Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T05:30:44.783Z Has data issue: false hasContentIssue false

From laboratory to life: associating brain reward processing with real-life motivated behaviour and symptoms of depression in non-help-seeking young adults

Published online by Cambridge University Press:  29 November 2018

Jindra M. Bakker*
Affiliation:
Department of Psychiatry and Psychology, Maastricht University, Maastricht University Medical Centre, School for Mental Health and Neuroscience, Maastricht, The Netherlands Department of Neuroscience, KU Leuven, Center for Contextual Psychiatry, Leuven, Belgium
Liesbet Goossens
Affiliation:
Department of Psychiatry and Psychology, Maastricht University, Maastricht University Medical Centre, School for Mental Health and Neuroscience, Maastricht, The Netherlands
Poornima Kumar
Affiliation:
McLean Hospital, Center for Depression, Anxiety and Stress Research, Belmont, MA, USA Department of Psychiatry, Harvard Medical School, Boston, MA, USA
Iris M. J. Lange
Affiliation:
Department of Psychiatry and Psychology, Maastricht University, Maastricht University Medical Centre, School for Mental Health and Neuroscience, Maastricht, The Netherlands
Stijn Michielse
Affiliation:
Department of Psychiatry and Psychology, Maastricht University, Maastricht University Medical Centre, School for Mental Health and Neuroscience, Maastricht, The Netherlands
Koen Schruers
Affiliation:
Department of Psychiatry and Psychology, Maastricht University, Maastricht University Medical Centre, School for Mental Health and Neuroscience, Maastricht, The Netherlands Department of Psychology, KU Leuven, Leuven, Belgium
Jojanneke A. Bastiaansen
Affiliation:
Department of Psychiatry (UCP), University of Groningen, University Medical Centre Groningen, Interdisciplinary Center Psychopathology and Emotion regulation (ICPE), Groningen, The Netherlands Friesland Mental Health Care Services, Leeuwarden, The Netherlands
Ritsaert Lieverse
Affiliation:
Department of Psychiatry and Psychology, Maastricht University, Maastricht University Medical Centre, School for Mental Health and Neuroscience, Maastricht, The Netherlands
Machteld Marcelis
Affiliation:
Department of Psychiatry and Psychology, Maastricht University, Maastricht University Medical Centre, School for Mental Health and Neuroscience, Maastricht, The Netherlands Institute for Mental Health Care Eindhoven (GGzE), Eindhoven, the Netherlands
Thérèse van Amelsvoort
Affiliation:
Department of Psychiatry and Psychology, Maastricht University, Maastricht University Medical Centre, School for Mental Health and Neuroscience, Maastricht, The Netherlands
Jim van Os
Affiliation:
Department of Psychiatry and Psychology, Maastricht University, Maastricht University Medical Centre, School for Mental Health and Neuroscience, Maastricht, The Netherlands Department of Psychiatry, Utrecht University, University Medical Center, Brain Center Rudolf Magnus, Utrecht, The Netherlands Department of Psychosis Studies, King's College, King's Health Partners, Institute of Psychiatry, London, UK
Inez Myin-Germeys
Affiliation:
Department of Neuroscience, KU Leuven, Center for Contextual Psychiatry, Leuven, Belgium
Diego A. Pizzagalli
Affiliation:
McLean Hospital, Center for Depression, Anxiety and Stress Research, Belmont, MA, USA Department of Psychiatry, Harvard Medical School, Boston, MA, USA
Marieke Wichers
Affiliation:
Department of Psychiatry (UCP), University of Groningen, University Medical Centre Groningen, Interdisciplinary Center Psychopathology and Emotion regulation (ICPE), Groningen, The Netherlands
*
Author for correspondence: Jindra M. Bakker, E-mail: jindra.bakker@maastrichtuniversity.nl

Abstract

Background

Depression has been associated with abnormalities in neural underpinnings of Reward Learning (RL). However, inconsistencies have emerged, possibly owing to medication effects. Additionally, it remains unclear how neural RL signals relate to real-life behaviour. The current study, therefore, examined neural RL signals in young, mildly to moderately depressed – but non-help-seeking and unmedicated – individuals and how these signals are associated with depressive symptoms and real-life motivated behaviour.

