History of childhood adversity is positively associated with ventral striatal dopamine responses to amphetamine
- First Online:
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.
This study was conducted to examine associations between childhood adversity and dopamine and subjective responses to amphetamine in humans.
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).
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.
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.
KeywordsDopamine Positron emission tomography (PET) Human Amphetamine Childhood adversity Stress
- American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders., Washington DC.Google Scholar
- 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
- 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
- Beck AT, Steer RA, Brown GK (1996) BDI-II: Beck Depression Inventory. Psychological Corp, San AntonioGoogle Scholar
- 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
- 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
- Cohen S (1994) Perceived stress scale. Mind Garden, Palo Alto, CAGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- MacKinnon DP (2008) Introduction to statistical mediation analysis. Routledge Academic, New YorkGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Shipley W, Gruber C, Martin T, Klein A (2009) Shipley-2. Western Psychological Services, Los AngelesGoogle Scholar
- 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
- Tidey JW, Miczek KA (1997) Acquisition of cocaine self-administration after social stress: role of accumbens dopamine. Psychopharmacol (Berl) 130:203–212Google Scholar
- 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