Psychopharmacology

, Volume 231, Issue 12, pp 2417–2433

History of childhood adversity is positively associated with ventral striatal dopamine responses to amphetamine

  • Lynn M. Oswald
  • Gary S. Wand
  • Hiroto Kuwabara
  • Dean F. Wong
  • Shijun Zhu
  • James R. Brasic
Original Investigation

Abstract

Rationale

Childhood exposure to severe or chronic trauma is an important risk factor for the later development of adult mental health problems, such as substance abuse. Even in nonclinical samples of healthy adults, persons with a history of significant childhood adversity seem to experience greater psychological distress than those without this history. Evidence from rodent studies suggests that early life stress may impair dopamine function in ways that increase risks for drug abuse. However, the degree to which these findings translate to other species remains unclear.

Objectives

This study was conducted to examine associations between childhood adversity and dopamine and subjective responses to amphetamine in humans.

Methods

Following intake assessment, 28 healthy male and female adults, aged 18–29 years, underwent two consecutive 90-min positron emission tomography studies with high specific activity [11C]raclopride. The first scan was preceded by intravenous saline; the second by amphetamine (AMPH 0.3 mg/kg).

Results

Consistent with prior literature, findings showed positive associations between childhood trauma and current levels of perceived stress. Moreover, greater number of traumatic events and higher levels of perceived stress were each associated with higher ventral striatal dopamine responses to AMPH. Findings of mediation analyses further showed that a portion of the relationship between childhood trauma and dopamine release may be mediated by perceived stress.

Conclusions

Overall, results are consistent with preclinical findings suggesting that early trauma may lead to enhanced sensitivity to psychostimulants and that this mechanism may underlie increased vulnerability for drug abuse.

Keywords

Dopamine Positron emission tomography (PET) Human Amphetamine Childhood adversity Stress 