Methods

Individuals with symptoms along the depression continuum (n = 87) were recruited from the community. They performed an RL task during functional Magnetic Resonance Imaging and were assessed with the Experience Sampling Method (ESM), completing short questionnaires on emotions and behaviours up to 10 times/day for 15 days. Q-learning model-derived Reward Prediction Errors (RPEs) were examined in striatal areas, and subsequently associated with depressive symptoms and an ESM measure capturing (non-linearly) how anticipation of reward experience corresponds to actual reward experience later on.

Results

Significant RPE signals were found in the striatum, insula, amygdala, hippocampus, frontal and occipital cortices. Region-of-interest analyses revealed a significant association between RPE signals and (a) self-reported depressive symptoms in the right nucleus accumbens (b = −0.017, p = 0.006) and putamen (b = −0.013, p = .012); and (b) the quadratic ESM variable in the left (b = 0.010, p = .010) and right (b = 0.026, p = 0.011) nucleus accumbens and right putamen (b = 0.047, p < 0.001).

Conclusions

Striatal RPE signals are disrupted along the depression continuum. Moreover, they are associated with reward-related behaviour in real-life, suggesting that real-life coupling of reward anticipation and engagement in rewarding activities might be a relevant target of psychological therapies for depression.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Aickin, M and Gensler, H (1996) Adjusting for multiple testing when reporting research results: the Bonferroni vs Holm methods. American Journal of Public Health 86, 726728.Google Scholar
Bakker, JM, Goossens, L, Lange, I, Michielse, S, Schruers, K, Lieverse, R, Marcelis, M, van Amelsvoort, T, van Os, J, Myin-Germeys, I and Wichers, M (2017) Real-life validation of reduced reward processing in emerging adults with depressive symptoms. Journal of Abnormal Psychology 126, 713725.Google Scholar
Bayer, HM and Glimcher, PW (2005) Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47, 129141.Google Scholar
Bylsma, LM, Taylor-Clift, A and Rottenberg, J (2011) Emotional reactivity to daily events in major and minor depression. Journal of Abnormal Psychology 120, 155.Google Scholar
Chase, HW, Kumar, P, Eickhoff, SB and Dombrovski, AY (2015) Reinforcement learning models and their neural correlates: an activation likelihood estimation meta-analysis. Cognitive, Affective, & Behavioral Neuroscience 15, 435459.Google Scholar
Craske, MG, Meuret, AE, Ritz, T, Treanor, M and Dour, HJ (2016) Treatment for anhedonia: a neuroscience driven approach. Depression and Anxiety 33, 927938.Google Scholar
Csikszentmihalyi, M and Larson, R (1987) Validity and reliability of the Experience-Sampling Method. Journal of Nervous and Mental Disease 175, 526536.Google Scholar
Daw, ND (2011) Trial-by-trial data analysis using computational models. In Delgado, MR, Phelps, EA and Robbins, TW (eds), Decision Making, Affect, and Learning: Attention and Performance XXIII. New York: Oxford University Press, pp. 338.Google Scholar
Delespaul, PAEG (1995) Assessing Schizophrenia in Daily Life: The Experience Sampling Method. Maastricht, The Netherlands: Maastricht University Press.Google Scholar
Eldar, E and Niv, Y (2015) Interaction between emotional state and learning underlies mood instability. Nature Communications 6, 6149.Google Scholar
Eldar, E, Rutledge, RB, Dolan, RJ and Niv, Y (2016) Mood as representation of momentum. Trends in Cognitive Sciences 20, 1524.Google Scholar
Fantino, B and Moore, N (2009) The self-reported Montgomery-Åsberg depression rating scale is a useful evaluative tool in major depressive disorder. BMC Psychiatry 9, 26.Google Scholar
