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Neural reward processing in individuals remitted from major depression

Published online by Cambridge University Press:  28 August 2015

B. Ubl ,
C. Kuehner ,
P. Kirsch ,
M. Ruttorf ,
H. Flor  and
C. Diener
B. Ubl*
Affiliation:
Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
C. Kuehner
Affiliation:
Research Group Longitudinal and Intervention Research, Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
P. Kirsch
Affiliation:
Department of Clinical Psychology, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
M. Ruttorf
Affiliation:
Computer Assisted Clinical Medicine, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
H. Flor
Affiliation:
Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
C. Diener
Affiliation:
School of Applied Psychology, SRH University of Applied Science, Heidelberg, Germany
*
* Address for correspondence: B. Ubl, Department of Cognitive and Clinical Neuroscience, Medical Faculty Mannheim, Heidelberg University, Central Institute of Mental Health, Square J5, 68159 Mannheim, Germany. (Email: [email protected])
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Abstract

Background.

Dysfunctional behavioural and neural processing of reward has been found in currently depressed individuals. However, little is known about altered reward processing in remitted depressed individuals.

Method.

A total of 23 medication-free individuals with remitted major depressive disorder (rMDD) and 23 matched healthy controls (HCs) performed a reward task during functional magnetic resonance imaging. We also investigated reward dependence, novelty seeking and harm avoidance using the Tridimensional Personality Questionnaire and their association with neural responses of reward processing.

Results.

Compared to HCs, individuals with rMDD exhibited enhanced responses to reward-predicting cues in the hippocampus, amygdala and superior frontal gyrus. When reward was delivered, rMDD subjects did not significantly differ from HCs. In both groups neural activity during reward anticipation was negatively correlated with harm avoidance.

Conclusions.

Our results show that rMDD is characterized by hyperactivation in fronto-limbic regions during reward anticipation. Alterations in neural activation during reward processing might reflect an increased effort in remitted depressed individuals to allocate neural activity for executive and evaluative processes during anticipatory reward processing.

Keywords

Functional magnetic resonance imagingremitted depressionrewardtemperament
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 16 , December 2015 , pp. 3549 - 3558
Copyright
Copyright © Cambridge University Press 2015 