References

  1. Abi-Dargham A, Kegeles LS, Martinez D, Innis RB, Laruelle M (2003) Dopamine mediation of positive reinforcing effects of amphetamine in stimulant naive healthy volunteers: results from a large cohort. Eur Neuropsychopharmacol 13:459–468PubMedGoogle Scholar
  2. Allen MT, Bocek CM, Burch AE (2011) Gender differences and the relationships of perceived background stress and psychological distress with cardiovascular responses to laboratory stressors. Int J Psychophysiol 81:209–217. doi:10.1016/j.ijpsycho.2011.06.013 PubMedGoogle Scholar
  3. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders., Washington DC.Google Scholar
  4. Andreou E, Alexopoulos EC, Lionis C, Varvogli L, Gnardellis C, Chrousos GP, Darviri C (2011) Perceived Stress Scale: reliability and validity study in Greece. Int J Environ Res Public Health 8:3287–3298. doi:10.3390/ijerph8083287 PubMedCentralPubMedGoogle Scholar
  5. Ashburner J, Friston KJ (2003) Rigid body registration. In: Frackowiak RSJ, Friston KJ, Frith C, Dolan R, Price CJ, Zeki S, Ashburner J, Penny WD (eds) Human Brain Function. Academic, San Diego, pp. 635–654Google Scholar
  6. Back SE, Hartwell K, DeSantis SM, Saladin M, McRae-Clark AL, Price KL, Moran-Santa Maria MM, Baker NL, Spratt E, Kreek MJ, Brady KT (2010) Reactivity to laboratory stress provocation predicts relapse to cocaine. Drug Alcohol Depend 106:21-–27. doi:10.1016/j.drugalcdep.2009.07.016 PubMedCentralPubMedGoogle Scholar
  7. Back SE, Brady KT, Waldrop AE, Yeatts SD, McRae AL, Spratt E (2008) Early life trauma and sensitivity to current life stressors in individuals with and without cocaine dependence. Am J Drug Alcohol Abuse 34:389–396. doi:10.1080/00952990802122614 PubMedCentralPubMedGoogle Scholar
  8. Baron RM, Kenny DA (1986) The moderator–mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol 51:1173–1182PubMedGoogle Scholar
  9. Baumann B, Danos P, Krell D, Diekmann S, Leschinger A, Stauch R, Wurthmann C, Bernstein HG, Bogerts B (1999) Reduced volume of limbic system-affiliated basal ganglia in mood disorders: preliminary data from a postmortem study. J Neuropsychiatry Clin Neurosci 11:71–78PubMedGoogle Scholar
  10. Beck AT, Steer RA, Brown GK (1996) BDI-II: Beck Depression Inventory. Psychological Corp, San AntonioGoogle Scholar
  11. Belujon P, Grace AA (2011) Hippocampus, amygdala, and stress: interacting systems that affect susceptibility to addiction. Ann N Y Acad Sci 1216:114–121. doi:10.1111/j.1749-6632.2010.05896.x PubMedCentralPubMedGoogle Scholar
  12. Benjet C, Borges G, Medina-Mora ME (2010) Chronic childhood adversity and onset of psychopathology during three life stages: childhood, adolescence and adulthood. J Psychiatr Res 44:732–740. doi:10.1016/j.jpsychires.2010.01.004 PubMedGoogle Scholar
  13. Bonci A, Bernardi G, Grillner P, Mercuri NB (2003) The dopamine-containing neuron: maestro or simple musician in the orchestra of addiction? Trends Pharmacol Sci 24:172–177. doi:10.1016/S0165-6147(03)00068-3 PubMedGoogle Scholar
  14. Brake WG, Zhang TY, Diorio J, Meaney MJ, Gratton A (2004) Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. Eur J Neurosci 19:1863–1874. doi:10.1111/j.1460-9568.2004.03286.x PubMedGoogle Scholar
  15. Breese GR, Sinha R, Heilig M (2011) Chronic alcohol neuroadaptation and stress contribute to susceptibility for alcohol craving and relapse. Pharmacol Ther 129:149–171. doi:10.1016/j.pharmthera.2010.09.007 PubMedCentralPubMedGoogle Scholar
  16. Bremner JD, Bolus R, Mayer EA (2007) Psychometric properties of the Early Trauma Inventory-Self Report. J Nerv Ment Dis 195:211–218. doi:10.1097/01.nmd.0000243824.84651.6c PubMedCentralPubMedGoogle Scholar
  17. Burgermeister D (2007) Childhood adversity: a review of measurement instruments. J Nurs Meas 15:163–176PubMedGoogle Scholar
  18. Cagampang FR, Poore KR, Hanson MA (2011) Developmental origins of the metabolic syndrome: body clocks and stress responses. Brain Behav Immun 25:214–220. doi:10.1016/j.bbi.2010.09.005 PubMedGoogle Scholar
  19. Carswell K, Chen Y, Nair RC, Shaw AK, Speechley KN, Barrera M, Maunsell E (2008) Smoking and binge drinking among Canadian survivors of childhood and adolescent cancers: a comparative, population-based study. Pediatr Blood Cancer 51:280–287. doi:10.1002/pbc.21568 PubMedGoogle Scholar
  20. Cervenka S, Halldin C, Farde L (2008) Age-related diurnal effect on D2 receptor binding: a preliminary PET study. Int J Neuropsychopharmacol 11:671–678. doi:10.1017/S1461145707008358 PubMedGoogle Scholar
  21. Chocyk A, Przyborowska A, Dudys D, Majcher I, Mackowiak M, Wedzony K (2011) The impact of maternal separation on the number of tyrosine hydroxylase-expressing midbrain neurons during different stages of ontogenesis. Neuroscience 182:43–61. doi:10.1016/j. neuroscience .2011.03.008 PubMedGoogle Scholar
  22. Choy KH, de Visser YP, van den Buuse M (2009) The effect of ‘two hit’ neonatal and young-adult stress on dopaminergic modulation of prepulse inhibition and dopamine receptor density. Br J Pharmacol 156:388–396. doi:10.1111/j.1476-5381.2008.00008.x PubMedCentralPubMedGoogle Scholar
  23. Chu DA, Williams LM, Harris AW, Bryant RA, Gatt JM (2013) Early life trauma predicts self-reported levels of depressive and anxiety symptoms in nonclinical community adults: relative contributions of early life stressor types and adult trauma exposure. J Psychiatr Res 47:23–32. doi:10.1016/j.jpsychires.2012.08.006 PubMedGoogle Scholar
  24. Cohen S (1994) Perceived stress scale. Mind Garden, Palo Alto, CAGoogle Scholar
  25. Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24:385–396PubMedGoogle Scholar
  26. Cole G, Tucker L, Friedman GM (1990) Relationships among measures of alcohol drinking behavior, life-events and perceived stress. Psychol Rep 67:587–591PubMedGoogle Scholar