Forbes, EE, Hariri, AR, Martin, SL, Silk, JS, Moyles, DL, Fisher, PM, Brown, SM, Ryan, ND, Birmaher, B, Axelson, DA and Dahl, RE (2009) Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder. The American Journal of Psychiatry 166, 6473.Google Scholar
Forbes, EE, Ryan, ND, Phillips, ML, Manuck, SB, Worthman, CM, Moyles, DL, Tarr, JA, Sciarrillo, SR and Dahl, RE (2010) Healthy adolescents’ neural response to reward: associations with puberty, positive affect, and depressive symptoms. Journal of the American Academy of Child & Adolescent Psychiatry 49, 162172.e5.Google Scholar
Gard, DE, Gard, MG, Kring, AM and John, OP (2006) Anticipatory and consummatory components of the experience of pleasure: a scale development study. Journal of Research in Personality 40, 10861102.Google Scholar
Garrison, J, Erdeniz, B and Done, J (2013) Prediction error in reinforcement learning: a meta-analysis of neuroimaging studies. Neuroscience and Biobehavioral Reviews 37, 12971310.Google Scholar
Gold, JM, Waltz, JA, Matveeva, TM, Kasanova, Z, Strauss, GP, Herbener, ES, Collins, AG and Frank, MJ (2012) Negative symptoms and the failure to represent the expected reward value of actions: behavioral and computational modeling evidence. Archives of General Psychiatry 69, 129138.Google Scholar
Gotlib, IH, Hamilton, JP, Cooney, RE, Singh, MK, Henry, ML and Joormann, J (2010) Neural processing of reward and loss in girls at risk for major depression. Archives of General Psychiatry 67, 380387.Google Scholar
Gradin, VB, Kumar, P, Waiter, G, Ahearn, T, Stickle, C, Milders, M, Reid, I, Hall, J and Steele, JD (2011) Expected value and prediction error abnormalities in depression and schizophrenia. Brain 134, 17511764.Google Scholar
Hamid, AA, Pettibone, JR, Mabrouk, OS, Hetrick, VL, Schmidt, R, Vander Weele, CM, Kennedy, RT, Aragona, BJ and Berke, JD (2016) Mesolimbic dopamine signals the value of work. Nature Neuroscience 19, 117126.Google Scholar
Hankin, BL, Fraley, RC, Lahey, BB and Waldman, ID (2005) Is depression best viewed as a continuum or discrete category? A taxometric analysis of childhood and adolescent depression in a population-based sample. Journal of Abnormal Psychology 114, 96110.Google Scholar
Heller, AS, Fox, AS, Wing, EK, McQuisition, KM, Vack, NJ and Davidson, RJ (2015) The neurodynamics of affect in the laboratory predicts persistence of real-world emotional responses. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 35, 1050310509.Google Scholar
Holm, S (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6, 6570.Google Scholar
Kasanova, Z, Ceccarini, J, Frank, MJ, Amelsvoort, TV, Booij, J, Heinzel, A, Mottaghy, F and Myin-Germeys, I (2017) Striatal dopaminergic modulation of reinforcement learning predicts reward-oriented behavior in daily life. Biological Psychology 127, 19.Google Scholar
Kramer, I, Simons, CJP, Hartmann, JA, Menne-Lothmann, C, Viechtbauer, W, Peeters, F, Schruers, K, Bemmel, AL, Myin-Germeys, I, Delespaul, P, Os, J and Wichers, M (2014) A therapeutic application of the experience sampling method in the treatment of depression: a randomized controlled trial. World Psychiatry 13, 6877.Google Scholar
Kumar, P, Waiter, G, Ahearn, T, Milders, M, Reid, I and Steele, D (2008) Abnormal temporal difference reward-learning signals in major depression. Brain 131, 20842093.Google Scholar
Lewinsohn, PM and Graf, M (1973) Pleasant activities and depression. Journal of Consulting and Clinical Psychology 41, 261.Google Scholar
Liu, RT (2016) Taxometric evidence of a dimensional latent structure for depression in an epidemiological sample of children and adolescents. Psychological Medicine 46, 12651275.Google Scholar
