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Research Articles, Behavioral/Cognitive

Influence of vmPFC on dmPFC Predicts Valence-Guided Belief Formation

Bojana Kuzmanovic, Lionel Rigoux and Marc Tittgemeyer
Journal of Neuroscience 12 September 2018, 38 (37) 7996-8010; DOI: https://doi.org/10.1523/JNEUROSCI.0266-18.2018
Bojana Kuzmanovic
1Translational Neurocircuitry Group, Max Planck Institute for Metabolism Research Cologne, 50931 Cologne, Germany, and
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Lionel Rigoux
1Translational Neurocircuitry Group, Max Planck Institute for Metabolism Research Cologne, 50931 Cologne, Germany, and
2Translational Neuromodeling Unit, Institute for Biomedical Engineering, University of Zurich and ETH Zurich, 8032 Zurich, Switzerland
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Marc Tittgemeyer
1Translational Neurocircuitry Group, Max Planck Institute for Metabolism Research Cologne, 50931 Cologne, Germany, and
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  • Figure 1.
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    Figure 1.

    Outline and examples of experimental trials. Each experimental trial consisted of four succeeding events. With respect to a specific adverse life event (e.g., suffering from cancer), subjects had to estimate the BR (eBR) and their own risk (E1). They were then presented with the actual BR and had the opportunity to estimate their own risk again (E2). After identical eBR and E1, the upper progression of the hypothetical trial example shows a BR lower than expected indicating good news, whereas the lower progression shows a BR higher than expected indicating bad news. EEs corresponded to the difference between the eBR and the actual BR and the update corresponded to the difference between the first and the second self-risk estimate. Note that, in both trial examples, the EE is 10 and the update is 8. For eBR, E1, and E2, subjects were instructed to use response buttons to adjust the displayed number to match their estimate as soon as the number font changed to green (after 2 s). Interstimulus intervals between eBR, E1, and E2, as well as intertrial intervals after E2, were jittered and consisted of a fixation cross (not shown here).

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    Figure 2.

    Task performance and computational modeling. A, Bars show subjects' updates, that were significantly larger after good news (GOOD) than after bad news (BAD). White dots represent simulations of updates by the “biased” computational model that assumes asymmetric learning rates for good and bad news (αA, two free parameters, α and A). Gray dots indicate simulated updates resulting from the “unbiased” model that assumes identical learning rates for good and bad news (α, one free parameter, α). The simulated unbiased updates provide a normative benchmark for rational updating with learning rates estimated for each subject under consideration of her or his exact trial history. Error bars indicate SEs. B, Bayesian model comparison confirmed that the biased model αA best predicted subjects' updates. Model frequencies show that the majority of subjects were best described by the αA model above and beyond chance (red dashed line). Error bars indicate the posterior variance. C, Learning rates extracted from the winning model αA were significantly higher after good than bad news. Error bars indicate SEs. D, Optimism bias (updateGOOD − updateBAD) and A (estimated for each subject by the model αA) were significantly correlated (dots represent single subjects). E, F, Correlations between task variables separately for trials with good news (E) and those with bad news (F). *p < 0.05, **p < 0.01.

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    Figure 3.