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References

Abrams, KY, Yune, SK, Kim, SJ, Jeon, HJ, Han, SJ, Hwang, J, Sung, YH, Lee, KJ, Lyoo, IK (2004). Trait and state aspects of harm avoidance and its implication for treatment in major depressive disorder, dysthymic disorder, and depressive personality disorder. Psychiatry and Clinical Neurosciences 58, 240–248.CrossRefGoogle ScholarPubMed
Adcock, RA, Thangavel, A, Whitfield-Gabrieli, S, Knutson, B, Gabrieli, JD (2006). Reward-motivated learning: mesolimbic activation precedes memory formation. Neuron 50, 507–517.CrossRefGoogle ScholarPubMed
Alloy, LB, Abramson, LY, Whitehouse, WG, Hogan, ME, Tashman, NA, Steinberg, DL, Rose, DT, Donovan, P (1999). Depressogenic cognitive styles: predictive validity, information processing and personality characteristics, and developmental origins. Behaviour Research and Therapy 37, 503–531.CrossRefGoogle ScholarPubMed
Berridge, KC, Kringelbach, ML (2008). Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology (Berlin) 199, 457–480.Google Scholar
Celikel, FC, Kose, S, Cumurcu, BE, Erkorkmaz, U, Sayar, K, Borckardt, JJ, Cloninger, CR (2009). Cloninger's temperament and character dimensions of personality in patients with major depressive disorder. Comprehensive Psychiatry 50, 556–561.Google Scholar
Cloninger, CR (1987). A systematic method for clinical description and classification of personality variants. A proposal. Archives of General Psychiatry 44, 573–588.Google Scholar
Cloninger, CR, Przybeck, TR, Svrakic, DM (1991). The Tridimensional Personality Questionnaire: U.S. normative data. Psychological Reports 69, 1047–1057.Google Scholar
Cloninger, CR, Svrakic, DM, Przybeck, TR (1993). A psychobiological model of temperament and character. Archives of General Psychiatry 50, 975–990.Google Scholar
Cowell, SF, Egan, GF, Code, C, Harasty, J, Watson, JD (2000). The functional neuroanatomy of simple calculation and number repetition: a parametric PET activation study. NeuroImage 12, 565–573.CrossRefGoogle ScholarPubMed
Di Martino, A, Scheres, A, Margulies, DS, Kelly, AM, Uddin, LQ, Shehzad, Z, Biswal, B, Walters, JR, Castellanos, FX, Milham, MP (2008). Functional connectivity of human striatum: a resting state fMRI study. Cerebral Cortex 18, 2735–2747.Google Scholar
Dichter, GS, Kozink, RV, McClernon, FJ, Smoski, MJ (2012). Remitted major depression is characterized by reward network hyperactivation during reward anticipation and hypoactivation during reward outcomes. Journal of Affective Disorders 136, 1126–1134.Google Scholar
Diener, C, Kuehner, C, Brusniak, W, Ubl, B, Wessa, M, Flor, H (2012). A meta-analysis of neurofunctional imaging studies of emotion and cognition in major depression. NeuroImage 61, 677–685.Google Scholar
Dillon, DG, Deveney, CM, Pizzagalli, DA (2011). From basic processes to real-world problems: how research on emotion and emotion regulation can inform understanding of psychopathology, and vice versa. Emotion Review 3, 74–82.Google Scholar
Dillon, DG, Holmes, AJ, Jahn, AL, Bogdan, R, Wald, LL, Pizzagalli, DA (2008). Dissociation of neural regions associated with anticipatory versus consummatory phases of incentive processing. Psychophysiology 45, 36–49.CrossRefGoogle ScholarPubMed
du Boisgueheneuc, F, Levy, R, Volle, E, Seassau, M, Duffau, H, Kinkingnehun, S, Samson, Y, Zhang, S, Dubois, B (2006). Functions of the left superior frontal gyrus in humans: a lesion study. Brain. A Journal of Neurology 129, 3315–3328.CrossRefGoogle ScholarPubMed
Farmer, A, Mahmood, A, Redman, K, Harris, T, Sadler, S, McGuffin, P (2003). A sib-pair study of the Temperament and Character Inventory scales in major depression. Archives of General Psychiatry 60, 490–496.Google Scholar
Farmer, RF, Seeley, JR (2009). Temperament and character predictors of depressed mood over a 4-year interval. Depression and Anxiety 26, 371–381.CrossRefGoogle Scholar
Fava, M, Farabaugh, AH, Sickinger, AH, Wright, E, Alpert, JE, Sonawalla, S, Nierenberg, AA, Worthington III, JJ (2002). Personality disorders and depression. Psychological Medicine 32, 1049–1057.Google Scholar
Friston, KJ (1996). Statistical parametric mapping and other analysis of functional imaging data. In Brain Mapping. The Methods (ed. Toga, A.W. and Mazziotta, J.C.), pp. 363–385. Academic Press: San Diego, CA.Google Scholar
