The temporal representation of experience in subjective mood

Hanna Keren, Charles Zheng, David C Jangraw, Katharine Chang, Aria Vitale, Robb B Rutledge, Francisco Pereira, Dylan M Nielson, Argyris Stringaris, Hanna Keren, Charles Zheng, David C Jangraw, Katharine Chang, Aria Vitale, Robb B Rutledge, Francisco Pereira, Dylan M Nielson, Argyris Stringaris

Abstract

Humans refer to their mood state regularly in day-to-day as well as clinical interactions. Theoretical accounts suggest that when reporting on our mood we integrate over the history of our experiences; yet, the temporal structure of this integration remains unexamined. Here, we use a computational approach to quantitatively answer this question and show that early events exert a stronger influence on reported mood (a primacy weighting) compared to recent events. We show that a Primacy model accounts better for mood reports compared to a range of alternative temporal representations across random, consistent, or dynamic reward environments, different age groups, and in both healthy and depressed participants. Moreover, we find evidence for neural encoding of the Primacy, but not the Recency, model in frontal brain regions related to mood regulation. These findings hold implications for the timing of events in experimental or clinical settings and suggest new directions for individualized mood interventions.

Trial registration: ClinicalTrials.gov NCT03388606.

Keywords: anterior cingulate cortex; computational psychiatry; fMRI; human; mood; neuroscience; primacy model; reward.