    Brain regions encoding errors and the valence of belief updating. A, When being confronted with the actual BR, errors in BR estimation (weighted by the PR) were tracked by the ACC, the IFG, the anterior insula, the middle orbital gyrus and the dlPFC. The line chart shows that the activity in the dlPFC (representative of all clusters) increased with decreasing error size (parametric modulation by error, negative correlation). Of all the involved regions, only in the dlPFC did the magnitude of the error tracking correlate with the general learning rate component α (see scatter plot). Therefore, subjects with a stronger error tracking in the dlPFC also more strongly adjusted their initial beliefs in response to errors. B, During the second risk estimation, the activity in the vmPFC encoded the valence of updating, adjusted for EE and PR. The gray box schematically illustrates the opposed valences of increasing updates after good and bad news (in this example, eBR = E1). After good news, large updates are favorable because they ultimately change beliefs toward lower risk estimates and small updates are unfavorable because they let the opportunity to improve risk estimates pass by. In contrast, after bad news, large updates are unfavorable because they ultimately change beliefs toward higher risk estimates and small updates are favorable because they prevent worsening of risk estimates. Resulting valences are summarized in the table below: unfavorable (U), mid (M), and favorable (F) updates. The line chart shows that the activity in the vmPFC tracked the positive valence because it increased with increasing update sizes after good news but decreased with increasing update sizes after bad news. The scatter plot shows that subjects with a stronger optimism bias also demonstrated a greater tracking of favorable updating in the vmPFC. In A and B, the line charts and the scatter plots were not used for statistical inference (which was performed in parametric modulation and covariate analyses within the SPM framework); they are shown solely for illustrative purposes. C, After demonstrating the valence effect with the more precise parametric modulation analysis presented in B, a simplified analysis of updating was conducted as a basis for DCM. Here, all trials were assigned to three valence categories: those with unfavorable (U), mid (M), and favorable (F) updates (adjusted for EE). Conjunction across these three categories revealed a distributed network involved in general updating, overlapping with the error tracking effect in the dlPFC. Comparing trials with favorable and unfavorable updates revealed the differential recruitment of the vmPFC and the dmPFC during updating. The line charts show contrast estimates in the dlPFC, vmPFC, and dmPFC, respectively.

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    Figure 4.

    Neurocircuitry mechanisms underlying optimistic belief updating. A, Ten different dynamic causal models varying in intrinsic connectivity and contextual modulation (unfavorable and favorable updating, U and F) were specified. The model space encompassed three brain regions involved in updating: dlPFC, vmPFC, and dmPFC. B, Bayesian model selection revealed that the model m1 best explained subjects' BOLD signal above and beyond chance (red dashed line). In this model, the coupling between dlPFC and vmPFC was differentially modulated by unfavorable and favorable updating. Therefore, the vmPFC filtered the incoming information in a valence-dependent manner and furthermore influenced the dmPFC. C, Connectivity parameters derived from m1 show that the coupling between dlPFC and vmPFC tended to be weaker in the context of unfavorable relative to favorable updating. D, Optimism bias correlated with two parameters of m1 (highlighted in red): differential modulation of the dlPFC-vmPFC connection by favorable versus unfavorable updating (F-U) and the strength of the vmPFC-dmPFC connection (vmPFC::dmPFC). Therefore, subjects with a stronger optimism bias also demonstrated a greater valence-dependent filtering of incoming information by vmPFC and a greater transmission of this differential signal further to dmPFC.

Tables

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    Table 1.

    Task variables

    ParameterM (SD)pSource
    Good newsBad news
    Number of trials39.96 (1.45)38.21 (2.38)0.024
    Estimated base rate (eBR)49.74 (12.67)45.92 (12.30)0.000Participants' response
    First estimate (E1)42.64 (11.10)37.85 (10.49)0.000Participants' response
    Presented base rate (BR)36.35 (12.57)59.76 (12.22)0.000Base rate algorithm
    Estimation error (EE)13.39 (0.95)13.84 (0.57)0.001EE = |eBR − BR|
    Second estimate (E2)35.12 (10.86)44.55 (11.26)0.000Participants' response
    Update7.51 (2.58)6.70 (2.20)0.045UpdateGOOD = E1 − E2, UpdateBAD = E2 − E1
    Personal relevance (PR)0.70 (0.12)0.69 (0.13)0.287for E1 < eBR: PR = 1 − ((eBR − E1)/(eBR − 1))
    for E1 > eBR: PR = 1 − ((E1 − eBR)/(99 − eBR))
    for E1 = eBR: PR = 1
    RT eBR (s)5.19 (0.84)5.11 (0.80)0.192Participants' response
    RT E1 (s)3.25 (0.91)3.30 (0.90)0.461Participants' response
    RT E2 (s)2.70 (0.62)2.56 (0.61)0.018Participants' response
    • All measures (except for number of trials) were recorded or computed for each trial and were then averaged separately for the conditions GOOD and BAD and separately for each participant. Positive update values indicated updates toward the BR and negative values updates away from the BR (<3% of the trials). PR: 1 indicates equal risk perception for the average and oneself and 0 indicates maximally different risk perception for the average and oneself; note that PR corresponds to “relative personal knowledge” in Kuzmanovic and Rigoux, 2017. RT, Reaction time. p-values refer to paired two-tailed paired t test with n = 24.

