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Articles, Behavioral/Cognitive

Interactions between Dorsolateral and Ventromedial Prefrontal Cortex Underlie Context-Dependent Stimulus Valuation in Goal-Directed Choice

Sarah Rudorf and Todd A. Hare
Journal of Neuroscience 26 November 2014, 34 (48) 15988-15996; https://doi.org/10.1523/JNEUROSCI.3192-14.2014
Sarah Rudorf
1Center for Economics and Neuroscience, and
2Department of Epileptology, University Hospital Bonn, 53127 Bonn, Germany, and
3Laboratory for Social and Neural Systems Research, Department of Economics, University of Zurich, 8006 Zürich, Switzerland
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Todd A. Hare
3Laboratory for Social and Neural Systems Research, Department of Economics, University of Zurich, 8006 Zürich, Switzerland
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  • Figure 1.
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    Figure 1.

    Timeline of the binary choice task. On each trial, the subject chooses between two visual stimuli that vary in shape, pattern, and color. Each attribute is associated with a monetary value that the subject has learned before scanning. At the beginning of each block of three to five trials, a cue that indicates which context applies to this block is presented for 1 s. In the shape context (60% of all trials) only the shape determines the value of a stimulus (top row), in the bonus context (40% of all trials), either the pattern (middle row) or the color (bottom row) add or subtract a value to or from the shape value. After a jittered fixation display the first choice pair is presented and the subject has up to 3.5 s to make a choice (mean RT = 1.17 s). Once a response is made, the chosen stimulus is highlighted with a white frame for 0.5 s. After choice feedback, a fixation cross is presented for a jittered interval of 4.5–8.5 s minus RT before the next trial begins.

  • Figure 2.
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    Figure 2.

    Overall value encoding. Activity in the vmPFC, ventral striatum, and PCC reflects the difference between chosen and nonchosen stimulus values at the time of choice. The figure shows statistical parametric maps of the random-effects analysis thresholded at a cluster-corrected FWE-threshold of p < 0.05, and projected on a template brain in MNI space. Colors indicate the magnitude of t values as shown by the color scale on the left. Circled regions were used as ROIs in further analyses.

  • Figure 3.
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    Figure 3.

    Default shape value encoding decreases in bonus contexts. A, B, Statistical parametric maps of the random effects analyses, color coded for the t values as indicated by the color bars, thresholded at a cluster-corrected FWE-threshold of p < 0.05, and projected on a template brain in MNI space. A, Activity in the vmPFC and PCC reflects the difference between the default shape value of the chosen and nonchosen option in shape trials. B, The default shape value encoding in these regions decreases in bonus compared with shape trials. C, The graphs show the mean (M) and SE of the β estimates for the shape values of the chosen, and nonchosen option in the indicated regions plotted for shape and bonus trials, separately.

  • Figure 4.
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    Figure 4.

    Context sensitivity. Activity in the dlPFC, IPL, anterior insula, dorsal ACC, and ventrolateral PFC is greater during choices in bonus compared with shape trials. The figure shows statistical parametric maps of the random-effects analysis, color-coded for the t values as indicated by the color bar, thresholded at a cluster-corrected FWE-threshold of p < 0.05, and projected on a template brain in MNI space. The circled region was used as ROI in the visualization of the functional connectivity effects in Figure 5.

  • Figure 5.
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    Figure 5.

    PPI effects seeded in the vmPFC when a context change is indicated. Functional coupling between the vmPFC (seed) and the dlPFC/IFG increases at display of the context cue, whereas coupling with the PCC decreases. A, Statistical parametric maps of the random-effects analysis, color coded for the t values as indicated by the color bar, thresholded at a cluster-corrected FWE-threshold of p < 0.05, and projected on a template brain in MNI space. B, Bar graph of the mean (M) and SE of the β estimates for the intrinsic coupling and cue PPI term for the vmPFC with the left dlPFC/IFG ROI circled in Figure 4. C, The PPI target regions (red), in particular the dlPFC/IFG, show substantial overlap (orange) with the regions that encode context sensitivity (yellow) as shown in Figure 4. Shown here are statistical parametric maps of the respective random-effects analysis and their overlap as indicated by the color legend, thresholds as specified in A.

  • Figure 6.
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    Figure 6.

