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Research ArticleResearch Article: New Research, Cognition and Behavior

Additive Effects of Monetary Loss and Positive Emotion in the Human Brain

Sagarika Jaiswal, Lakshman N.C. Chakravarthula and Srikanth Padmala
eNeuro 2 April 2024, 11 (4) ENEURO.0374-23.2024; https://doi.org/10.1523/ENEURO.0374-23.2024
Sagarika Jaiswal
Centre for Neuroscience, Indian Institute of Science, Bangalore, Karnataka 560012, India
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Lakshman N.C. Chakravarthula
Centre for Neuroscience, Indian Institute of Science, Bangalore, Karnataka 560012, India
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Srikanth Padmala
Centre for Neuroscience, Indian Institute of Science, Bangalore, Karnataka 560012, India
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  • Figure 1.
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    Figure 1.

    Experimental design. A, On each trial, during the initial choice stage, participants viewed images of chairs and planes displayed side-by-side on the screen for 2 s and were asked to select one of those images. A yellow-colored square highlighted the selected choice. After a jittered ISI, an emotional image (positive or neutral) was shown as feedback during the subsequent outcome stage (2 s). The valence of the emotional image signaled monetary loss or no-loss outcome. In the example trial shown, if participants saw a positive image, it indicated that they lost money on that trial, while neutral indicated no loss. This emotion–loss mapping was reversed in the other phase. Each trial ended with a blank jittered ITI period. B, In one phase (Phase 1), positive stimulus indicated a loss outcome, and neutral stimulus indicated a no-loss outcome. This valence–outcome mapping was reversed in the second phase (Phase 2). Each participant completed both phases of the experiment, and the order of phases was counterbalanced across participants. ISI, interstimulus interval; ITI, intertrial interval.

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    Figure 2.

    Main effects of emotion and loss. Clusters that exhibited the main effects of (A) Emotion and (B) Loss outcomes at an uncorrected p = 0.001 and 37-voxel cluster extent (cluster-level α of 0.05). Because cluster-extent–based thresholding was used for multiple-comparison correction, voxels are displayed using a binary threshold. For further rationale about using binary maps in the context of cluster-based thresholding, see Woo et al., 2014.

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    Figure 3.

    Conjunction of emotion and loss effects. Clusters that exhibited conjunction of the main effects of Emotion and Loss factors in (A) vmPFC, (B) bilateral caudate, (C) bilateral amygdala, and (D) bilateral lateral occipital cortex. For each cluster, the bar plot shows the average group-level estimates of the four outcome conditions of interest. It should be noted that the primary purpose of these average bar plots is to illustrate the overlapping pattern of the main effects and not to draw any statistical inference. Hence, error bars were not plotted on top of the average estimates to avoid issues of circularity (Kriegeskorte et al., 2009).

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    Figure 4.

    Relationship between emotion and loss effects. Pearson's correlation between Emotion and Loss main effects across participants in clusters that exhibited conjunction of the main effects in (A) vmPFC, (B) bilateral caudate, and (C) bilateral amygdala. Emotion main effect index: (loss + no loss)Positive – (loss + no loss)Neutral; Loss main effect index: (positive + neutral)Loss – (positive + neutral)No loss.

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    Figure 5.

    Subjective hedonic ratings of experienced outcomes. The bar plot shows the average self-reported pleasantness ratings for the four outcome conditions on a scale of 1–9 (1 being unpleasant and 9 being pleasant). Each dot indicates the individual participant ratings.

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    Figure 6.

    Estimated learning rates from the RL model. A, The bar plot shows the average estimated learning rates for the chair and plane stimulus for two phases separately. In phase 1, positive stimulus signaled a loss outcome and neutral stimulus signaled a no-loss outcome. In phase 2, neutral stimulus signaled a loss outcome and positive stimulus signaled a no-loss outcome. B, The bar plot shows the average estimated learning rates for the deemed high inherent valued and low inherent valued stimulus for two phases separately. Each dot indicates the estimated learning rate of each participant.

Tables

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    Table 1.

    Mean self-reported valence and arousal ratings (with standard deviation in parentheses) of the two sets of 36 scene stimuli each that were employed in this study

    Valence ratings
    Descriptive valuesTwo-way ANOVA results
    Set1Set2EffectF valuep value
    EmotionMeanSDMeanSDMain effect: emotion41.391<0.001
    Positive7.190.227.160.19Main effect: set1.8620.202
    Neutral5.220.295.160.25Interaction effect: emotion*set0.0940.766
    Arousal ratings
    Descriptive valuesTwo-way ANOVA results
    Set1Set2EffectF valuep value
    EmotionMeanSDMeanSDMain effect: emotion134.683<0.001
    Positive6.280.986.161.18Main effect: set6.5370.029
    Neutral1.880.361.750.36Interaction effect: emotion*set0.0020.969
    • A 2 emotion (positive, neutral) × 2 set (Set1, Set2) two-way ANOVA was performed on the valence and arousal ratings of the scene stimuli. A main effect of emotion was observed in both the valence and arousal ratings with the positive scenes being rated higher in both valence and arousal than the neutral scenes. No emotion × set interaction was observed for both valence and arousal ratings.

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    Table 2.

