Advertisement
Archival Report| Volume 72, ISSUE 2, P157-163, July 15, 2012

Ventral Striatum Reactivity to Reward and Recent Life Stress Interact to Predict Positive Affect

      Background

      Stressful life events are among the most reliable precipitants of major depressive disorder; yet, not everyone exposed to stress develops depression. It has been hypothesized that robust neural reactivity to reward and associated stable levels of positive affect (PA) may protect against major depressive disorder in the context of environmental adversity. However, little empirical data exist to confirm this postulation. Here, we test the hypothesis that individuals with relatively low ventral striatum (VS) reactivity to reward will show low PA levels in the context of recent life stress, while those with relatively high VS reactivity will be protected against these potentially depressogenic effects.

      Methods

      Differential VS reactivity to positive feedback was assessed using blood oxygen level-dependent functional magnetic resonance imaging in a sample of 200 nonpatient young adults. Recent life stress, current depressive symptoms, and PA were assessed via self-report. Linear regression models were used to investigate the moderating effects of VS reactivity on the relationship between recent stress and state PA across participants.

      Results

      Recent life stress interacted with VS reactivity to predict self-reported state PA, such that higher levels of life stress were associated with lower PA for participants with relatively low, but not for those with high, VS reactivity. These effects were independent of age, gender, race/ethnicity, trait PA, and early childhood trauma.

      Conclusions

      The current results provide empirical evidence for the potentially protective role of robust reward-related neural responsiveness against reductions in PA that may occur in the wake of life stress and possibly vulnerability to depression precipitated by stressful life events.

