Alcohol
Volume 43, Issue 7 , Pages 547-554 , November 2009

Contribution of early environmental stress to alcoholism vulnerability

  • Joannalee C. Campbell

      Affiliations

    • Department of Psychology, University of California, Santa Barbara, CA 93106-9660, USA
  • ,
  • Karen K. Szumlinski

      Affiliations

    • Department of Psychology, University of California, Santa Barbara, CA 93106-9660, USA
    • Neuroscience Research Institute, University of California, Santa Barbara, CA 93106-9660, USA
  • ,
  • Tod E. Kippin

      Affiliations

    • Department of Psychology, University of California, Santa Barbara, CA 93106-9660, USA
    • Neuroscience Research Institute, University of California, Santa Barbara, CA 93106-9660, USA
    • Corresponding Author InformationCorresponding author. Department of Psychology, University of California, Santa Barbara, CA 93106-9660. Tel.: +1-805-893-2459; fax: +1-805-893-4303.

Received 16 December 2008 ,Revised 6 May 2009 ,Accepted 11 August 2009.

References 

  1. American Psychiatric Association . Diagnostic and Statistical Manual of Mental Disorders DSM-IV-TR. Washington, DC.: American Psychiatric Publishing, Inc; 2000;
  2. Ary AW, Aguilar VR, Szumlinski KK, Kippin TE. Prenatal stress alters limbo-corticostriatal Homer protein expression. Synapse. 2007;61:938–941
  3. Ary AW, Lominac KD, Klugmann M, Szumlinski KK. Prefrontal cortex Homer2 over-expression enhances cocaine-seeking and produces abnormalities in extracellular glutamate. Soc. Neurosci. Abstr. 2008;767:11
  4. Barr CS, Newman TK, Lindell S, Shannon C, Champoux M, Lesch KP, et al. Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Arch. Gen. Psychiatry. 2004;61:1146–1152
  5. Barros VG, Berger MA, Martijena ID, Sarchi MI, Pérez AA, Molina VA, et al. Early adoption modifies the effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. J. Neurosci. Res. 2004;76:488–496
  6. Bell RL, Rodd ZA, Sable HJ, Schultz JA, Hsu CC, Lumeng L, et al. Daily patterns of ethanol drinking in peri-adolescent and adult alcohol-preferring (P) rats. Pharmacol. Biochem. Behav. 2006;83:35–46
  7. Bell RL, Rodd-Henricks ZA, Kuc KA, Lumeng L, Li TK, Murphy JM, et al. Effects of concurrent access to a single concentration or multiple concentrations of ethanol on the intake of ethanol by male and female periadolescent alcohol-preferring (P) rats. Alcohol. 2003;29:137–148
  8. Berger MA, Barros VG, Sarchi MI, Tarazi FI, Antonelli MC. Long-term effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. Neurochem. Res. 2002;27:1525–1533
  9. Beydoun H, Saftlas AF. Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence. Paediatr. Perinat. Epidemiol. 2008;22:438–466
  10. Boone EM, Cook MN, Hou X, Jones BC. Sex and strain influence the effect of ethanol on central monoamines. J. Stud. Alcohol. 1997;58:590–599
  11. Campbell, J. C., Dunn, C. P., Nayak, R. R., Carnatean, R. J., Lopez, M., Becker, H.C., et al. (2009). Prenatal stress increases operant responding and alcohol intake during alcohol reinforcement in adult C57B6/J mice. San Diego: Annual Meeting of the Research Society on Alcoholism, June, 2009.
  12. Clancy B, Darlington RB, Finlay BL. Translating developmental time across mammalian species. Neuroscience. 2001;105:7–17
  13. Cornelius JR, Bukstein O, Salloum I, Clark D. Alcohol and psychiatric comorbidity. Recent Dev. Alcohol. 2003;16:361–374
