Cited by 47Neural and Behavioral Psychology StudiesAnxiety, Depression, Psychometrics, Treatment, Cognitive ProcessesMemory Processes and Influences

Depressive symptoms bias the prediction-error enhancement of memory towards negative events in reinforcement learning

Open access
Rouhani, Nina, Niv, Yael·2019·Psychopharmacology

Abstract

Rationale Depression is a disorder characterized by sustained negative affect and blunted positive affect, suggesting potential abnormalities in reward learning and its interaction with episodic memory. Objectives This study investigated how reward prediction errors experienced during learning modulate memory for rewarding events in individuals with depressive and non-depressive symptoms. Methods Across three experiments, participants learned the average values of two scene categories in two learning contexts. Each learning context had either high or low outcome variance, allowing us to test the effects of small and large prediction errors on learning and memory. Participants were later tested for their memory of trial-unique scenes that appeared alongside outcomes. We compared learning and memory performance of individuals with self-reported depressive symptoms (N = 101) to those without (N = 184). Results Although there were no overall differences in reward learning between the depressive and non-depressive group, depression severity within the depressive group predicted greater error in estimating the values of the scene categories. Similarly, there were no overall differences in memory performance. However, in depressive participants, negative prediction errors enhanced episodic memory more so than did positive prediction errors, and vice versa for non-depressive participants who showed a larger effect of positive prediction errors on memory. These results reflected differences in memory both within group and across groups. Conclusions Individuals with self-reported depressive symptoms showed relatively intact reinforcement learning, but demonstrated a bias for encoding events that accompanied surprising negative outcomes versus surprising positive ones. We discuss a potential neural mechanism supporting these effects, which may underlie or contribute to the excessive negative affect observed in depression.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s00213-019-05322-z

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Individuals with depression often display emotionally biased prediction-error processing, characterized by attenuated reward prediction-error signals and heightened sensitivity to punishment- or risk-related prediction errors.

    “Individuals with depression often display emotionally biased prediction-error processing, characterized by attenuated reward prediction-error signals and heightened sensitivity to punishment- or risk-related prediction errors (Kumar et al., 2018; Rouhani and Niv, 2019).”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 39

