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Childhood anhedonia symptoms and stressful life events predict the development of reward-related brain activity across adolescence

Published online by Cambridge University Press:  17 May 2024

A.K. Szenczy Open the ORCID record for A.K. Szenczy [Opens in a new window] ,
E.M. Adams ,
M.T. Hawes ,
J. Anatala ,
K. Gair ,
D.N. Klein ,
G. Hajcak  and
B.D. Nelson
A.K. Szenczy*
Affiliation:
Stony Brook University, Stony Brook, NY, USA
E.M. Adams
Affiliation:
Stony Brook University, Stony Brook, NY, USA
M.T. Hawes
Affiliation:
Stony Brook University, Stony Brook, NY, USA
J. Anatala
Affiliation:
Stony Brook University, Stony Brook, NY, USA
K. Gair
Affiliation:
Stony Brook University, Stony Brook, NY, USA
D.N. Klein
Affiliation:
Stony Brook University, Stony Brook, NY, USA
G. Hajcak
Affiliation:
Santa Clara University, Santa Clara, CA, USA
B.D. Nelson
Affiliation:
Stony Brook University, Stony Brook, NY, USA
*
Corresponding author: Aline Szenczy; Email: aline.szenczy@stonybrook.edu
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Abstract

The reward positivity (RewP) is an event-related potential that indexes reinforcement learning and reward system activation. The RewP has been shown to increase across adolescence; however, most studies have examined the RewP across two assessments, and no studies have examined within-person changes across adolescence into young adulthood. Moreover, the RewP has been identified as a neurobiological risk factor for adolescent-onset depression, but it is unclear whether childhood psychosocial risk factors might predict RewP development across adolescence. In a sample of 317 8- to 14-year-old girls (Mage = 12.4, SD = 1.8), the present study examined self-report measures of depression symptoms and stressful life events at baseline and the ΔRewP during the doors guessing task across three timepoints. Growth modeling indicated that, across all participants, the ΔRewP did not demonstrate linear change across adolescence. However, baseline anhedonia symptoms predicted within-person changes in the ΔRewP, such that individuals with low anhedonia symptoms demonstrated a linear increase in the ΔRewP, but individuals with high anhedonia symptoms had no change in the ΔRewP across adolescence. Similar patterns were observed for stressful life events. The present study suggests that childhood risk factors impact the development of reward-related brain activity, which might subsequently increase risk for psychopathology.

Keywords

Adolescencedepressionreward positivitystress
Type
Regular Article
Information
Development and Psychopathology , First View , pp. 1 - 11
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© The Author(s), 2024. Published by Cambridge University Press

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References

Banica, I., Schell, S. E., Racine, S. E., & Weinberg, A. (2022). Associations between different facets of anhedonia and neural response to monetary, social, and food reward in emerging adults. Biological Psychology, 172, 108363. https://doi.org/10.1016/J.BIOPSYCHO.2022.108363 CrossRefGoogle ScholarPubMed
Bates, D., Mächler, M., Bolker, B. M., & Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1–48. https://doi.org/10.18637/JSS.V067.I01 CrossRefGoogle Scholar
Belden, A. C., Irvin, K., Hajcak, G., Kappenman, E. S., Kelly, D., Karlow, S., Luby, J. L., & Barch, D. M. (2016). Neural correlates of reward processing in depressed and healthy preschool-age children. Journal of the American Academy of Child and Adolescent Psychiatry, 55(12), 1081–1089. https://doi.org/10.1016/J.JAAC.2016.09.503 CrossRefGoogle ScholarPubMed
