Advertisement
Archival Report| Volume 66, ISSUE 12, P1083-1090, December 15, 2009

Functional Neuroimaging of Reward Circuitry Responsivity to Monetary Gains and Losses in Posttraumatic Stress Disorder

      Background

      Clinical impressions and preclinical work suggest that posttraumatic stress disorder (PTSD) might be associated with dysfunctional reward processing. To pursue this issue, we administered a validated passive-viewing monetary reward task during functional magnetic resonance imaging (fMRI) to subjects with chronic PTSD and to mentally healthy individuals.

      Methods

      The protocol evaluated fMRI signal changes that anticipated or accompanied monetary gains and losses under varying conditions of controlled expectation. The “expectancy phase” entailed presentation of a promising, unpromising, or intermediate Wheel of Fortune–type spinner, whereas the “outcome phase” was defined by the arrow landing on one of three sectors of that spinner, thereby determining the subjects' gain or loss for that trial.

      Results

      Neuroimaging data from 20 PTSD and 26 healthy subjects withstood quality control procedures and were included. In voxelwise and anatomically defined region-of-interest analyses, when gains were contrasted to losses, between-group comparison revealed smaller bilateral striatal activations in the PTSD subjects. In the PTSD group, less striatal activation to gains versus losses was associated with more self-reported motivational and social deficits.

