Psychopharmacology

, Volume 214, Issue 1, pp 197–208 | Cite as

Effect of prenatal stress on alcohol preference and sensitivity to chronic alcohol exposure in male rats

  • Vincent Van Waes
  • Mihaela Enache
  • Olivier Berton
  • Elisabeth Vinner
  • Michel Lhermitte
  • Stefania Maccari
  • Muriel Darnaudéry
Original Investigation

Abstract

Rationale

In rats, prenatal restraint stress (PRS) induces persistent behavioral and neurobiological alterations leading to a greater consumption of psychostimulants during adulthood. However, little is known about alcohol vulnerability in this animal model.

Objectives

We examined in adolescent and adult male Sprague Dawley rats the long-lasting impact of PRS exposure on alcohol consumption.

Methods

PRS rats were subjected to a prenatal stress (three daily 45-min sessions of restraint stress to the mothers during the last 10 days of pregnancy). Alcohol preference was assessed in a two-bottle choice paradigm (alcohol 2.5%, 5%, or 10% versus water), in both naïve adolescent rats and adult rats previously exposed to a chronic alcohol treatment. Behavioral indices associated with incentive motivation for alcohol were investigated. Finally, plasma levels of transaminases (marker of hepatic damages) and ΔFosB levels in the nucleus accumbens (a potential molecular switch for addiction) were evaluated following the chronic alcohol exposure.

Results

Alcohol preference was not affected by PRS. Contrary to our expectations, stressed and unstressed rats did not display signs of compulsive alcohol consumption. The consequences of the alcohol exposure on locomotor reactivity and on transaminase levels were more prominent in PRS group. Similarly, PRS potentiated alcohol-induced ΔFosB levels in the nucleus accumbens.

Conclusion

Our data suggest that negative events occurring in utero do not modulate alcohol preference in male rats but potentiate chronic alcohol-induced molecular neuroadaptation in the brain reward circuitry. Further studies are needed to determine whether the exacerbated ΔFosB upregulation in PRS rats could be extended to other reinforcing stimuli.

Keywords

Maternal restraint stress Ethanol Locomotor reactivity to novelty Gene regulation AST/ALT Corticosterone 

Notes

Acknowledgments

This research was supported by the “Mission Interministérielle de Lutte contre les Drogues et les Toxicomanies” and the “Institut National de la Santé et de la Recherche Médicale” (MILDT-INSERM), the “Institut de Recherches Scientifiques sur les Boissons” (IREB), the “Pôle Interdisciplinaire de Recherche sur les Conduites Addictives” (PIRCAD), and the University of Lille 1. Vincent VAN WAES was funded by the “Conseil Régional du Nord–Pas de Calais.” Mihaela ENACHE was funded by the “Fonds Européens de Développement Régional.” We are grateful to Dr. Julien JACQUES for his statistical advice and to Giovanna BERNAL for the English revision of the manuscript. We thank Daniel DESCHAMPS and Serge LEFEVRE for animal care.

