Psychopharmacology

, Volume 232, Issue 10, pp 1705–1716 | Cite as

Amphetamine sensitization and cross-sensitization with acute restraint stress: impact of prenatal alcohol exposure in male and female rats

Original Investigation

Abstract

Rationale

Individuals with fetal alcohol spectrum disorder (FASD) are at increased risk for substance use disorders (SUD). In typically developing individuals, susceptibility to SUD is associated with alterations in dopamine and hypothalamic-pituitary-adrenal (HPA) systems, and their interactions. Prenatal alcohol exposure (PAE) alters dopamine and HPA systems, yet effects of PAE on dopamine-HPA interactions are unknown. Amphetamine-stress cross-sensitization paradigms were utilized to investigate sensitivity of dopamine and stress (HPA) systems, and their interactions following PAE.

Methods

Adult Sprague-Dawley offspring from PAE, pair-fed, and ad libitum-fed control groups were assigned to amphetamine-(1–2 mg/kg) or saline-treated conditions, with injections every other day for 15 days. Fourteen days later, all animals received an amphetamine challenge (1 mg/kg) and 5 days later, hormones were measured under basal or acute stress conditions. Amphetamine sensitization (augmented locomotion, days 1–29) and cross-sensitization with acute restraint stress (increased stress hormones, day 34) were assessed.

Results

PAE rats exhibited a lower threshold for amphetamine sensitization compared to controls, suggesting enhanced sensitivity of dopaminergic systems to stimulant-induced changes. Cross-sensitization between amphetamine (dopamine) and stress (HPA hormone) systems was evident in PAE, but not in control rats. PAE males exhibited increased dopamine receptor expression (medial prefrontal cortex (mPFC)) compared to controls.

Conclusions

PAE alters induction and expression of sensitization/cross-sensitization, as reflected in locomotor, neural, and endocrine changes, in a manner consistent with increased sensitivity of dopamine and stress systems. These results provide insight into possible mechanisms that could underlie increased prevalence of SUD, as well as the impact of widely prescribed stimulant medications among adolescents with FASD.

Keywords

Prenatal alcohol Amphetamine Stress Dopamine Addiction Sex differences Sensitization Prefrontal cortex Nucleus accumbens Striatum 