    Context-dependent vmPFC–dlPFC connectivity increases with the reweighting of stimulus attributes. The context-dependent connectivity (bonus PPI > shape PPI) between vmPFC and two regions in the dlPFC correlates positively with the relative bonus value encoding in the vmPFC at the time of choice. Top, Shown here are statistical parametric maps of the random-effects analysis (between-subjects correlation), color coded for the t values as indicated by the color bars, thresholded at a cluster-corrected FWE-threshold of p < 0.05, and projected on a template brain in MNI space. Bottom, Graphs show the single-subject means of the β estimates in the indicated regions for the bonus PPI minus shape PPI effect seeded in the vmPFC (x-axes) plotted against the single-subject means of the β estimates in the vmPFC for the difference between chosen and nonchosen bonus values (y-axes). The left and right scatter plots correspond to the left dlPFC/SFG and the left dlPFC/MFG clusters shown in the left and rightmost coronal sections.

Tables

  • Figures
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    Table 1.

    Regions positively correlated with the difference between chosen and nonchosen stimulus values or vice versa

    RegionSideMNI coordinatesCluster size kEMax stat t
    xyz
    Chosen > nonchosen value
        vmPFC/ventral striatumR351−165727.84
        Caudate/white matterR182615956.91
        Putamen/lentiform nucleusL−273−10706.88
        Parahippocampal gyrus/PCCL−30−35−16626.82
        Postcentral gyrusR46−1224316.52
        CerebellumR18−52−164846.41
        Occipital lobeL−25−9712766.39
        Occipital lobeR18−10092606.22
        Middle temporal gyrusL−601−22285.83
        IFGR3333−10275.67
        Superior temporal gyrusL−62−273235.47
        Caudate/white matterR61815355.27
        Occipital lobeL−20−65−13344.58
        Parietal lobe/posterior insulaL−45−1521254.55
    Nonchosen > chosen value
        aIns/IFGL−3023330113.34
        IPLR48−37495039.95
        aIns/IFG/ACC/SFGR3323021769.61
        dlPFC/IFGL−3736187568.95
        IPLL−30−52436618.53
        Thalamus/midbrainR6−2001056.96
        Middle temporal gyrusL−27−5461926.72
        CaudateR8136265.89
        CaudateL−10136254.70
        Parietal lobeR11−7046284.70
    • Results from the random effects analysis are shown. Height threshold, t(21) = 3.53; extent threshold, kE > 23 voxels. Note that a higher t threshold was used here only for the purpose of separating large clusters from these contrasts in order to create a more informative table. The activations survive whole-brain correction for multiple comparisons based on FWE-control at the cluster level. aIns, Anterior insula.

    • View popup
    Table 2.

    Regions encoding the relative bonus value in bonus trials, the relative shape value in shape trials, and the relative shape value in bonus compared with shape trials

    RegionSideMNI coordinatesCluster size kEMax stat t
    xyz
    Relative bonus value encoding in bonus trials
        Parietal lobe/PCC/precuneusL−20−5231347.08
        vmPFCR18510506.64
        Parietal lobe/PCCR31−5221645.93
        CaudateR181321615.67
        Occipital lobeR11−9518255.48
        ACC/white matterR233115295.48
        Occipital lobeR46−750215.10
        CuneusR1−8218205.04
        Fusiform gyrusR21−60−13214.89
        Putamen/lentiform nucleusL−27−179324.85
        Precentral gyrusR18−2765304.79
    Relative shape value encoding in shape trials
        PCCL−7−62153149.67
        vmPFC/ventral striatumR14803618.00
        Parahippocampal gyrusL−30−35−16556.50
    Decreased shape value encoding in bonus > shape trials
        vmPFCR346−19236.28
        PCCR13−6018336.21
        PCCL−7−6215915.95
    • Results from the random effects analyses are shown. Height threshold, t(17) = 3.65; extent threshold, kE > 20 voxels. Note that a higher t threshold was used here only for the purpose of separating large clusters from these contrasts to create a more informative table. All activations survive whole-brain correction for multiple comparisons based on FWE-control at the cluster level. aIns, Anterior insula.

    • View popup
    Table 3.