Conflict of interest statement

HK, CZ, DJ, KC, AV, RR, FP, DN, AS No competing interests declared

Figures

Figure 1.. The Primacy versus Recency mood…
Figure 1.. The Primacy versus Recency mood models.
(A) Participants played a probabilistic task where they experienced different reward prediction error values, while reporting subjective mood every 2-3 gambling trials. In each trial, participants chose whether to gamble between two monetary values or to receive a certain amount (Gamble decision). During Expectation, the chosen option remained on the screen, followed by the presentation of the Outcome value. (B)Mood ∝ βE∑j=1tγt−jEjpresents the expectation term of the mood models, where βE is the influence of expectation values on subjective mood reports. The expectation term of the Recency mood model as developed by Rutledge et al., 2014 is presented belowEt=Hight+Lowt2where it consists of the trial’s high and low gamble values. In the alternative Primacy model, as presented inEt=1t-1∑i=1t-1Aithe expectation term is replaced by the average of all previous outcomes (Ai). Moreover, as can be seen in Equations 6–8 in Materials and methods, the Primacy model has overall fewer parameters compared to the Recency model. The theoretical scaling curves for the influence of previous events on mood due to expected outcomes are presented for each model respectively below (see Figure 1—figure supplement 1 for additional illustrations).
Figure 1—figure supplement 1.. The Primacy effect…
Figure 1—figure supplement 1.. The Primacy effect of outcomes on mood.
In the Primacy model, the expectation term Ej is the unweighted average of previous outcomes. At each trial, all previous expectation terms are combined in an exponentially weighted sum: ∑j=1tγt-jEj . Here, we illustrate how this gives rise to a primacy weighting of previous outcomes that depends on the value of γ (each subplot represents a different magnitude of exponential weighting γ). The total height of each bar represents the influence of the outcome of the corresponding trial on the result of the exponential sum at the end of trial 9. Each color indicates the contributions of the outcomes that form an expectation term Ej at the end of trial j. The dark yellow block represents the contribution of the expectation term E1 from the end of trial 1 (comprised only of the first outcome). The gray blocks represent the contributions of the expectation term E2 that is being added from the end of trial 2 (which is the average of the outcomes from trials 1 and 2, and therefore it appears in both the first and the second bars). This continues for the rest of the expectation terms until the last expectation term E9 is added, which is formed by averaging the outcomes from trials 1 to 9 as shown by the blue bars.
Figure 2.. Different experimental reward environments.
Figure 2.. Different experimental reward environments.
(A) Reward prediction error (RPE) values received during each task version, averaged across all participants (shaded areas represent SEM). (B) The influence of RPE values on mood reports along the task, averaged across all participants (shaded areas are SEM). See Materials and methods for a link to the online repository from where the source data of this figure can be downloaded.
Figure 3.. The better performance of the…
Figure 3.. The better performance of the Primacy model.
(A) Model comparison between the Primacy and the Recency models, using the streaming prediction criterion, where the model is predicting each mood rating using the preceding ratings. On the left, the trial-level errors in predicting mood with the Recency and the Primacy models are shown for all participants, during the structure-adaptive task (bold line depicts average across all participants). This error is calculated by predicting the t-th mood rating using all preceding (1 to t-1) mood ratings, and therefore fitting iterations start only as of the fourth mood rating (~15 gambling trials), which ensures that models have sufficient data to fit all parameters. The right panel presents the median of mean squared errors (MSEs) of the Primacy model relative to the Recency model in this criterion across all datasets (edges indicate 25th and 75th percentiles, and error bars show the most extreme data point not considered an outlier). (B) Model comparison between the Primacy and three variants of the Recency model, which also shows lower MSEs for the Primacy model. Values are median MSEs of the Primacy model relative to each of the alternative models (i.e., Recency with dynamic probability model marked with circles, Recency without the Certain term model marked with squares, and the Recency with outcomes as expectation model marked by crosses), and error bars are standard deviation across participants. The values used to derive these plots are available in Table 1, fit coefficients are presented in Figure 3—figure supplement 2, and a link for downloading all the modeling scripts can be found in Materials and methods.