  27. Corbin WR, Farmer NM, Nolen-Hoekesma S (2013) Relations among stress, coping strategies, coping motives, alcohol consumption and related problems: a mediated moderation model. Addict Behav 38:1912–1919. doi:10.1016/j.addbeh.2012.12.005 PubMedGoogle Scholar
  28. Cuadra G, Zurita A, Gioino G, Molina V (2001) Influence of different antidepressant drugs on the effect of chronic variable stress on restraint-induced dopamine release in frontal cortex. Neuropsychopharmacology 25:384–394. doi:10.1016/S0893-133X(01)00234-2 PubMedGoogle Scholar
  29. Cuijpers P, Smit F, Unger F, Stikkelbroek Y, Ten Have M, de Graaf R (2011) The disease burden of childhood adversities in adults: a population-based study. Child Abuse Negl 35:937–945. doi:10.1016/j.chiabu.2011.06.005 PubMedGoogle Scholar
  30. Czoty PW, Riddick NV, Gage HD, Sandridge M, Nader SH, Garg S, Bounds M, Garg PK, Nader MA (2009) Effect of menstrual cycle phase on dopamine D2 receptor availability in female cynomolgus monkeys. Neuropsychopharmacology 34:548–554. doi:10.1038/npp.2008.3 PubMedGoogle Scholar
  31. D’Andrea W, Ford J, Stolbach B, Spinazzola J, van der Kolk BA (2012) Understanding interpersonal trauma in children: why we need a developmentally appropriate trauma diagnosis. Am J Orthopsychiatry 82:187–200. doi:10.1111/j.1939-0025.2012.01154.x PubMedGoogle Scholar
  32. Das D, Cherbuin N, Tan X, Anstey KJ, Easteal S (2011) DRD4-exonIII-VNTR moderates the effect of childhood adversities on emotional resilience in young-adults. PLoS One 6:e20177. doi:10.1371/journal.pone.0020177 PubMedCentralPubMedGoogle Scholar
  33. Del Arco A, Segovia G, Mora F (2001) Dopamine release during stress in the prefrontal cortex of the rat decreases with age. Neuroreport 12:4019–4022PubMedGoogle Scholar
  34. DeWit DJ, MacDonald K, Offord DR (1999) Childhood stress and symptoms of drug dependence in adolescence and early adulthood: social phobia as a mediator. Am J Orthopsychiatry 69:61–72PubMedGoogle Scholar
  35. Di Chiara G, Bassareo V, Fenu S, De Luca MA, Spina L, Cadoni C, Acquas E, Carboni E, Valentini V, Lecca D (2004) Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47(Suppl 1):227–241. doi:10.1016/j.neuropharm.2004.06.032 PubMedGoogle Scholar
  36. Dillon DG, Holmes AJ, Birk JL, Brooks N, Lyons-Ruth K, Pizzagalli DA (2009) Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood. Biol Psychiatry 66:206–213. doi:10.1016/j.biopsych.2009.02.019 PubMedCentralPubMedGoogle Scholar
  37. Douglas KR, Chan G, Gelernter J, Arias AJ, Anton RF, Weiss RD, Brady K, Poling J, Farrer L, Kranzler HR (2010) Adverse childhood events as risk factors for substance dependence: partial mediation by mood and anxiety disorders. Addict Behav 35:7–13. doi:10.1016/j.addbeh.2009.07.004 PubMedCentralPubMedGoogle Scholar
  38. Doyon WM, York JL, Diaz LM, Samson HH, Czachowski CL, Gonzales RA (2003) Dopamine activity in the nucleus accumbens during consummatory phases of oral ethanol self-administration. Alcohol Clin Exp Res 27:1573–1582. doi:10.1097/01.ALC.0000089959.66222.B8 PubMedGoogle Scholar
  39. Drevets WC, Gautier C, Price JC, Kupfer DJ, Kinahan PE, Grace AA, Price JL, Mathis CA (2001) Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria. Biol Psychiatry 49:81–96PubMedGoogle Scholar
  40. Edwards VJ, Holden GW, Felitti VJ, Anda RF (2003) Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: results from the adverse childhood experiences study. Am J Psychiatry 160:1453–1460PubMedGoogle Scholar
  41. Ehrin E, Farde L, de Paulis T, Eriksson L, Greitz T, Johnstrom P, Litton JE, Nilsson JL, Sedvall G, Stone-Elander S (1985) Preparation of 11C-labelled Raclopride, a new potent dopamine receptor antagonist: preliminary PET studies of cerebral dopamine receptors in the monkey. Int J Appl Radiat Isot 36:269–273PubMedGoogle Scholar
  42. Enoch MA (2011) The role of early life stress as a predictor for alcohol and drug dependence. Psychopharmacology (Berl) 214:17–31. doi:10.1007/s00213-010-1916-6 Google Scholar
  43. Erb S, Shaham Y, Stewart J (1996) Stress reinstates cocaine-seeking behavior after prolonged extinction and a drug-free period. Psychopharmacol(Berl) 128:408–412Google Scholar
  44. Evans SM (2007) The role of estradiol and progesterone in modulating the subjective effects of stimulants in humans. Exp Clin Psychopharmacol 15:418–426. doi:10.1037/1064-1297.15.5.418 PubMedGoogle Scholar
  45. Everitt BJ, Robbins TW (2013) From the ventral to the dorsal striatum: devolving views of their roles in drug addiction. Neurosci Biobehav Rev. doi:10.1016/j.neubiorev.2013.02.010 PubMedGoogle Scholar
  46. Felitti VJ, Anda RF, Nordenberg D, Williamson DF, Spitz AM, Edwards V, Koss MP, Marks JS (1998) Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. Am J Prev Med 14:245–258PubMedGoogle Scholar
  47. Festa ED, Russo SJ, Gazi FM, Niyomchai T, Kemen LM, Lin SN, Foltz R, Jenab S, Quinones-Jenab V (2004) Sex differences in cocaine-induced behavioral responses, pharmacokinetics, and monoamine levels. Neuropharmacology 46:672–687. doi:10.1016/j.neuropharm.2003.11.017 PubMedGoogle Scholar
  48. Finkelhor D, Ormrod RK, Turner HA (2007) Poly-victimization: a neglected component in child victimization. Child Abuse Negl 31:7–26. doi:10.1016/j.chiabu.2006.06.008 PubMedGoogle Scholar
  49. First MB, Spitzer RL, Gibbon M, Williams JBW (2002) Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-patient Edition. Biometrics Research, New York State Psychiatric Institute, New YorkGoogle Scholar
  50. Fishbein D, Novak SP, Krebs C, Warner T, Hammond J (2011) The mediating effect of depressive symptoms on the relationship between traumatic childhood experiences and drug use initiation. Addict Behav 36:527–531. doi:10.1016/j.addbeh.2010.12.030 PubMedCentralPubMedGoogle Scholar