References

  1. Ahmed SH, Cador M (2006) Dissociation of psychomotor sensitization from compulsive cocaine consumption. Neuropsychopharmacology 31:563–571CrossRefPubMedGoogle Scholar
  2. Alati R, Clavarino A, Najman JM, O’Callaghan M, Bor W, Mamun AA, Williams GM (2008) The developmental origin of adolescent alcohol use: findings from the Mater University study of pregnancy and its outcomes. Drug Alcohol Depend 98:136–143CrossRefPubMedGoogle Scholar
  3. Antelman SM, Eichler AJ, Black CA, Kocan D (1980) Interchangeability of stress and amphetamine in sensitization. Science 207:329–331CrossRefPubMedGoogle Scholar
  4. Badiani A, Robinson TE (2004) Drug-induced neurobehavioral plasticity: the role of environmental context. Behav Pharmacol 15:327–339CrossRefPubMedGoogle Scholar
  5. Baer JS, Sampson PD, Barr HM, Connor PD, Streissguth AP (2003) A 21-year longitudinal analysis of the effects of prenatal alcohol exposure on young adult drinking. Arch Gen Psychiatry 60:377–385CrossRefPubMedGoogle Scholar
  6. Barbier E, Houchia H, Warnaulta V, Pierrefichea O, Daousta M, Naassila M (2009) Effects of prenatal and postnatal maternal ethanol on offspring response to alcohol and psychostimulants in long evans rats. Neuroscience 161:427–440CrossRefPubMedGoogle Scholar
  7. Barr AM, Hofmann CE, Weinberg J, Phillips AG (2002) Exposure to repeated, intermittent d-amphetamine induces sensitization of HPA axis to a subsequent stressor. Neuropsychopharmacology 26:286–294CrossRefPubMedGoogle Scholar
  8. Becker JB, Molenda H, Hummer DL (2001) Gender differences in the behavioral responses to cocaine and amphetamine. Implications for mechanisms mediating gender differences in drug abuse. Ann N Y Acad Sci 937:172–187CrossRefPubMedGoogle Scholar
  9. Berman RF, Hannigan JH (2000) Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10:94–110CrossRefPubMedGoogle Scholar
  10. Blanchard BA, Steindorf S, Wang S, LeFevre R, Mankes RF, Glick SD (1993) Prenatal ethanol exposure alters ethanol-induced dopamine release in nucleus accumbens and striatum in male and female rats. Alcohol Clin Exp Res 17:974–981CrossRefPubMedGoogle Scholar
  11. Browman KE, Badiani A, Robinson TE (1998) Modulatory effect of environmental stimuli on the susceptibility to amphetamine sensitization: a dose-effect study in rats. J Pharmacol Exp Ther 287:1007–1014PubMedGoogle Scholar
  12. Cabib S, Puglisi-Allegra S (2012) The mesoaccumbens dopamine in coping with stress. Neurosci Biobehav Rev 36:79–89CrossRefPubMedGoogle Scholar
  13. Capper-Loup C, Canales JJ, Kadaba N, Graybiel AM (2002) Concurrent activation of dopamine D1 and D2 receptors is required to evoke neural and behavioral phenotypes of cocaine sensitization. J Neurosci 22:6218–6227Google Scholar
  14. Carlson JN, Glick SD (1989) Cerebral lateralization as a source of interindividual differences in behavior. Experientia 45:788–798Google Scholar
  15. Carlson JN, Fitzgerald LW, Keller RW Jr, Glick SD (1993) Lateralized changes in prefrontal cortical dopamine activity induced by controllable and uncontrollable stress in the rat. Brain Res 630:178–187CrossRefPubMedGoogle Scholar
  16. Castner SA, Williams GV (2007) From vice to virtue: insights from sensitization in the nonhuman primate. Prog Neuropsychopharmacol Biol Psychiatry 31:1572–1592CrossRefPubMedGoogle Scholar
  17. Chen W, Maier S, West J (1997) Prenatal alcohol treatment attenuated postnatal cocaine-induced elevation of dopamine concentration in nucleus accumbens: a preliminary study. Neurotoxicol Teratol 19:39–46CrossRefPubMedGoogle Scholar
  18. Chotro MG, Arias C, Laviola G (2007) Increased ethanol intake after prenatal ethanol exposure: studies with animals. Neurosci Biobehav Rev 31:181–191CrossRefPubMedGoogle Scholar
  19. Deroche V, Piazza PV, Maccari S, Le Moal M, Simon H (1992) Repeated corticosterone administration sensitizes the locomotor response to amphetamine. Brain Res 584:309–313CrossRefPubMedGoogle Scholar
  20. Doig J, McLennan JD, Gibbard WB (2008) Medication effects on symptoms of attention-deficit/hyperactivity disorder in children with fetal alcohol spectrum disorder. J Child Adolesc Psychopharmacol 18:365–371CrossRefPubMedGoogle Scholar
  21. Gallo PV, Weinberg J (1981) Corticosterone rhythmicity in the rat: interactive effects of dietary restriction and schedule of feeding. J Nutr 111:208–218PubMedGoogle Scholar
  22. Haley DW, Handmaker NS, Lowe J (2006) Infant stress reactivity and prenatal alcohol exposure. Alcohol Clin Exp Res 30:2055–2064CrossRefPubMedGoogle Scholar
