Skip to main content

Advertisement

SpringerLink
Log in

Neural correlates of reward magnitude and delay during a probabilistic delay discounting task in alcohol use disorder

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

A Correction to this article was published on 21 December 2019

This article has been updated

Abstract

Rationale

Alcohol-use disorder (AUD) is associated with the propensity to choose smaller sooner options on the delay discounting task. It is unclear, however, how inherent risk underlies delay discounting behavior. As impulsive choice is a hallmark feature in AUD, it is important to understand the neural response to reward and delay while accounting for risk in impulsive decision-making.

Objective

This study examined activation associated with delay and reward magnitude, while controlling for risk in a probabilistic delay discounting task in AUD and examined if differences in activation were associated with treatment outcomes.

Methods

Thirty-nine recently abstinent alcohol-dependent volunteers and 46 controls completed a probabilistic delay discounting task paired with functional magnetic resonance imaging. Alcohol use was collected using a self-report journal for 3 months following baseline scan.

Results

During delay stimulus presentations, Controls exhibited greater activation compared to the Alcohol group notably in the anterior insula, middle/dorsal anterior cingulate cortex (ACC), dorsolateral prefrontal cortex (PFC), and inferior parietal lobule. For magnitude, the Alcohol group exhibited greater activation than Controls primarily in medial PFC, rostral ACC, left posterior parietal cortex, and right precuneus. Within the Alcohol group, alcohol craving severity negatively correlated with right lateral PFC activation during reward magnitude in individuals who completed the 3-month study without relapse, while non-completers showed the opposite relationship.

Conclusions

The results of this study extend previous findings that alcohol use disorder is associated with differences in activation during an immediate or delayed choice by delineating activation associated with the parameters of impulsive choice.

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

Change history

  • 21 December 2019

    After publication of this paper, the authors determined an error in the funding information section CX17008-CDA2 should be CX001790 (MK).

References

  • Agabio R, Pisanu C, Gessa GL, Franconi F (2017) Sex differences in alcohol use disorder. Curr Med Chem 24:2661–2670

    CAS  PubMed  Google Scholar 

  • Amlung M, Sweet LH, Acker J, Brown CL, MacKillop J (2014) Dissociable brain signatures of choice conflict and immediate reward preferences in alcohol use disorders. Addict Biol 19:743–753

    PubMed  Google Scholar 

  • Anderson BA (2016) What is abnormal about addiction-related attentional biases? Drug Alcohol Depend 167:8–14

    PubMed  PubMed Central  Google Scholar 

  • Ballard K, Knutson B (2009) Dissociable neural representations of future reward magnitude and delay during temporal discounting. Neuroimage 45:143–150

    PubMed  Google Scholar 

  • Bickel WK, Pitcock JA, Yi R, Angtuaco EJ (2009) Congruence of BOLD response across intertemporal choice conditions: fictive and real money gains and losses. J Neurosci 29:8839–8846

    CAS  PubMed  PubMed Central  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

    PubMed  Google Scholar 

  • Bjork JM, Hommer DW, Grant SJ, Danube C (2004) Impulsivity in abstinent alcohol-dependent patients: relation to control subjects and type 1-/type 2-like traits. Alcohol 34:133–150

    PubMed  Google Scholar 

  • Bjork JM, Smith AR, Chen G, Hommer DW (2012) Mesolimbic recruitment by nondrug rewards in detoxified alcoholics: effort anticipation, reward anticipation, and reward delivery. Hum Brain Mapp 33:2174–2188

    PubMed  Google Scholar 

  • Blum K, Braverman ER, Holder JM, Lubar JF, Monastra VJ, Miller D, Lubar JO, Chen TJ, Comings DE (2000) Reward deficiency syndrome: a biogenetic model for the diagnosis and treatment of impulsive, addictive, and compulsive behaviors. J Psychoactive Drugs i-iv(32 Suppl):1–112

    Google Scholar 

  • Bobova L, Finn PR, Rickert ME, Lucas J (2009) Disinhibitory psychopathology and delay discounting in alcohol dependence: personality and cognitive correlates. Exp Clin Psychopharmacol 17:51–61