  51. Ford JD, Elhai JD, Connor DF, Frueh BC (2010) Poly-victimization and risk of posttraumatic, depressive, and substance use disorders and involvement in delinquency in a national sample of adolescents. J Adolesc Health 46:545–552. doi:10.1016/j.jadohealth.2009.11.212 PubMedGoogle Scholar
  52. Fulford AJ, Marsden CA (1998) Effect of isolation-rearing on conditioned dopamine release in vivo in the nucleus accumbens of the rat. J Neurochem 70:384–390PubMedGoogle Scholar
  53. Gabbay FH (2005) Family history of alcoholism and response to amphetamine: sex differences in the effect of risk. Alcohol Clin Exp Res 29:773–780PubMedGoogle Scholar
  54. Gjedde A, Kumakura Y, Cumming P, Linnet J, Moller A (2010) Inverted-U-shaped correlation between dopamine receptor availability in striatum and sensation seeking. Proc Natl Acad Sci U S A 107:3870–3875. doi:10.1073/pnas.0912319107 PubMedCentralPubMedGoogle Scholar
  55. Glaser JP, van Os J, Portegijs PJ, Myin-Germeys I (2006) Childhood trauma and emotional reactivity to daily life stress in adult frequent attenders of general practitioners. J Psychosom Res 61:229–236. doi:10.1016/j.jpsychores.2006.04.014 PubMedGoogle Scholar
  56. Gordon HW (2002) Early environmental stress and biological vulnerability to drug abuse. Psychoneuroendocrinology 27:115–126PubMedGoogle Scholar
  57. Gustafsson L, Ploj K, Nylander I (2005) Effects of maternal separation on voluntary ethanol intake and brain peptide systems in female Wistar rats. Pharmacol Biochem Behav 81:506–516. doi:10.1016/j.pbb.2005.03.016 PubMedGoogle Scholar
  58. Hall FS, Wilkinson LS, Humby T, Robbins TW (1999) Maternal deprivation of neonatal rats produces enduring changes in dopamine function. Synapse 32:37–43PubMedGoogle Scholar
  59. Hamburger ME, Leeb RT, Swahn MH (2008) Childhood maltreatment and early alcohol use among high-risk adolescents. J Stud Alcohol Drugs 69:291–295PubMedGoogle Scholar
  60. Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom KO (1991) The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict 86:1119–1127PubMedGoogle Scholar
  61. Heffner JL, Blom TJ, Anthenelli RM (2011) Gender differences in trauma history and symptoms as predictors of relapse to alcohol and drug use. Am J Addict 20:307–311. doi:10.1111/j.1521-0391.2011.00141.x PubMedCentralPubMedGoogle Scholar
  62. Heim C, Binder EB (2012) Current research trends in early life stress and depression: review of human studies on sensitive periods, gene–environment interactions, and epigenetics. Exp Neurol 233:102–111. doi:10.1016/j.expneurol.2011.10.032 PubMedGoogle Scholar
  63. Huang S, Trapido E, Fleming L, Arheart K, Crandall L, French M, Malcolm S, Prado G (2011) The long-term effects of childhood maltreatment experiences on subsequent illicit drug use and drug-related problems in young adulthood. Addict Behav 36:95–102. doi:10.1016/j.addbeh.2010.09.001 PubMedCentralPubMedGoogle Scholar
  64. Husted JA, Ahmed R, Chow EW, Brzustowicz LM, Bassett AS (2012) Early environmental exposures influence schizophrenia expression even in the presence of strong genetic predisposition. Schizophr Res 137:166–168. doi:10.1016/j.schres.2012.02.009 PubMedCentralPubMedGoogle Scholar
  65. Hyman SM, Paliwal P, Sinha R (2007) Childhood maltreatment, perceived stress, and stress-related coping in recently abstinent cocaine dependent adults. Psychol Addict Behav 21:233–238. doi:10.1037/0893-164X.21.2.233 PubMedCentralPubMedGoogle Scholar
  66. Innis RB, Cunningham VJ, Delforge J, Fujita M, Gjedde A, Gunn RN, Holden J, Houle S, Huang SC, Ichise M, Iida H, Ito H, Kimura Y, Koeppe RA, Knudsen GM, Knuuti J, Lammertsma AA, Laruelle M, Logan J, Maguire RP, Mintun MA, Morris ED, Parsey R, Price JC, Slifstein M, Sossi V, Suhara T, Votaw JR, Wong DF, Carson RE (2007) Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab 27:1533–1539. doi:10.1038/sj.jcbfm.9600493 PubMedGoogle Scholar
  67. Innis RB, Malison RT, al-Tikriti M, Hoffer PB, Sybirska EH, Seibyl JP, Zoghbi SS, Baldwin RM, Laruelle M, Smith EO (1992) Amphetamine-stimulated dopamine release competes in vivo for [123I]IBZM binding to the D2 receptor in nonhuman primates. Synapse 10:177–184. doi:10.1002/syn.890100302 PubMedGoogle Scholar
  68. Inoue M, Suhara T, Sudo Y, Okubo Y, Yasuno F, Kishimoto T, Yoshikawa K, Tanada S (2001) Age-related reduction of extrastriatal dopamine D2 receptor measured by PET. Life Sci 69:1079–1084PubMedGoogle Scholar
  69. Jahng JW, Ryu V, Yoo SB, Noh SJ, Kim JY, Lee JH (2010) Mesolimbic dopaminergic activity responding to acute stress is blunted in adolescent rats that experienced neonatal maternal separation. Neuroscience 171:144–152. doi:10.1016/j. neuroscience .2010.08.063 PubMedGoogle Scholar
  70. 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. Psychopharmacol (Berl) 181:8–15. doi:10.1007/s00213-005-2232-4 Google Scholar
  71. Kaplan MS (2013) Acute alcohol consumption as a contributing factor to suicidal behavior. Am J Public Health 103:e2–3. doi:10.2105/AJPH.2013.301422 PubMedGoogle Scholar
  72. Karlsgodt KH, Lukas SE, Elman I (2003) Psychosocial stress and the duration of cocaine use in non-treatment seeking individuals with cocaine dependence. Am J Drug Alcohol Abuse 29:539–551PubMedGoogle Scholar
  73. Kendler KS, Kuhn JW, Prescott CA (2004) Childhood sexual abuse, stressful life events and risk for major depression in women. Psychol Med 34:1475–1482PubMedGoogle Scholar
  74. Kendler KS, Sheth K, Gardner CO, Prescott CA (2002) Childhood parental loss and risk for first-onset of major depression and alcohol dependence: the time-decay of risk and sex differences. Psychol Med 32:1187–1194PubMedGoogle Scholar
  75. Kendler KS, Bulik CM, Silberg J, Hettema JM, Myers J, Prescott CA (2000) Childhood sexual abuse and adult psychiatric and substance use disorders in women: an epidemiological and cotwin control analysis. Arch Gen Psychiatry 57:953–959PubMedGoogle Scholar