      Conclusions

      The present data support the hypothesis that PTSD is associated with abnormal processing of monetary outcomes and that this alteration might be related to some aspects of emotional numbing.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • American Psychiatric Association
        Diagnostic and Statistical Manual of Mental Disorders.
        4th ed. American Psychiatric Association, Washington, DC2000 (Text Revision (DSM-IV-TR).)
        • Rauch S.L.
        • Shin L.M.
        • Phelps E.A.
        Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research—past, present, and future.
        Biol Psychiatry. 2006; 60: 376-382
        • Bremner J.D.
        Neuroimaging in posttraumatic stress disorder and other stress-related disorders.
        Neuroimaging Clin North Am. 2007; 17 (ix.): 523-538
        • Liberzon I.
        • Sripada C.S.
        The functional neuroanatomy of PTSD: A critical review.
        Prog Brain Res. 2008; 167: 151-169
        • Elman I.
        • Ariely D.
        • Mazar N.
        • Aharon I.
        • Lasko N.B.
        • Macklin M.L.
        • et al.
        Probing reward function in post-traumatic stress disorder with beautiful facial images.
        Psychiatry Res. 2005; 135: 179-183
        • Hopper J.W.
        • Pitman R.K.
        • Su Z.
        • Heyman G.M.
        • Lasko N.B.
        • Macklin M.L.
        • et al.
        Probing reward function in posttraumatic stress disorder: Expectancy and satisfaction with monetary gains and losses.
        J Psychiatr Res. 2008; 42: 802-807
        • Comings D.E.
        • Blum K.
        Reward deficiency syndrome: Genetic aspects of behavioral disorders.
        Prog Brain Res. 2000; 126: 325-341
        • Blum K.
        • Braverman E.R.
        • Holder J.M.
        • Lubar J.F.
        • Monastra V.J.
        • Miller D.
        • et al.
        Reward deficiency syndrome: A biogenetic model for the diagnosis and treatment of impulsive, addictive, and compulsive behaviors.
        J Psychoact Drugs. 2000; 32 (i–iv.): 1-112
        • Kessler R.C.
        • Sonnega A.
        • Bromet E.
        • Hughes M.
        • Nelson C.B.
        Posttraumatic stress disorder in the National Comorbidity Survey.
        Arch Gen Psychiatry. 1995; 52: 1048-1060
        • Pizzagalli D.A.
        • Iosifescu D.
        • Hallett L.A.
        • Ratner K.G.
        • Fava M.
        Reduced hedonic capacity in major depressive disorder: Evidence from a probabilistic reward task.
        J Psychiatr Res. 2008; 43: 76-87
        • Harvey P.O.
        • Pruessner J.
        • Czechowska Y.
        • Lepage M.
        Individual differences in trait anhedonia: A structural and functional magnetic resonance imaging study in non-clinical subjects.
        Mol Psychiatry. 2007; 703: 767-775
        • Cabib S.
        • Puglisi-Allegra S.
        Stress, depression and the mesolimbic dopamine system.
        Psychopharmacology. 1996; 128: 331-342
        • Puglisi-Allegra S.
        • Imperato A.
        • Angelucci L.
        • Cabib S.
        Acute stress induces time-dependent responses in dopamine mesolimbic system.
        Brain Res. 1991; 554: 217-222
        • Willner P.
        • Muscat R.
        • Papp M.
        Chronic mild stress-induced anhedonia: A realistic animal model of depression.
        Neurosci Biobehav Rev. 1992; 16: 525-534
        • Zacharko R.M.
        • Anisman H.
        Stressor-induced anhedonia in the mesocorticolimbic system.
        Neurosci Biobehav Rev. 1991; 15: 391-405
        • Yehuda R.
        • Antelman S.M.
        Criteria for rationally evaluating animal models of posttraumatic stress disorder.
        Biol Psychiatry. 1993; 33: 479-486
        • Baum A.
        • Cohen L.
        • Hall M.
        Control and intrusive memories as possible determinants of chronic stress.
        Psychosom Med. 1993; 55: 274-286
        • Spahic-Mihajlovic A.
        • Crayton J.W.
        • Neafsey E.J.
        Selective numbing and hyperarousal in male and female Bosnian refugees with PTSD.
        J Anxiety Disord. 2005; 19: 383-402
        • Jatzko A.
        • Schmitt A.
        • Demirakca T.
        • Weimer E.
        • Braus D.F.
        Disturbance in the neural circuitry underlying positive emotional processing in post-traumatic stress disorder (PTSD).
        Eur Arch Psychiatry Clin Neurosci. 2006; 256: 112-114
        • Sailer U.
        • Robinson S.
        • Fischmeister F.P.
        • Konig D.
        • Oppenauer C.
        • Lueger-Schuster B.
        • et al.
        Altered reward processing in the nucleus accumbens and mesial prefrontal cortex of patients with posttraumatic stress disorder.
        Neuropsychologia. 2008; 46: 2836-2844
        • Breiter H.C.
        • Aharon I.
        • Kahneman D.
        • Dale A.
        • Shizgal P.
        Functional imaging of neural responses to expectancy and experience of monetary gains and losses.
        Neuron. 2001; 30: 619-639
        • Redelmeier D.A.
        • Rozin P.
        • Kahneman D.
        Understanding patients' decisions.
        JAMA. 1993; 270: 72-76
        • First M.B.
        • Gibbon M.
        • Spitzer R.L.
        • Williams J.B.W.
        User's Guide for the SCID-I: Structured Clinical Interview for DSM-IV-TR Axis I Disorders (Research Version).
        Biometrics Research Department, Psychiatric Institute, New York2002
        • Weathers F.W.
        • Keane T.M.
        • Davidson J.R.
        Clinician-administered PTSD scale: A review of the first ten years of research.
        Depress Anxiety. 2001; 13: 132-156
        • Oldfield R.C.
