Skip to main content
SpringerLink
Log in

Monetary discounting and ventral striatal dopamine receptor availability in nontreatment-seeking alcoholics and social drinkers

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

Dopamine (DA) in the ventral striatum (VST) has long been implicated in addiction pathologies, yet its role in temporal decision-making is not well-understood.

Objectives

To determine if VST DA D2 receptor availability corresponds with greater impulsive choice in both nontreatment-seeking alcoholics (NTS) and social drinkers (SD).

Methods

NTS subjects (n = 10) and SD (n = 13) received PET scans at baseline with the D2/D3 radioligand [11C]raclopride (RAC). Outside the scanner, subjects performed a delay discounting procedure with monetary rewards. RAC binding potential (BPND) was estimated voxelwise, and correlations were performed to test for relationships between VST BPND and delay discounting performance. Self-reported impulsivity was also tested for correlations with BPND.

Results

Across all subjects, greater impulsive choice for $20 correlated with lower BPND in the right VST. NTS showed greater impulsive choice than SD and were more impulsive by self-report. Across all subjects, the capacity of larger rewards to reduce impulsive choice (the magnitude effect) correlated negatively (p = 0.028) with problematic alcohol use (AUDIT) scores. Self-reported impulsivity did not correlate with BPND in VST.

Conclusions

Preference for immediate reinforcement may reflect greater endogenous striatal DA or lower D2 number, or both. Alcoholic status did not mediate significant effects on VST BPND, suggesting minimal effects from alcohol exposure. The apparent lack of BPND correlation with self-reported impulsivity highlights the need for objective behavioral assays in the study of the neurochemical substrates of behavior. Finally, our results suggest that the magnitude effect may be more sensitive to alcohol-induced problems than single discounting measures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. Amphetamine’s ability to reduce impulsive choice in animal studies is known to be sensitive to the presence of a cue bridging the delay (Cardinal et al. 2000), order of delay presentation (Tanno et al. 2014), as well as sex, strain, and baseline impulsivity differences (Eubig et al. 2014; Huskinson et al. 2012; Krebs and Anderson 2012). Some discrepancies in this literature are likely due to these varied factors across studies.

References

  • Ayduk O, Mendoza-Denton R, Mischel W, Downey G, Peake PK, Rodriguez M (2000) Regulating the interpersonal self: strategic self-regulation for coping with rejection sensitivity. J Pers Soc Psychol 79(5):776–792

    Article  CAS  PubMed  Google Scholar 

  • Berridge KC (2007) The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacology (Berl) 191(3):391–431

    Article  CAS  Google Scholar 

  • Bickel WK, Koffarnus MN, Moody L, Wilson AG (2014) The behavioral- and neuro-economic process of temporal discounting: a candidate behavioral marker of addiction. Neuropharmacology 76 Pt B:518–527

    Article  PubMed  Google Scholar 

  • Blum K, Sheridan PJ, Wood RC, Braverman ER, Chen TJ, Cull JG et al (1996) The D2 dopamine receptor gene as a determinant of reward deficiency syndrome. J R Soc Med 89(7):396–400

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bucholz KK, Cadoret R, Cloninger CR, Dinwiddie SH, Hesselbrock VM, Nurnberger JI Jr et al (1994) A new, semi-structured psychiatric interview for use in genetic linkage studies: a report on the reliability of the SSAGA. J Stud Alcohol 55(2):149–158

    Article  CAS  PubMed  Google Scholar 

  • Cardinal RN, Robbins TW, Everitt BJ (2000) The effects of d-amphetamine, chlordiazepoxide, alpha-flupenthixol and behavioural manipulations on choice of signalled and unsignalled delayed reinforcement in rats. Psychopharmacology (Berl) 152(4):362–375

    Article  CAS  Google Scholar 

  • Carter RM, Meyer JR, Huettel SA (2010) Functional neuroimaging of intertemporal choice models: a review. J Neurosci Psychol Econ 3(1):27–45

    Article  Google Scholar 

  • Chaudhri N, Sahuque LL, Janak PH (2008) Context-induced relapse of conditioned behavioral responding to ethanol cues in rats. Biol Psychiatry 64(3):203–210

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Czachowski CL, Chappell AM, Samson HH (2001) Effects of raclopride in the nucleus accumbens on ethanol seeking and consumption. Alcohol Clin Exp Res 25(10):1431–1440

    Article  CAS  PubMed  Google Scholar 

  • de Wit H, Enggasser JL, Richards JB (2002) Acute administration of d-amphetamine decreases impulsivity in healthy volunteers. Neuropsychopharmacology 27(5):813–825