  76. Kerr T, Stoltz JA, Marshall BD, Lai C, Strathdee SA, Wood E (2009) Childhood trauma and injection drug use among high-risk youth. J Adolesc Health 45:300–302. doi:10.1016/j.jadohealth.2009.03.007 PubMedCentralPubMedGoogle Scholar
  77. Kessler RC, McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM, Aguilar-Gaxiola S, Alhamzawi AO, Alonso J, Angermeyer M, Benjet C, Bromet E, Chatterji S, de Girolamo G, Demyttenaere K, Fayyad J, Florescu S, Gal G, Gureje O, Haro JM, Hu CY, Karam EG, Kawakami N, Lee S, Lepine JP, Ormel J, Posada-Villa J, Sagar R, Tsang A, Ustun TB, Vassilev S, Viana MC, Williams DR (2010) Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br J Psychiatry 197:378–385. doi:10.1192/bjp.bp.110.080499 PubMedCentralPubMedGoogle Scholar
  78. Kim-Cohen J, Turkewitz R (2012) Resilience and measured gene–environment interactions. Dev Psychopathol 24:1297–1306. doi:10.1017/S0954579412000715 PubMedGoogle Scholar
  79. Kirschbaum C, Pirke KM, Hellhammer DH (1993) The ‘Trier Social Stress Test’—a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28:76–81PubMedGoogle Scholar
  80. Koob GF (2003) Alcoholism: allostasis and beyond. Alcohol Clin Exp Res 27:232–243. doi:10.1097/01.ALC.0000057122.36127.C2 PubMedGoogle Scholar
  81. Kosten TA, Zhang XY, Kehoe P (2006) Heightened cocaine and food self-administration in female rats with neonatal isolation experience. Neuropsychopharmacology 31:70–76. doi:10.1038/sj.npp.1300779 PubMedGoogle Scholar
  82. Kosten TA, Zhang XY, Kehoe P (2005) Neurochemical and behavioral responses to cocaine in adult male rats with neonatal isolation experience. J Pharmacol Exp Ther 314:661–667. doi:10.1124/jpet.104.081216 PubMedGoogle Scholar
  83. Kosten TA, Zhang XY, Kehoe P (2003) Chronic neonatal isolation stress enhances cocaine-induced increases in ventral striatal dopamine levels in rat pups. Brain Res Dev Brain Res 141:109–116PubMedGoogle Scholar
  84. Kosten TA, Ambrosio E (2002) HPA axis function and drug addictive behaviors: insights from studies with Lewis and Fischer 344 inbred rats. Psychoneuroendocrinology 27:35–69PubMedGoogle Scholar
  85. 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. doi:10.1038/nn1583 PubMedGoogle Scholar
  86. Kumar A, Kuwabara H, Rousset O, Alexander M, Brasic J, Ye W, Wong D (2007) Effects of head-motion correction and modeling approaches on SPM analyses. J Nucl Med 48(41)Google Scholar
  87. Lataster J, Collip D, Ceccarini J, Haas D, Booij L, van Os J, Pruessner J, Van Laere K, Myin-Germeys I (2011) Psychosocial stress is associated with in vivo dopamine release in human ventromedial prefrontal cortex: a positron emission tomography study using [(1)(8)F]fallypride. Neuroimage 58:1081–1089. doi:10.1016/j. neuroimage .2011.07.030 PubMedGoogle Scholar
  88. Laudet AB, Magura S, Vogel HS, Knight EL (2004) Perceived reasons for substance misuse among persons with a psychiatric disorder. Am J Orthopsychiatry 74:365–375. doi:10.1037/0002-9432.74.3.365 PubMedCentralPubMedGoogle Scholar
  89. Leyton M, Boileau I, Benkelfat C, Diksic M, Baker G, Dagher A (2002) Amphetamine-induced increases in extracellular dopamine, drug wanting, and novelty seeking: a PET/[11C]raclopride study in healthy men. Neuropsychopharmacology 27:1027–1035. doi:10.1016/S0893-133X(02)00366-4 PubMedGoogle Scholar
  90. Logan J, Fowler JS, Volkow ND, Wang GJ, Ding YS, Alexoff DL (1996) Distribution volume ratios without blood sampling from graphical analysis of PET data. J Cereb Blood Flow Metab 16:834–840. doi:10.1097/00004647-199609000-00008 PubMedGoogle Scholar
  91. Lovic V, Belay H, Walker CD, Burton CL, Meaney MJ, Sokolowski M, Fleming AS (2013) Early postnatal experience and DRD2 genotype affect dopamine receptor expression in the rat ventral striatum. Behav Brain Res 237:278–282. doi:10.1016/j.bbr.2012.09.046 PubMedGoogle Scholar
  92. Lu L, Shepard JD, Hall FS, Shaham Y (2003) Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 27:457–491PubMedGoogle Scholar
  93. MacKinnon DP (2008) Introduction to statistical mediation analysis. Routledge Academic, New YorkGoogle Scholar
  94. Mackinnon DP, Lockwood CM, Williams J (2004) Confidence limits for the indirect effect: distribution of the product and resampling methods. Multivariate Behav Res 39:99. doi:10.1207/s15327906mbr3901_4 PubMedCentralPubMedGoogle Scholar
  95. MacKinnon DP, Lockwood CM, Hoffman JM, West SG, Sheets V (2002) A comparison of methods to test mediation and other intervening variable effects. Psychol Methods 7:83–104PubMedCentralPubMedGoogle Scholar
  96. Mangiavacchi S, Masi F, Scheggi S, Leggio B, De Montis MG, Gambarana C (2001) Long-term behavioral and neurochemical effects of chronic stress exposure in rats. J Neurochem 79:1113–1121PubMedGoogle Scholar
  97. Marinelli M, Piazza PV (2002) Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur J Neurosci 16:387–394PubMedGoogle Scholar
  98. Martinez D, Slifstein M, Broft A, Mawlawi O, Hwang DR, Huang Y, Cooper T, Kegeles L, Zarahn E, Abi-Dargham A, Haber SN, Laruelle M (2003) Imaging human mesolimbic dopamine transmission with positron emission tomography. Part II: amphetamine-induced dopamine release in the functional subdivisions of the striatum. J Cereb Blood Flow Metab 23:285–300PubMedGoogle Scholar
  99. Marx BP, Sloan DM (2003) The effects of trauma history, gender, and race on alcohol use and posttraumatic stress symptoms in a college student sample. Addict Behav 28:1631–1647PubMedGoogle Scholar
  100. Matheson SL, Shepherd AM, Pinchbeck RM, Laurens KR, Carr VJ (2012) Childhood adversity in schizophrenia: a systematic meta-analysis. Psychol Med 30:1–13. doi:10.1017/S0033291712000785 Google Scholar