References

  1. Adrover E, Berger MA, Perez AA, Tarazi FI, Antonelli MC (2007) Effects of prenatal stress on dopamine D2 receptor asymmetry in rat brain. Synapse 61:459–462PubMedCrossRefGoogle Scholar
  2. Ahmed SH (2005) Imbalance between drug and non-drug reward availability: a major risk factor for addiction. Eur J Pharmacol 526:9–20PubMedCrossRefGoogle Scholar
  3. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders (4th ed., text revision). American Psychiatric Association, WashingtonGoogle Scholar
  4. Aufrere G, Le Bourhis B, Beauge F (1997) Ethanol intake after chronic intoxication by inhalation of ethanol vapour in rats: behavioural dependence. Alcohol 14:247–253PubMedCrossRefGoogle Scholar
  5. Bachtell RK, Wang YM, Freeman P, Risinger FO, Ryabinin AE (1999) Alcohol drinking produces brain region-selective changes in expression of inducible transcription factors. Brain Res 847:157–165PubMedCrossRefGoogle Scholar
  6. Barros VG, Berger MA, Martijena ID, Sarchi MI, Perez AA, Molina VA, Tarazi FI, Antonelli MC (2004) Early adoption modifies the effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. J Neurosci Res 76:488–496PubMedCrossRefGoogle Scholar
  7. Barros VG, Rodriguez P, Martijena ID, Perez A, Molina VA, Antonelli MC (2006) Prenatal stress and early adoption effects on benzodiazepine receptors and anxiogenic behavior in the adult rat brain. Synapse 60:609–618PubMedCrossRefGoogle Scholar
  8. Berger MA, Barros VG, Sarchi MI, Tarazi FI, Antonelli MC (2002) Long-term effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. Neurochem Res 27:1525–1533PubMedCrossRefGoogle Scholar
  9. Berton O, Covington HE III, Ebner K, Tsankova NM, Carle TL, Ulery P, Bhonsle A, Barrot M, Krishnan V, Singewald GM, Singewald N, Birnbaum S, Neve RL, Nestler EJ (2007) Induction of deltaFosB in the periaqueductal gray by stress promotes active coping responses. Neuron 55:289–300PubMedCrossRefGoogle Scholar
  10. Bessa JM, Ferreira D, Melo I, Marques F, Cerqueira JJ, Palha JA, Almeida OF, Sousa N (2009) The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol Psychiatry 14:764–773, 739PubMedCrossRefGoogle Scholar
  11. Brady KT, Sonne SC (1999) The role of stress in alcohol use, alcoholism treatment, and relapse. Alcohol Res Health 23:263–271PubMedGoogle Scholar
  12. Breese GR, Chu K, Dayas CV, Funk D, Knapp DJ, Koob GF, Le DA, O’Dell LE, Overstreet DH, Roberts AJ, Sinha R, Valdez GR, Weiss F (2005) Stress enhancement of craving during sobriety: a risk for relapse. Alcohol Clin Exp Res 29:185–195PubMedCrossRefGoogle Scholar
  13. Campbell JC, Szumlinski KK, Kippin TE (2009) Contribution of early environmental stress to alcoholism vulnerability. Alcohol 43:547–554PubMedCrossRefGoogle Scholar
  14. Chen J, Kelz MB, Hope BT, Nakabeppu Y, Nestler EJ (1997) Chronic Fos-related antigens: stable variants of deltaFosB induced in brain by chronic treatments. J Neurosci 17:4933–4941PubMedGoogle Scholar
  15. Colby CR, Whisler K, Steffen C, Nestler EJ, Self DW (2003) Striatal cell type-specific overexpression of DeltaFosB enhances incentive for cocaine. J Neurosci 23:2488–2493PubMedGoogle Scholar
  16. Conigrave KM, Davies P, Haber P, Whitfield JB (2003) Traditional markers of excessive alcohol use. Addiction 98(Suppl 2):31–43PubMedCrossRefGoogle Scholar
  17. Cruz FC, Quadros IM, da S Planeta C, Miczek KA (2008) Maternal separation stress in male mice: long-term increases in alcohol intake. Psychopharmacology (Berl) 201:459–468CrossRefGoogle Scholar