Figure 3—figure supplement 1.. Distributions of the…
Figure 3—figure supplement 1.. Distributions of the estimated coefficients for the parameters of the Primacy and the different Recency models.
Figure 3—figure supplement 2.. Expanding the Primacy…
Figure 3—figure supplement 2.. Expanding the Primacy model.
(A) Equations S1 and S2 show the two additional parameters that were included in the Primacy model to test other scaling curves for most influential events on mood. (B) Examples of theoretical scaling curves that were tested with the extended model that were also outperformed by the Primacy model.
Figure 3—figure supplement 3.. Mood ratings and…
Figure 3—figure supplement 3.. Mood ratings and the respective trial-wise model parameters.
The left two columns show the task mood ratings and outcomes (A) above the expectation and reward prediction error (RPE) parameters of the Primacy (B) and the Recency (C) models (of a single participant during the Structured task). The rightmost column shows the average across all participants of mood ratings, above the combination between the expectation and RPE parameters of each model (shaded areas represent standard deviation).
Figure 4.. Neural correlates of the Primacy…
Figure 4.. Neural correlates of the Primacy model.
(A) Extracting individual whole-brain BOLD signal activation maps (βbrain) during the time interval preceding each mood rating, and individual model parameters by fitting mood ratings with the Primacy model (βE). (B) Correlation across participants between the individual weights of the model expectation term, βE , and the individual voxel-wise neural activations. A significant cluster was received with a peak at [–3,52,6], size of 132 voxels, threshold at p = 0.0017 (after a multiple comparisons correction as well as a Bonferroni correction for the three 3dMVM models we tested). Below, the resulting cluster of significant correlation is presented aligned on the Automated Anatomical Labeling (AAL) brain atlas for spatial orientation (focus point of the image is at [–7.17,50,4.19], which is located in the ACC region). (C) A statistical comparison between the relation of brain activation to the Primacy versus the Recency models. We compared the regression coefficients of the correlation between participants’ brain activation and the Primacy expectation term weights versus the regression coefficients of the relation to the Recency model expectation term (see Figure 4—figure supplement 1 for the two images before thresholding and before contrasting against each other). This contrast showed a significantly stronger relation of the Primacy model expectation weight to brain signals at [–11,49,9], extending to a cluster of 529 voxels (p = 0.0017). See Materials and methods for a link to the online repository from where the neural analyses scripts and the presented images can be downloaded.
Figure 4—figure supplement 1.. Uncorrected raw data…
Figure 4—figure supplement 1.. Uncorrected raw data neural correlates of the Primacy model and two Recency models, the original one and the one with the most similar characteristics to the Primacy model (with both dynamic win probability and elimination of the Certain term).
None of the Recency models’ clusters survived correction. Images show correlation across participants between the individual weights of the model expectation term, βE, and the individual whole-brain BOLD signal activation during the time interval preceding each mood rating (an uncorrected threshold of p = 0.05 and a minimal cluster size of 50 voxels).
Figure 4—figure supplement 2.. Mood encoding at…
Figure 4—figure supplement 2.. Mood encoding at the whole-brain level in the structured-adaptive task: mood encoding values are derived using the mood ratings as the parametric linear modulator of the BOLD signals during the pre-rating interval (at this interval, which lasts between 2.5 and 4 s, participants are presented with the mood question, but cannot rate their mood yet).
Cluster peaks in the nucleus accumbens (NACC) and covers the ACC and Caudate (337 voxels, t = 4.96).