  14. Darnaudery M, Louvart H, Defrance L, Leonhardt M, Morley-Fletcher S, Gruber SH, et al. Impact of an intense stress on ethanol consumption in female rats characterized by their prestress preference: modulation by prenatal stress. Brain Res. 2007;1131:181–186
  15. Deminière JM, Piazza PV, Guegan G, Abrous N, Maccari S, Le Moal M, et al. Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res. 1992;586:135–139
  16. DeTurck KH, Pohorecky LA. Ethanol sensitivity in rats: effect of prenatal stress. Physiol. Behav. 1987;40:407–410
  17. Enoch MA. Genetic and environmental influences on the development of alcoholism: resilience vs. risk. Ann. N.Y. Acad. Sci. 2006;1094:193–201
  18. Epstein DH, Preston KL, Stewart J, Shaham Y. Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology (Berl). 2006;189:1–16
  19. Ferre S, Agnati LF, Ciruela F, Lluis C, Woods AS, Fuxe K, et al. Neurotransmitter receptor heteromers and their integrative role in ‘local modules’: the striatal spine module. Brain Res. Rev. 2007;55:55–67
  20. Finn DA, Belknap JK, Cronise K, Yoneyama N, Murillo A, Crabbe JC. A procedure to produce high alcohol intake in mice. Psychopharmacology. 2005;178:471–480
  21. Finn DA, Mark GP, Fretwell AM, Gililland-Kaufman KR, Strong MN, Ford MM. Reinstatement of ethanol and sucrose seeking by the neurosteroid allopregnanolone in C57BL/6 mice. Psychopharmacology (Berl). 2008;201:423–433
  22. Flagel SB, Vázquez DM, Robinson TE. Manipulations during the second, but not the first, week of life increase susceptibility to cocaine self- administration in female rats. Neuropsychopharmacology. 2003;28:1741–1751
  23. Francis D, Diorio J, LaPlante P, Weaver S, Seckl JR, Meaney MJ. The role of early environmental events in regulating neuroendocrine development. Moms, pups, stress, and glucocorticoid receptors. Ann. N.Y. Acad. Sci. 1996;794:136–152
  24. Fuchs RA, See RE, Middaugh LD. Conditioned stimulus-induced reinstatement of extinguished cocaine seeking in C57BL/6 mice: a mouse model of drug relapse. Brain Res. 2003;973:99–106
  25. Fuller JL. Measurement of alcohol preference in genetic experiments. J. Comp. Physiol. Psychol. 1964;57:85–88
  26. Glynn LM, Wadhwa PD, Dunkel-Schetter C, Chicz-DeMet A, Sandman CA. When stress happens matters: effects of earthquake timing on stress responsivity in pregnancy. Am. J. Obstet. Gynecol. 2001;184:637–642
  27. Gongwer MA, Murphy JM, McBride WJ, Lumeng L, Li T-K. Regional brain contents of serotonin, dopamine, and their metabolites in the selectively bred high- and low-alcohol drinking lines of rats. Alcohol. 1989;6:317–320
  28. Gustafsson L, Nylander I. Time-dependent alterations in ethanol intake in male wistar rats exposed to short and prolonged daily maternal separation in a 4-bottle free-choice paradigm. Alcohol. Clin. Exp. Res. 2006;30:2008–2016
  29. Gustafsson L, Ploj K, Nylander I. Effects of maternal separation on voluntary ethanol intake and brain peptide systems in female Wistar rats. Pharmacol. Biochem. Behav. 2005;81:506–516
  30. Gutman DA, Nemeroff CB. Neurobiology of early life stress: rodent studies. Semin. Clin. Neuropsychiatry. 2002;7:89–95
  31. Hara Y, Pickel VM. Overlapping intracellular and differential synaptic distributions of dopamine D1 and glutamate N-methyl-D-aspartate receptors in rat nucleus accumbens. J. Comp. Neurol. 2005;492:442–455