Bress, J. N., Foti, D., Kotov, R., Klein, D. N., & Hajcak, G. (2013). Blunted neural response to rewards prospectively predicts depression in adolescent girls. Psychophysiology, 50(1), 74–81. https://doi.org/10.1111/j.1469-8986.2012.01485.x CrossRefGoogle ScholarPubMed
Bress, J. N., Meyer, A., & Proudfit, G. H. (2015). The stability of the feedback negativity and its relationship with depression during childhood and adolescence. Development and Psychopathology, 27(4 Pt 1), 1285–1294. https://doi.org/10.1017/S0954579414001400 CrossRefGoogle ScholarPubMed
Bress, J. N., Smith, E., Foti, D., Klein, D. N., & Hajcak, G. (2012). Neural response to reward and depressive symptoms in late childhood to early adolescence. Biological Psychology, 89(1), 156–162. https://doi.org/10.1016/J.BIOPSYCHO.2011.10.004 CrossRefGoogle ScholarPubMed
Burani, K., Brush, C. J., Shields, G. S., Klein, D. N., Nelson, B. D., Slavich, G. M., & Hajcak, G. (2022). Greater cumulative lifetime stressor exposure predicts a blunted RewP in adolescent girls over two years. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 7, 1017–1024. https://doi.org/10.1016/J.BPSC.2022.05.011 Google Scholar
Burani, K., Klawohn, J., Levinson, A. R., Klein, D. N., Nelson, B. D., & Hajcak, G. (2019). Neural response to rewards, stress and sleep interact to prospectively predict depressive symptoms in adolescent girls. Journal of Clinical Child & Adolescent Psychology, 50(1), 131–140. https://doi.org/10.1080/15374416.2019.1630834 CrossRefGoogle ScholarPubMed
Burani, K., Mulligan, E. M., Klawohn, J., Luking, K. R., Nelson, B. D., & Hajcak, G. (2019). Longitudinal increases in reward-related neural activity in early adolescence: Evidence from event-related potentials (ERPs). Developmental Cognitive Neuroscience, 36, 100620. https://doi.org/10.1016/j.dcn.2019.100620 CrossRefGoogle ScholarPubMed
Casement, M. D., Shaw, D. S., Sitnick, S. L., Musselman, S. C., & Forbes, E. E. (2015). Life stress in adolescence predicts early adult reward-related brain function and alcohol dependence. Social Cognitive and Affective Neuroscience, 10(3), 416–423. https://doi.org/10.1093/SCAN/NSU061 CrossRefGoogle ScholarPubMed
Casey, B. J., Getz, S., & Galvan, A. (2008a). The adolescent brain. Developmental Review, 28(1), 62–77. https://doi.org/10.1016/J.DR.2007.08.003 CrossRefGoogle ScholarPubMed
Casey, B. J., Getz, S., & Galvan, A. (2008b). The adolescent brain. Developmental Review, 28(1), 62–77. https://doi.org/10.1016/j.dr.2007.08.003 CrossRefGoogle ScholarPubMed
Curran, P. J., Obeidat, K., & Losardo, D. (2010). Twelve frequently asked questions about growth curve modeling. Journal of Cognition and Development : Official Journal of the Cognitive Development Society, 11(2), 121–136. https://doi.org/10.1080/15248371003699969 CrossRefGoogle ScholarPubMed
Epstein, J., Pan, H., Kocsis, J. H., Yang, Y., Butler, T., Chusid, J., Hochberg, H., Murrough, J., Strohmayer, E., Stern, E., & Silbersweig, D. A. (2006). Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. American Journal of Psychiatry, 163(10), 1784–1790. https://doi.org/10.1176/AJP.2006.163.10.1784/ASSET/IMAGES/LARGE/Q923F1.JPEG CrossRefGoogle ScholarPubMed
Ethridge, P., & Weinberg, A. (2018). Psychometric properties of neural responses to monetary and social rewards across development. International Journal of Psychophysiology, 132, 311–322. https://doi.org/10.1016/J.IJPSYCHO.2018.01.011 CrossRefGoogle ScholarPubMed
Foti, D., Carlson, J. M., Sauder, C. L., & Proudfit, G. H. (2014a). Reward dysfunction in major depression: Multimodal neuroimaging evidence for refining the melancholic phenotype. NeuroImage, 101, 50–58. https://doi.org/10.1016/J.NEUROIMAGE.2014.06.058 CrossRefGoogle ScholarPubMed