Friston, KJ, Holmes, AP, Poline, JB, Grasby, PJ, Williams, SC, Frackowiak, RS, Turner, R (1995). Analysis of fMRI time-series revisited. NeuroImage 2, 45–53.Google Scholar
Gusnard, DA, Ollinger, JM, Shulman, GL, Cloninger, CR, Price, JL, Van Essen, DC, Raichle, ME (2003). Persistence and brain circuitry. Proceedings of the National Academy of Sciences 100, 3479–3484.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 56–62.Google Scholar
Hasler, G, Drevets, WC, Manji, HK, Charney, DS (2004). Discovering endophenotypes for major depression. Neuropsychopharmacology 29, 1765–1781.Google Scholar
Hautzinger, M, Keller, F, Kühner, C (2006). “BDI II” Beck Depressions-Inventar (“BDI II” Beck Depression Inventory), 2nd revision. Harcourt-test Services: Frankfurt.Google Scholar
Holland, PC, Gallagher, M (2004). Amygdala–frontal interactions and reward expectancy. Current Opinion in Neurobiology 14, 148–155.Google Scholar
Huffziger, S, Ebner-Priemer, U, Zamoscik, V, Reinhard, I, Kirsch, P, Kuehner, C (2013). Effects of mood and rumination on cortisol levels in daily life: an ambulatory assessment study in remitted depressed patients and healthy controls. Psychoneuroendocrinology 38, 2258–2267.Google Scholar
Kerestes, R, Ladouceur, CD, Meda, S, Nathan, PJ, Blumberg, HP, Maloney, K, Ruf, B, Saricicek, A, Pearlson, GD, Bhagwagar, Z, Phillips, ML (2012). Abnormal prefrontal activity subserving attentional control of emotion in remitted depressed patients during a working memory task with emotional distracters. Psychological Medicine 42, 29–40.Google Scholar
Kirsch, P, Schienle, A, Stark, R, Sammer, G, Blecker, C, Walter, B, Ott, U, Burkart, J, Vaitl, D (2003). Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study. NeuroImage 20, 1086–1095.Google Scholar
Knutson, B, Bhanji, JP, Cooney, RE, Atlas, LY, Gotlib, IH (2008). Neural responses to monetary incentives in major depression. Biological Psychiatry 63, 686–692.Google Scholar
Knutson, B, Taylor, J, Kaufman, M, Peterson, R, Glover, G (2005). Distributed neural representation of expected value. Journal of Neuroscience 25, 4806–4812.Google Scholar
Kohls, G, Chevallier, C, Troiani, V, Schultz, RT (2012). Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications. Journal of Neurodevelopmental Disorders 4, 10.CrossRefGoogle ScholarPubMed
Lieberman, MD, Cunningham, WA (2009). Type I and type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience 4, 423–428.Google Scholar
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19, 1233–1239.Google Scholar
Mayberg, HS (2003). Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. British Medical Bulletin 65, 193–207.CrossRefGoogle ScholarPubMed
McCabe, C, Cowen, PJ, Harmer, CJ (2009). Neural representation of reward in recovered depressed patients. Psychopharmacology (Berlin) 205, 667–677.CrossRefGoogle ScholarPubMed
McCabe, C, Mishor, Z, Cowen, PJ, Harmer, CJ (2010). Diminished neural processing of aversive and rewarding stimuli during selective serotonin reuptake inhibitor treatment. Biological Psychiatry 67, 439–445.Google Scholar
McCabe, C, Woffindale, C, Harmer, CJ, Cowen, PJ (2012). Neural processing of reward and punishment in young people at increased familial risk of depression. Biological Psychiatry 72, 588–594.CrossRefGoogle ScholarPubMed
Mochcovitch, MD, Nardi, AE, Cardoso, A (2012). Temperament and character dimensions and their relationship to major depression and panic disorder. Revista Brasileira de Psiquiatria 34, 342–351.Google Scholar
Nelson, EC, Cloninger, CR (1995). The Tridimensional Personality Questionnaire as a predictor of response to nefazodone treatment of depression. Journal of Affective Disorders 35, 51–57.Google Scholar
Nery, FG, Hatch, JP, Nicoletti, MA, Monkul, ES, Najt, P, Matsuo, K, Cloninger, CR, Soares, JC (2009). Temperament and character traits in major depressive disorder: influence of mood state and recurrence of episodes. Depression and Anxiety 26, 382–388.Google Scholar
Ongur, D, Farabaugh, A, Iosifescu, DV, Perlis, R, Fava, M (2005). Tridimensional Personality Questionnaire factors in major depressive disorder: relationship to anxiety disorder comorbidity and age of onset. Psychotherapy and Psychosomatics 74, 173–178.Google Scholar