    PubMed  PubMed Central  Google Scholar 

  • Boettiger CA, Mitchell JM, Tavares VC, Robertson M, Joslyn G, D'Esposito M, Fields HL (2007) Immediate reward bias in humans: fronto-parietal networks and a role for the catechol-O-methyltransferase 158(Val/Val) genotype. J Neurosci 27:14383–14391

    CAS  PubMed  PubMed Central  Google Scholar 

  • Botvinick MM, Cohen JD, Carter CS (2004) Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn Sci 8:539–546

    PubMed  Google Scholar 

  • Braus DF, Wrase J, Grusser S, Hermann D, Ruf M, Flor H, Mann K, Heinz A (2001) Alcohol-associated stimuli activate the ventral striatum in abstinent alcoholics. J Neural Transm (Vienna) 108:887–894

    CAS  Google Scholar 

  • Carter CS, van Veen V (2007) Anterior cingulate cortex and conflict detection: an update of theory and data. Cogn Affect Behav Neurosci 7:367–379

    PubMed  Google Scholar 

  • de Wit H (2009) Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict Biol 14:22–31

    PubMed  Google Scholar 

  • Deane FP, Wootton DJ, Hsu CI, Kelly PJ (2012) Predicting dropout in the first 3 months of 12-step residential drug and alcohol treatment in an Australian sample. J Stud Alcohol Drugs 73:216–225

    PubMed  Google Scholar 

  • Drobes DJ, Thomas SE (1999) Assessing craving for alcohol. Alcohol Res Health 23:179–186

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ernst M, Paulus MP (2005) Neurobiology of decision making: a selective review from a neurocognitive and clinical perspective. Biol Psychiatry 58:597–604

    PubMed  Google Scholar 

  • Flannery BA, Volpicelli JR, Pettinati HM (1999) Psychometric properties of the Penn alcohol craving scale. Alcohol Clin Exp Res 23:1289–1295

    CAS  PubMed  Google Scholar 

  • Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12:652–669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grusser SM, Wrase J, Klein S, Hermann D, Smolka MN, Ruf M, Weber-Fahr W, Flor H, Mann K, Braus DF, Heinz A (2004) Cue-induced activation of the striatum and medial prefrontal cortex is associated with subsequent relapse in abstinent alcoholics. Psychopharmacology 175:296–302

    PubMed  Google Scholar 

  • Hare TA, Hakimi S, Rangel A (2014) Activity in dlPFC and its effective connectivity to vmPFC are associated with temporal discounting. Front Neurosci 8:50

    PubMed  PubMed Central  Google Scholar 

  • Ho MY, Mobini S, Chiang TJ, Bradshaw CM, Szabadi E (1999) Theory and method in the quantitative analysis of “impulsive choice” behaviour: implications for psychopharmacology. Psychopharmacology 146:362–372

    CAS  PubMed  Google Scholar 

  • Johnston K, Levin HM, Koval MJ, Everling S (2007) Top-down control-signal dynamics in anterior cingulate and prefrontal cortex neurons following task switching. Neuron 53:453–462

    CAS  PubMed  Google Scholar 

  • Keyes KM, Grant BF, Hasin DS (2008) Evidence for a closing gender gap in alcohol use, abuse, and dependence in the United States population. Drug Alcohol Depend 93:21–29

    PubMed  Google Scholar 

  • Kober H, Mende-Siedlecki P, Kross EF, Weber J, Mischel W, Hart CL, Ochsner KN (2010) Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci USA 107:14811–14816

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kohno M, Dennis LE, McCready H, Hoffman WF (2017) Executive control and striatal resting-state network interact with risk factors to influence treatment outcomes in alcohol-use disorder. Front Psychiatry 8:182

    PubMed  PubMed Central  Google Scholar 

  • Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24:97–129

    CAS  PubMed  Google Scholar 

  • Le Berre AP, Fama R, Sullivan EV (2017) Executive functions, memory, and social cognitive deficits and recovery in chronic alcoholism: a critical review to inform future research. Alcohol Clin Exp Res 41:1432–1443

    PubMed  PubMed Central  Google Scholar 

  • Lim AC, Cservenka A, Ray LA (2017) Effects of alcohol dependence severity on neural correlates of delay discounting. Alcohol Alcohol 52:506–515