McCabe, C, Cowen, PJ and Harmer, CJ (2009) Neural representation of reward in recovered depressed patients. Psychopharmacology 205, 667677.Google Scholar
McCabe, C, Woffindale, C, Harmer, CJ and Cowen, PJ (2012) Neural processing of reward and punishment in young people at increased familial risk of depression. Biological Psychiatry 72, 588594.Google Scholar
Montgomery, SA and Åsberg, M (1979) A new depression scale designed to be sensitive to change. The British Journal of Psychiatry 134, 382389.Google Scholar
Myin-Germeys, I, Oorschot, M, Collip, D, Lataster, J, Delespau, P and van Os, J (2009) Experience sampling research in psychopathology: opening the black box of daily life. Psychological Medicine 39, 15331547.Google Scholar
O'Doherty, JP, Hampton, A and Kim, H (2007) Model-based fMRI and its application to reward learning and decision making. Annals of the New York Academy of Sciences 1104, 3553.Google Scholar
Olino, TM, McMakin, DL, Morgan, JK, Silk, JS, Birmaher, B, Axelson, DA, Williamson, DE, Dahl, RE, Ryan, ND and Forbes, EE (2014) Reduced reward anticipation in youth at high-risk for unipolar depression: a preliminary study. Developmental Cognitive Neuroscience 8, 5564.Google Scholar
Overbeek, T, Schruers, K and Griez, E (1999) Mini International Neuropsychiatric Interview, Nederlandse Versie 5.0.0. Maastricht, the Netherlands: Maastricht University.Google Scholar
Pessiglione, M, Seymour, B, Flandin, G, Dolan, RJ and Frith, CD (2006) Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442, 10421045.Google Scholar
Pizzagalli, DA, Holmes, A, Dillon, DG, Goetz, EL, Birk, JL, Ryan, B, Dougherty, DD, Iosifescu, DV, Rauch, SL and Fava, M (2009) Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. The American Journal of Psychiatry 166, 702710.Google Scholar
Prisciandaro, JJ and Roberts, JE (2009) A comparison of the predictive abilities of dimensional and categorical models of unipolar depression in the National Comorbidity Survey. Psychological Medicine 39, 10871096.Google Scholar
Rakofsky, JJ, Schettler, PJ, Kinkead, BL, Frank, E, Judd, LL, Kupfer, DJ, Rush, AJ, Thase, ME, Yonkers, KA and Rapaport, MH (2013) The prevalence and severity of depressive symptoms along the spectrum of unipolar depressive disorders: a post hoc analysis. Journal of Clinical Psychiatry 74, 10841091.Google Scholar
Robinson, OJ, Cools, R, Carlisi, CO, Sahakian, BJ and Drevets, WC (2012) Ventral striatum response during reward and punishment reversal learning in unmedicated major depressive disorder. American Journal of Psychiatry 169, 152159.Google Scholar
Rogers, WH (1993) Sg17: Regression standard errors in clustered samples. Stata Technical Bulletin 13, pp. 1923.Google Scholar
Rolls, ET (1999) The Brain and Emotion. New York, NY: Oxford University Press.Google Scholar
Rothkirch, M, Tonn, J, Kohler, S and Sterzer, P (2017) Neural mechanisms of reinforcement learning in unmedicated patients with major depressive disorder. Brain 140, 11471157.Google Scholar
Ruscio, J, Brown, TA and Meron Ruscio, A (2009) A taxometric investigation of DSM-IV major depression in a large outpatient sample: interpretable structural results depend on the mode of assessment. Assessment 16, 127144.Google Scholar
Rush, AJ, Gullion, CM, Basco, MR, Jarrett, RB and Trivedi, MH (2009) The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychological Medicine 26, 477486.Google Scholar
Rutledge, RB, Skandali, N, Dayan, P and Dolan, RJ (2014) A computational and neural model of momentary subjective well-being. Proceedings of the National Academy of Sciences 111, 1225212257.Google Scholar
Schultz, W, Tremblay, L and Hollerman, JR (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cerebral Cortex 10, 272283.Google Scholar