Pearce, JM, Hall, G (1980). A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychological Review 87, 532–552.Google Scholar
Peterson, BS, Weissman, MM (2011). A brain-based endophenotype for major depressive disorder. Annual Review of Medicine 62, 461–474.Google Scholar
Pizzagalli, DA (2011). Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology 36, 183–206.Google Scholar
Pizzagalli, DA, Holmes, AJ, Dillon, DG, Goetz, EL, Birk, JL, Bogdan, R, Dougherty, DD, Iosifescu, DV, Rauch, SL, Fava, M (2009). Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. American Journal of Psychiatry 166, 702–710.CrossRefGoogle ScholarPubMed
Plichta, MM, Schwarz, AJ, Grimm, O, Morgen, K, Mier, D, Haddad, L, Gerdes, AB, Sauer, C, Tost, H, Esslinger, C, Colman, P, Wilson, F, Kirsch, P, Meyer-Lindenberg, A (2012). Test–retest reliability of evoked BOLD signals from a cognitive-emotive fMRI test battery. NeuroImage 60, 1746–1758.Google Scholar
Poldrack, RA, Mumford, JA (2009). Independence in ROI analysis: where is the voodoo? Social Cognitive and Affective Neuroscience 4, 208–213.Google Scholar
Simmons, WK, Drevets, WC (2012). A “taste” of what is to come: reward sensitivity as a potential endophenotype for major depressive disorder. Biological Psychiatry 72, 526–527.Google Scholar
Smith, DJ, Duffy, L, Stewart, ME, Muir, WJ, Blackwood, DH (2005). High harm avoidance and low self-directedness in euthymic young adults with recurrent, early-onset depression. Journal of Affective Disorders 87, 83–89.Google Scholar
Smoski, MJ, Felder, J, Bizzell, J, Green, SR, Ernst, M, Lynch, TR, Dichter, GS (2009). fMRI of alterations in reward selection, anticipation, and feedback in major depressive disorder. Journal of Affective Disorders 118, 69–78.CrossRefGoogle ScholarPubMed
Stoy, M, Schlagenhauf, F, Schlochtermeier, L, Wrase, J, Knutson, B, Lehmkuhl, U, Huss, M, Heinz, A, Strohle, A (2011). Reward processing in male adults with childhood ADHD – a comparison between drug-naive and methylphenidate-treated subjects. Psychopharmacology (Berlin) 215, 467–481.Google Scholar
Strange, BA, Duggins, A, Penny, W, Dolan, RJ, Friston, KJ (2005). Information theory, novelty and hippocampal responses: unpredicted or unpredictable? Neural Networks 18, 225–230.Google Scholar
Suzuki, WA, Amaral, DG (1994). Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. Journal of Comparative Neurology 350, 497–533.CrossRefGoogle ScholarPubMed
Treadway, MT, Zald, DH (2011). Reconsidering anhedonia in depression: lessons from translational neuroscience. Neuroscience and Biobehavioral Reviews 35, 537–555.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273–289.Google Scholar
Ubl, B, Kuehner, C, Kirsch, P, Ruttorf, M, Diener, C, Flor, H (2015). Altered neural reward and loss processing and prediction error signalling in depression. Social Cognitive and Affective Neuroscience 10, 1102–1112.Google Scholar
Vanni-Mercier, G, Mauguiere, F, Isnard, J, Dreher, JC (2009). The hippocampus codes the uncertainty of cue-outcome associations: an intracranial electrophysiological study in humans. Journal of Neuroscience 29, 5287–5294.CrossRefGoogle ScholarPubMed
Volz, KG, Schubotz, RI, von Cramon, DY (2005). Variants of uncertainty in decision-making and their neural correlates. Brain Research Bulletin 67, 403–412.CrossRefGoogle ScholarPubMed
Wittchen, H-U, Zaudig, M, Fydrich, T (1997). Strukturiertes Klinisches Interview für DSM-IV (Structured Clinical Interview for DSM-IV). Hogrefe: Göttingen.Google Scholar
Yacubian, J, Glascher, J, Schroeder, K, Sommer, T, Braus, DF, Buchel, C (2006). Dissociable systems for gain- and loss-related value predictions and errors of prediction in the human brain. Journal of Neuroscience 26, 9530–9537.Google Scholar
Zald, DH (2003). The human amygdala and the emotional evaluation of sensory stimuli. Brain Research Reviews 41, 88–123.Google Scholar
Zappitelli, MC, Bordin, IA, Hatch, JP, Caetano, SC, Zunta-Soares, G, Olvera, RL, Soares, JC (2013). Temperament and character traits in children and adolescents with major depressive disorder: a case–control study. Comprehensive Psychiatry 54, 346–353.Google Scholar