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    Table 2.

    Error coding during base rate presentation and its relation to the learning rate component alpha

    Cluster sizePeak
    pFWE-corrTxyz
    (1) Parametric modulation of BRGOOD and BRBAD by error
        (a) Conjunction: PM_errorGOOD and PM_errorBAD, positive correlation
            No significant results
        (b) Conjunction: PM_errorGOOD and PM_errorBAD, negative correlation
            Anterior cingulate cortex630.0005.18103420
            Inferior frontal gyrus (p. triangularis)450.0014.0946440
            Anterior insula370.0014.0528226
            Middle orbital gyrus300.0024.001650−2
            dlPFCCOV_Alpha320.0043.81404028
        (c) PM_errorGOOD > PM_errorBAD
            No significant results
        (d) PM_errorBAD > PM_errorGOOD
            Cerebellum480.0016.90−18−76−46
            Middle occipital gyrus830.0056.17−34−8428
            Superior parietal lobule470.0066.1524−5648
            Conjunction: PM_errorBAD, positive correlation and PM_errorGOOD, negative correlation
                Inferior occipital gyrus220.0014.1640−84−10
    (2) Covariate analysis of error coding with alpha (masked with contrast 1b)
    dlPFC120.0084.46403830
    • Error = EE * PR, based on the computational modeling of task performance. For significant differences between PM_errorGOOD and PM_errorBAD, we report global conjunction results to clarify whether the difference relates to different magnitudes of the same modulation effect (e.g., the positive correlation between BOLD and error was stronger in BAD than in GOOD) or to modulation effects of opposite direction (e.g., the correlation between BOLD and error was positive in BAD, but negative in GOD). COV_Alpha indicates that in this cluster the magnitude of the error tracking correlated with the learning rate component alpha across subjects (covariate analysis). Peak coordinates refer to the MNI space.

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    Table 3.