  18. Darnaudery M, Maccari S (2008) Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57:571–585PubMedCrossRefGoogle Scholar
  19. Darnaudery M, Louvart H, Defrance L, Leonhardt M, Morley-Fletcher S, Gruber SH, Galietta G, Mathe AA, Maccari S (2007) Impact of an intense stress on ethanol consumption in female rats characterized by their pre-stress preference: modulation by prenatal stress. Brain Res 1131:181–186PubMedCrossRefGoogle Scholar
  20. Deminiere JM, Piazza PV, Le Moal M, Simon H (1989) Experimental approach to individual vulnerability to psychostimulant addiction. Neurosci Biobehav Rev 13:141–147PubMedCrossRefGoogle Scholar
  21. Deminiere JM, Piazza PV, Guegan G, Abrous N, Maccari S, Le Moal M, Simon H (1992) Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res 586:135–139PubMedCrossRefGoogle Scholar
  22. DeTurck KH, Pohorecky LA (1987) Ethanol sensitivity in rats: effect of prenatal stress. Physiol Behav 40:407–410PubMedCrossRefGoogle Scholar
  23. Dole VP, Ho A, Gentry RT (1985) Toward an analogue of alcoholism in mice: criteria for recognition of pharmacologically motivated drinking. Proc Natl Acad Sci USA 82:3469–3471PubMedCrossRefGoogle Scholar
  24. Driessen M, Meier S, Hill A, Wetterling T, Lange W, Junghanns K (2001) The course of anxiety, depression and drinking behaviours after completed detoxification in alcoholics with and without comorbid anxiety and depressive disorders. Alcohol Alcohol 36:249–255PubMedGoogle Scholar
  25. Garcia-Burgos D, Gonzalez F, Manrique T, Gallo M (2009) Patterns of ethanol intake in preadolescent, adolescent, and adult wistar rats under acquisition, maintenance, and relapse-like conditions. Alcohol Clin Exp Res 7:722–728CrossRefGoogle Scholar
  26. Henry C, Guegant G, Cador M, Arnauld E, Arsaut J, Le Moal M, Demotes-Mainard J (1995) Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine receptors in the nucleus accumbens. Brain Res 685:179–186PubMedCrossRefGoogle Scholar
  27. Heyser CJ, Schulteis G, Koob GF (1997) Increased ethanol self-administration after a period of imposed ethanol deprivation in rats trained in a limited access paradigm. Alcohol Clin Exp Res 21:784–791PubMedGoogle Scholar
  28. Huot RL, Thrivikraman KV, Meaney MJ, Plotsky PM (2001) Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology (Berl) 158:366–373CrossRefGoogle Scholar
  29. Jacobsen LK, Southwick SM, Kosten TR (2001) Substance use disorders in patients with posttraumatic stress disorder: a review of the literature. Am J Psychiatry 158:1184–1190PubMedCrossRefGoogle Scholar
  30. Jaworski JN, Francis DD, Brommer CL, Morgan ET, Kuhar MJ (2005) Effects of early maternal separation on ethanol intake, GABA receptors and metabolizing enzymes in adult rats. Psychopharmacology (Berl) 181:8–15CrossRefGoogle Scholar
  31. Kaufman J, Yang BZ, Douglas-Palumberi H, Crouse-Artus M, Lipschitz D, Krystal JH, Gelernter J (2007) Genetic and environmental predictors of early alcohol use. Biol Psychiatry 61:1228–1234PubMedCrossRefGoogle Scholar
  32. Kelz MB, Chen J, Carlezon WA Jr, Whisler K, Gilden L, Beckmann AM, Steffen C, Zhang YJ, Marotti L, Self DW, Tkatch T, Baranauskas G, Surmeier DJ, Neve RL, Duman RS, Picciotto MR, Nestler EJ (1999) Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401:272–276PubMedCrossRefGoogle Scholar
