocaine-associated environment before cocaine challenge on day 20. In contrast, only GN animals exhibited significant locomotor sensitization to the cocaine challenge.

Conclusions

Gestational nicotine and MAOIs both influence brain development. Such interactions may sensitize adolescents to drug abuse and should be considered in animal models of maternal smoking.

Keywords

Adolescence Clorgyline Deprenyl Dopamine Fetal Sensitization Maternal smoking Tobacco 

References

  1. Berlin I, Anthenelli RM (2001) Monoamine oxidases and tobacco smoking. Int J Neuropsychopharmacol 4:33–42PubMedCrossRefGoogle Scholar
  2. Brennan PA, Grekin ER, Mortensen EL, Mednick SA (2002) Relationship of maternal smoking during pregnancy with criminal arrest and hospitalization for substance abuse in male and female adult offspring. Am J Psychiatry 159:48–54PubMedCrossRefGoogle Scholar
  3. Carey RJ, Gui J (1998) Cocaine conditioning and cocaine sensitization: what is the relationship? Behav Brain Res 92:67–76PubMedCrossRefGoogle Scholar
  4. Carr LA, Basham JK (1991) Effects of tobacco smoke constituents on MPTP-induced toxicity and monoamine oxidase activity in the mouse brain. Life Sci 48:1173–1177PubMedCrossRefGoogle Scholar
  5. Chambers RA, Taylor JR, Potenza MN (2003) Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 160:1041–1052PubMedCrossRefGoogle Scholar
  6. Cnattingius S (2004) The epidemiology of smoking during pregnancy: smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine Tob Res 6(Suppl 2):S125–S140PubMedCrossRefGoogle Scholar
  7. Collins SL, Izenwasser S (2002) Cocaine differentially alters behavior and neurochemistry in periadolescent versus adult rats. Brain Res Dev Brain Res 138:27–34PubMedCrossRefGoogle Scholar
  8. Dempsey DA, Benowitz NL (2001) Risks and benefits of nicotine to aid smoking cessation in pregnancy. Drug Saf 24:277–322PubMedCrossRefGoogle Scholar
  9. Ernst M, Moolchan ET, Robinson ML (2001) Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psych 40:630–641CrossRefGoogle Scholar
  10. Frantz KJ, O’dell LE, Parsons LH (2006) Behavioral and neurochemical responses to cocaine in periadolescent and adult rats. Neuropsychopharmacology 32:625–637PubMedCrossRefGoogle Scholar
  11. Fried PA, Watkinson B (2001) Differential effects on facets of attention in adolescents prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 23:421–430PubMedCrossRefGoogle Scholar
  12. Fowler JS, Logan J, Wang GJ, Volkow ND (2003) Monoamine oxidase and cigarette smoking. Neurotoxicology 24:75–82PubMedCrossRefGoogle Scholar
  13. Fung YK (1988) Postnatal behavioural effects of maternal nicotine exposure in rats. J Pharm Pharmacol 40:870–872PubMedGoogle Scholar
  14. Guillem K, Vouillac C, Azar MR, Parsons LH, Koob GF, Cador M, Stinus L (2005) Monoamine oxidase inhibition dramatically increases the motivation to self-administer nicotine in rats. J Neurosci 25:8593–8600PubMedCrossRefGoogle Scholar
  15. Heinonen OP, Slone D, Shapiro S (1977) Birth defects and drugs in pregnancy. Publishing Sciences Group, Littleton, MAGoogle Scholar
  16. Horne RS, Franco P, Adamson TM, Groswasser J, Kahn A (2004) Influences of maternal cigarette smoking on infant arousability. Early Hum Dev 79:49–58PubMedCrossRefGoogle Scholar
  17. Jacobsen LK, Slotkin TA, Westerveld M, Mencl WE, Pugh KR (2006) Visuospatial memory deficits emerging during nicotine withdrawal in adolescents with prenatal exposure to active maternal smoking. Neuropsychopharmacology 31:1550–1561PubMedCrossRefGoogle Scholar