      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

        • van Praag H.M.
        Can stress cause depression?.
        Prog Neuropsychopharmacol Biol Psychiatry. 2004; 28: 891-907
        • Brown G.
        • Harris T.O.
        Social Origins of Depression.
        The Free Press, New York1978
        • Anisman H.
        • Matheson K.
        Stress, depression, and anhedonia: Caveats concerning animal models.
        Neurosci Biobehav Rev. 2005; 29: 525-546
        • Willner P.
        Chronic mild stress (CMS) revisited: Consistency and behavioural-neurobiological concordance in the effects of CMS.
        Neuropsychobiology. 2005; 52: 90-110
        • Bogdan R.
        • Pizzagalli D.A.
        Acute stress reduces reward responsiveness: Implications for depression.
        Biol Psychiatry. 2006; 60: 1147-1154
        • Berenbaum H.
        • Connelly J.
        The effect of stress on hedonic capacity.
        J Abnorm Psychol. 1993; 102: 474-481
        • Steele J.D.
        • Kumar P.
        • Ebmeier K.P.
        Blunted response to feedback information in depressive illness.
        Brain. 2007; 130: 2367-2374
        • Epstein J.
        • Pan H.
        • Kocsis J.H.
        • Yang Y.
        • Butler T.
        • Chusid J.
        • et al.
        Lack of ventral striatal response to positive stimuli in depressed versus normal subjects.
        Am J Psychiatry. 2006; 163: 1784-1790
        • Keedwell P.A.
        • Andrew C.
        • Williams S.C.
        • Brammer M.J.
        • Phillips M.L.
        The neural correlates of anhedonia in major depressive disorder.
        Biol Psychiatry. 2005; 58: 843-853
        • Surguladze S.
        • Brammer M.J.
        • Keedwell P.
        • Giampietro V.
        • Young A.W.
        • Travis M.J.
        • et al.
        A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder.
        Biol Psychiatry. 2005; 57: 201-209
        • Charney D.S.
        Psychobiological mechanisms of resilience and vulnerability: Implications for successful adaptation to extreme stress.
        Am J Psychiatry. 2004; 161: 195-216
        • Feder A.
        • Nestler E.J.
        • Charney D.S.
        Psychobiology and molecular genetics of resilience.
        Nat Rev Neurosci. 2009; 10: 446-457
        • Radloff L.S.
        The CES-D scale: A self-report depression scale for research in the general population.
        Appl Psychol Meas. 1977; 1: 385-401
        • Folkman S.
        • Moskowitz J.T.
        Positive affect and the other side of coping.
        Am Psychol. 2000; 55: 647-654
        • Watson D.
        • Clark L.A.
        • Carey G.
        Positive and negative affectivity and their relation to anxiety and depressive disorders.
        J Abnorm Psychol. 1988; 97: 346-353
        • Forbes E.E.
        • Hariri A.R.
        • Martin S.L.
        • Silk J.S.
        • Moyles D.L.
        • Fisher P.M.
        • et al.
        Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder.
        Am J Psychiatry. 2009; 166: 64-73
        • Berridge K.C.
        • Robinson T.E.
        • Aldridge J.W.
        Dissecting components of reward: 'Liking', 'wanting', and learning.
        Curr Opin Pharmacol. 2009; 9: 65-73
        • Haber S.N.
        • Knutson B.
        The reward circuit: Linking primate anatomy and human imaging.
        Neuropsychopharmacology. 2010; 35: 4-26
        • Forbes E.E.
        • Brown S.M.
        • Kimak M.
        • Ferrell R.E.
        • Manuck S.B.
        • Hariri A.R.
        Genetic variation in components of dopamine neurotransmission impacts ventral striatal reactivity associated with impulsivity.
        Mol Psychiatry. 2009; 14: 60-70
        • Hariri A.R.
        • Brown S.M.
        • Williamson D.E.
        • Flory J.D.
        • de Wit H.
        • Manuck S.B.
        Preference for immediate over delayed rewards is associated with magnitude of ventral striatal activity.
        J Neurosci. 2006; 26: 13213-13217
        • Sheehan D.V.
        • Lecrubier Y.
        • Sheehan K.H.
        • Amorim P.
        • Janavs J.
        • Weiller E.
        • et al.
        The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10.
        J Clin Psychiatry. 1998; 59 (quiz 34–57): 22-33
        • First M.B.
        • Spitzer R.L.
        • Gibbon M.
        • Williams J.B.M.
        Structured Clinical Interview for DSM-IV Axis I Disorders, Research Version, Non-patient Edition. New York State Psychiatric Institute, Biometrics Research Department, New York1996
        • Ojemann J.G.
        • Akbudak E.
        • Snyder A.Z.
        • McKinstry R.C.
        • Raichle M.E.
        • Conturo T.E.
        Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts.
        Neuroimage. 1997; 6: 156-167
        • Viviani R.
        Unbiased ROI selection in neuroimaging studies of individual differences.
        Neuroimage. 2010; 50: 184-189
        • Hyde L.W.
        • Gorka A.
        • Manuck S.B.
        • Hariri A.R.
        Perceived social support moderates the link between threat-related amygdala reactivity and trait anxiety.
        Neuropsychologia. 2011; 49: 651-656
        • Carre J.M.
        • Fisher P.M.
        • Manuck S.B.
        • Hariri A.R.
        Interaction between trait anxiety and trait anger predict amygdala reactivity to angry facial expressions in men but not women.
        Soc Cogn Affect Neurosci. 2012; 7: 213-221
        • Nikolova Y.S.
        • Ferrell R.E.
        • Manuck S.B.
        • Hariri A.R.
        Multilocus genetic profile for dopamine signaling predicts ventral striatum reactivity.
        Neuropsychopharmacology. 2011; 36: 1940-1947
        • Weissman M.M.
        • Sholomskas D.
        • Pottenger M.
        • Prusoff B.A.
        • Locke B.Z.
        Assessing depressive symptoms in five psychiatric populations: A validation study.
        Am J Epidemiol. 1977; 106: 203-214
        • Shafer A.B.
        Meta-analysis of the factor structures of four depression questionnaires: Beck, CES-D, Hamilton, and Zung.
        J Clin Psychol. 2006; 62: 123-146
        • Leventhal A.M.
        • Ramsey S.E.
        • Brown R.A.
        • LaChance H.R.
        • Kahler C.W.
        Dimensions of depressive symptoms and smoking cessation.
        Nicotine Tob Res. 2008; 10: 507-517
        • Costa P.T.
        • McCrae R.R.
        Normal personality assessment in clinical practice: The NEO Personality Inventory.
        Psychol Assess. 1992; 4: 5-13
        • Clements K.
        • Turpin G.
        The life events scale for students: Validation for use with British samples.