  32. Heidbreder CA, Andreoli M, Marcon C, Hutcheson DM, Gardner EL, Ashby CR. Evidence for the role of dopamine D3 receptors in oral operant alcohol self-administration and reinstatement of alcohol-seeking behavior in mice. Addict. Biol. 2007;12:35–50
  33. Henry C, Guegant G, Cador M, Arnauld E, Arsaut J, Le Moal M, et al. Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine receptors in the nucleus accumbens. Brain Res. 1995;685:179–186
  34. Highfield DA, Mead AN, Grimm JW, Rocha BA, Shaham Y. Reinstatement of cocaine seeking in 129X1/SvJ mice: effects of cocaine priming, cocaine cues and food deprivation. Psychopharmacology (Berl). 2002;161:417–424
  35. Holahan CJ, Moos RH, Holahan CK, Cronkite RC, Randall PK. Drinking to cope, emotional distress and alcohol use and abuse: a ten-year model. J. Stud. Alcohol. 2001;62:190–198
  36. Huizink AC, Mulder EJ, Buitelaar JK. Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility?. Psychol. Bull. 2004;130:115–142
  37. Huot RL, Thrivikraman KV, Meaney MJ, Plotshy PM. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology (Berlin). 2001;158:366–373
  38. Jaworski JN, Francis DD, Brommer CL, Morgan ET, Kuhar MJ. Effects of early maternal separation on ethanol intake, GABA receptors and metabolizing enzymes in adult rats. Psychopharmacology. 2005;181:8–15
  39. Kalivas PW, Volkow N, Seamans J. Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron. 2005;45:647–650
  40. Kapasova Z, Szumlinski KK. Strain differences in alcohol-induced neurochemical plasticity: a role for accumbens glutamate in alcohol intake. Alcohol. Clin. Exp. Res. 2008;32:617–631
  41. Katner SN, Weiss F. Neurochemical characteristics associated with ethanol preference in selected alcohol-preferring and -nonpreferring rats: a quantitative microdialysis study. Alcohol. Clin. Exp. Res. 2001;25:198–205
  42. Katz JL, Higgins ST. The validity of the reinstatement model of craving and relapse to drug use. Psychopharmacology (Berlin). 2003;168:21–30
  43. Kiianmaa K, Nurmi M, Nykänen I, Sinclair JD. Effect of ethanol on extracellular dopamine in the nucleus accumbens of alcohol-preferring AA and alcohol-avoiding ANA rats. Pharmacol. Biochem. Behav. 1995;52:29–34
  44. King S, Laplante DP. The effects of prenatal maternal stress on children's cognitive development: Project Ice Storm. Stress. 2005;8:35–45
  45. Kippin TE, Szumlinski KK, Kapasova Z, Rezner B, See RE. Prenatal stress enhances responsiveness to cocaine. Neuropsychopharmacology. 2008;33:769–782
  46. Kofman O. The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci. Biobehav. Rev. 2002;26:457–470
  47. Koob GF. Alcoholism: allostasis and beyond. Alcohol. Clin. Exp. Res. 2003;27:232–243
  48. Kosten TA, Miserendino MJ, Kehoe P. Enhanced acquisition of cocaine self-administration in adult rats with neonatal isolation stress experience. Brain Res. 2000;875:44–50
  49. Kushner MG, Abrams K, Borchardt C. The relationship between anxiety disorders and alcohol use disorders: a review of major perspectives and findings. Clin. Psychol. Rev. 2000;20:149–171
  50. Kruzich PJ. Does response-contingent access to cocaine reinstate previously extinguished cocaine-seeking behavior in C57BL/6J mice?. Brain Res. 2007;1149:165–171
  51. Krystal JH, D'Souza DC, Gallinat J, Driesen N, Abi-Dargham A, Petrakis I, et al. The vulnerability to alcohol and substance abuse in individuals diagnosed with schizophrenia. Neurotox. Res. 2006;10:235–252