    Article  PubMed  Google Scholar 

  • Di Chiara G, Imperato A (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci U S A 85(14):5274–5278

    Article  PubMed Central  PubMed  Google Scholar 

  • Doyon WM, Anders SK, Ramachandra VS, Czachowski CL, Gonzales RA (2005) Effect of operant self-administration of 10% ethanol plus 10% sucrose on dopamine and ethanol concentrations in the nucleus accumbens. J Neurochem 93(6):1469–1481

    Article  CAS  PubMed  Google Scholar 

  • Du W, Green L, Myerson J (2002) Cross-cultural comparisons of discounting delayed and probabilistic rewards. Psychol Rec 52(4):479–492

    Google Scholar 

  • Eubig PA, Noe TE, Floresco SB, Sable JJ, Schantz SL (2014) Sex differences in response to amphetamine in adult Long-Evans rats performing a delay-discounting task. Pharmacol Biochem Behav 118:1–9

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eysenck SBG, Pearson PR, Easting G, Allsopp JF (1985) Age norms for impulsiveness, venturesomeness, and empathy in adults. Personal Individ Differ 6(5):613–619

    Article  Google Scholar 

  • Fei X, Mock BH, DeGrado TR, Wang JQ, Glick-Wilson BE, Sullivan ML et al (2004) An improved synthesis of PET dopamine D2 receptors radioligand [11C]raclopride. Synth Commun 34(10):1897–1907

    Article  CAS  Google Scholar 

  • Grosset KA, Macphee G, Pal G, Stewart D, Watt A, Davie J et al (2006) Problematic gambling on dopamine agonists: not such a rarity. Mov Disord 21(12):2206–2208

    Article  PubMed  Google Scholar 

  • Heinz A, Siessmeier T, Wrase J, Hermann D, Klein S, Grusser SM et al (2004) Correlation between dopamine D(2) receptors in the ventral striatum and central processing of alcohol cues and craving. Am J Psychiatry 161(10):1783–1789

    Article  PubMed  Google Scholar 

  • Huskinson SL, Krebs CA, Anderson KG (2012) Strain differences in delay discounting between Lewis and Fischer 344 rats at baseline and following acute and chronic administration of d-amphetamine. Pharmacol Biochem Behav 101(3):403–416

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ichise M, Liow JS, Lu JQ, Takano A, Model K, Toyama H et al (2003) Linearized reference tissue parametric imaging methods: application to [11C]DASB positron emission tomography studies of the serotonin transporter in human brain. J Cereb Blood Flow Metab 23(9):1096–1112

    Article  PubMed  Google Scholar 

  • Innis RB, Cunningham VJ, Delforge J, Fujita M, Gjedde A, Gunn RN et al (2007) Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab 27(9):1533–1539

    Article  CAS  PubMed  Google Scholar 

  • Johnson MW, Bickel WK (2002) Within-subject comparison of real and hypothetical money rewards in delay discounting. J Exp Anal Behav 77(2):129–146

    Article  PubMed Central  PubMed  Google Scholar 

  • Johnson MW, Bickel WK (2008) An algorithm for identifying nonsystematic delay-discounting data. Exp Clin Psychopharmacol 16(3):264–274

    Article  PubMed Central  PubMed  Google Scholar 

  • Johnson PM, Kenny PJ (2010) Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13(5):635–641

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kirby KN, Petry NM, Bickel WK (1999) Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. J Exp Psychol Gen 128(1):78–87

    Article  CAS  PubMed  Google Scholar 

  • Krebs CA, Anderson KG (2012) Preference reversals and effects of D-amphetamine on delay discounting in rats. Behav Pharmacol 23(3):228–240

    Article  CAS  PubMed  Google Scholar 

  • Krishnan-Sarin S, Reynolds B, Duhig AM, Smith A, Liss T, McFetridge A et al (2007) Behavioral impulsivity predicts treatment outcome in a smoking cessation program for adolescent smokers. Drug Alcohol Depend 88(1):79–82

    Article  PubMed Central  PubMed  Google Scholar 

  • Martinez D, Gil R, Slifstein M, Hwang DR, Huang Y, Perez A et al (2005) Alcohol dependence is associated with blunted dopamine transmission in the ventral striatum. Biol Psychiatry 58(10):779–786

    Article  CAS  PubMed  Google Scholar 

  • Mawlawi O, Martinez D, Slifstein M, Broft A, Chatterjee R, Hwang DR et al (2001) Imaging human mesolimbic dopamine transmission with positron emission tomography: I. Accuracy and precision of D(2) receptor parameter measurements in ventral striatum. J Cereb Blood Flow Metab 21(9):1034–1057