References

    1. Ambady N, Rosenthal R. Thin slices of expressive behavior as predictors of interpersonal consequences: a meta-analysis. Psychological Bulletin. 1992;111:256–274. doi: 10.1037/0033-2909.111.2.256.
    1. Beesdo K, Höfler M, Leibenluft E, Lieb R, Bauer M, Pfennig A. Mood episodes and mood disorders: patterns of incidence and conversion in the first three decades of life. Bipolar Disorders. 2009;11:637–649. doi: 10.1111/j.1399-5618.2009.00738.x.
    1. Behrens TE, Woolrich MW, Walton ME, Rushworth MF. Learning the value of information in an uncertain world. Nature Neuroscience. 2007;10:1214–1221. doi: 10.1038/nn1954.
    1. Braams BR, van Duijvenvoorde AC, Peper JS, Crone EA. Longitudinal changes in adolescent risk-taking: a comprehensive study of neural responses to rewards, pubertal development, and risk-taking behavior. Journal of Neuroscience. 2015;35:7226–7238. doi: 10.1523/JNEUROSCI.4764-14.2015.
    1. Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences. 2000;4:215–222. doi: 10.1016/S1364-6613(00)01483-2.
    1. Casey BJ, Jones RM, Levita L, Libby V, Pattwell SS, Ruberry EJ, Soliman F, Somerville LH. The storm and stress of adolescence: insights from human imaging and mouse genetics. Developmental Psychobiology. 2010;52:225–235. doi: 10.1002/dev.20447.
    1. Chen G, Adleman NE, Saad ZS, Leibenluft E, Cox RW. Applications of multivariate modeling to neuroimaging group analysis: a comprehensive alternative to univariate general linear model. NeuroImage. 2014;99:571–588. doi: 10.1016/j.neuroimage.2014.06.027.
    1. Clark LA, Watson D. Mood and the mundane: relations between daily life events and self-reported mood. Journal of Personality and Social Psychology. 1988;54:296–308. doi: 10.1037/0022-3514.54.2.296.
    1. Cohen JD, Daw N, Engelhardt B, Hasson U, Li K, Niv Y, Norman KA, Pillow J, Ramadge PJ, Turk-Browne NB, Willke TL. Computational approaches to fMRI analysis. Nature Neuroscience. 2017;20:304–313. doi: 10.1038/nn.4499.
    1. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research. 1996;29:162–173. doi: 10.1006/cbmr.1996.0014.
    1. Daviss WB, Birmaher B, Melhem NA, Axelson DA, Michaels SM, Brent DA. Criterion validity of the mood and feelings questionnaire for depressive episodes in clinic and non-clinic subjects. Journal of Child Psychology and Psychiatry. 2006;47:927–934. doi: 10.1111/j.1469-7610.2006.01646.x.
    1. Douglas KR, Chan G, Gelernter J, Arias AJ, Anton RF, Weiss RD, Brady K, Poling J, Farrer L, Kranzler HR. Adverse childhood events as risk factors for substance dependence: partial mediation by mood and anxiety disorders. Addictive Behaviors. 2010;35:7–13. doi: 10.1016/j.addbeh.2009.07.004.
    1. Eldar E, Rutledge RB, Dolan RJ, Niv Y. Mood as representation of momentum. Trends in Cognitive Sciences. 2016;20:15–24. doi: 10.1016/j.tics.2015.07.010.
    1. Etkin A, Egner T, Kalisch R. Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences. 2011;15:85–93. doi: 10.1016/j.tics.2010.11.004.
    1. Etkin A, Büchel C, Gross JJ. The neural bases of emotion regulation. Nature Reviews Neuroscience. 2015;16:693–700. doi: 10.1038/nrn4044.
    1. Forgas JP, Bower GH, Krantz SE. The influence of mood on perceptions of social interactions. Journal of Experimental Social Psychology. 1984;20:497–513. doi: 10.1016/0022-1031(84)90040-4.
    1. Hastie T, Tibshirani R, Friedman JH. The Elements of Statistical Learning: Data Mining, Inference, and Prediction. Springer; 2009.
    1. Heller AS, Casey BJ. The neurodynamics of emotion: delineating typical and atypical emotional processes during adolescence. Developmental Science. 2016;19:3–18. doi: 10.1111/desc.12373.
    1. Hiser J, Koenigs M. The multifaceted role of the ventromedial prefrontal cortex in emotion, decision making, social cognition, and psychopathology. Biological Psychiatry. 2018;83:638–647. doi: 10.1016/j.biopsych.2017.10.030.
    1. Houser ML, Furler LA. Predicting relational outcomes: an investigation of thin slice judgments in speed dating. Human Communication. 2007;102:69–81.
    1. Huys QJ, Maia TV, Frank MJ. Computational psychiatry as a bridge from neuroscience to clinical applications. Nature Neuroscience. 2016;19:404–413. doi: 10.1038/nn.4238.