Foti, D., Carlson, J. M., Sauder, C. L., & Proudfit, G. H. (2014b). Reward dysfunction in major depression: Multimodal neuroimaging evidence for refining the melancholic phenotype. NeuroImage, 101, 50–58. https://doi.org/10.1016/J.NEUROIMAGE.2014.06.058 CrossRefGoogle ScholarPubMed
Foti, D., Kotov, R., & Klein, D. N. (2011). Abnormal neural sensitivity to monetary gains versus losses among adolescents at risk for depression. Journal of Abnormal Child Psychology, 39(7), 913–924. https://doi.org/10.1007/s10802-011-9503-9 CrossRefGoogle ScholarPubMed
Foti, D., Weinberg, A., Dien, J., & Hajcak, G. (2011). Event-related potential activity in the basal ganglia differentiates rewards from nonrewards: Temporospatial principal components analysis and source localization of the feedback negativity. Human Brain Mapping, 32(12), 2207–2216. https://doi.org/10.1002/HBM.21182 CrossRefGoogle ScholarPubMed
Galvan, A. (2010). Adolescent development of the reward system. Frontiers in Human Neuroscience, 4, 1018. https://doi.org/10.3389/NEURO.09.006.2010/BIBTEX Google ScholarPubMed
Gibb, B. E., Tsypes, A., Israel, E., & Owens, M. (2022). Age differences in neural response to reward and loss in children. Psychophysiology, 59(8), e14039. https://doi.org/10.1111/PSYP.14039 CrossRefGoogle ScholarPubMed
Gold, J. M., Waltz, J. A., Prentice, K. J., Morris, S. E., & Heerey, E. A. (2008). Reward processing in schizophrenia: A deficit in the representation of value. Schizophrenia Bulletin, 34(5), 835–847. https://doi.org/10.1093/SCHBUL/SBN068 CrossRefGoogle ScholarPubMed
Goldstein, B. L., Kessel, E. M., Kujawa, A., Finsaas, M. C., Davila, J., Hajcak, G., & Klein, D. N. (2020). Stressful life events moderate the effect of neural reward responsiveness in childhood on depressive symptoms in adolescence. Psychological Medicine, 50(9), 1548–1555. https://doi.org/10.1017/S0033291719001557 CrossRefGoogle ScholarPubMed
Gratton, G., Coles, M. G. H., & Donchin, E. (1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology, 55(4), 468–484. https://doi.org/10.1016/0013-4694(83)90135-9 CrossRefGoogle ScholarPubMed
Hankin, B. L., & Abramson, L. Y. (2002). Measuring cognitive vulnerability to depression in adolescence: Reliability, validity, and gender differences. Journal of Clinical Child and Adolescent Psychology, 31(4), 491–504. https://doi.org/10.1207/S15374424JCCP3104_8 CrossRefGoogle ScholarPubMed
Hanson, J. L., Hariri, A. R., & Williamson, D. E. (2015). Blunted ventral striatum development in adolescence reflects emotional neglect and predicts depressive symptoms. Biological Psychiatry, 78(9), 598–605. https://doi.org/10.1016/J.BIOPSYCH.2015.05.010 CrossRefGoogle ScholarPubMed
Harvey, P. O., Pruessner, J., Czechowska, Y., & Lepage, M. (2007). Individual differences in trait anhedonia: A structural and functional magnetic resonance imaging study in non-clinical subjects. Molecular Psychiatry, 12(8), 767–775. https://doi.org/10.1038/sj.mp.4002021.CrossRefGoogle ScholarPubMed
Hasler, G., Drevets, W. C., Manji, H. K., & Charney, D. S. (2004). Discovering endophenotypes for major depression. Neuropsychopharmacology, 29(10), 1765–1781. https://doi.org/10.1038/sj.npp.1300506.CrossRefGoogle ScholarPubMed
Hennefield, L., Gilbert, K., Whalen, D., Giorio, C., Camacho, L. E. Q., Kelly, D., Fleuchaus, E., Barch, D. M., Luby, J. L., & Hajcak, G. (2022). The reward positivity shows increased amplitude and decreased latency with increasing age in early childhood. Developmental Science, 25(3), e13196. https://doi.org/10.1111/DESC.13196 CrossRefGoogle ScholarPubMed