    Article  CAS  PubMed  Google Scholar 

  • McBride WJ, Chernet E, Dyr W, Lumeng L, Li TK (1993) Densities of dopamine D2 receptors are reduced in CNS regions of alcohol-preferring P rats. Alcohol 10(5):387–390

    Article  CAS  PubMed  Google Scholar 

  • Meda SA, Stevens MC, Potenza MN, Pittman B, Gueorguieva R, Andrews MM et al (2009) Investigating the behavioral and self-report constructs of impulsivity domains using principal component analysis. Behav Pharmacol 20(5–6):390–399

    Article  PubMed Central  PubMed  Google Scholar 

  • Moore TJ, Glenmullen J, Mattison DR (2014) Reports of pathological gambling, hypersexuality, and compulsive shopping associated with dopamine receptor agonist drugs. JAMA Intern Med

  • Myerson J, Green L, Warusawitharana M (2001) Area under the curve as a measure of discounting. J Exp Anal Behav 76(2):235–243

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oberlin BG, Grahame NJ (2009) High-alcohol preferring mice are more impulsive than low-alcohol preferring mice as measured in the delay discounting task. Alcohol Clin Exp Res 33(7):1294–1303

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oberlin BG, Dzemidzic M, Tran SM, Soeurt CM, Albrecht DS, Yoder KK et al (2013) Beer flavor provokes striatal dopamine release in male drinkers: mediation by family history of alcoholism. Neuropsychopharmacology 38(9):1617–1624

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • O’Brien CP, Childress AR, McLellan T, Ehrman R (1990) Integrating systemic cue exposure with standard treatment in recovering drug dependent patients. Addict Behav 15(4):355–365

    Article  PubMed  Google Scholar 

  • Peciña S, Berridge KC (2013) Dopamine or opioid stimulation of nucleus accumbens similarly amplify cue-triggered ‘wanting’ for reward: entire core and medial shell mapped as substrates for PIT enhancement. Eur J Neurosci 37(9):1529–1540

    Article  PubMed Central  PubMed  Google Scholar 

  • Perry JL, Larson EB, German JP, Madden GJ, Carroll ME (2005) Impulsivity (delay discounting) as a predictor of acquisition of IV cocaine self-administration in female rats. Psychopharmacology (Berl) 178(2–3):193–201

    Article  CAS  Google Scholar 

  • Pine A, Shiner T, Seymour B, Dolan RJ (2010) Dopamine, time, and impulsivity in humans. J Neurosci 30(26):8888–8896

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Richards JB, Sabol KE, de Wit H (1999) Effects of methamphetamine on the adjusting amount procedure, a model of impulsive behavior in rats. Psychopharmacology (Berl) 146(4):432–439

    Article  CAS  Google Scholar 

  • Rinne JO, Hietala J, Ruotsalainen U, Sako E, Laihinen A, Nagren K et al (1993) Decrease in human striatal dopamine D2 receptor density with age: a PET study with [11C]raclopride. J Cereb Blood Flow Metab 13(2):310–314

    Article  CAS  PubMed  Google Scholar 

  • Saunders JB, Aasland OG, Babor TF, de la Fuente JR, Grant M (1993) Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO Collaborative project on early detection of persons with harmful alcohol consumption—II. Addiction 88(6):791–804

    Article  CAS  PubMed  Google Scholar 

  • Sobell MB, Sobell LC, Klajner F, Pavan D, Basian E (1986) The reliability of a timeline method for assessing normal drinker college students’ recent drinking history: utility for alcohol research. Addict Behav 11(2):149–161

    Article  CAS  PubMed  Google Scholar 

  • Stefanini E, Frau M, Garau MG, Garau B, Fadda F, Gessa GL (1992) Alcohol-preferring rats have fewer dopamine D2 receptors in the limbic system. Alcohol Alcohol 27(2):127–130

    CAS  PubMed  Google Scholar 

  • Sullivan JT, Sykora K, Schneiderman J, Naranjo CA, Sellers EM (1989) Assessment of alcohol withdrawal: the revised clinical institute withdrawal assessment for alcohol scale (CIWA-Ar). Br J Addict 84(11):1353–1357

    Article  CAS  PubMed  Google Scholar 

  • Tanno T, Maguire DR, Henson C, France CP (2014) Effects of amphetamine and methylphenidate on delay discounting in rats: interactions with order of delay presentation. Psychopharmacology (Berl) 231(1):85–95