    1. Imbens G, Rubin DB. Causal Inference for Statistics, Social, and Biomedical Sciences: An Introduction. New York: Cambridge University Press; 2015.
    1. Kahneman D, Krueger AB, Schkade DA, Schwarz N, Stone AA. A survey method for characterizing daily life experience: the day reconstruction method. Science. 2004;306:1776–1780. doi: 10.1126/science.1103572.
    1. Kahneman D, Tversky A. Choices, Values, and Frames. New York Cambridge: Cambridge University Press; 2000.
    1. Katsimerou C, Redi JA, Heynderickx I. A computational model for mood recognition. User Modeling, Adaptation, and Personalization, Umap. 2014;2014:122–133. doi: 10.1007/978-3-319-08786-3_11.
    1. Kayser A, Op de Macks Z, Dahl R, Frank M. A functional MRI study of exploratory behaviors in early adolescence. Neurology. 2015;84:P2.243
    1. Keren H, O'Callaghan G, Vidal-Ribas P, Buzzell GA, Brotman MA, Leibenluft E, Pan PM, Meffert L, Kaiser A, Wolke S, Pine DS, Stringaris A. Reward processing in depression: a conceptual and Meta-Analytic review across fMRI and EEG studies. American Journal of Psychiatry. 2018;175:1111–1120. doi: 10.1176/appi.ajp.2018.17101124.
    1. Larson R, Csikszentmihalyi M, Graef R. Mood variability and the psychosocial adjustment of adolescents. Journal of Youth and Adolescence. 1980;9:469–490. doi: 10.1007/BF02089885.
    1. Levine SW. Control Handbook: Control System Advanced Methods. CRC Press; 2011.
    1. Lewis-Morrarty E, Degnan KA, Chronis-Tuscano A, Pine DS, Henderson HA, Fox NA. Infant attachment security and early childhood behavioral inhibition interact to predict adolescent social anxiety symptoms. Child Development. 2015;86:598–613. doi: 10.1111/cdev.12336.
    1. Maciejewski DF, van Lier PA, Branje SJ, Meeus WH, Koot HM. A 5-Year longitudinal study on mood variability across adolescence using daily diaries. Child Development. 2015;86:1908–1921. doi: 10.1111/cdev.12420.
    1. Neter J, Wasserman W, Kutner MH. Applied linear statistical models: regression, analysis of variance, and experimental designs. 3rd ed. Homewood, IL: Irwin; 1990.
    1. Nettle D, Bateson M. The evolutionary origins of mood and its disorders. Current Biology. 2012;22:R712–R721. doi: 10.1016/j.cub.2012.06.020.
    1. Ng TH, Alloy LB, Smith DV. Meta-analysis of reward processing in major depressive disorder reveals distinct abnormalities within the reward circuit. Translational Psychiatry. 2019;9:293. doi: 10.1038/s41398-019-0644-x.
    1. O'Doherty JP, Hampton A, Kim H. Model-based fMRI and its application to reward learning and decision making. Annals of the New York Academy of Sciences. 2007;1104:35–53. doi: 10.1196/annals.1390.022.
    1. Olsson LE, Gärling T, Ettema D, Friman M, Ståhl M. Current mood vs. recalled impacts of current moods after exposures to sequences of uncertain monetary outcomes. Frontiers in Psychology. 2017;8:66. doi: 10.3389/fpsyg.2017.00066.
    1. Ophir Y, Sisso I, Asterhan CSC, Tikochinski R, Reichart R. The turker blues: hidden factors behind increased depression rates among Amazon’s Mechanical Turkers. Clinical Psychological Science. 2020;8:65–83. doi: 10.1177/2167702619865973.
    1. Raby KL, Roisman GI, Fraley RC, Simpson JA. The enduring predictive significance of early maternal sensitivity: social and academic competence through age 32 years. Child Development. 2015;86:695–708. doi: 10.1111/cdev.12325.
    1. Ronen T, Hamama L, Rosenbaum M, Mishely-Yarlap A. Subjective Well-Being in adolescence: the role of Self-Control, social support, age, gender, and familial crisis. Journal of Happiness Studies. 2016;17:81–104. doi: 10.1007/s10902-014-9585-5.
    1. Rudebeck PH, Putnam PT, Daniels TE, Yang T, Mitz AR, Rhodes SE, Murray EA. A role for primate subgenual cingulate cortex in sustaining autonomic arousal. PNAS. 2014;111:5391–5396. doi: 10.1073/pnas.1317695111.
    1. Russell JA, Weiss A, Mendelsohn GA. Affect grid: a single-item scale of pleasure and arousal. Journal of Personality and Social Psychology. 1989;57:493–502. doi: 10.1037/0022-3514.57.3.493.