  52. Krystal JH, Petrakis IL, Krupitsky E, Schutz C, Trevisan L, D'Souza DC. NMDA receptor antagonism and the ethanol intoxication signal: from alcoholism risk to pharmacotherapy. Ann. N.Y. Acad. Sci. 2003;1003:176–184
  53. Lancaster FE. Sex differences in voluntary drinking by Long Evans rats following early stress. Alcohol. Clin. Exp. Res. 1998;22:830–836
  54. Lancaster FE, Speigel KS. Sex differences in pattern of drinking. Alcohol. 1992;9:415–420
  55. Lapish CC, Seamans JK, Chandler LJ. Glutamate-dopamine cotransmission and reward processing in addiction. Alcohol. Clin. Exp. Res. 2006;30:1451–1465
  56. Lê A, Shaham Y. Neurobiology of relapse to alcohol in rats. Pharmacol. Ther. 2002;94:137–156
  57. Lehmann J, Feldon J. Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing?. Rev. Neurosci. 2000;11:383–408
  58. Lominac KD, Kapasova Z, Hannun RA, Patterson C, Middaugh LD, Szumlinski KK. Behavioral and neurochemical interactions between Group 1 mGluR antagonists and ethanol: potential insight into their anti-addictive properties. Drug Alcohol Dep. 2006;85:142–156
  59. Lominac KD, Oleson EB, Pava M, Klugmann M, Schwarz MK, Seeburg PH, et al. Distinct roles for different Homer1 isoforms in behaviors and associated prefrontal cortex function. J. Neurosci. 2005;25:11586–11594
  60. Lovinger DM, White G, Weight FF. Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science. 1989;243:1721–1724
  61. Lynch WJ, Mangini LD, Taylor JR. Neonatal isolation stress potentiates cocaine seeking behavior in adult male and female rats. Neuropsychopharmacology. 2005;30:322–329
  62. Matthews K, Robbins TW, Everitt BJ, Caine SB. Repeated neonatal maternal separation alters intravenous cocaine self-administration in adult rats. Psychopharmacology (Berlin). 1999;141:123–134
  63. McBride WJ, Bodart B, Lumeng L, Li T-K. Association between low contents of dopamine and serotonin in the nucleus accumbens and high alcohol preference. Alcohol. Clin. Exp. Res. 1995;19:1420–1432
  64. McBride WJ, Li T-K. Animal models of alcoholism: neurobiology of high alcohol-drinking behavior in rodents. Crit. Rev. Neurobiol. 1998;12:339–369
  65. McBride WJ, Murphy JM, Lumeng L, Li T-K. Effects of ethanol on monoamine and amino acid release from cerebral cortical slices of the alcohol-preferring P line of rats. Alcohol. Clin. Exp. Res. 1986;10:205–208
  66. McCormick CM, Smythe JW, Sharma S, Meaney MJ. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res. Dev. Brain Res. 1995;84:55–61
  67. Minami K, Gereau RW, Minami M, Heinemann SF, Harris RA. Effects of ethanol and anesthetics on type 1 and 5 metabotropic glutamate receptors expressed in Xenopus oocytes. Mol. Pharmacol. 1998;53:148–156
  68. Moffett MC, Vicentic A, Kozel M, Plotsky P, Francis DD, Kuhar MJ. Maternal separation alters drug intake patterns in adulthood in rats. Biochem. Pharmacol. 2007;73:321–330
  69. Moselhy HF, Georgiou G, Kahn A. Frontal lobe changes in alcoholism: a review of the literature. Alcohol Alcohol. 2001;36:357–368
  70. Murphy JM, McBride WJ, Lumeng L, Li T-K. Alcohol preference and regional brain monoamine contents of N/Nih heterogeneous stock rats. Alcohol Drug Res. 1987;7:33–39
  71. Newton PM, Zeng L, Wang V, Connolly J, Wallace MJ, Kim C, et al. A blocker of N- and T-type voltage-gated calcium channels attenuates ethanol-induced intoxication, place preference, self-administration, and reinstatement. J. Neurosci. 2008;28:11712–11719