  101. Matthews KA, Gump BB, Owens JF (2001) Chronic stress influences cardiovascular and neuroendocrine responses during acute stress and recovery, especially in men. Health Psychol 20:403–410PubMedGoogle Scholar
  102. McArthur S, McHale E, Gillies GE (2007) The size and distribution of midbrain dopaminergic populations are permanently altered by perinatal glucocorticoid exposure in a sex- region- and time-specific manner. Neuropsychopharmacology 32:1462–1476. doi:10.1038/sj.npp.1301277 PubMedGoogle Scholar
  103. McFarlane A, Clark CR, Bryant RA, Williams LM, Niaura R, Paul RH, Hitsman BL, Stroud L, Alexander DM, Gordon E (2005) The impact of early life stress on psychophysiological, personality and behavioral measures in 740 non-clinical subjects. J Integr Neurosci 4:27–40PubMedGoogle Scholar
  104. McGinty VB, Lardeux S, Taha SA, Kim JJ, Nicola SM (2013) Invigoration of reward seeking by cue and proximity encoding in the nucleus accumbens. Neuron 78:910–922. doi:10.1016/j. neuron .2013.04.010 PubMedGoogle Scholar
  105. Meaney MJ, Brake W, Gratton A (2002) Environmental regulation of the development of mesolimbic dopamine systems: a neurobiological mechanism for vulnerability to drug abuse? Psychoneuroendocrinology 27:127–138PubMedGoogle Scholar
  106. Medrano MA, Hatch JP, Zule WA, Desmond DP (2002) Psychological distress in childhood trauma survivors who abuse drugs. Am J Drug Alcohol Abuse 28:1–13PubMedGoogle Scholar
  107. Mehta MA (2010) Hyporesponsive reward anticipation in the basal ganglia following severe institutional deprivation early in life. J Cogn Neurosci 22:2316. doi:10.1162/jocn.2009.21394 PubMedGoogle Scholar
  108. Miczek KA, Nikulina EM, Shimamoto A, Covington HE 3rd (2011) Escalated or suppressed cocaine reward, tegmental BDNF, and accumbal dopamine caused by episodic versus continuous social stress in rats. J Neurosci 31:9848–9857. doi:10.1523/JNEUROSCI.0637-11.2011 PubMedCentralPubMedGoogle Scholar
  109. Min M, Farkas K, Minnes S, Singer LT (2007) Impact of childhood abuse and neglect on substance abuse and psychological distress in adulthood. J Trauma Stress 20:833–844. doi:10.1002/jts.20250 PubMedGoogle Scholar
  110. Miura H, Qiao H, Ohta T (2002) Attenuating effects of the isolated rearing condition on increased brain serotonin and dopamine turnover elicited by novelty stress. Brain Res 926:10–17PubMedGoogle Scholar
  111. Moffett MC, Vicentic A, Kozel M, Plotsky P, Francis DD, Kuhar MJ (2007) Maternal separation alters drug intake patterns in adulthood in rats. Biochem Pharmacol 73:321–330. doi:10.1016/j.bcp.2006.08.003 PubMedCentralPubMedGoogle Scholar
  112. Moffett MC, Harley J, Francis D, Sanghani SP, Davis WI, Kuhar MJ (2006) Maternal separation and handling affects cocaine self-administration in both the treated pups as adults and the dams. J Pharmacol Exp Ther 317:1210–1218. doi:10.1124/jpet.106.101139 PubMedGoogle Scholar
  113. Montgomery AJ (2006) Correction of head movement on PET studies: comparison of methods. J Nucl Med 47:1936PubMedGoogle Scholar
  114. Montgomery AJ, Mehta MA, Grasby PM (2006) Is psychological stress in man associated with increased striatal dopamine levels?: A [11C]raclopride PET study. Synapse 60:124–131. doi:10.1002/syn.20282 PubMedGoogle Scholar
  115. Munro CA, McCaul ME, Wong DF, Oswald LM, Zhou Y, Brasic J, Kuwabara H, Kumar A, Alexander M, Ye W, Wand GS (2006) Sex differences in striatal dopamine release in healthy adults. Biol Psychiatry 59:966–974. doi:10.1016/j.biopsych.2006.01.008 PubMedGoogle Scholar
  116. Nakajima M, al’Absi M (2012) Predictors of risk for smoking relapse in men and women: a prospective examination. Psychol Addict Behav 26:633–637. doi:10.1037/a0027280 PubMedCentralPubMedGoogle Scholar
  117. Nanni V, Uher R, Danese A (2012) Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: a meta-analysis. Am J Psychiatry 169:141–151PubMedGoogle Scholar
  118. Nazarian A, Sun WL, Zhou L, Kemen LM, Jenab S, Quinones-Jenab V (2009) Sex differences in basal and cocaine-induced alterations in PKA and CREB proteins in the nucleus accumbens. Psychopharmacology (Berl) 203:641–650. doi:10.1007/s00213-008-1411-5 Google Scholar
  119. Nelson EC, Heath AC, Madden PA, Cooper ML, Dinwiddie SH, Bucholz KK, Glowinski A, McLaughlin T, Dunne MP, Statham DJ, Martin NG (2002) Association between self-reported childhood sexual abuse and adverse psychosocial outcomes: results from a twin study. Arch Gen Psychiatry 59:139–145PubMedGoogle Scholar
  120. Niwa M, Jaaro-Peled H, Tankou S, Seshadri S, Hikida T, Matsumoto Y, Cascella NG, Kano S, Ozaki N, Nabeshima T, Sawa A (2013) Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. Science 339:335–339. doi:10.1126/science.1226931 PubMedCentralPubMedGoogle Scholar
  121. Oswald LM, Wong DF, McCaul M, Zhou Y, Kuwabara H, Choi L, Brasic J, Wand GS (2005) Relationships among ventral striatal dopamine release, cortisol secretion, and subjective responses to amphetamine. Neuropsychopharmacology 30:821–832. doi:10.1038/sj.npp.1300667 PubMedGoogle Scholar
  122. Piazza PV, Le Moal ML (1996) Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids, and dopaminergic neurons. Annu Rev Pharmacol Toxicol 36:359–378. doi:10.1146/annurev.pa.36.040196.002043 PubMedGoogle Scholar
  123. Pierrehumbert B, Torrisi R, Glatz N, Dimitrova N, Heinrichs M, Halfon O (2009) The influence of attachment on perceived stress and cortisol response to acute stress in women sexually abused in childhood or adolescence. Psychoneuroendocrinology 34:924–938. doi:10.1016/j.psyneuen.2009.01.006 PubMedGoogle Scholar
  124. Pilowsky DJ, Keyes KM, Hasin DS (2009) Adverse childhood events and lifetime alcohol dependence. Am J Public Health 99:258–263. doi:10.2105/AJPH.2008.139006 PubMedCentralPubMedGoogle Scholar
