Hostname: page-component-5d59c44645-mrcq8 Total loading time: 0 Render date: 2024-02-25T15:18:14.930Z Has data issue: false hasContentIssue false

Multi-modal assessment of reward functioning in adolescent anhedonia

Published online by Cambridge University Press:  17 June 2022

Laura Murray*
Department of Psychiatry, Harvard Medical School, Boston, MA, USA Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
Elana S. Israel
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
Emma G. Balkind
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
Brianna Pastro
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
Nathaniel Lovell-Smith
Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
Scott E. Lukas
Department of Psychiatry, Harvard Medical School, Boston, MA, USA
Erika E. Forbes
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Diego A. Pizzagalli
Department of Psychiatry, Harvard Medical School, Boston, MA, USA Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
Christian A. Webb
Department of Psychiatry, Harvard Medical School, Boston, MA, USA Center for Depression, Anxiety and Stress Research, McLean Hospital, Belmont, MA, USA
Author for correspondence: Laura Murray, E-mail:



Anhedonia is a core symptom of depression that predicts worse treatment outcomes. Dysfunction in neural reward circuits is thought to contribute to anhedonia. However, whether laboratory-based assessments of anhedonia and reward-related neural function translate to adolescents' subjective affective experiences in real-world contexts remains unclear.


We recruited a sample of adolescents (n = 82; ages 12–18; mean = 15.83) who varied in anhedonia and measured the relationships among clinician-rated and self-reported anhedonia, behaviorally assessed reward learning ability, neural response to monetary reward and loss (as assessed with functional magnetic resonance imaging), and repeated ecological momentary assessment (EMA) of positive affect (PA) and negative affect (NA) in daily life.


Anhedonia was associated with lower mean PA and higher mean NA across the 5-day EMA period. Anhedonia was not related to impaired behavioral reward learning, but low PA was associated with reduced nucleus accumbens response during reward anticipation and reduced medial prefrontal cortex (mPFC) response during reward outcome. Greater mean NA was associated with increased mPFC response to loss outcome.


Traditional laboratory-based measures of anhedonia were associated with lower subjective PA and higher subjective NA in youths' daily lives. Lower subjective PA and higher subjective NA were associated with decreased reward-related striatal functioning. Higher NA was also related to increased mPFC activity to loss. Collectively, these findings demonstrate that laboratory-based measures of anhedonia translate to real-world contexts and that subjective ratings of PA and NA may be associated with neural response to reward and loss.

Original Article
Copyright © The Author(s), 2022. Published by Cambridge University Press

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.)