    PubMed  Google Scholar 

  • Lopez-Guzman S, Konova AB, Louie K, Glimcher PW (2018) Risk preferences impose a hidden distortion on measures of choice impulsivity. PLoS One 13:e0191357

    PubMed  PubMed Central  Google Scholar 

  • Luijten M, Schellekens AF, Kuhn S, Machielse MW, Sescousse G (2017) Disruption of reward processing in addiction : an image-based meta-analysis of functional magnetic resonance imaging studies. JAMA Psychiatry 74:387–398

    PubMed  Google Scholar 

  • MacKillop J (2013) Integrating behavioral economics and behavioral genetics: delayed reward discounting as an endophenotype for addictive disorders. J Exp Anal Behav 99:14–31

    PubMed  Google Scholar 

  • MacKillop J, Amlung MT, Few LR, Ray LA, Sweet LH, Munafo MR (2011) Delayed reward discounting and addictive behavior: a meta-analysis. Psychopharmacology 216:305–321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maisto SA, Pollock NK, Cornelius JR, Lynch KG, Martin CS (2003) Alcohol relapse as a function of relapse definition in a clinical sample of adolescents. Addict Behav 28:449–459

    PubMed  Google Scholar 

  • MATLAB and Statistics Toolbox Release 2013b, Copyright 1984-2012, The MathWorks, Inc., Natick, Massachusetts, United States

  • Matusiewicz AK, Carter AE, Landes RD, Yi R (2013) Statistical equivalence and test-retest reliability of delay and probability discounting using real and hypothetical rewards. Behav Process 100:116–122

    Google Scholar 

  • McClure SM, Laibson DI, Loewenstein G, Cohen JD (2004) Separate neural systems value immediate and delayed monetary rewards. Science 306:503–507

    CAS  PubMed  Google Scholar 

  • Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655–667

    PubMed  PubMed Central  Google Scholar 

  • Miedl SF, Peters J, Buchel C (2012) Altered neural reward representations in pathological gamblers revealed by delay and probability discounting. Arch Gen Psychiatry 69:177–186

    PubMed  Google Scholar 

  • Mitchell SH, Wilson VB (2012) Differences in delay discounting between smokers and nonsmokers remain when both rewards are delayed. Psychopharmacology 219:549–562

    CAS  PubMed  Google Scholar 

  • Mitchell JM, Fields HL, D'Esposito M, Boettiger CA (2005) Impulsive responding in alcoholics. Alcohol Clin Exp Res 29:2158–2169

    PubMed  Google Scholar 

  • Moos RH, Moos BS (2006) Rates and predictors of relapse after natural and treated remission from alcohol use disorders. Addiction 101:212–222

    PubMed  PubMed Central  Google Scholar 

  • O'Connor PG, Gottlieb LD, Kraus ML, Segal SR, Horwitz RI (1991) Social and clinical features as predictors of outcome in outpatient alcohol withdrawal. J Gen Intern Med 6:312–316

    CAS  PubMed  Google Scholar 

  • Patak M, Reynolds B (2007) Question-based assessments of delay discounting: do respondents spontaneously incorporate uncertainty into their valuations for delayed rewards? Addict Behav 32:351–357

    PubMed  Google Scholar 

  • Petry NM (2001) Delay discounting of money and alcohol in actively using alcoholics, currently abstinent alcoholics, and controls. Psychopharmacology 154:243–250

    CAS  PubMed  Google Scholar 

  • Stark M (1992) Dropping out of substance abuse treatment: a clinically oriented review. Clin Psychol Rev 12:93–116

    Google Scholar 

  • Stevens L, Verdejo-Garcia A, Roeyers H, Goudriaan AE, Vanderplasschen W (2015) Delay discounting, treatment motivation and treatment retention among substance-dependent individuals attending an in inpatient detoxification program. J Subst Abus Treat 49:58–64

    Google Scholar 

  • Vanderveldt A, Green L, Myerson J (2015) Discounting of monetary rewards that are both delayed and probabilistic: delay and probability combine multiplicatively, not additively. J Exp Psychol Learn Mem Cogn 41:148–162