Sharp, C, Kim, S, Herman, L, Pane, H, Reuter, T and Strathearn, L (2014) Major depression in mothers predicts reduced ventral striatum activation in adolescent female offspring with and without depression. Journal of Abnormal Psychology 123, 298309.Google Scholar
Sharpley, CF and Bitsika, V (2013) Differences in neurobiological pathways of four “clinical content” subtypes of depression. Behavioural Brain Research 256, 368376.Google Scholar
Sherdell, L, Waugh, CE and Gotlib, IH (2012) Anticipatory pleasure predicts motivation for reward in major depression. Journal of Abnormal Psychology 121, 5160.Google Scholar
Smoski, MJ, Felder, J, Bizzell, J, Green, SR, Ernst, M, Lynch, TR and Dichter, GS (2009) fMRI of alterations in reward selection, anticipation, and feedback in major depressive disorder. Journal of Affective Disorders 118, 6978.Google Scholar
Snijders, T and Bosker, R (1999) Multilevel Analysis: An introduction to Basis and Advanced Multilevel Modeling. London, UK: Sage.Google Scholar
StataCorp (2013). Stata Statistical Software: Release 13. College Station, TX: StataCorp LP.Google Scholar
Sutton, RS and Barto, AG (1998) Reinforcement Learning: An Introduction. Cambridge, MA: MIT press.Google Scholar
Thompson, RJ, Mata, J, Jaeggi, SM, Buschkuehl, M, Jonides, J and Gotlib, IH (2012) The everyday emotional experience of adults with major depressive disorder: examining emotional instability, inertia, and reactivity. Journal of Abnormal Psychology 121, 819829.Google Scholar
Uher, R, Farmer, A, Maier, W, Rietschel, M, Hauser, J, Marusic, A, Mors, O, Elkin, A, Williamson, RJ, Schmael, C, Henigsberg, N, Perez, J, Mendlewicz, J, Janzing, JGE, Zobel, A, Skibinska, M, Kozel, D, Stamp, AS, Bajs, M, Placentino, A, Barreto, M, McGuffin, P and Aitchison, KJ (2007) Measuring depression: comparison and integration of three scales in the GENDEP study. Psychological Medicine 38, 289300.Google Scholar
Uher, R, Perlis, RH, Placentino, A, Dernovšek, MZ, Henigsberg, N, Mors, O, Maier, W, McGuffin, P and Farmer, A (2012) Self-report and clinician-rated measures of depression severity: can one replace the other? Depression and Anxiety 29, 10431049.Google Scholar
van Os, J (2013) The dynamics of subthreshold psychopathology: implications for diagnosis and treatment. American Journal of Psychiatry 170, 695698.Google Scholar
van Roekel, E, Bennik, EC, Bastiaansen, JA, Verhagen, M, Ormel, J, Engels, RCME and Oldehinkel, AJ (2016) Depressive symptoms and the experience of pleasure in daily life: an exploration of associations in early and late adolescence. Journal of Abnormal Child Psychology 44, 9991009.Google Scholar
Wichers, M (2014) The dynamic nature of depression: a new micro-level perspective of mental disorder that meets current challenges. Psychological Medicine 44, 13491360.Google Scholar
Wilson, SJ, Smyth, JM and MacLean, RR (2013) Integrating ecological momentary assessment and functional brain imaging methods: new avenues for studying and treating tobacco dependence. Nicotine & Tobacco Research 16, S102S110.Google Scholar
Wu, H, Mata, J, Furman, DJ, Whitmer, AJ, Gotlib, IH and Thompson, RJ (2016) Anticipatory and consummatory pleasure and displeasure in major depressive disorder: an experience sampling study. Journal of Abnormal Psychology 126, 149159.Google Scholar
Zimmerman, M, Ellison, W, Young, D, Chelminski, I and Dalrymple, K (2015) How many different ways do patients meet the diagnostic criteria for major depressive disorder? Comprehensive Psychiatry 56, 2934.Google Scholar
Supplementary material: File

Bakker et al. supplementary material

Bakker et al. supplementary material
Download Bakker et al. supplementary material(File)
File 12 MB