  18. Kandel D, Yamaguchi K (1992) From beer to crack: developmental patterns of drug involvement. Am J Public Health 83:851–855Google Scholar
  19. Kandel DB, Wu P, Davies M (1994) Maternal smoking during pregnancy and smoking by adolescent daughters. Am J Public Health 84:1407–1413PubMedCrossRefGoogle Scholar
  20. Kane VB, Fu Y, Matta SG, Sharp BM (2004) Gestational nicotine exposure attenuates nicotine-stimulated dopamine release in the nucleus accumbens shell of adolescent Lewis rats. J Pharmacol Exp Ther 308:521–528PubMedCrossRefGoogle Scholar
  21. Kuhar MJ, Ritz MC, Boja JW (1991) The dopamine hypothesis of the reinforcing properties of cocaine. Trends Neurosci 14:299–302PubMedCrossRefGoogle Scholar
  22. Laviola G, Wood RD, Kuhn C, Francis R, Spear LP (1995) Cocaine sensitization in periadolescent and adult rats. J Pharmacol Exp Ther 275:345–357PubMedGoogle Scholar
  23. Le Foll B, Frances H, Diaz J, Schwartz JC, Sokoloff P (2002) Role of the dopamine D3 receptor in reactivity to cocaine-associated cues in mice. Eur J Neurosci 15:2016–2026PubMedCrossRefGoogle Scholar
  24. Lewis A, Miller JH, Lea RA (2006) Monoamine oxidase and tobacco dependence. Neurotoxicology 28:182–195PubMedCrossRefGoogle Scholar
  25. Liu Z, Neff RA, Berg DK (2006) Sequential interplay of nicotinic and GABAergic signaling guides neuronal development. Science 314:1610–1613PubMedCrossRefGoogle Scholar
  26. Maldonado AM, Kirstein CL (2005) Cocaine-induced locomotor activity is increased by prior handling in adolescent but not adult female rats. Physiol Behav 86:568–572PubMedCrossRefGoogle Scholar
  27. Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, Caggiula AR, Craig CR, Collins AC, Damaj MI, Donny EC, Gardiner PS, Grady SR, Heberlein U, Leonard SS, Levin ED, Lukas RJ, Markou A, Marks MJ, McCallum SE, Parameswaran N, Perkins KA, Picciotto MR, Quik M, Rose JE, Rothenfluh A, Schafer WR, Stolerman IP, Tyndale RF, Wehner JM, Zirger JM (2006) Guidelines on nicotine dose selection for in vivo research. Psychopharmacology 190:269–319PubMedCrossRefGoogle Scholar
  28. McCartney JS, Fried PA, Watkinson B (1994) Central auditory processing in school-age children prenatally exposed to cigarette smoke. Neurotoxicol Teratol 16:269–276PubMedCrossRefGoogle Scholar
  29. Mejia JM, Ervin FR, Baker GB, Palmour RM (2002) Monoamine oxidase inhibition during brain development induces pathological aggressive behavior in mice. Biol Psychiatry 52:811–821PubMedCrossRefGoogle Scholar
  30. Metherate R, Hsieh CY (2003) Regulation of glutamate synapses by nicotinic acetylcholine receptors in auditory cortex. Neurobiol Learn Mem 80:285–290PubMedCrossRefGoogle Scholar
  31. Milberger S, Biederman J, Faraone SV, Chen L, Jones J (1997) ADHD is associated with early initiation of cigarette smoking in children and adolescents. J Am Acad Child Adolesc Psych 36:37–44CrossRefGoogle Scholar
  32. Miller CA, Marshall JF (2005) Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron 47:873–884PubMedCrossRefGoogle Scholar
  33. Nagatsu T (2004) Progress in monoamine oxidase (MAO) research in relation to genetic engineering. Neurotoxicology 25:11–20PubMedCrossRefGoogle Scholar
  34. Navarro HA, Seidler FJ, Schwartz RD, Baker FE, Dobbins SS, Slotkin TA (1989) Prenatal exposure to nicotine impairs nervous system development at a dose which does not affect viability or growth. Brain Res Bull 23:187–192PubMedCrossRefGoogle Scholar
  35. NSDUH Series H-30 (2006) Substance Abuse and Mental Health Services Administration. Results from the 2005 National Survey on Drug Use and Health: national findings (Office of Applied Studies, DHHS Publication no SMA 06-4194). Available at http://www.oas.samhsa.gov/nsduh/2k5nsduh/2k5Results.htm#4.3