  1. Admon R, Nickerson LD, Dillon DG, Holmes AJ, Bogdan R, Kumar P, … Pizzagalli DA (2015). Dissociable cortico-striatal connectivity abnormalities in major depression in response to monetary gains and penalties. Psychological Medicine, 45(1), 121– 131. 10.1017/S0033291714001123 25055809 PMC4233014 · DOI
  2. Admon R, & Pizzagalli DA (2015). Dysfunctional reward processing in depression. Current Opinion in Psychology. 10.1016/j.copsyc.2014.12.011 PMC4525714 26258159 · DOI · Paper page
  3. Barto AG (1995). Adaptive critic and the basal ganglia In Houk JC, Davis JL, & Beiser DG (Eds.), Models of information processing in the basal ganglia (p. 215). MIT press.
  4. Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, … Grothendieck G (2015). Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software, 67(1), 1– 48. 10.18637/jss.v067.i01 · DOI · Paper page
  5. Bornstein AM, Khaw MW, Shohamy D, & Daw ND (2017). Reminders of past choices bias decisions for reward in humans. Nature Communications, 8, 15958 10.1038/ncomms15958 PMC5490260 28653668 · DOI
  6. Burt DB, Zembar MJ, & Niederehe G (1995). Depression and memory impairment: A meta-analysis of the association, its pattern, and specificity. Psychological Bulletin, 117(2), 285– 305. 10.1037/0033-2909.117.2.285 7724692 · DOI · Paper page
  7. Chase HW, Frank MJ, Michael A, Bullmore ET, Sahakian BJ, & Robbins TW (2010). Approach and avoidance learning in patients with major depression and healthy controls: Relation to anhedonia. Psychological Medicine, 40(3), 433– 440. 10.1017/S0033291709990468 19607754 · DOI
  8. Clewett D, Huang R, Velasco R, Lee T-H, & Mather M (2018). Locus coeruleus activity strengthens prioritized memories under arousal. The Journal of Neuroscience, 2097– 17. 10.1523/JNEUROSCI.2097-17.2017 PMC5815354 29301874 · DOI · Paper page
  9. Dillon DG, Dobbins IG, & Pizzagalli DA (2014). Weak Reward Source Memory in Depression Reflects Blunted Activation of VTA/SN and Parahippocampus. Social Cognitive and Affective Neuroscience, 9(10), 1576– 1583. Retrieved from http://scan.oxfordjournals.org/ 24078019 PMC4187280
  10. Dillon DG, & Pizzagalli DA (2018). Mechanisms of Memory Disruption in Depression. Trends in Neurosciences. 10.1016/j.tins.2017.12.006 PMC5835184 29331265 · DOI
  11. Duncan KD, & Shohamy D (2016). Memory States Influence Value-Based Decisions. Journal of Experimental Psychology: General, 145(9), 3– 9. PMC5953570 27797556
  12. Duszkiewicz AJ, Mcnamara CG, Takeuchi T, & Genzel L (2018). Novelty and Dopaminergic Modulation of Memory Persistence: A Tale of Two Systems. Trends in Neurosciences. 10.1016/j.tins.2018.10.002 PMC6352318 30455050 · DOI
  13. Gaddy MA, & Ingram RE (2014). A meta-analytic review of mood-congruent implicit memory in depressed mood. Clinical Psychology Review, 34, 402– 416. 10.1016/j.cpr.2014.06.001 24980699 · DOI
  14. Gershman SJ, & Daw ND (2017). Reinforcement Learning and Episodic Memory in Humans and Animals: An Integrative Framework. Annual Review of Psychology, 68, 101– 128. 10.1146/annurev-psych-122414-033625 PMC5953519 27618944 · DOI · Paper page
  15. Gradin VB, Kumar P, Waiter G, Ahearn T, Stickle C, Milders M, … Steele JD (2011). Expected value and prediction error abnormalities in depression and schizophrenia. Brain, 134(6), 1751– 1764. 10.1093/brain/awr059 21482548 · DOI · Paper page
  16. Knutson B, Bhanji JP, Cooney RE, Atlas LY, & Gotlib IH (2008). Neural Responses to Monetary Incentives in Major Depression. Biological Psychiatry, 63(7), 686– 692. 10.1016/j.biopsych.2007.07.023 17916330 PMC2290738 · DOI · Paper page
  17. Kumar P, Goer F, Murray L, Dillon DG, Beltzer ML, Cohen AL, … Pizzagalli DA (2018). Impaired reward prediction error encoding and striatal-midbrain connectivity in depression. Neuropsychopharmacology, 43(7), 1581– 1588. 10.1038/s41386-018-0032-x 29540863 PMC5983542 · DOI · Paper page
  18. Leal SL, Tighe SK, Jones CK, & Yassa MA (2014). Pattern separation of emotional information in hippocampal dentate and CA3. Hippocampus, 24(9), 1146– 1155. 10.1002/hipo.22298 24796287 PMC4172604 · DOI
  19. Matt GE, Vázquez C, & Campbell WK (1992). Mood-congruent recall of affectively toned stimuli: A meta-analytic review. Clinical Psychology Review, 12(2), 227– 255. 10.1016/0272-7358(92)90116-P · DOI · Paper page
  20. Mueller EM, Pechtel P, Cohen AL, Douglas SR, & Pizzagalli DA (2015). Potentiated processing of negative feedback in depression is attenuated by anhedonia. Depression and Anxiety, 32(4), 296– 305. 10.1002/da.22338 25620272 PMC4374007 · DOI
  21. Nassar MR, Rumsey KM, Wilson RC, Parikh K, Heasly B, & Gold JI (2012). Rational regulation of learning dynamics by pupil-linked arousal systems. Nature Neuroscience, 15(7), 1040– 1046. 10.1038/nn.3130 22660479 PMC3386464 · DOI · Paper page
  22. Pollack I, & Norman DA (1964). A non-parametric analysis of recognition experiments. Psychonomic Science, 1(1–12), 125– 126. 10.3758/BF03342823 · DOI