  125. Plaza A, Torres A, Martin-Santos R, Gelabert E, Imaz ML, Navarro P, Bremner JD, Valdes M, Garcia-Esteve L (2011) Validation and test-retest reliability of Early Trauma Inventory in Spanish postpartum women. J Nerv Ment Dis 199:280–285. doi:10.1097/NMD.0b013e31821245b9 PubMedCentralPubMedGoogle Scholar
  126. 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 121:787–799PubMedGoogle Scholar
  127. Pruessner JC, Champagne F, Meaney MJ, Dagher A (2004) Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. J Neurosci 24:2825–2831. doi:10.1523/JNEUROSCI.3422-03.2004 PubMedGoogle Scholar
  128. Rahmim A, Cheng JC, Blinder S, Camborde ML, Sossi V (2005) Statistical dynamic image reconstruction in state-of-the-art high-resolution PET. Phys Med Biol 50:4887–4912. doi:10.1088/0031-9155/50/20/010 PubMedGoogle Scholar
  129. Robison AJ, Vialou V, Mazei-Robison M, Feng J, Kourrich S, Collins M, Wee S, Koob G, Turecki G, Neve R, Thomas M, Nestler EJ (2013) Behavioral and structural responses to chronic cocaine require a feedforward loop involving DeltaFosB and calcium/calmodulin-dependent protein kinase II in the nucleus accumbens shell. J Neurosci 33:4295–4307. doi:10.1523/JNEUROSCI.5192-12.2013 PubMedCentralPubMedGoogle Scholar
  130. Rodrigues AJ, Leao P, Carvalho M, Almeida OF, Sousa N (2011) Potential programming of dopaminergic circuits by early life stress. Psychopharmacol (Berl) 214:107–120. doi:10.1007/s00213-010-2085-3 Google Scholar
  131. Roman E, Ploj K, Nylander I (2004) Maternal separation has no effect on voluntary ethanol intake in female Wistar rats. Alcohol 33:31–39. doi:10.1016/j.alcohol.2004.04.002 PubMedGoogle Scholar
  132. Rosa AM, Silva MF, Ferreira S, Murta J, Castelo-Branco M (2013) Plasticity in the human visual cortex: an ophthalmology-based perspective. Biomed Res Int 2013:568354. doi:10.1155/2013/568354 PubMedCentralGoogle Scholar
  133. Rothman EF, Edwards EM, Heeren T, Hingson RW (2008) Adverse childhood experiences predict earlier age of drinking onset: results from a representative US sample of current or former drinkers. Pediatrics 122:e298–304. doi:10.1542/peds.2007-3412 PubMedGoogle Scholar
  134. Rouge-Pont F, Piazza PV, Kharouby M, Le Moal M, Simon H (1993) Higher and longer stress-induced increase in dopamine concentrations in the nucleus accumbens of animals predisposed to amphetamine self-administration. A microdialysis study. Brain Res 602:169–174PubMedGoogle Scholar
  135. Saal D, Dong Y, Bonci A, Malenka RC (2003) Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37:577–582PubMedGoogle Scholar
  136. Samplin E, Ikuta T, Malhotra AK, Szeszko PR, Derosse P (2013) Sex differences in resilience to childhood maltreatment: effects of trauma history on hippocampal volume, general cognition and subclinical psychosis in healthy adults. J Psychiatr Res. doi:10.1016/j.jpsychires.2013.05.008 PubMedGoogle Scholar
  137. Sansone RA, Whitecar P, Wiederman MW (2009) The prevalence of childhood trauma among those seeking buprenorphine treatment. J Addict Dis 28:64–67. doi:10.1080/10550880802545101 PubMedGoogle Scholar
  138. Sesar K, Simic N, Barisic M (2010) Multi-type childhood abuse, strategies of coping, and psychological adaptations in young adults. Croat Med J 51:406–416PubMedCentralPubMedGoogle Scholar
  139. Shimamoto A, Debold JF, Holly EN, Miczek KA (2011) Blunted accumbal dopamine response to cocaine following chronic social stress in female rats: exploring a link between depression and drug abuse. Psychopharmacology (Berl) 218:271–279. doi:10.1007/s00213-011-2364-7 Google Scholar
  140. Shin SH, Miller DP, Teicher MH (2013) Exposure to childhood neglect and physical abuse and developmental trajectories of heavy episodic drinking from early adolescence into young adulthood. Drug Alcohol Depend 127:31–38. doi:10.1016/j.drugalcdep.2012.06.005 PubMedGoogle Scholar
  141. Shipley W, Gruber C, Martin T, Klein A (2009) Shipley-2. Western Psychological Services, Los AngelesGoogle Scholar
  142. Shrout PE, Bolger N (2002) Mediation in experimental and nonexperimental studies: new procedures and recommendations. Psychol Methods 7:422–445PubMedGoogle Scholar
  143. Simpson TL, Miller WR (2002) Concomitance between childhood sexual and physical abuse and substance use problems. A review. Clin Psychol Rev 22:27–77PubMedGoogle Scholar
  144. Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacol (Berl) 158:343–359. doi:10.1007/s002130100917 Google Scholar
  145. Sobell LC, Sobell MB (1992) Timeline followback: a technique for assessing self-reported alcohol consumption. In: Litten RZ, Allen J (eds) Measuring alcohol consumption: psychosocial and biological methods. Humana, Totowa, pp 41–72Google Scholar
  146. Soderpalm AH, de Wit H (2002) Effects of stress and alcohol on subjective state in humans. Alcohol Clin Exp Res 26:818–826PubMedGoogle Scholar
  147. Strine TW, Dube SR, Edwards VJ, Prehn AW, Rasmussen S, Wagenfeld M, Dhingra S, Croft JB (2012) Associations between adverse childhood experiences, psychological distress, and adult alcohol problems. Am J Health Behav 36:408–423. doi:10.5993/AJHB.36.3.11 PubMedGoogle Scholar
  148. Tian T, Qin W, Liu B, Jiang T, Yu C (2013) Functional connectivity in healthy subjects is nonlinearly modulated by the COMT and DRD2 polymorphisms in a functional system-dependent manner. J Neurosci 33:17519–17526. doi:10.1523/JNEUROSCI.2163-13.2013 PubMedGoogle Scholar
  149. Tidey JW, Miczek KA (1997) Acquisition of cocaine self-administration after social stress: role of accumbens dopamine. Psychopharmacol (Berl) 130:203–212Google Scholar
  150. Tidey JW, Miczek KA (1996) Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res 721:140–149PubMedGoogle Scholar
  151. Tonmyr L, Draca J, Crain J, Macmillan HL (2011) Measurement of emotional/psychological child maltreatment: a review. Child Abuse Negl 35:767–782. doi:10.1016/j.chiabu.2011.04.011 PubMedGoogle Scholar