Keren, H., O’Callaghan, G., Vidal-Ribas, P., Buzzell, G. A., Brotman, M. A., Leibenluft, E., Pan, P. M., Meffert, L., Kaiser, A., Wolke, S., Pine, D. S., & Stringaris, A. (2018). Reward processing in depression: A conceptual and meta-analytic review across fMRI and EEG studies. American Journal of Psychiatry, 175(11), 1111–1120. https://doi.org/10.1176/APPI.AJP.2018.17101124/ASSET/IMAGES/LARGE/APPI.AJP.2018.17101124F2.JPEG CrossRefGoogle ScholarPubMed
Kessler, R. C. (1997). The effects of stressful life events on depression. Annual Review of Psychology, 48(3), 191–214. https://doi.org/10.1176/foc.8.3.foc459 CrossRefGoogle ScholarPubMed
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Koretz, D., Merikangas, K. R., Rush, A. J., Walters, E. E., & Wang, P. S. (2003). The epidemiology of major depressive disorder: Results from the National Comorbidity Survey Replication (NCS-R). JAMA, 289(23), 3095–3105. https://doi.org/10.1001/JAMA.289.23.3095 CrossRefGoogle ScholarPubMed
Kovacs, M. (1992). Children’s depression inventory (CDI). Multi-Health Systems Inc.Google Scholar
Kujawa, A., Carroll, A., Mumper, E., Mukherjee, D., Kessel, E. M., Olino, T., Hajcak, G., & Klein, D. N. (2018). A longitudinal examination of event-related potentials sensitive to monetary reward and loss feedback from late childhood to middle adolescence. International Journal of Psychophysiology, 132(Pt B), 323–330. https://doi.org/10.1016/j.ijpsycho.2017.11.001 CrossRefGoogle ScholarPubMed
Kujawa, A., Proudfit, G. H., & Klein, D. N. (2014). Neural reactivity to rewards and losses in offspring of mothers and fathers with histories of depressive and anxiety disorders. Journal of Abnormal Psychology, 123(2), 287–297. https://doi.org/10.1037/a0036285 CrossRefGoogle ScholarPubMed
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). LmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82(13), 1–26. https://doi.org/10.18637/JSS.V082.I13 CrossRefGoogle Scholar
Liu, W., Wang, L., Shang, H., Shen, Y., Li, Z., Cheung, E. F. C., & Chan, R. C. K. (2014). The influence of anhedonia on feedback negativity in major depressive disorder. Neuropsychologia, 53, 213–220. https://doi.org/10.1016/j.neuropsychologia.2013.11.023 CrossRefGoogle ScholarPubMed
Loas, G. (1996). Vulnerability to depression: A model centered on anhedonia. Journal of Affective Disorders, 41(1), 39–53. https://doi.org/10.1016/0165-0327(96)00065-1 CrossRefGoogle Scholar
Lukie, C. N., Montazer-Hojat, S., & Holroyd, C. B. (2014). Developmental changes in the reward positivity: An electrophysiological trajectory of reward processing. Developmental Cognitive Neuroscience, 9, 191–199. https://doi.org/10.1016/j.dcn.2014.04.003 CrossRefGoogle ScholarPubMed
Luking, K. R., Pagliaccio, D., Luby, J. L., & Barch, D. M. (2016). Reward processing and risk for depression across development. Trends in Cognitive Sciences, 20(6), 456–468. https://doi.org/10.1016/J.TICS.2016.04.002 CrossRefGoogle ScholarPubMed
Mackin, D. M., Goldstein, B. L., Mumper, E., Kujawa, A., Kessel, E. M., Olino, T. M., Nelson, B. D., Hajcak, G., & Klein, D. N. (2023). Longitudinal associations between reward responsiveness and depression across adolescence. Journal of the American Academy of Child and Adolescent Psychiatry, 62(7), 816–828. https://doi.org/10.1016/J.JAAC.2022.11.013 CrossRefGoogle ScholarPubMed
Mehra, L. M., Hajcak, G., & Meyer, A. (2022). The relationship between stressful life events and the error-related negativity in children and adolescents. Developmental Cognitive Neuroscience, 55, 101110. https://doi.org/10.1016/J.DCN.2022.101110 CrossRefGoogle ScholarPubMed