        Pers Individ Dif. 1996; 20: 747-751
        • Bernstein D.
        • Stein J.A.
        • Newcomb M.D.
        • Walker E.
        • Pogge D.
        • Ahluvalia T.
        • et al.
        Development and validation of a brief screening version of the Childhood Trauma Questionnaire.
        Child Abuse Negl. 2002; 27: 169-190
        • Johnson P.O.
        • Fay L.C.
        The Johnson-Neyman technique, its theory and application.
        Psychometrika. 1950; 15: 349-367
        • Hayes A.F.
        • Matthes J.
        Computational procedures for probing interactions in OLS and logistic regression: SPSS and SAS implementations.
        Behav Res Methods. 2009; 41: 924-936
        • Spreckelmeyer K.N.
        • Krach S.
        • Kohls G.
        • Rademacher L.
        • Irmak A.
        • Konrad K.
        • et al.
        Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women.
        Soc Cogn Affect Neurosci. 2009; 4: 158-165
        • Pizzagalli D.A.
        • Holmes A.J.
        • Dillon D.G.
        • Goetz E.L.
        • Birk J.L.
        • Bogdan R.
        • et al.
        Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder.
        Am J Psychiatry. 2009; 166: 702-710
        • Elovainio M.
        • Jokela M.
        • Kivimaki M.
        • Pulkki-Raback L.
        • Lehtimaki T.
        • Airla N.
        • Keltikangas-Järvinen L.
        Genetic variants in the DRD2 gene moderate the relationship between stressful life events and depressive symptoms in adults: Cardiovascular risk in young Finns study.
        Psychosom Med. 2007; 69: 391-395
        • Haeffel G.J.
        • Getchell M.
        • Koposov R.A.
        • Yrigollen C.M.
        • Deyoung C.G.
        • Klinteberg B.A.
        • et al.
        Association between polymorphisms in the dopamine transporter gene and depression: Evidence for a gene-environment interaction in a sample of juvenile detainees.
        Psychol Sci. 2008; 19: 62-69
        • Dillon D.G.
        • Holmes A.J.
        • Birk J.L.
        • Brooks N.
        • Lyons-Ruth K.
        • Pizzagalli D.A.
        Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood.
        Biol Psychiatry. 2009; 66: 206-213
        • Bogdan R.
        • Santesso D.L.
        • Fagerness J.
        • Perlis R.H.
        • Pizzagalli D.A.
        Corticotropin-releasing hormone receptor type 1 (CRHR1) genetic variation and stress interact to influence reward learning.
        J Neurosci. 2011; 31: 13246-13254
        • Heim C.
        • Owens M.J.
        • Plotsky P.M.
        • Nemeroff C.B.
        The role of early adverse life events in the etiology of depression and posttraumatic stress disorder.
        Ann N Y Acad Sci. 1997; 821: 194-207
        • Vythilingam M.
        • Nelson E.E.
        • Scaramozza M.
        • Waldeck T.
        • Hazlett G.
        • Southwick S.M.
        • et al.
        Reward circuitry in resilience to severe trauma: An fMRI investigation of resilient special forces soldiers.
        Psychiatry Res. 2009; 172: 75-77
        • Paykel E.S.
        Methodological aspects of life events research.
        J Psychosom Res. 1983; 27: 341-352
        • Duggal S.
        • Malkoff-Schwartz S.
        • Birmaher B.
        • Anderson B.P.
        • Matty M.K.
        • Houck P.R.
        • et al.
        Assessment of life stress in adolescents: Self-report versus interview methods.
        J Am Acad Child Adolesc Psychiatry. 2000; 39: 445-452
        • Jocham G.
        • Klein T.A.
        • Neumann J.
        • von Cramon D.Y.
        • Reuter M.
        • Ullsperger M.
        Dopamine DRD2 polymorphism alters reversal learning and associated neural activity.
        J Neurosci. 2009; 29: 3695-3704
        • Yacubian J.
        • Sommer T.
        • Schroeder K.
        • Glascher J.
        • Kalisch R.
        • Leuenberger B.
        • et al.
        Gene-gene interaction associated with neural reward sensitivity.
        Proc Natl Acad Sci U S A. 2007; 104: 8125-8130
        • Young E.J.
        • Williams C.L.
        Valence dependent asymmetric release of norepinephrine in the basolateral amygdala.
        Behav Neurosci. 2010; 124: 633-644
        • Besson C.
        • Louilot A.
        Asymmetrical involvement of mesolimbic dopaminergic neurons in affective perception.
        Neuroscience. 1995; 68: 963-968
        • Sullivan R.M.
        • Dufresne M.M.
        Mesocortical dopamine and HPA axis regulation: Role of laterality and early environment.
        Brain Res. 2006; 1076: 49-59
        • Merali Z.
        • McIntosh J.
        • Anisman H.
        Anticipatory cues differentially provoke in vivo peptidergic and monoaminergic release at the medial prefrontal cortex.
        Neuropsychopharmacology. 2004; 29: 1409-1418
        • Watson D.
        Rethinking the mood and anxiety disorders: A quantitative hierarchical model for DSM-V.
        J Abnorm Psychol. 2005; 114: 522-536
        • Sheeber L.B.
        • Allen N.B.
        • Leve C.
        • Davis B.
        • Shortt J.W.
        • Katz L.F.
        Dynamics of affective experience and behavior in depressed adolescents.
        J Child Psychol Psychiatry. 2009; 50: 1419-1427
        • Kendler K.S.
        • Karkowski L.M.
        • Prescott C.A.
        Stressful life events and major depression: Risk period, long-term contextual threat, and diagnostic specificity.
        J Nerv Ment Dis. 1998; 186: 661-669
        • Post R.M.
        Transduction of psychosocial stress into the neurobiology of recurrent affective disorder.
        Am J Psychiatry. 1992; 149: 999-1010
        • Caspi A.
        • Sugden K.
        • Moffitt T.E.
        • Taylor A.
        • Craig I.W.
        • Harrington H.
        • et al.
        Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene.
        Science. 2003; 301: 386-389
        • Pizzagalli D.A.
        • Bogdan R.
        • Ratner K.G.
        • Jahn A.L.
        Increased perceived stress is associated with blunted hedonic capacity: Potential implications for depression research.
        Behav Res Ther. 2007; 45: 2742-2753
        • Buckholtz J.W.
        • Treadway M.T.
        • Cowan R.L.
        • Woodward N.D.
        • Benning S.D.
        • Li R.
        • et al.
        Mesolimbic dopamine reward system hypersensitivity in individuals with psychopathic traits.
        Nat Neurosci. 2010; 13: 419-421
        • Hariri A.R.
        The neurobiology of individual differences in complex behavioral traits.
        Annu Rev Neurosci. 2009; 32: 225-247