  33. King A, Munisamy G, de Wit H, Lin S (2006) Attenuated cortisol response to alcohol in heavy social drinkers. Int J Psychophysiol 59:203–209PubMedCrossRefGoogle Scholar
  34. Kippin TE, Szumlinski KK, Kapasova Z, Rezner B, See RE (2007) Prenatal stress enhances responsiveness to cocaine. Neuropsychopharmacology 33:769–782PubMedCrossRefGoogle Scholar
  35. Korkosz A, Kolomanska P, Kowalska K, Rogowski A, Radwanska K, Kaczmarek L, Mierzejewski P, Scinska A, Kostowski W, Bienkowski P (2004) Dissociation of ethanol and saccharin preference in fosB knockout mice. Physiol Behav 82:391–395PubMedCrossRefGoogle Scholar
  36. Lancaster FE (1998) Sex differences in voluntary drinking by Long Evans rats following early stress. Alcohol Clin Exp Res 22:830–836PubMedGoogle Scholar
  37. Lardeux S, Baunez C (2008) Alcohol preference influences the subthalamic nucleus control on motivation for alcohol in rats. Neuropsychopharmacology 33:634–642PubMedCrossRefGoogle Scholar
  38. Le Bourhis B, Aufrere G (1983) Pattern of alcohol administration and physical dependence. Alcohol Clin Exp Res 7:378–381PubMedCrossRefGoogle Scholar
  39. Lenoir M, Serre F, Cantin L, Ahmed SH (2007) Intense sweetness surpasses cocaine reward. PLoS ONE 2:e698PubMedCrossRefGoogle Scholar
  40. Lieber CS, De Carli LM (1973) Ethanol dependence and tolerance: a nutritionally controlled experimental model in the rat. Res Commun Chem Pathol Pharmacol 6:983–991PubMedGoogle Scholar
  41. Louvart H, Maccari S, Darnaudery M (2005) Prenatal stress affects behavioral reactivity to an intense stress in adult female rats. Brain Res 1031:67–73PubMedCrossRefGoogle Scholar
  42. Maccari S, Morley-Fletcher S (2007) Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32(Suppl 1):S10–S15PubMedCrossRefGoogle Scholar
  43. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M (1995) Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neurosci 15:110–116PubMedGoogle Scholar
  44. Maldonado AM, Finkbeiner LM, Alipour KK, Kirstein CL (2008) Voluntary ethanol consumption differs in adolescent and adult male rats using a modified sucrose-fading paradigm. Alcohol Clin Exp Res 32:1574–1582PubMedCrossRefGoogle Scholar
  45. Marttila K, Petteri PT, Kiianmaa K, Ahtee L (2007) Accumbal FosB/DeltaFosB immunoreactivity and conditioned place preference in alcohol-preferring AA rats and alcohol-avoiding ANA rats treated repeatedly with cocaine. Brain Res 1160:82–90PubMedCrossRefGoogle Scholar
  46. McClung CA, Ulery PG, Perrotti LI, Zachariou V, Berton O, Nestler EJ (2004) DeltaFosB: a molecular switch for long-term adaptation in the brain. Brain Res Mol Brain Res 20(132):146–154CrossRefGoogle Scholar
  47. Morley-Fletcher S, Darnaudery M, Koehl M, Casolini P, Van Reeth O, Maccari S (2003) Prenatal stress in rats predicts immobility behavior in the forced swim test. Effects of a chronic treatment with tianeptine. Brain Res 989:246–251PubMedCrossRefGoogle Scholar
  48. Mormede P, Colas A, Jones BC (2004) High ethanol preferring rats fail to show dependence following short- or long-term ethanol exposure. Alcohol Alcohol 39:183–189PubMedGoogle Scholar
  49. Nadal R, Armario A, Janak PH (2002) Positive relationship between activity in a novel environment and operant ethanol self-administration in rats. Psychopharmacology (Berl) 162:333–338CrossRefGoogle Scholar
  50. Nestler EJ, Barrot M, Self DW (2001) DeltaFosB: a sustained molecular switch for addiction. Proc Natl Acad Sci USA 98:11042–11046PubMedCrossRefGoogle Scholar