  152. Tsukada H, Ohba H, Nishiyama S, Kakiuchi T (2011) Differential effects of stress on [(1)(1)C]raclopride and [(1)(1)C]MNPA binding to striatal D(2)/D(3) dopamine receptors: a PET study in conscious monkeys. Synapse 65:84–89. doi:10.1002/syn.20845 PubMedGoogle Scholar
  153. Tupala E, Hall H, Bergstrom K, Mantere T, Rasanen P, Sarkioja T, Hiltunen J, Tiihonen J (2003) Different effect of age on dopamine transporters in the dorsal and ventral striatum of controls and alcoholics. Synapse 48:205–211. doi:10.1002/syn.10206 PubMedGoogle Scholar
  154. Tyrka AR, Price LH, Marsit C, Walters OC, Carpenter LL (2012) Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS One 7:e30148. doi:10.1371/journal.pone.0030148 PubMedCentralPubMedGoogle Scholar
  155. Tyrka AR, Wier L, Price LH, Ross NS, Carpenter LL (2008) Childhood parental loss and adult psychopathology: effects of loss characteristics and contextual factors. Int J Psychiatry Med 38:329–344PubMedCentralPubMedGoogle Scholar
  156. Uhart M, Chong RY, Oswald L, Lin PI, Wand GS (2006) Gender differences in hypothalamic–pituitary–adrenal (HPA) axis reactivity. Psychoneuroendocrinology 31:642–652. doi:10.1016/j.psyneuen.2006.02.003 PubMedGoogle Scholar
  157. Urban NB, Kegeles LS, Slifstein M, Xu X, Martinez D, Sakr E, Castillo F, Moadel T, O’Malley SS, Krystal JH, Abi-Dargham A (2010) Sex differences in striatal dopamine release in young adults after oral alcohol challenge: a positron emission tomography imaging study with [(1)(1)C]raclopride. Biol Psychiatry 68:689–696. doi:10.1016/j.biopsych.2010.06.005 PubMedCentralPubMedGoogle Scholar
  158. Volkow ND, Wang GJ, Fowler JS, Thanos PP, Logan J, Gatley SJ, Gifford A, Ding YS, Wong C, Pappas N (2002) Brain DA D2 receptors predict reinforcing effects of stimulants in humans: replication study. Synapse 46:79–82. doi:10.1002/syn.10137 PubMedGoogle Scholar
  159. Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Gifford A, Hitzemann R, Ding YS, Pappas N (1999) Prediction of reinforcing responses to psychostimulants in humans by brain dopamine D2 receptor levels. Am J Psychiatry 156:1440–1443PubMedGoogle Scholar
  160. Waldrop AE, Back SE, Brady KT, Upadhyaya HP, McRae AL, Saladin ME (2007) Daily stressor sensitivity, abuse effects, and cocaine use in cocaine dependence. Addict Behav 32:3015–3025. doi:10.1016/j.addbeh.2007.07.006 PubMedCentralPubMedGoogle Scholar
  161. Walker QD, Ray R, Kuhn CM (2006) Sex differences in neurochemical effects of dopaminergic drugs in rat striatum. Neuropsychopharmacology 31:1193–1202. doi:10.1038/sj.npp.1300915 PubMedGoogle Scholar
  162. Wand GS, Oswald LM, McCaul ME, Wong DF, Johnson E, Zhou Y, Kuwabara H, Kumar A (2007) Association of amphetamine-induced striatal dopamine release and cortisol responses to psychological stress. Neuropsychopharmacology 32:2310–2320. doi:10.1038/sj.npp.1301373 PubMedGoogle Scholar
  163. Wang Z, Du J, Sun H, Wu H, Xiao Z, Zhao M (2010) Patterns of childhood trauma and psychological distress among injecting heroin users in China. PLoS One 5:e15882. doi:10.1371/journal.pone.0015882 PubMedCentralPubMedGoogle Scholar
  164. Weber K, Rockstroh B, Borgelt J, Awiszus B, Popov T, Hoffmann K, Schonauer K, Watzl H, Propster K (2008) Stress load during childhood affects psychopathology in psychiatric patients. BMC Psychiatry 8:63PubMedCentralPubMedGoogle Scholar
  165. White HR, Widom CS (2008) Three potential mediators of the effects of child abuse and neglect on adulthood substance use among women. J Stud Alcohol Drugs 69:337–347PubMedGoogle Scholar
  166. White TL, Justice AJ, de Wit H (2002) Differential subjective effects of D-amphetamine by gender, hormone levels and menstrual cycle phase. Pharmacol Biochem Behav 73:729–741PubMedGoogle Scholar
  167. Wise RA (1998) Drug-activation of brain reward pathways. Drug Alcohol Depend 51:13–22PubMedGoogle Scholar
  168. Wise RA (1996) Neurobiology of addiction. Curr Opin Neurobiol 6:243–251PubMedGoogle Scholar
  169. Womersley JS, Hsieh JH, Kellaway LA, Gerhardt GA, Russell VA (2011) Maternal separation affects dopamine transporter function in the spontaneously hypertensive rat: an in vivo electrochemical study. Behav Brain Funct 7:49. doi:10.1186/1744-9081-7-49 PubMedCentralPubMedGoogle Scholar
  170. Yavich L, Tiihonen J (2000) Ethanol modulates evoked dopamine release in mouse nucleus accumbens: dependence on social stress and dose. Eur J Pharmacol 401:365–373PubMedGoogle Scholar
  171. Yoder KK, Constantinescu CC, Kareken DA, Normandin MD, Cheng TE, O’Connor SJ, Morris ED (2007) Heterogeneous effects of alcohol on dopamine release in the striatum: a PET study. Alcohol Clin Exp Res 31:965–973. doi:10.1111/j.1530-0277.2007.00390.x PubMedGoogle Scholar
  172. Zhang XY, Sanchez H, Kehoe P, Kosten TA (2005) Neonatal isolation enhances maintenance but not reinstatement of cocaine self-administration in adult male rats. Psychopharmacol (Berl) 177:391–399. doi:10.1007/s00213-004-1963-y Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Lynn M. Oswald
    • 1
    • 2
  • Gary S. Wand
    • 2
    • 3
  • Hiroto Kuwabara
    • 4
  • Dean F. Wong
    • 3
    • 4
    • 5
    • 6
  • Shijun Zhu
    • 1
  • James R. Brasic
    • 4
  1. 1.Department of Family and Community HealthUniversity of Maryland School of NursingBaltimoreUSA
  2. 2.Department of MedicineThe Johns Hopkins University School of MedicineBaltimoreUSA
  3. 3.Department of Psychiatry and Behavioral SciencesThe Johns Hopkins University School of MedicineBaltimoreUSA
  4. 4.Department of RadiologyThe Johns Hopkins University School of MedicineBaltimoreUSA
  5. 5.Department of NeuroscienceThe Johns Hopkins University School of MedicineBaltimoreUSA
  6. 6.Department of Environmental Health SciencesThe Johns Hopkins University School of MedicineBaltimoreUSA

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