    1. Rutledge RB, Skandali N, Dayan P, Dolan RJ. A computational and neural model of momentary subjective well-being. PNAS. 2014;111:12252–12257. doi: 10.1073/pnas.1407535111.
    1. Rutledge RB, Moutoussis M, Smittenaar P, Zeidman P, Taylor T, Hrynkiewicz L, Lam J, Skandali N, Siegel JZ, Ousdal OT, Prabhu G, Dayan P, Fonagy P, Dolan RJ. Association of neural and emotional impacts of reward prediction errors with major depression. JAMA Psychiatry. 2017;74:790–797. doi: 10.1001/jamapsychiatry.2017.1713.
    1. Scholl J, Kolling N, Nelissen N, Wittmann MK, Harmer CJ, Rushworth MF. The good, the bad, and the irrelevant: neural mechanisms of learning real and hypothetical rewards and effort. Journal of Neuroscience. 2015;35:11233–11251. doi: 10.1523/JNEUROSCI.0396-15.2015.
    1. Scholl J, Kolling N, Nelissen N, Stagg CJ, Harmer CJ, Rushworth MF. Excitation and inhibition in anterior cingulate predict use of past experiences. eLife. 2017;6:e20365. doi: 10.7554/eLife.20365.
    1. Somerville LH, Jones RM, Casey BJ. A time of change: behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain and Cognition. 2010;72:124–133. doi: 10.1016/j.bandc.2009.07.003.
    1. Stevens FL, Hurley RA, Taber KH. Anterior cingulate cortex: unique role in cognition and emotion. The Journal of Neuropsychiatry and Clinical Neurosciences. 2011;23:121–125. doi: 10.1176/jnp.23.2.jnp121.
    1. Stringaris A, Vidal-Ribas Belil P, Artiges E, Lemaitre H, Gollier-Briant F, Wolke S, Vulser H, Miranda R, Penttilä J, Struve M, Fadai T, Kappel V, Grimmer Y, Goodman R, Poustka L, Conrod P, Cattrell A, Banaschewski T, Bokde AL, Bromberg U, Büchel C, Flor H, Frouin V, Gallinat J, Garavan H, Gowland P, Heinz A, Ittermann B, Nees F, Papadopoulos D, Paus T, Smolka MN, Walter H, Whelan R, Martinot JL, Schumann G, Paillère-Martinot ML, IMAGEN Consortium The brain's Response to Reward Anticipation and Depression in Adolescence: Dimensionality, Specificity, and Longitudinal Predictions in a Community-Based Sample. American Journal of Psychiatry. 2015;172:1215–1223. doi: 10.1176/appi.ajp.2015.14101298.
    1. Stringaris A, Goodman R. Mood lability and psychopathology in youth. Psychological Medicine. 2009;39:1237–1245. doi: 10.1017/S0033291708004662.
    1. Taquet M, Quoidbach J, Gross JJ, Saunders KEA, Goodwin GM. Mood homeostasis, low mood, and history of depression in 2 large population samples. JAMA Psychiatry. 2020;77:944. doi: 10.1001/jamapsychiatry.2020.0588.
    1. Vinckier F, Rigoux L, Oudiette D, Pessiglione M. Neuro-computational account of how mood fluctuations arise and affect decision making. Nature Communications. 2018;9:1708. doi: 10.1038/s41467-018-03774-z.
    1. Walker DM, Bell MR, Flores C, Gulley JM, Willing J, Paul MJ. Adolescence and reward: making sense of neural and behavioral changes amid the Chaos. The Journal of Neuroscience. 2017;37:10855–10866. doi: 10.1523/JNEUROSCI.1834-17.2017.
    1. Watson D, Tellegen A. Toward a consensual structure of mood. Psychological Bulletin. 1985;98:219–235. doi: 10.1037/0033-2909.98.2.219.
    1. Whitmer AJ, Frank MJ, Gotlib IH. Sensitivity to reward and punishment in major depressive disorder: effects of rumination and of single versus multiple experiences. Cognition & Emotion. 2012;26:1475–1485. doi: 10.1080/02699931.2012.682973.
    1. Wilson RC, Collins AG. Ten simple rules for the computational modeling of behavioral data. eLife. 2019;8:e49547. doi: 10.7554/eLife.49547.
    1. Wittmann MK, Kolling N, Akaishi R, Chau BK, Brown JW, Nelissen N, Rushworth MF. Predictive decision making driven by multiple time-linked reward representations in the anterior cingulate cortex. Nature Communications. 2016;7:12327. doi: 10.1038/ncomms12327.
    1. Wood A, Kroll L, Moore A, Harrington R. Properties of the mood and feelings questionnaire in adolescent psychiatric outpatients: a research note. Journal of Child Psychology and Psychiatry. 1995;36:327–334. doi: 10.1111/j.1469-7610.1995.tb01828.x.
    1. Zald DH, Mattson DL, Pardo JV. Brain activity in ventromedial prefrontal cortex correlates with individual differences in negative affect. PNAS. 2002;99:2450–2454. doi: 10.1073/pnas.042457199.

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