    Activity during second estimation that was modulated by update size

    Cluster sizePeak
    pFWE-corrTxyz
    (1) Parametric modulation of E2GOOD and E2BAD by update
        (a) PM_updateGOOD > PM_updateBAD
            vmPFC490.0005.63−1244−16
            Conjunction: PM_updateGOOD, positive correlation & PM_updateBAD, negative correlation0.0105.40−644−20
                vmPFC440.0003.67−846−18
    0.0203.35−1054−12
        (b) PM_updateBAD > PM_updateGOOD
            No significant results
        (c) Conjunction: PM_updateGOOD and PM_updateBAD, positive correlation
            No significant results
        (d) Conjunction: PM_updateGOOD and PM_updateBAD, negative correlation
            Fusiform gyrus (V4)8160.0007.3328−72−8
            Lingual gyrus (V1)0.0004.596−722
            Lingual gyrus (V3)7360.0006.70−10−86−6
            Superior occipital gyrus (V3)0.0004.11−16−8818
            Superior occipital gyrus2310.0005.1722−8020
            Precentral gyrus4940.0004.54−32−1864
            Postcentral gyrus0.0004.34−42−2654
            Fusiform gyrus250.0103.5324−46−14
    (2) Covariate analysis of valence coding with optimism bias
        (a) Masked with contrast 1a, conjunction
            vmPFC390.00015.59−650−18
        (b) Whole brain
            vmPFC140.0117.28−248−18
    (3) Three categories of E2: unfavorable, mid, favorable
        (a) E2favorable > E2unfavorable
            vmPFCDCM270.0005.84−246−22
            Dorsomedial prefrontal cortex300.0205.39−164440
        (b) E2unfavorable > E2favorable
            No significant results
        (c) Conjunction: all 3 categories of E2
            Lingual gyrus (V3)575710.00024.0024−86−12
            Fusiform gyrus0.00018.90−30−58−14
            Lingual gyrus (V4)0.00018.70−24−86−14
            Fusiform gyrus0.00016.4032−50−18
            Inferior parietal lobule0.00014.80−44−4048
            Inferior parietal lobule0.00012.6050−3448
            Thalamus0.0008.3820−30−2
            Middle frontal gyrus69590.00010.5042260
            Inferior frontal gyrus (p. opercularis)0.0009.62461036
            dlPFCDCM0.0008.99444226
            dlPFC14140.0008.46−285228
            dlPFC0.0008.21−403032
            Inferior frontal gyrus (p.triangularis)0.0007.44−343424
            Thalamus1360.0006.58−8−228
            Posterior cingulate cortex1250.0006.13−2−2428
            Precentral gyrus230.0105.6534−2872
    • For significant differences between PM_updateGOOD and PM_updateBAD, we report global conjunction results to clarify whether the difference relates to different magnitudes of the same modulation effect (e.g., the positive correlation between BOLD and update was stronger in GOOD than in BAD), or to modulation effects of opposite direction (e.g., the correlation between BOLD and update was positive in GOOD, but negative in BAD). Peak coordinates refer to the MNI space.

    • View popup
    Table 4.

    DCM parameter estimates of the model m1 and correlations with measures of optimism bias

    M (SD)p, t testr, optimism biaspr, asymmetryp
    Matrix A
        dl::dl−0.01 (0.09)0.000*−0.190.361−0.210.323
        dl::vm−0.06 (0.12)0.030−0.230.277−0.050.819
        vm::dl0.10 (0.15)0.000*−0.090.679−0.150.485
        vm::vm−0.07 (0.09)0.000*−0.200.348−0.200.342
        vm::dm0.15 (0.14)0.000*0.470.020*0.490.015
        dm::vm0.08 (0.124)0.004*0.270.2070.320.127
        dm::dm−0.02 (0.03)0.001*−0.490.015−0.560.005
    Matrix B
        U on dl::vm−0.35 (1.06)0.123−0.230.275−0.310.147
        F on dl::vm0.05 (1.00)0.8220.490.0150.360.088
        F - U0.39 (1.42)0.1880.520.009*0.480.018
    Matrix C
        U M F to dl0.12 (0.07)0.0000.200.3400.130.541
    • Parameter estimates are shown in Hertz, self-connections were log-transformed.

    • dl, Dorsolateral prefrontal cortex; vm, ventromedial prefrontal cortex; dm, dorsomedial prefrontal cortex; “::,” endogenous connection; U, unfavorable updating; M, mid-updating; F, favorable updating.

    • ↵*Equivalent to p < 0.05, Bonferroni-corrected for multiple comparisons (Matrix A, t test, p < 0.007 corrected for 7 comparisons; r, optimism bias, p < 0.025 corrected for 2 comparisons with a priori hypotheses).

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Journal of Neuroscience
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12 Sep 2018
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Influence of vmPFC on dmPFC Predicts Valence-Guided Belief Formation
Bojana Kuzmanovic, Lionel Rigoux, Marc Tittgemeyer
Journal of Neuroscience 12 September 2018, 38 (37) 7996-8010; DOI: 10.1523/JNEUROSCI.0266-18.2018

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Influence of vmPFC on dmPFC Predicts Valence-Guided Belief Formation
Bojana Kuzmanovic, Lionel Rigoux, Marc Tittgemeyer
Journal of Neuroscience 12 September 2018, 38 (37) 7996-8010; DOI: 10.1523/JNEUROSCI.0266-18.2018
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  • belief update
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