    Regions differentially active in bonus trials compared to shape trials

    RegionSideMNI coordinatesCluster size kEMax stat t
    xyz
    Bonus > shape choices
        IPLL−27−5037281611.24
        aInsL−3221313611.11
        aInsR362301779.44
        dorsal ACCL−721403578.46
        dlPFC/IFGL−456315328.20
        BrainstemR23−30151277.90
        Lateral PFCR3841187657.65
        BrainstemL−7−15−131727.42
        PCCL−7−3031296.93
        dlPFC/MFG/SFGR313493476.71
        Inferior temporal gyrusR56−40−19876.65
        CerebellumR1−57−221176.63
        ThalamusL−15−17181276.58
        dlPFC/MFGL−30−2522036.35
        Inferior temporal gyrusL−50−55−161146.23
        vlPFCL−405801435.73
    Shape > bonus choices
        vmPFCL−251−4783510.48
        Precentral gyrus/parietal lobeR58−101234279.21
        Superior parietal lobeL−20−47651276.84
        Postcentral gyrusR21−30621826.31
        IFG/vlPFCR56313866.07
        IFG/vlPFCL−522331375.87
        Temporal poleL−226−41305.78
        Occipital lobeL−22−9215685.28
        Precentral gyrus/parietal lobeL−22−3062434.86
    • Results from the random effects analysis are shown. Height threshold, t(21) = 3.53; extent threshold, kE > 27 voxels. Note that a higher t threshold was used here only for the purpose of separating large clusters from these contrasts to create a more informative table. All activations survive whole-brain correction for multiple comparisons based on FWE-control at the cluster level. aIns, Anterior insula; vlPFC, ventrolateral prefrontal cortex.

    • View popup
    Table 4.

    Regions showing increased or decreased functional connectivity with the vmPFC during cue display

    RegionSideMNI coordinatesCluster size kEMax stat t
    xyz
    Increased functional connectivity at cue
        IPL/precentral gyrusL−35−25523946.51
        dlPFC/IFG/aInsL−551131665.61
        IPLL−30−5746855.10
        IPLR43−45461254.75
        dlPFC/IFGR561327644.64
    Decreased functional connectivity at cue
        PCCR8−55152685.63
        Middle temporal gyrusL−40−6727904.56
    • Results from the random effects analysis are shown. Height threshold, t(21) = 2.83; extent threshold, kE > 53 voxels. All activations survive whole-brain correction for multiple comparisons based on FWE-control at the cluster level. aIns, Anterior insula.

    • View popup
    Table 5.

    Regions showing increased or decreased functional connectivity with the vmPFC during choices in bonus compared with shape trials

    RegionSideMNI coordinatesCluster size kEMax stat t
    xyz
    Increased functional connectivity for bonus > shape choices
        IPLR58−42401425.10
    Decreased functional connectivity for bonus > shape choices
        PCCR1−65243605.46
        Superior temporal gyrusR56−6521604.87
        ACCR116−10944.79
        vmPFCL−1241−16994.34
    • Results from the random effects analysis are shown. Height threshold, t(21) = 2.83; extent threshold, kE > 58 voxels. All activations survive whole-brain correction for multiple comparisons based on FWE-control at the cluster level.

    • View popup
    Table 6.

    Regions where the bonus PPI minus shape PPI contrast is associated with individual differences in vmPFC bonus value encoding

    RegionSideMNI coordinatesCluster size kEMax stat t
    xyz
    dlPFC/SFGL−155637675.22
    dlPFC/MFGL−372637544.81
    Middle temporal gyrusL−60−30−7554.68
    PCCL−7−7234694.42
    Middle temporal gyrusL−42−6227613.91
    • Results from the random effects analysis are shown. Height threshold, t(17) = 2.92; extent threshold, kE > 54 voxels. All activations survive whole-brain correction for multiple comparisons based on FWE-control at the cluster level.

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The Journal of Neuroscience: 34 (48)
Journal of Neuroscience
Vol. 34, Issue 48
26 Nov 2014
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Interactions between Dorsolateral and Ventromedial Prefrontal Cortex Underlie Context-Dependent Stimulus Valuation in Goal-Directed Choice
Sarah Rudorf, Todd A. Hare
Journal of Neuroscience 26 November 2014, 34 (48) 15988-15996; DOI: 10.1523/JNEUROSCI.3192-14.2014

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Interactions between Dorsolateral and Ventromedial Prefrontal Cortex Underlie Context-Dependent Stimulus Valuation in Goal-Directed Choice
Sarah Rudorf, Todd A. Hare
Journal of Neuroscience 26 November 2014, 34 (48) 15988-15996; DOI: 10.1523/JNEUROSCI.3192-14.2014
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