  72. Ploj K, Roman E, Nylander I. Long-term effects of maternal separation on ethanol intake and brain opioid and opamine receptors in male Wistar rats. Neuroscience. 2003;121:787–799
  73. Rhodes JS, Best K, Belknap JK, Finn DA, Crabbe JC. Evaluation of a simple model of ethanol drinking to intoxication in C57BL/6J mice. Physiol. Behav. 2005;84:53–63
  74. Rodgers DA, McClearn GE. Mouse strain differences in preference for various concentrations of alcohol. Q.J. Stud. Alcohol. 1962;23:26–33
  75. Roman E, Hyytia P, Nylander I. Maternal separation alters acquisition of ethanol intake in male ethanol-preferring AA rats. Alcohol. Clin. Exp. Res. 2003;27:31–37
  76. Roman E, Nylander I. The impact of emotional stress early in life on adult voluntary ethanol intake—results of maternal separation in rats. Stress. 2005;8:157–174
  77. Samson HH. Initiation of ethanol reinforcement using a sucrose-substitution procedure in food- and water-sated rats. Alcohol. Clin. Exp. Res. 1986;10:436–442
  78. Sanchis-Segura C, Borchardt T, Vengeliene V, Zghoul T, Bachteler D, Gass P, et al. Involvement of the AMPA receptor GluR-C subunit in alcohol-seeking behavior and relapse. J. Neurosci. 2006;26:1231–1238
  79. Schmidt NB, Bunkner JD, Keough ME. Anxiety sensitivity as a prospective predictor of alcohol use disorders. Behav. Modif. 2007;31:202–219
  80. Schuckit MA. Comorbidity between substance use disorders and psychiatric conditions. Addiction. 2006;101(Suppl 1):76–88
  81. Schuckit MA, Smith TL, Kalmijn J. The search for genes contributing to the low level of response to alcohol: patterns of findings across studies. Alcohol. Clin. Exp. Res. 2004;28:1449–1458
  82. Seckl JR, Meaney MJ. Glucocorticoid "programming" and PTSD risk. Ann. N.Y. Acad. Sci. 2006;1071:351–378
  83. See RE. Neural substrates of cocaine-cue associations that trigger relapse. Eur. J. Pharmacol. 2005;526:140–146
  84. Selim M, Bradberry CW. Effect of ethanol on extracellular 5-HT and glutamate in the nucleus accumbens and prefrontal cortex: comparison between the Lewis and Fischer 344 rat strains. Brain Res. 1996;716:157–164
  85. Sheng M, Hoogenraad CC. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu. Rev. Biochem. 2007;76:823–847
  86. Shiraishi-Yamaguchi Y, Furuichi T. The Homer family proteins. Genome Biol. 2007;8:206
  87. Silvagni A, Barros VG, Mura C, Antonelli MC, Carboni E. Prenatal restraint stress differentially modifies basal and stimulated dopamine and noradrenaline release in the nucleus accumbens shell: an ‘in vivo’ microdialysis study in adolescent and young adult rats. Eur. J. Neurosci. 2008;28:744–758
  88. Smith AD, Weiss F. Ethanol exposure differentially alters central monoamine neurotransmission in alcohol-preferring versus -nonpreferring rats. J. Pharmacol. Exp. Ther. 1999;288:1223–1228
  89. Soria G, Barbano MF, Maldonado R, Valverde O. A reliable method to study cue-, priming-, and stress-induced reinstatement of cocaine self- administration in mice. Psychopharmacology (Berl). 2008;199:593–603
  90. Szumlinski KK, Ary AW, Lominac KD. Homers regulate drug-induced neuroplasticity: implications for addiction. Biochem. Pharmacol. 2008;75:112–133