        The assessment and analysis of handedness: The Edinburgh inventory.
        Neuropsychologia. 1971; 9: 97-113
        • Seymour G.E.
        The structure and predictive ability of the Cornell Medical Index for a normal sample.
        J Psychosom Res. 1976; 20: 469-478
        • Bremner J.D.
        Neuroimaging studies in post-traumatic stress disorder.
        Curr Psychiatry Rep. 2002; 4: 254-263
        • Liberzon I.
        • Taylor S.F.
        • Amdur R.
        • Jung T.D.
        • Chamberlain K.R.
        • Minoshima S.
        • et al.
        Brain activation in PTSD in response to trauma-related stimuli.
        Biol Psychiatry. 1999; 45: 817-826
        • Lanius R.A.
        • Bluhm R.
        • Lanius U.
        • Pain C.
        A review of neuroimaging studies in PTSD: Heterogeneity of response to symptom provocation.
        J Psychiatr Res. 2006; 40: 709-729
        • Rohan M.
        • Killgore W.
        • Eskesen J.
        • Renshaw P.
        • Yurgelun-Todd D.
        Match-Warped EPI Anatomic Images and the Amygdala: Imaging in Hard Places.
        2001 (International Society for Magnetic Resonance and Medicine 9th Scientific Meeting and Exhibition and the European Society for Magnetic Resonance in Medicine and Biology 18th Annual Meeting and Exhibition; Glasgow, United Kingdom.)
        • Jenkinson M.
        • Bannister P.
        • Brady M.
        • Smith S.
        Improved optimization for the robust and accurate linear registration and motion correction of brain images.
        Neuroimage. 2002; 17: 825-841
        • Woolrich M.W.
        • Ripley B.D.
        • Brady M.
        • Smith S.M.
        Temporal autocorrelation in univariate linear modeling of FMRI data.
        Neuroimage. 2001; 14: 1370-1386
        • Madsen K.H.
        • Lund T.E.
        Filtering fMRI data by unsupervised modelling of physiological noise artifacts.
        12th Annual Meeting of the Organization for Human Brain Mapping. The Organization for Human Brain Mapping, Minneapolis2006
        • Worsley K.J.
        • Evans A.C.
        • Marrett S.
        • Neelin P.
        A three-dimensional statistical analysis for CBF activation studies in human brain.
        J Cereb Blood Flow Metab. 1992; 12: 900-918
        • Abelson R.P.
        Statistics as Principled Argument.
        Lawrence Erlbaum Associates, Hove, United Kingdom1995
        • North C.S.
        • Suris A.M.
        • Davis M.
        • Smith R.P.
        Toward validation of the diagnosis of posttraumatic stress disorder.
        Am J Psychiatry. 2009; 166: 34-41
        • Delgado M.R.
        • Locke H.M.
        • Stenger V.A.
        • Fiez J.A.
        Dorsal striatum responses to reward and punishment: Effects of valence and magnitude manipulations.
        Cogn Affect Behav Neurosci. 2003; 3: 27-38
        • Tom S.M.
        • Fox C.R.
        • Trepel C.
        • Poldrack R.A.
        The neural basis of loss aversion in decision-making under risk.
        Science. 2007; 315: 515-518
        • Elliott R.
        • Newman J.L.
        • Longe O.A.
        • Deakin J.F.
        Differential response patterns in the striatum and orbitofrontal cortex to financial reward in humans: A parametric functional magnetic resonance imaging study.
        J Neurosci. 2003; 23: 303-307
        • Knutson B.
        • Fong G.W.
        • Adams C.M.
        • Varner J.L.
        • Hommer D.
        Dissociation of reward anticipation and outcome with event-related fMRI.
        Neuroreport. 2001; 12: 3683-3687
        • Marco-Pallarés J.
        • Cucurell D.
        • Cunillera T.
        • Krämer U.M.
        • Càmara E.
        • Nager W.
        • et al.
        Genetic variability in the dopamine system (dopamine receptor D4, catechol-O-methyltransferase) modulates neurophysiological responses to gains and losses.
        Biol Psychiatry. 2009; 66: 154-161
        • Dreher J.C.
        Sensitivity of the brain to loss aversion during risky gambles.
        Trends Cogn Sci. 2007; 11: 270-272
        • Marco-Pallarés J.
        • Müller S.V.
        • Münte T.F.
        Learning by doing: An fMRI study of feedback-related brain activations.
        Neuroreport. 2007; 18: 1423-1426
        • Knutson B.
        • Fong G.W.
        • Bennett S.M.
        • Adams C.M.
        • Hommer D.
        A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: Characterization with rapid event-related fMRI.
        Neuroimage. 2003; 18: 263-272
        • Briers B.
        • Pandelaere M.
        • Dewitte S.
        • Warlop L.
        Hungry for money: The desire for caloric resources increases the desire for financial resources and vice versa.
        Psych Sci. 2006; 17: 939-943
        • Delgado M.R.
        • Labouliere C.D.
        • Phelps E.A.
        Fear of losing money?.
        Soc Cogn Affect Neurosci. 2006; 1: 250-259
        • Loewenstein G.
        • Rick S.
        • Cohen J.D.
        Neuroeconomics.
        Annu Rev Psych. 2008; 59: 647-672
        • Balleine B.W.
        • Delgado M.R.
        • Hikosaka O.
        The role of the dorsal striatum in reward and decision-making.
        J Neurosci. 2007; 27: 8161-8165
        • O'Doherty J.
        • Dayan P.
        • Schultz J.
        • Deichmann R.
        • Friston K.
        • Dolan R.J.
        Dissociable roles of ventral and dorsal striatum in instrumental conditioning.
        Science. 2004; 304: 452-454
        • Schultz W.
        Behavioral theories and the neurophysiology of reward.
        Annu Rev Psych. 2006; 57: 87-115
        • McClure S.M.
        • Ericson K.M.
        • Laibson D.I.
        • Loewenstein G.