  51. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 4th edn. Academic, San DiegoGoogle Scholar
  52. Perrotti LI, Hadeishi Y, Ulery PG, Barrot M, Monteggia L, Duman RS, Nestler EJ (2004) Induction of deltaFosB in reward-related brain structures after chronic stress. J Neurosci 24:10594–10602PubMedCrossRefGoogle Scholar
  53. Perrotti LI, Weaver RR, Robison B, Renthal W, Maze I, Yazdani S, Elmore RG, Knapp DJ, Selley DE, Martin BR, Sim-Selley L, Bachtell RK, Self DW, Nestler EJ (2008) Distinct patterns of DeltaFosB induction in brain by drugs of abuse. Synapse 62:358–369PubMedCrossRefGoogle Scholar
  54. Piazza PV, Deminiere JM, Le Moal M, Simon H (1989) Factors that predict individual vulnerability to amphetamine self-administration. Science 245:1511–1513PubMedCrossRefGoogle Scholar
  55. Ploj K, Roman E, Nylander I (2003) Long-term effects of maternal separation on ethanol intake and brain opioid and dopamine receptors in male Wistar rats. Neuroscience 121:787–799PubMedCrossRefGoogle Scholar
  56. Richardson HN, Lee SY, O’Dell LE, Koob GF, Rivier CL (2008) Alcohol self-administration acutely stimulates the hypothalamic-pituitary-adrenal axis, but alcohol dependence leads to a dampened neuroendocrine state. Eur J NeuroSci 28:1641–1653PubMedCrossRefGoogle Scholar
  57. Rodd-Henricks ZA, McKinzie DL, Shaikh SR, Murphy JM, McBride WJ, Lumeng L, Li TK (2000) Alcohol deprivation effect is prolonged in the alcohol preferring (P) rat after repeated deprivations. Alcohol Clin Exp Res 24:8–16PubMedCrossRefGoogle Scholar
  58. Rogers J, Wiener SG, Bloom FE (1979) Long-term ethanol administration methods for rats: advantages of inhalation over intubation or liquid diets. Behav Neural Biol 27:466–486PubMedCrossRefGoogle Scholar
  59. Schuckit MA, Gold E, Risch C (1987) Plasma cortisol levels following ethanol in sons of alcoholics and controls. Arch Gen Psychiatry 44:942–945PubMedGoogle Scholar
  60. Schuckit MA, Risch SC, Gold EO (1988) Alcohol consumption, ACTH level, and family history of alcoholism. Am J Psychiatry 145:1391–1395PubMedGoogle Scholar
  61. Siegmund S, Vengeliene V, Singer MV, Spanagel R (2005) Influence of age at drinking onset on long-term ethanol self-administration with deprivation and stress phases. Alcohol Clin Exp Res 29:1139–1145PubMedCrossRefGoogle Scholar
  62. Solinas M, Thiriet N, El RR, Lardeux V, Jaber M (2009) Environmental enrichment during early stages of life reduces the behavioral, neurochemical, and molecular effects of cocaine. Neuropsychopharmacology 34:1102–1111PubMedCrossRefGoogle Scholar
  63. Spanagel R, Holter SM (1999) Long-term alcohol self-administration with repeated alcohol deprivation phases: an animal model of alcoholism? Alcohol Alcohol 34:231–243PubMedGoogle Scholar
  64. Spanagel R, Montkowski A, Allingham K, Stohr T, Shoaib M, Holsboer F, Landgraf R (1995) Anxiety: a potential predictor of vulnerability to the initiation of ethanol self-administration in rats. Psychopharmacology (Berl) 122:369–373CrossRefGoogle Scholar
  65. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463PubMedCrossRefGoogle Scholar
  66. Terenina-Rigaldie E, Jones BC, Mormede P (2004) The High-Ethanol Preferring rat as a model to study the shift between alcohol abuse and dependence. Eur J Pharmacol 504:199–206PubMedCrossRefGoogle Scholar
  67. Thomas MB, Hu M, Lee TM, Bhatnagar S, Becker JB (2009) Sex-specific susceptibility to cocaine in rats with a history of prenatal stress. Physiol Behav 97:270–277PubMedCrossRefGoogle Scholar