  91. Szumlinski KK, Diab ME, Friedman R, Henze LM, Lominac KD, Bowers MS. Accumbens neurochemical adaptations produced by binge-like alcohol consumption. Psychopharmacology. 2007;190:415–431
  92. Szumlinski KK, Lominac KD, Kleschen M, Oleson EB, Dehoff M, Schwartz M, et al. Behavioural and neurochemical phenotyping of Homer1 mutant mice: possible implications for schizophrenia. Genes Brain Behav. 2005;4:273–288
  93. Szumlinski KK, Lominac KD, Oleson EB, Walker JK, Mason A, Dehoff MH, et al. Homer2 is necessary for ethanol-induced neuroplasticity. J. Neurosci. 2005;25:7054–7061
  94. Tiet QQ, Bird HR, Davies M, Hoven C, Cohen P, Jensen PS, et al. Adverse life events and resilience. J. Am. Acad. Child. Adolesc. Psychiatry. 1998;37:1191–1200
  95. Trudeau LE. Glutamate co-transmission as an emerging concept in monoamine neuron function. J. Psychiatry Neurosci. 2004;29:296–310
  96. Tsiang MT, Janak PH. Alcohol seeking in C57BL/6 mice induced by conditioned cues and contexts in the extinction-reinstatement model. Alcohol. 2006;38:81–88
  97. Van Waes V, Enache M, Dutriez I, Lesage J, Morley-Fletcher S, Vinner E, et al. Hypo-response of the hypothalamic-pituitary-adrenocortical axis after an ethanol challenge in prenatally stressed adolescent male rats. Eur. J. Neurosci. 2006;24:1193–1200
  98. Volkow ND, Hitzemann R, Wolf AP, Logan J, Fowler JS, Christman D, et al. Acute effects of ethanol on regional brain glucose metabolism and transport. Psychiatry Res. 1990;35:39–48
  99. Weems CF, Overstreet S. Child and adolescent mental health research in the context of Hurricane Katrina: an ecological needs-based perspective and introduction to the special section. J. Clin. Child Adolesc. Psychol. 2008;37:487–494
  100. Weinberg J. Effects of early experience on responsiveness to ethanol: a preliminary report. Physiol. Behav. 1987;40:401–406
  101. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog. Neurobiol. 2001;65:427–451
  102. Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav. Immun. 2005;19:296–308
  103. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev. 2008;32:1073–1086
  104. Welberg LA, Seckl JR. Prenatal stress, glucocorticoids and the programming of the brain. J. Neuroendocrinol. 2001;13:113–128
  105. Wiren KM, Hashimoto JG, Alele PE, Devaud LL, Price KL, Middaugh LD, et al. Impact of sex: determination of alcohol neuroadaptation and reinforcement. Alcohol. Clin. Exp. Res. 2006;30:233–242
  106. Witt ED. Puberty, hormones, and sex differences in alcohol abuse and dependence. Neurotoxicol. Teratol. 2007;29:81–95
  107. Yager JY, Ashwal S. Animal models of perinatal hypoxic-ischemic brain damage. Pediatr. Neurol. 2009;40:156–167
  108. Zghoul T, Abarca C, Sanchis-Segura C, Albrecht U, Schumann G, Spanagel R. Ethanol self-administration and reinstatement of ethanol-seeking behavior in Per1(Brdm1) mutant mice. Psychopharmacology (Berl). 2007;190:13–19
  109. Zimmermann US, Blomeyer D, Laucht M, Mann KF. How gene-stress-behavior interactions can promote adolescent alcohol use: the roles of predrinking allostatic load and childhood behavior disorders. Pharm. Biochem. Behav. 2007;86:246–262
  110. Zuker RA, Donovan JE, Masten AS, Mattson ME, Moss HB. Early developmental processes and the continuity of risk for underage drinking and problem drinking. Pediatrics. 2008;121(Suppl 4):S225–S272

PII: S0741-8329(09)00161-X

doi: 10.1016/j.alcohol.2009.09.029

Alcohol
Volume 43, Issue 7 , Pages 547-554 , November 2009