    PubMed  Google Scholar 

  • Zhang Z, Friedmann PD, Gerstein DR (2003) Does retention matter? Treatment duration and improvement in drug use. Addiction 98:673–684

    PubMed  Google Scholar 

  • Zilverstand A, Huang AS, Alia-Klein N, Goldstein RZ (2018) Neuroimaging impaired response inhibition and salience attribution in human drug addiction: a systematic review. Neuron 98:886–903

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank the staff of the Veterans Affairs Portland Health Care System Substance Abuse Treatment Program, CODA Treatment Recovery, Hooper Detox Stabilization Center, Central City Concern, and Volunteers of America Residential Treatment Centers, Portland, OR, for their help and recruitment efforts and also Ethan Sawyer for his help with the manuscript.

Funding

This work was supported in part by the National Institute on Alcohol Abuse and Alcoholism R21AA020039 (WFH); Department of Veterans Affairs Clinical Sciences Research and Development Merit Review Program, I01 CX001558-01A1 (WFH); Department of Justice 2010-DD-BX-0517 (WFH); National Institute on Drug Abuse P50DA018165 (WFH); and Oregon Clinical and Translational Research Institute, 1 UL1 RR024140 01 from the National Center for Research Resources, a component of the National Institutes of Health and National Institute of Health Roadmap for Medical Research. Dr. Kohno was supported by National Institute on Drug Abuse T32 DA007262, National Institute on Alcohol Abuse and Alcoholism T32 AA007468, Department of Veterans Affairs Clinical Sciences Research and Development Career Development Award CX17008-CDA2, Oregon Health & Science University Collins Medical Trust Award APSYC0249, and Medical Research Foundation of Oregon APSYC0250.

Author information

Authors and Affiliations

  1. Mental Health Division P35C, Veterans Affairs Portland Health Care System, 3710 SW US Veterans Hospital Rd, Portland, OR, 97239, USA

    Laura E. Dennis, Milky Kohno, Holly D. McCready, Britta Schwartz & William F. Hoffman

  2. Department of Psychiatry, Oregon Health & Science University, Portland, OR, USA

    Laura E. Dennis, Milky Kohno, Holly D. McCready, Britta Schwartz, Bonnie J. Nagel, Suzanne H. Mitchell & William F. Hoffman

  3. Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, USA

    Laura E. Dennis, Milky Kohno, Holly D. McCready, Britta Schwartz, Bonnie J. Nagel, Suzanne H. Mitchell & William F. Hoffman

  4. Neurology and Advanced Imaging Research Center, Oregon Health & Science University, Portland, OR, USA

    Daniel L. Schwartz & David Lahna

  5. Oregon Institute for Occupational Health Sciences, Oregon Health & Science University, Portland, OR, USA

    Suzanne H. Mitchell

  6. Methamphetamine Abuse Research Center (MARC), Oregon Health & Science University and Veterans Affairs Portland Health Care System, Portland, OR, USA

    William F. Hoffman

Authors
  1. Laura E. Dennis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Milky Kohno
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Holly D. McCready
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel L. Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Britta Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David Lahna
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bonnie J. Nagel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Suzanne H. Mitchell
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. William F. Hoffman
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MK conceptualized this approach, made significant contributions to the analysis and writing of this manuscript, and mentored LD in the interpretation of results and writing of this manuscript. LD, HM, BT, DS, and DL collected these data. DS, DL, WH, and SM each contributed significantly to designing the PDD task. BN was a Co-I on the grant and advised on imaging and design. LD performed initial data analyses with the neuroimages. WH was the PI on the project, supervised the collection and analysis of data, and contributed to the writing of the manuscript.

Corresponding author

Correspondence to Milky Kohno.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Laura E. Dennis and Milky Kohno share co-first authorship.

The contents of this paper do not represent the views of the U.S. Department of Veterans Affairs or the United States Government.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dennis, L.E., Kohno, M., McCready, H.D. et al. Neural correlates of reward magnitude and delay during a probabilistic delay discounting task in alcohol use disorder. Psychopharmacology 237, 263–278 (2020). https://doi.org/10.1007/s00213-019-05364-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-019-05364-3

Keywords

Search

Navigation