Alarcón, G., Sauder, M., Teoh, J. Y., Forbes, E. E., & Quevedo, K. (2019). Amygdala functional connectivity during self-face processing in depressed adolescents with recent suicide attempt. Journal of the American Academy of Child & Adolescent Psychiatry, 58(2), 221231.10.1016/j.jaac.2018.06.036CrossRefGoogle ScholarPubMed
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders, fifth edition (DSM-5). Washington, DC: American Psychiatric Association.Google Scholar
Auerbach, R. P., Admon, R., & Pizzagalli, D. A. (2014). Adolescent depression: Stress and reward dysfunction. Harvard review of psychiatry, 22(3), 139. doi: 10.1097/HRP.0000000000000034.CrossRefGoogle ScholarPubMed
Avenevoli, S., Swendsen, J., He, J.-P., Burstein, M., & Merikangas, K. R. (2015). Major depression in the national comorbidity survey–adolescent supplement: Prevalence, correlates, and treatment. Journal of the American Academy of Child & Adolescent Psychiatry, 54(1), 3744. e32. doi: 10.1016/j.jaac.2014.10.010.CrossRefGoogle ScholarPubMed
Bailen, N. H., Green, L. M., & Thompson, R. J. (2018). Understanding emotion in adolescents: A review of emotional frequency, intensity, instability, and clarity. Emotion Review, 11(1), 6373. doi: 10.1177/1754073918768878.CrossRefGoogle Scholar
Belleau, E. L., Kremens, R., Ang, Y.-S., Pisoni, A., Bondy, E., Durham, K., … Pizzagalli, D. A. (2020). Reward functioning abnormalities in adolescents at high familial risk for depressive disorders. Biological Psychiatry: Cognitive Neuroscience Neuroimaging, 6(3), 270279. doi: 10.1016/j.bpsc.2020.08.016.Google ScholarPubMed
Birmaher, B., Brent, D., & Issues, A. W. G. O. Q. (2007). Practice parameter for the assessment and treatment of children and adolescents with depressive disorders. Journal of the American Academy of Child & Adolescent Psychiatry, 46(11), 15031526. doi: 10.1097/chi.0b013e318145ae1c.CrossRefGoogle ScholarPubMed
Blain, S. D., Sassenberg, T. A., Xi, M., Zhao, D., & DeYoung, C. G. (2021). Extraversion but not depression predicts reward sensitivity: Revisiting the measurement of anhedonic phenotypes. Journal of Personality and Social Psychology, 121(2), e1e18. doi: 10.1037/pspp0000371.CrossRefGoogle Scholar
Borsini, A., Wallis, A. S. J., Zunszain, P., Pariante, C. M., & Kempton, M. J. (2020). Characterizing anhedonia: A systematic review of neuroimaging across the subtypes of reward processing deficits in depression. Cognitive, Affective, & Behavioral Neuroscience, 20(4), 816841. doi: 10.3758/s13415-020-00804-6.CrossRefGoogle ScholarPubMed
Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain's default network: Anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 138. doi: 10.1196/annals.1440.011.CrossRefGoogle ScholarPubMed
Elliott, M. L., Knodt, A. R., Ireland, D., Morris, M. L., Poulton, R., Ramrakha, S., … Hariri, A. R. (2020). What is the test-retest reliability of common task-fMRI measures? New empirical evidence and a meta-analysis. Psychological Science, 31(7), 792806. doi: 10.1177/0956797620916786.CrossRefGoogle ScholarPubMed
Forbes, E. E., & Dahl, R. E. (2012). Research review: Altered reward function in adolescent depression: What, when and how? Journal of Child Psychology and Psychiatry, 53(1), 315. doi: 10.1111/j.1469-7610.2011.02477.x.CrossRefGoogle ScholarPubMed
Forbes, E. E., Hariri, A. R., Martin, S. L., Silk, J. S., Moyles, D. L., Fisher, P. M., … Dahl, R. E. (2009). Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder. American Journal of Psychiatry, 166(1), 6473. doi: 10.1176/appi.ajp.2008.07081336.CrossRefGoogle ScholarPubMed
Forbes, E. E., Olino, T. M., Ryan, N. D., Birmaher, B., Axelson, D., Moyles, D. L., & Dahl, R. E. (2010a). Reward-related brain function as a predictor of treatment response in adolescents with major depressive disorder. Cognitive, Affective, Behavioral Neuroscience, 10(1), 107118. doi: 10.3758/CABN.10.1.107.CrossRefGoogle ScholarPubMed