  36. Pauly JR, Sparks JA, Hauser KF, Pauly TH (2004) In utero nicotine exposure causes persistent, gender-dependent changes in lomotor activity and sensitivity to nicotine in C57BI/6 mice. Int J Del Neurosci 22:329–337CrossRefGoogle Scholar
  37. Ribary U, Lichtensteiger W (1989) Effects of acute and chronic prenatal nicotine treatment on central catecholamine systems of male and female rat fetuses and offspring. J Pharmacol Exp Ther 248:786–792PubMedGoogle Scholar
  38. Richardson SA, Tizabi Y (1994) Hyperactivity in the offspring of nicotine-treated rats: role of the mesolimbic and nigrostriatal dopaminergic pathways. Pharmacol Biochem Behav 47:331–337PubMedCrossRefGoogle Scholar
  39. Robinson TE, Berridge KC (2000) The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction (Suppl) 2:S91–S117Google Scholar
  40. Rose JE (2006) Nicotine and nonnicotine factors in cigarette addiction. Psychopharmacology 186:462–472PubMedCrossRefGoogle Scholar
  41. Shenassa ED, McCaffery JM, Swan GE, Khroyan TV, Shakib S, Lerman C, Lyons M, Mouttapa M, Niaura RS, Buka SL, Leslie F, Santangelo SL (2003) Intergenerational transmission of tobacco use and dependence: a transdisciplinary perspective. Nicotine Tob Res 5(Suppl 1):S55–S69PubMedCrossRefGoogle Scholar
  42. Shih JC (2004) Cloning, after cloning, knock-out mice, and physiological functions of MAO A and B. Neurotoxicology 25:21–30PubMedCrossRefGoogle Scholar
  43. Shih J, Chen K, Ridd MJ (1999) Monoamine oxidase: from genes to behavior. Annu Rev Neurosci 22:197–217PubMedCrossRefGoogle Scholar
  44. Slotkin TA (1998) Fetal nicotine or cocaine exposure: which one is worse? J Pharmacol Exp Ther 285:931–945PubMedGoogle Scholar
  45. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463PubMedCrossRefGoogle Scholar
  46. Vaglenova J, Birru S, Pandiella NM, Breese CR (2004) An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure. Behav Brain Res 150:159–170PubMedCrossRefGoogle Scholar
  47. Vanderschuren LJ, Kalivas PW (2000) Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology 151:99–120PubMedCrossRefGoogle Scholar
  48. Villegier AS, Blanc G, Glowinski J, Tassin JP (2003) Transient behavioral sensitization to nicotine becomes long-lasting with monoamine oxidases inhibitors. Pharmacol Biochem Behav 76:267–274PubMedCrossRefGoogle Scholar
  49. Villegier AS, Salomon L, Granon S, Changeux JP, Belluzzi JD, Leslie FM, Tassin JP (2006) Monoamine oxidase inhibitors allow locomotor and rewarding responses to nicotine. Neuropsychopharmacology 31:1704–1713PubMedCrossRefGoogle Scholar
  50. Wakschlag LS, Lahey BB, Loeber R, Green SM, Gordon RA, Leventhal BL (1997) Maternal smoking during pregnancy and the risk of conduct disorder in boys. Arch Gen Psychiatry 54:670–676PubMedGoogle Scholar
  51. Weissman MM, Warner V, Wickramaratne PJ, Kandel DB (1999) Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. J Am Acad Child Adolesc Psych 38:892–899CrossRefGoogle Scholar
  52. Whitaker-Azmitia PM, Zhang X, Clarke C (1994) Effects of gestational exposure to monoamine oxidase inhibitors in rats: preliminary behavioral and neurochemical studies. Neuropsychopharmacology 11:125–132PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Ryan M. Franke
    • 1
  • James D. Belluzzi
    • 1
  • Frances M. Leslie
    • 1
    • 2
  1. 1.Department of Pharmacology, School of MedicineUniversity of CaliforniaIrvineUSA
  2. 2.Department of Anatomy and Neurobiology, School of MedicineUniversity of CaliforniaIrvineUSA

Personalised recommendations