    Article  CAS  Google Scholar 

  • Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289

    Article  CAS  PubMed  Google Scholar 

  • Volkow ND, Wang GJ, Fowler JS, Logan J, Hitzemann R, Ding YS et al (1996) Decreases in dopamine receptors but not in dopamine transporters in alcoholics. Alcohol Clin Exp Res 20(9):1594–1598

    Article  CAS  PubMed  Google Scholar 

  • Volkow ND, Wang GJ, Begleiter H, Porjesz B, Fowler JS, Telang F et al (2006) High levels of dopamine D2 receptors in unaffected members of alcoholic families: possible protective factors. Arch Gen Psychiatry 63(9):999–1008

    Article  CAS  PubMed  Google Scholar 

  • Weiss F, Lorang MT, Bloom FE, Koob GF (1993) Oral alcohol self-administration stimulates dopamine release in the rat nucleus accumbens: genetic and motivational determinants. J Pharmacol Exp Ther 267(1):250–258

    CAS  PubMed  Google Scholar 

  • Wilhelm CJ, Mitchell SH (2008) Rats bred for high alcohol drinking are more sensitive to delayed and probabilistic outcomes. Genes Brain Behav 7(7):705–713

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yates JR, Marusich JA, Gipson CD, Beckmann JS, Bardo MT (2012) High impulsivity in rats predicts amphetamine conditioned place preference. Pharmacol Biochem Behav 100(3):370–376

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoder KK, Kareken DA, Morris ED (2011) Assessing dopaminergic neurotransmission with PET: basic theory and applications in alcohol research. Curr Med Imaging Rev 7:118–124

    Article  CAS  Google Scholar 

  • Yoder KK, Albrecht DS, Kareken DA, Federici LM, Perry KM, Patton EA et al (2012) Reliability of striatal [11C]raclopride binding in smokers wearing transdermal nicotine patches. Eur J Nucl Med Mol Imaging 39(2):220–225

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zuckerman M, Eysenck S, Eysenck HJ (1978) Sensation seeking in England and America: cross-cultural, age, and sex comparisons. J Consult Clin Psychol 46(1):139–149

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge Kevin Perry, Wendy Territo, Michele Beal, Courtney Robbins (Department of Radiology and Imaging Sciences) for technical and regulatory assistance, as well as Dr. Jaroslaw Harezlak for statistical consultation. We also thank Dr. Mark Green, Dr. Qi-Huang Zheng, Barbara Glick-Wilson, and Brandon Steele for radiochemical synthesis of [11C]raclopride. This study is supported by R01 AA018354 to KKY, T32 AA007462 to BGO, and R01 AA017661 to DAK; additionally supported by the Indiana Clinical and Translational Sciences Institute Clinical Research Center, UL1TR001108, NIH, National Center for Advancing Translational Sciences, Clinical and Translational Sciences Award.

Conflict of interest

The authors declare no conflict of interest. Authors maintain full control of all primary data and agree to review by journal upon request.

Author information

Authors and Affiliations

  1. Indiana University Center for Neuroimaging, Indianapolis, IN, USA

    Brandon G. Oberlin, Daniel S. Albrecht, Christine M. Herring, James W. Walters, Karen L. Hile, David A. Kareken & Karmen K. Yoder

  2. Department of Neurology, Indiana University School of Medicine (IUSOM), Indianapolis, IN, USA

    Brandon G. Oberlin & David A. Kareken

  3. Department of Radiology and Imaging Sciences, Indiana University School of Medicine (IUSOM), 950 W Walnut St., R2 E124, Indianapolis, IN, 46202, USA

    Daniel S. Albrecht, Christine M. Herring, James W. Walters, Karen L. Hile, David A. Kareken & Karmen K. Yoder

  4. Department of Psychiatry, IUSOM, Indianapolis, IN, USA

    David A. Kareken

  5. Stark Neurosciences Research Institute, IUSOM, Indianapolis, IN, USA

    Daniel S. Albrecht, David A. Kareken & Karmen K. Yoder

  6. Department of Psychology, Indiana University Purdue University Indianapolis, Indianapolis, IN, USA

    Karmen K. Yoder

Authors
  1. Brandon G. Oberlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel S. Albrecht
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christine M. Herring
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James W. Walters
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Karen L. Hile
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David A. Kareken
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Karmen K. Yoder
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karmen K. Yoder.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oberlin, B.G., Albrecht, D.S., Herring, C.M. et al. Monetary discounting and ventral striatal dopamine receptor availability in nontreatment-seeking alcoholics and social drinkers. Psychopharmacology 232, 2207–2216 (2015). https://doi.org/10.1007/s00213-014-3850-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-014-3850-5

Keywords

Search

Navigation