        • Cohen J.D.
        Time discounting for primary rewards.
        J Neurosci. 2007; 27: 5796-5804
        • Belin D.
        • Everitt B.J.
        Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum.
        Neuron. 2008; 57: 432-441
        • Palmiter R.D.
        Dopamine signaling in the dorsal striatum is essential for motivated behaviors: Lessons from dopamine-deficient mice.
        Ann N Y Acad Sci. 2008; 1129: 35-46
        • Martinez D.
        • Broft A.
        • Foltin R.W.
        • Slifstein M.
        • Hwang D.R.
        • Huang Y.
        • et al.
        Cocaine dependence and d2 receptor availability in the functional subdivisions of the striatum: Relationship with cocaine-seeking behavior.
        Neuropsychopharmacology. 2004; 29: 1190-1202
        • Volkow N.D.
        • Wang G.J.
        • Telang F.
        • Fowler J.S.
        • Logan J.
        • Childress A.R.
        • et al.
        Cocaine cues and dopamine in dorsal striatum: Mechanism of craving in cocaine addiction.
        J Neurosci. 2006; 26: 6583-6588
        • Mawlawi O.
        • Martinez D.
        • Slifstein M.
        • Broft A.
        • Chatterjee R.
        • Hwang D.R.
        • et al.
        Imaging human mesolimbic dopamine transmission with positron emission tomography.
        J Cereb Blood Flow Metab. 2001; 21: 1034-1057
        • Comings D.E.
        • Comings B.G.
        • Muhleman D.
        • Dietz G.
        • Shahbahrami B.
        • Tast D.
        • et al.
        The dopamine D2 receptor locus as a modifying gene in neuropsychiatric disorders.
        JAMA. 1991; 266: 1793-1800
        • Comings D.E.
        • Muhleman D.
        • Gysin R.
        Dopamine D2 receptor (DRD2) gene and susceptibility to posttraumatic stress disorder: A study and replication.
        Biol Psychiatry. 1996; 40: 368-372
        • Lawford B.R.
        • Young R.
        • Noble E.P.
        • Kann B.
        • Ritchie T.
        The D2 dopamine receptor (DRD2) gene is associated with co-morbid depression, anxiety and social dysfunction in untreated veterans with post-traumatic stress disorder.
        Eur Psychiatry. 2006; 21: 180-185
        • Gelernter J.
        • Southwick S.
        • Goodson S.
        • Morgan A.
        • Nagy L.
        • Charney D.S.
        No association between D2 dopamine receptor (DRD2) “A” system alleles, or DRD2 haplotypes, and posttraumatic stress disorder.
        Biol Psychiatry. 1999; 45: 620-625
        • Noble E.P.
        D2 dopamine receptor gene in psychiatric and neurologic disorders and its phenotypes.
        Am J Med Genet B Neuropsychiatr Genet. 2003; 116B: 103-125
        • Volkow N.D.
        • Fowler J.S.
        • Wang G.J.
        • Swanson J.M.
        Dopamine in drug abuse and addiction: Results from imaging studies and treatment implications.
        Mol Psychiatry. 2004; 9: 557-569
        • Paterson N.E.
        • Markou A.
        Animal models and treatments for addiction and depression co-morbidity.
        Neurotox Res. 2007; 11: 1-32
        • Maleki S.A.
        • Samini M.
        • Babapour V.
        • Mehr S.E.
        • Cheraghiyan S.
        • Nouri M.H.
        Potentiation of morphine-induced conditioned place preference with concurrent use of amantadine and fluvoxamine by the intraperitoneal and intracerebroventricular injection in rat.
        Behav Brain Res. 2008; 190: 189-192
        • Moeller F.G.
        • Schmitz J.M.
        • Steinberg J.L.
        • Green C.M.
        • Reist C.
        • Lai L.Y.
        • et al.
        Citalopram combined with behavioral therapy reduces cocaine use: A double-blind, placebo-controlled trial.
        Am J Drug Alcohol Abus. 2007; 33: 367-378
        • Kumar P.
        • Waiter G.
        • Ahearn T.
        • Milders M.
        • Reid I.
        • Steele J.D.
        Abnormal temporal difference reward-learning signals in major depression.
        Brain. 2008; 131: 2084-2093
        • Krupitsky E.M.
        • Rudenko A.A.
        • Burakov A.M.
        • Slavina T.Y.
        • Grinenko A.A.
        • Pittman B.
        • et al.
        Antiglutamatergic strategies for ethanol detoxification: Comparison with placebo and diazepam.
        Alcohol Clin Exp Res. 2007; 31: 604-611
        • Charney D.S.
        Psychobiological mechanisms of resilience and vulnerability: Implications for successful adaptation to extreme stress.
        Am J Psychiatry. 2004; 161: 195-216
        • Schlagenhauf F.
        • Juckel G.
        • Koslowski M.
        • Kahnt T.
        • Knutson B.
        • Dembler T.
        • et al.
        Reward system activation in schizophrenic patients switched from typical neuroleptics to olanzapine.
        Psychopharmacology. 2008; 196: 673-684
        • Green A.I.
        • Noordsy D.L.
        • Brunette M.F.
        • O'Keefe C.
        Substance abuse and schizophrenia: Pharmacotherapeutic intervention.
        J Substance Abus Treat. 2008; 34: 61-71
        • Monnelly E.P.
        • Ciraulo D.A.
        • Knapp C.
        • Keane T.
        Low-dose risperidone as adjunctive therapy for irritable aggression in posttraumatic stress disorder.
        J Clin Psychopharmacol. 2003; 23: 193-196
        • Siddiqui Z.
        • Marcil W.A.
        • Bhatia S.C.
        • Ramaswamy S.
        • Petty F.
        Ziprasidone therapy for post-traumatic stress disorder.
        J Psychiatry Neurosci. 2005; 30: 430-431
        • Sattar S.P.
        • Ucci B.
        • Grant K.
        • Bhatia S.C.
        • Petty F.
        Quetiapine therapy for posttraumatic stress disorder.
        Ann Pharmacother. 2002; 36: 1875-1878