  23. Hannigan JH, Pilati ML (1991) The effects of chronic postweaning amphetamine on rats exposed to alcohol in utero: weight gain and behavior. Neurotoxicol Teratol 13:649–656CrossRefPubMedGoogle Scholar
  24. Haseltine FP (2000) Gender differences in addiction and recovery. J Womens Health Gend Based Med 9:579–583CrossRefPubMedGoogle Scholar
  25. Hellemans KG, Verma P, Yoon E, Yu WK, Young AH, Weinberg J (2010) Prenatal alcohol exposure and chronic mild stress differentially alter depressive- and anxiety-like behaviors in male and female offspring. Alcohol Clin Exp Res 34:633–645CrossRefPubMedGoogle Scholar
  26. Hooks MS, Juncos JL, Justice JB Jr, Meiergerd SM, Povlock SL, Schenk JO, Kalivas PW (1994) Individual locomotor response to novelty predicts selective alterations in D1 and D2 receptors and mRNAs. J Neurosci 14:6144–6152PubMedGoogle Scholar
  27. Hu M, Becker JB (2003) Effects of sex and estrogen on behavioral sensitization to cocaine in rats. J Neurosci 23:693–699CrossRefPubMedGoogle Scholar
  28. Ikemoto S (2002) Ventral striatal anatomy of locomotor activity induced by cocaine, D-amphetamine, dopamine and D1/D2 agonists. Neuroscience 113:939–955CrossRefPubMedGoogle Scholar
  29. Jacobson SW, Bihun JT, Chiodo LM (1999) Effects of prenatal alcohol and cocaine exposure on infant cortisol levels. Dev Psychopathol 11:195–208CrossRefPubMedGoogle Scholar
  30. Kajimoto K, Allan A, Cunningham LA (2013) Fate analysis of adult hippocampal progenitors in a murine model of fetal alcohol spectrum disorder (FASD). PLoS One 8:e73788CrossRefPubMedCentralPubMedGoogle Scholar
  31. Koob GF (2008) A role for brain stress systems in addiction. Neuron 59:11–34CrossRefPubMedCentralPubMedGoogle Scholar
  32. Koob G, Kreek MJ (2007) Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am J Psychiatry 164:1149–1159CrossRefPubMedCentralPubMedGoogle Scholar
  33. Krieger DT (1974) Food and water restriction shifts corticosterone. Temp Act Brain Amine Periodicity Endocrinol 95:1195–1201Google Scholar
  34. Le Moal M (2009) Drug abuse: vulnerability and transition to addiction. Pharmacopsychiatry 42(Suppl 1):S42–S55CrossRefPubMedGoogle Scholar
  35. Lee S, Schmidt D, Tilders F, Rivier C (2000) Increased activity of the hypothalamic-pituitary-adrenal axis of rats exposed to alcohol in utero: role of altered pituitary and hypothalamic function. Mol Cell Neurosci 16:515–528CrossRefPubMedGoogle Scholar
  36. Livy DJ, Miller EK, Maier SE, West JR (2003) Fetal alcohol exposure and temporal vulnerability: effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicol Teratol 25:447–458CrossRefPubMedGoogle Scholar
  37. Lovallo WR (2006) Cortisol secretion patterns in addiction and addiction risk. Int J Psychophysiol 59:195–202CrossRefPubMedCentralPubMedGoogle Scholar
  38. MacLennan AJ, Maier SF (1983) Coping and the stress-induced potentiation of stimulant stereotypy in the rat. Science 219:1091–1093CrossRefPubMedGoogle Scholar
  39. McLachlan K, Rasmussen C, Pei J, Reynolds J, Weinberg J (2013) Diurnal cortisol patterns in children with FASD. Alcohol Clin Exp Res 133A: Poster.Google Scholar
  40. Nielsen DM, Crosley KJ, Keller RW Jr, Glick SD, Carlson JN (1999) Rotation, locomotor activity and individual differences in voluntary ethanol consumption. Brain Res 823:80–87CrossRefPubMedGoogle Scholar
  41. O’Connor MJ, Paley B (2009) Psychiatric conditions associated with prenatal alcohol exposure. Dev Disabil Res Rev 15:225–234CrossRefPubMedGoogle Scholar
  42. Pacak K, Palkovits M (2001) Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 22:502–548CrossRefPubMedGoogle Scholar
  43. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. Academic PressGoogle Scholar
  44. Piazza PV, Deminiere JM, le Moal M, Simon H (1990) Stress- and pharmacologically-induced behavioral sensitization increases vulnerability to acquisition of amphetamine self-administration. Brain Res 514:22–26CrossRefPubMedGoogle Scholar
  45. Ramsay DS, Bendersky MI, Lewis M (1996) Effect of prenatal alcohol and cigarette exposure on two- and six-month-old infants’ adrenocortical reactivity to stress. J Pediatr Psychol 21:833–840CrossRefPubMedCentralPubMedGoogle Scholar
  46. Rasband WS (1997–2011) ImageJ. (Health, N. I. o., ed) Bethesda, Maryland, USA: http://imagej.nih.gov/ij/
  47. Robinson TE, Becker JB (1986) Enduring changes in brain and behavior produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis. Brain Res 396:157–198CrossRefPubMedGoogle Scholar
  48. Sarnyai Z, Shaham Y, Heinrichs SC (2001) The role of corticotropin-releasing factor in drug addiction. Pharmacol Rev 53:209–243PubMedGoogle Scholar