  68. Vallee M, Mayo W, Dellu F, Le Moal M, Simon H, Maccari S (1997) Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 17:2626–2636PubMedGoogle Scholar
  69. Van Waes V, Enache M, Dutriez I, Lesage J, Morley-Fletcher S, Vinner E, Lhermitte M, Vieau D, Maccari S, Darnaudery M (2006) Hypo-response of the hypothalamic-pituitary-adrenocortical axis after an ethanol challenge in prenatally stressed adolescent male rats. Eur J NeuroSci 24:1193–1200PubMedCrossRefGoogle Scholar
  70. Van Waes V, Enache M, Zuena A, Mairesse J, Nicoletti F, Vinner E, Lhermitte M, Maccari S, Darnaudery M (2009) Ethanol attenuates spatial memory deficits and increases mGlu1a receptor expression in the hippocampus of rats exposed to prenatal stress. Alcohol Clin Exp Res 33:1346–1354PubMedCrossRefGoogle Scholar
  71. Vengeliene V, Siegmund S, Singer MV, Sinclair JD, Li TK, Spanagel R (2003) A comparative study on alcohol-preferring rat lines: effects of deprivation and stress phases on voluntary alcohol intake. Alcohol Clin Exp Res 27:1048–1054PubMedCrossRefGoogle Scholar
  72. Vilpoux C, Warnault V, Pierrefiche O, Daoust M, Naassila M (2009) Ethanol-sensitive brain regions in rat and mouse: a cartographic review, using immediate early gene expression. Alcohol Clin Exp Res 33:945–969PubMedCrossRefGoogle Scholar
  73. Weinberg J (1987) Effects of early experience on responsiveness to ethanol: a preliminary report. Physiol Behav 40:401–406PubMedCrossRefGoogle Scholar
  74. Werme M, Messer C, Olson L, Gilden L, Thoren P, Nestler EJ, Brene S (2002) Delta FosB regulates wheel running. J Neurosci 22:8133–8138PubMedGoogle Scholar
  75. 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 70:77–94PubMedCrossRefGoogle Scholar
  76. Zachariou V, Bolanos CA, Selley DE, Theobald D, Cassidy MP, Kelz MB, Shaw-Lutchman T, Berton O, Sim-Selley LJ, DiLeone RJ, Kumar A, Nestler EJ (2006) An essential role for DeltaFosB in the nucleus accumbens in morphine action. Nat Neurosci 9:205–211PubMedCrossRefGoogle Scholar
  77. Zernig G, Ahmed SH, Cardinal RN, Morgan D, Acquas E, Foltin RW, Vezina P, Negus SS, Crespo JA, Stockl 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 80:65–119PubMedCrossRefGoogle Scholar
  78. Zuena AR, Mairesse J, Casolini P, Cinque C, Alema GS, Morley-Fletcher S, Chiodi V, Spagnoli LG, Gradini R, Catalani A, Nicoletti F, Maccari S (2008) Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE 3:e2170PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Vincent Van Waes
    • 1
    • 5
  • Mihaela Enache
    • 1
  • Olivier Berton
    • 2
  • Elisabeth Vinner
    • 3
  • Michel Lhermitte
    • 3
  • Stefania Maccari
    • 1
    • 4
  • Muriel Darnaudéry
    • 6
  1. 1.Neurostress UPRES EA 4347 and CNRS UMR 8576Université Lille Nord de France, University of Lille 1Villeneuve d’AscqFrance
  2. 2.Department of PsychiatryUniversity of Pennsylvania Medical SchoolPhiladelphiaUSA
  3. 3.Laboratory of Toxicology and Genopathy UPRES EA 2679Université Lille Nord de France and Calmette HospitalLilleFrance
  4. 4.Department of Human Physiology and PharmacologySapienza University of RomaRomeItaly
  5. 5.Department of Cellular and Molecular PharmacologyRosalind Franklin University of Medicine and Science/The Chicago Medical SchoolNorth ChicagoUSA
  6. 6.INRA UMR 1286 and CNRS UMR 5226University of BordeauxBordeaux CedexFrance

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