Moser, J. S., Fisher, M., Hicks, B. M., Zucker, R. A., & Durbin, C. E. (2018). Feedback-related neurophysiology in children and their parents: Developmental differences, familial transmission, and relationship to error-monitoring. International Journal of Psychophysiology, 132, 338–352. https://doi.org/10.1016/J.IJPSYCHO.2018.08.015 CrossRefGoogle ScholarPubMed
Nelson, B. D., Ph, D., Perlman, G., Ph, D., Klein, D. N., Ph, D., Kotov, R., Ph, D., Hajcak, G., & Ph, D. (2016). Blunted neural response to rewards as a prospective predictor of the development of depression in adolescent girls. American Journal of Psychiatry, 173(12), 1223–1230. https://doi.org/10.1176/appi.ajp.2016.15121524 CrossRefGoogle ScholarPubMed
Novick, A. M., Levandowski, M. L., Laumann, L. E., Philip, N. S., Price, L. H., & Tyrka, A. R. (2018). The effects of early life stress on reward processing. Journal of Psychiatric Research, 101, 80–103. https://doi.org/10.1016/J.JPSYCHIRES.2018.02.002 CrossRefGoogle ScholarPubMed
Pechtel, P., & Pizzagalli, D. A. (2010). Effects of early life stress on cognitive and affective function: An integrated review of human literature. Psychopharmacology, 214(1), 55–70. https://doi.org/10.1007/S00213-010-2009-2.CrossRefGoogle ScholarPubMed
Pegg, S., Ethridge, P., Shields, G. S., Slavich, G. M., Weinberg, A., & Kujawa, A. (2019). Blunted social reward responsiveness moderates the effect of lifetime social stress exposure on depressive symptoms. Frontiers in Behavioral Neuroscience, 13, 178. https://doi.org/10.3389/FNBEH.2019.00178/BIBTEX CrossRefGoogle ScholarPubMed
Pelizza, L., & Ferrari, A. (2009). Anhedonia in schizophrenia and major depression: State or trait? Annals of General Psychiatry, 8(1), 22. https://doi.org/10.1186/1744-859X-8-22/FIGURES/4 CrossRefGoogle ScholarPubMed
Proudfit, G. H. (2015). The reward positivity: From basic research on reward to a biomarker for depression. Psychophysiology, 52(4), 449–459. https://doi.org/10.1111/psyp.12370 CrossRefGoogle ScholarPubMed
Saylor, C. F., Finch, A. J., Spirito, A., & Bennett, B. (1984). The Children’s Depression Inventory: A systematic evaluation of psychometric properties. Journal of Consulting and Clinical Psychology, 52(6), 955–967. https://doi.org/10.1037/0022-006X.52.6.955 CrossRefGoogle ScholarPubMed
Silverman, M. H., Jedd, K., & Luciana, M. (2015). Neural networks involved in adolescent reward processing: An activation likelihood estimation meta-analysis of functional neuroimaging studies. NeuroImage, 122, 427–439. https://doi.org/10.1016/J.NEUROIMAGE.2015.07.083 CrossRefGoogle ScholarPubMed
Steinberg, L., Albert, D., Cauffman, E., Banich, M., Graham, S., & Woolard, J. (2008). Age differences in sensation seeking and impulsivity as indexed by behavior and self-report: Evidence for a dual systems model. Developmental Psychology, 44(6), 1764–1778. https://doi.org/10.1037/A0012955 CrossRefGoogle ScholarPubMed
Suor, J. H., Granros, M., Calentino, A. E., Luan Phan, K., & Burkhouse, K. L. (2021). The interplay of childhood maltreatment and maternal depression in relation to the reward positivity in youth. Development and Psychopathology, 35(1), 1–11. https://doi.org/10.1017/S0954579421000857 Google Scholar
Weinberg, A., Liu, H., Hajcak, G., & Shankman, S. A. (2015). Blunted neural response to rewards as a vulnerability factor for depression: Results from a family study. Journal of Abnormal Psychology, 124(4), 878–889. https://doi.org/10.1037/ABN0000081 CrossRefGoogle ScholarPubMed
Whitton, A. E., Treadway, M. T., & Pizzagalli, D. A. (2015). Reward processing dysfunction in major depression, bipolar disorder and schizophrenia. Current Opinion in Psychiatry, 28(1), 7–12. https://doi.org/10.1097/YCO.0000000000000122 CrossRefGoogle Scholar
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