  49. Shen RY, Hannigan JH, Kapatos G (1999) Prenatal ethanol reduces the activity of adult midbrain dopamine neurons. Alcohol Clin Exp Res 23:1801–1807CrossRefPubMedGoogle Scholar
  50. Shen RY, Choong KC, Thompson AC (2007) Long-term reduction in ventral tegmental area dopamine neuron population activity following repeated stimulant or ethanol treatment. Biol Psychiatry 61:93–100CrossRefPubMedGoogle Scholar
  51. Shetty A, Burrows R, Phillips D (1993) Alterations in neuronal development in the substantia nigra pars compacta following in utero ethanol exposure: immunohistochemical and Golgi studies. Neuroscience 52:311–322CrossRefPubMedGoogle Scholar
  52. Sinha R (2008) Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 1141:105–130CrossRefPubMedCentralPubMedGoogle Scholar
  53. Sliwowska JH, Barker JM, Barha CK, Lan N, Weinberg J, Galea LA (2010) Stress-induced suppression of hippocampal neurogenesis in adult male rats is altered by prenatal ethanol exposure. Stress 13:301–313CrossRefPubMedGoogle Scholar
  54. Spear LP (1996) Assessment of the effects of developmental toxicants: pharmacological and stress vulnerability of offspring. NIDA Res Monogr 164:125–145PubMedGoogle Scholar
  55. Sweitzer MM, Donny EC, Hariri AR (2012) Imaging genetics and the neurobiological basis of individual differences in vulnerability to addiction. Drug Alcohol Depend 123(Suppl 1):S59–S71CrossRefPubMedGoogle Scholar
  56. Taylor AN, Branch BJ, Van Zuylen JE, Redei E (1988) Maternal alcohol consumption and stress responsiveness in offspring. Adv Exp Med Biol 245:311–317CrossRefPubMedGoogle Scholar
  57. Thanh NX, Jonsson E (2010) Drinking alcohol during pregnancy: evidence from Canadian Community Health Survey 2007/2008. J Popul Ther Clin Pharmacol 17:e302–e307PubMedGoogle Scholar
  58. Uban KA, Sliwowska JH, Lieblich S, Ellis LA, Yu WK, Weinberg J, Galea LAM (2010) Prenatal alcohol exposure reduces the proportion of newly produced neurons and glia in the dentate gyrus of the hippocampus in female rats. Horm Behav 58:835–843CrossRefPubMedCentralPubMedGoogle Scholar
  59. Uban KA, Rummel J, Floresco SB, Galea LA (2012) Estradiol modulates effort-based decision making in female rats. Neuropsychopharmacology 37:390–401CrossRefPubMedCentralPubMedGoogle Scholar
  60. Uban KA, Comeau W, Ellis L, Galea LAM, Weinberg J (2013) Basal regulation of HPA and dopamine systems is altered differentially in males and females by prenatal alcohol exposure and chronic variable stress. PNEC 38:1953–1966Google Scholar
  61. Vanderschuren LJ, Pierce RC (2010) Sensitization processes in drug addiction. Curr Top Behav Neurosci 3:179–195CrossRefPubMedGoogle Scholar
  62. Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Wong C, Hitzemann R, Pappas NR (1999) Reinforcing effects of psychostimulants in humans are associated with increases in brain dopamine and occupancy of D(2) receptors. J Pharmacol Exp Ther 291:409–415PubMedGoogle Scholar
  63. Volkow ND, Fowler JS, Wang GJ, Swanson JM, Telang F (2007) Dopamine in drug abuse and addiction: results of imaging studies and treatment implications. Arch Neurol 64:1575–1579CrossRefPubMedGoogle Scholar
  64. Volkow ND, Wang GJ, Fowler JS, Tomasi D, Telang F (2011) Addiction: beyond dopamine reward circuitry. Proc Natl Acad Sci U S A 108:15037–15042CrossRefPubMedCentralPubMedGoogle Scholar
  65. Wang J, Haj-Dahmane S, Shen RY (2006) Effects of prenatal ethanol exposure on the excitability of ventral tegmental area dopamine neurons in vitro. J Pharmacol Exp Ther 319:857–863CrossRefPubMedGoogle Scholar
  66. Wang YC, Wang CC, Lee CC, Huang AC (2010) Effects of single and group housing conditions and alterations in social and physical contexts on amphetamine-induced behavioral sensitization in rats. Neurosci Lett 486:34–37CrossRefPubMedGoogle Scholar
  67. Weinberg J, Sliwowska JH, Lan N, Hellemans KG (2008) Prenatal alcohol exposure: foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J Neuroendocrinol 20:470–488CrossRefPubMedGoogle Scholar
  68. Xu C, Shen RY (2001) Amphetamine normalizes the electrical activity of dopamine neurons in the ventral tegmental area following prenatal ethanol exposure. J Pharmacol Exp Ther 297:746–752PubMedGoogle Scholar
  69. Young EA (1998) Sex differences and the HPA axis: implications for psychiatric disease. J Gend Specif Med 1:21–27PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of British ColumbiaVancouverCanada
  2. 2.Brain Research CentreUniversity of British ColumbiaVancouverCanada
  3. 3.Department of Cellular and Physiological SciencesUniversity of British ColumbiaVancouverCanada

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