Forbes, E. E., Ryan, N. D., Phillips, M. L., Manuck, S. B., Worthman, C. M., Moyles, D. L., … Dahl, R. E. (2010b). Healthy adolescents’ neural response to reward: Associations with puberty, positive affect, and depressive symptoms. Journal of the American Academy of Child & Adolescent Psychiatry, 49(2), 162172. e165. doi: 10.1016/j.jaac.2009.11.006.Google ScholarPubMed
Franken, I. H., Rassin, E., & Muris, P. (2007). The assessment of anhedonia in clinical and non-clinical populations: Further validation of the Snaith–Hamilton Pleasure Scale (SHAPS). Journal of Affective Disorders, 99(1–3), 8389. doi: 10.1016/j.jad.2006.08.020CrossRefGoogle ScholarPubMed
Gandhi, A., Mote, J., & Fulford, D. (2022). A transdiagnostic meta-analysis of physical and social anhedonia in major depressive disorder and schizophrenia spectrum disorders. Psychiatry Research, 114379. doi: 10.1016/j.psychres.2021.114379.CrossRefGoogle ScholarPubMed
Gradin, V. B., Kumar, P., Waiter, G., Ahearn, T., Stickle, C., Milders, M., … Steele, J. D. (2011). Expected value and prediction error abnormalities in depression and schizophrenia. Brain, 134(6), 17511764. doi: 10.1093/brain/awr059.CrossRefGoogle ScholarPubMed
Heekeren, H. R., Wartenburger, I., Marschner, A., Mell, T., Villringer, A., & Reischies, F. M. (2007). Role of ventral striatum in reward-based decision making. Neuroreport, 18(10), 951955. doi: 10.1097/WNR.0b013e3281532bd7.CrossRefGoogle ScholarPubMed
Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., … Wang, P. (2010). Research domain criteria (RDoC): Toward a new classification framework for research on mental disorders. American Journal of Psychiatry, 167(7), 748751. doi: 10.1176/appi.ajp.2010.09091379.CrossRefGoogle Scholar
Kaiser, R. H., Kang, M. S., Lew, Y., Van Der Feen, J., Aguirre, B., Clegg, R., … Hutchison, R. M. (2019). Abnormal frontoinsular-default network dynamics in adolescent depression and rumination: A preliminary resting-state co-activation pattern analysis. Neuropsychopharmacology, 44(9), 16041612. doi: 10.1038/s41386-019-0399-3.CrossRefGoogle ScholarPubMed
Kaiser, R. H., Treadway, M. T., Wooten, D. W., Kumar, P., Goer, F., Murray, L., … Pizzagalli, D. A. (2018). Frontostriatal and dopamine markers of individual differences in reinforcement learning: A multi-modal investigation. Cerebral Cortex, 28(12), 42814290. doi: 10.1093/cercor/bhx281.CrossRefGoogle Scholar
Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., … Ryan, N. (1997). Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry, 36(7), 980988. doi: 10.1097/00004583-199707000-00021.CrossRefGoogle ScholarPubMed
Kennedy, J. T., Harms, M. P., Korucuoglu, O., Astafiev, S. V., Barch, D. M., Thompson, W. K., … Anokhin, A. P. (2022). Reliability and stability challenges in ABCD task fMRI data. NeuroImage, 252, 119046. doi: 10.1016/j.neuroimage.2022.119046.CrossRefGoogle ScholarPubMed
Keren, H., O'Callaghan, G., Vidal-Ribas, P., Buzzell, G. A., Brotman, M. A., Leibenluft, E., … Wolke, S. (2018). Reward processing in depression: A conceptual and meta-analytic review across fMRI and EEG studies. The American Journal of Psychiatry, 175(11), 11111120. doi: 10.1176/appi.ajp.2018.17101124.CrossRefGoogle ScholarPubMed
Laurent, J., Catanzaro, S. J., Joiner, T. E. Jr., Rudolph, K. D., Potter, K. I., Lambert, S., … Gathright, T. (1999). A measure of positive and negative affect for children: Scale development and preliminary validation. Psychological Assessment, 11(3), 326.10.1037/1040-3590.11.3.326CrossRefGoogle Scholar
Lawlor, V. M., Webb, C. A., Wiecki, T. V., Frank, M. J., Trivedi, M., Pizzagalli, D. A., & Dillon, D. G. (2020). Dissecting the impact of depression on decision-making. Psychological Medicine, 50(10), 16131622. doi: 10.1017/S0033291719001570.CrossRefGoogle ScholarPubMed
Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: A network model of insula function. Brain Structure and Function, 214(5–6), 655667. doi: 10.1007/s00429-010-0262-0.CrossRefGoogle Scholar
Moos, R. H., & Cronkite, R. C. (1999). Symptom-based predictors of a 10-year chronic course of treated depression. The Journal of Nervous Mental Disease, 187(6), 360368. Retrieved from Scholar