  23. Read Montague P, Dayan P, & Sejnowskw TJ (1996). A Framework for Mesencephalic Dopamine Systems Based on Predictive Hebbian Learning. The Journal of Neuroscience (Vol. 76). Retrieved from http://www.jneurosci.Org/content/jneuro/16/5/1936.full.pdf PMC6578666 8774460
  24. Roesch MR, Esber GR, Li J, Daw ND, & Schoenbaum G (2012). Surprise! Neural correlates of Pearce-Hall and Rescorla-Wagner coexist within the brain. European Journal of Neuroscience, 35(7), 1190– 1200. 10.1111/j.1460-9568.2011.07986.x 22487047 PMC3325511 · DOI
  25. Rouhani N, Norman KA, & Niv Y (2018). Dissociable Effects of Surprising Rewards on Learning and Memory. Journal of Experimental Psychology: Learning, Memory, and Cognition. 10.1037/xlm0000518 PMC6117220 29553767 · DOI
  26. Rush AJ, Gullion CM, Basco MR, Jarrett RB, & Trivedi MH (1996). The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychological Medicine, 26(03), 477 10.1017/S0033291700035558 8733206 · DOI · Paper page
  27. Rutledge RB, Moutoussis M, Smittenaar P, Zeidman P, Taylor T, Hrynkiewicz L, … Dolan RJ (2017). Association of Neural and Emotional Impacts of Reward Prediction Errors With Major Depression. JAMA Psychiatry, 10– 12. 10.1001/jamapsychiatry.2017.1713 PMC5710549 28678984 · DOI · Paper page
  28. Sacchet MD, Levy BJ, Hamilton JP, Maksimovskiy A, Hertel PT, Joormann J, … Gotlib IH (2017). Cognitive and neural consequences of memory suppression in major depressive disorder. Cognitive, Affective and Behavioral Neuroscience, 17(1), 77– 93. 10.3758/s13415-016-0464-x PMC5272890 27649971 · DOI
  29. Sara SJ (2009). The locus coeruleus and noradrenergic modulation of cognition. Nature Reviews Neuroscience, 10 10.1038/nrn2573 19190638 · DOI · Paper page
  30. Shohamy D, & Adcock RA (2010). Dopamine and adaptive memory. Trends in Cognitive Sciences. 10.1016/j.tics.2010.08.002 20829095 · DOI
  31. 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. 10.1016/j.jad.2009.01.034 19261334 PMC2745481 · DOI · Paper page
  32. Takeuchi T, Duszkiewicz AJ, Sonneborn A, Spooner PA, Yamasaki M, Watanabe M, … Morris RGM (2016). Locus coeruleus and dopaminergic consolidation of everyday memory. Nature, 537(7620), 1– 18. 10.1038/nature19325 PMC5161591 27602521 · DOI · Paper page
  33. 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(8), 1102– 1112. 10.1093/scan/nsu158 25567763 PMC4526479 · DOI · Paper page
  34. Walters K, Christakis DA, & Wright DR (2018). Are Mechanical Turk worker samples representative of health status and health behaviors in the U.S.? PLoS ONE, 13(6). 10.1371/journal.pone.0198835 PMC5991724 29879207 · DOI
  35. Weber EU, Blais A-R, & Betz NE (2002). A domain-specific risk-attitude scale: measuring risk perceptions and risk behaviors. Journal of Behavioral Decision Making, 15(4), 263– 290. 10.1002/bdm.414 · DOI · Paper page
  36. Whitton AE, Kakani P, Foti D, Van’t Veer A, Haile A, Crowley DJ, & Pizzagalli DA (2016). Blunted neural responses to reward in remitted major depression: A high-density event-related potential study. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 1(1), 87– 95. 10.1016/j.bpsc 26858994 PMC4743048 · DOI
  37. Wimmer GE, & Shohamy D (2012). Preference by Association: How Memory Mechanisms in the Hippocampus Bias Decisions. Science, 338, 270– 273. 10.1126/science.1223252 23066083 · DOI
  38. Young KD, Siegle GJ, Bodurka J, & Drevets WC (2016). Amygdala Activity During Autobiographical Memory Recall in Depressed and Vulnerable Individuals: Association With Symptom Severity and Autobiographical Overgenerality. Am J Psychiatry, 173, 78– 89. 10.1176/appi.ajp.2015.15010119 26541813 · DOI
  39. Young KD, Siegle GJ, Zotev V, Phillips R, Misaki M, Yuan H, … Bodurka J (2017). Randomized Clinical Trial of Real-Time fMRI Amygdala Neurofeedback for Major Depressive Disorder: Effects on Symptoms and Autobiographical Memory Recall. Am J Psychiatry, 174, 748– 755. 10.1176/appi.ajp.2017.16060637 28407727 PMC5538952 · DOI · Paper page

Cited by

Sorted by citations

Authors
Rouhani, N., & Niv, Y.
Affiliations
Princeton University (US)
Corresponding author
Rouhani, Nina
Venue
Psychopharmacology
Published
2019-07-26
Volume
236
Issue
8
Pages
2425-2435
ISSN
  • 0033-3158 (ISSN-L)
  • 1432-2072
OpenAlex
W2966747958
Cited by
47
References
7
Citations by year
2026: 3 · 2025: 5 · 2024: 8 · 2023: 14 · 2022: 4 · 2021: 8 · 2020: 4 · 2018: 1
FWCI
2.33
Type
journal article
Language
en
Open access
Locations
  • Psychopharmacology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Mental Health (R01MH098861)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords
depressive symptoms, depression, reward prediction error, episodic memory, reinforcement learning, memory bias, negative affect, outcome variance, memory encoding, reward learning
MeSH terms
Adult, Depression, Female, Forecasting, Humans, Learning, Male, Photic Stimulation, Reinforcement, Psychology, Reward, Young Adult, Memory, Episodic

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review