Murray, L., Lopez-Duran, N. L., Mitchell, C., Monk, C. S., & Hyde, L. W. (2022). Antisocial behavior is associated with reduced frontoparietal activity to loss in a population-based sample of adolescents. Psychological Medicine, 19. doi: 10.1017/S0033291722000307.CrossRefGoogle Scholar
Olino, T. M., McMakin, D. L., Morgan, J. K., Silk, J. S., Birmaher, B., Axelson, D. A., … Forbes, E. E. (2014). Reduced reward anticipation in youth at high-risk for unipolar depression: A preliminary study. Developmental Cognitive Neuroscience, 8, 5564. doi: 10.1016/j.dcn.2013.11.005.CrossRefGoogle ScholarPubMed
Pizzagalli, D. A. (2014). Depression, stress, and anhedonia: Toward a synthesis and integrated model. Annual Review of Clinical Psychology, 10, 393423. doi: 10.1146/annurev-clinpsy-050212-185606.CrossRefGoogle Scholar
Pizzagalli, D. A., Holmes, A. J., Dillon, D. G., Goetz, E. L., Birk, J. L., Bogdan, R., … Fava, M. (2009). Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. American Journal of Psychiatry, 166(6), 702710. doi: 10.1176/appi.ajp.2008.08081201.CrossRefGoogle Scholar
Pizzagalli, D. A., Iosifescu, D., Hallett, L. A., Ratner, K. G., & Fava, M. (2008). Reduced hedonic capacity in major depressive disorder: Evidence from a probabilistic reward task. Journal of Psychiatric Research, 43(1), 7687. doi: 10.1016/j.jpsychires.2008.03.001.CrossRefGoogle ScholarPubMed
Pizzagalli, D. A., Jahn, A. L., & O'Shea, J. P. (2005). Toward an objective characterization of an anhedonic phenotype: A signal-detection approach. Biological Psychiatry, 57(4), 319327. Retrieved from ScholarPubMed
Ribot, T. (1905). La psychologie des sentiments. Paris, France: Alcan.Google Scholar
Rizvi, S. J., Pizzagalli, D. A., Sproule, B. A., & Kennedy, S. H. (2016). Assessing anhedonia in depression: Potentials and pitfalls. Neuroscience & Biobehavioral Reviews, 65, 2135. doi: 10.1016/j.neubiorev.2016.03.004.CrossRefGoogle ScholarPubMed
Rolls, E. T., Huang, C.-C., Lin, C.-P., Feng, J., & Joliot, M. (2020). Automated anatomical labelling atlas 3. Neuroimage, 206, 116189. doi: 10.1016/j.neuroimage.2019.116189.CrossRefGoogle ScholarPubMed
Santesso, D. L., Dillon, D. G., Birk, J. L., Holmes, A. J., Goetz, E., Bogdan, R., & Pizzagalli, D. A. (2008). Individual differences in reinforcement learning: Behavioral, electrophysiological, and neuroimaging correlates. Neuroimage, 42(2), 807816. doi: 10.1016/j.neuroimage.2008.05.032.CrossRefGoogle ScholarPubMed
Snaith, R., Hamilton, M., Morley, S., Humayan, A., Hargreaves, D., & Trigwell, P. (1995). A scale for the assessment of hedonic tone the Snaith–Hamilton Pleasure Scale. The British Journal of Psychiatry, 167(1), 99103. doi: 10.1192/bjp.167.1.99.CrossRefGoogle ScholarPubMed
Stoy, M., Schlagenhauf, F., Sterzer, P., Bermpohl, F., Hägele, C., Suchotzki, K., … Knutson, B. (2012). Hyporeactivity of ventral striatum towards incentive stimuli in unmedicated depressed patients normalizes after treatment with escitalopram. Journal of Psychopharmacology, 26(5), 677688. doi: 10.1177/0269881111416686.CrossRefGoogle ScholarPubMed
Tanner, J., & Davies, P. S. (1985). Clinical longitudinal standards for height and height velocity for North American children. The Journal of Pediatrics, 107(3), 317329. doi: 10.1016/S0022-3476(85)80501-1.CrossRefGoogle ScholarPubMed
Treadway, M. T., & Zald, D. H. (2011). Reconsidering anhedonia in depression: Lessons from translational neuroscience. Neuroscience & Biobehavioral Reviews, 35(3), 537555. doi: 10.1016/j.neubiorev.2010.06.006.CrossRefGoogle ScholarPubMed
Von Neumann, J., Kent, R., Bellinson, H., & Hart, B. (1941). The mean square successive difference. The Annals of Mathematical Statistics, 12(2), 153162. Retrieved from Scholar
Vrieze, E., Pizzagalli, D. A., Demyttenaere, K., Hompes, T., Sienaert, P., de Boer, P., … Claes, S. (2013). Reduced reward learning predicts outcome in major depressive disorder. Biological Psychiatry, 73(7), 639645. doi: 10.1016/j.biopsych.2012.10.014.CrossRefGoogle ScholarPubMed
Supplementary material: File

Murray et al. supplementary material

Murray et al. supplementary material

Download Murray et al. supplementary material(File)
File 25 KB