    Main effect of Emotion outcome

    Positive > neutral

    ES = [(loss + no loss)Positive – (loss + no loss)Neutral]

    ClusterxyzkF(1,34)ES
    Medial frontal cortex, cingulate cortex, precuneus, fusiform gyrus, cerebellum, thalamus, brainstem, midbrain56−72−442,26750.691.36
    R. precentral gyrus506361,62247.140.46
    L. precentral gyrus−500341,11923.020.26
    R. inferior frontal gyrus54401023126.930.34
    R. middle temporal gyrus640−2217714.030.14
    L. anterior insula−4026414660.660.14
    L. inferior frontal gyrus−52401014620.170.19
    R. superior frontal gyrus2106212414.690.11
    L. perirhinal/rhinal sulcus−38−4−3411125.330.16
    L. middle insula−36−6186135.660.11
    R. globus pallidus22−285314.450.06
    R. middle insula38−2143827.440.12

    Neutral > positive

    ES, [(loss + no loss)Neutral – (loss + no loss)Positive]

    Brain regionsxyzkF(1,34)ES
    R. parahippocampal gyrus28−46−10537168.180.30
    L. parahippocampal gyrus−28−60−1047970.270.25
    R. angular gyrus52−605043317.170.18
    R. medial frontal gyrus, inferior frontal sulcus42264033624.260.16
    L. anterior transverse temporal gyrus−56−161027118.330.14
    R. superior temporal gyrus68−10−619614.590.18
    R. superior frontal gyrus4284415537.620.11
    R. transverse temporal gyrus50−281411019.210.14
    R. superior/middle temporal gyrus−46−3286420.730.11
    Calcarine sulcus/striate cortex0−84223713.240.11
    • The following clusters survived multiple-comparison correction in univariate whole-brain voxel-wise analysis at the outcome phase [peak MNI coordinates, cluster size (k), F(1,34) values, and unstandardized effect size in terms of % signal change (ES)].

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    Table 3.

    Main effect of Loss outcome

    No loss > loss

    ES = [(positive + neutral)No loss – (positive + neutral)Loss]

    ClusterxyzkF(1,34)ES
    Bilateral striatum−6043,93615.230.35
    Medial frontal cortex (vmPFC)06242,38531.570.24
    R. cerebellum (lateral zone)48−72−422,15840.870.29
    R. middle/inferior temporal gyrus60−56−161,17114.470.20
    R. inferior occipital gyrus26−98−1286319.520.29
    L. middle temporal gyrus−64−54−879113.580.19
    L. inferior occipital gyrus−6−98−1876313.310.32
    L. middle/inferior frontal gyrus−50401869315.050.15
    L. cerebellum (lateral zone)−42−74−4865816.670.21
    R. posterior cingulate cortex/precuneus0−463845914.060.13
    R. anterior orbital gyrus4040−2039416.500.19
    Cerebellum (vermis)−2−42−3635414.160.17
    L. precentral gyrus, inferior precentral sulcus−5484222315.030.19
    R. superior frontal gyrus (lateral part), accessory superior frontal sulcus26305220422.080.09
    Midcingulate cortex0−82815515.530.12
    L. cerebellum (posterior lobe)−20−86−4614413.310.22
    L. lateral posterior Orbital gyrus, sulcus−2036−2213313.330.14
    L. inferior frontal gyrus−60122212916.330.12
    L. superior frontal gyrus, paracingulate0304212014.050.13
    L. angular gyrus−50−704210613.290.16
    L. cerebellum (anterior lobe)−10−84−2410514.400.13
    Cerebellum (posterior lobe, vermis)4−58−2210017.580.09
    L. superior temporal gyrus−68−28149014.480.18
    L. paracentral lobule−2−24588314.280.10
    L. superior frontal gyrus, accessory superior frontal sulcus−2232568014.660.12
    L. cerebellum (anterior lobule)−10−36−167513.130.11
    R. cerebellum (anterior lobule)18−28−286913.480.11
    Cerebellum (central lobule)−4−44−86120.100.09
    L. striate cortex−2−102126013.410.19
    L. supramarginal gyrus/superior parietal lobule−34−44385718.340.08
    L. middle temporal gyrus, superior temporal sulcus−58−3804613.770.08
    R. paracentral lobule4−28584014.260.10
    L. precentral gyrus−10−30663927.560.08
    L. lateral caudate−18−6263821.480.18

    Loss > no loss

    ES = [(positive + neutral)Loss–(positive + neutral)No Loss]

    No clusters found.
    • The following clusters survived multiple-comparison correction in univariate voxel-wise analysis at the outcome phase [peak MNI coordinates, cluster size (k), F(1,34) values, and unstandardized effect size in terms of % signal change (ES)].

    • View popup
    Table 4.

    Conjunction of main effects of Emotion and Loss

    ClusterxyzkBF01
    vmPFC226−281,8954.39
    R. lateral occipital cortex30−92−147641.23
    R. cerebellum (lateral zone)18−76−465623.05
    R. amygdala32−4−224863.87
    L. lateral occipital cortex−32−96−144511.70
    L. amygdala−26−4−202413.51
    L. posterior Cingulate cortex−8−54202122.21
    R. lateral Orbitofrontal cortex3036−201693.90
    Midcingulate cortex−26261412.32
    R. inferior temporal gyrus/fusiform gyrus46−50−201232.83
    Cerebellum (posterior lateral fissure)−10−46−481201.66
    L. lateral Orbitofrontal cortex−2028−181202.36
    R. caudate/ventral Striatum68−101131.53
    Inferior thalamic peduncle6−42941.28
    L. intermediate Frontal sulcus−52364831.28
    L. caudate/ventral Striatum−44−8801.08
    L. inferior frontal gyrus−52620693.94
    Cerebellum (vermis)0−60−32604.09
    L. cerebellum (lateral zone)−30−74−42532.44
    L. cerebellum (intermediate zone)−6−80−49522.11
    R. posterior cingulate cortex8−5218492.04
    L. inferior precentral sulcus−42436491.33
    R. middle temporal gyrus62−2−24404.30
    L. supramarginal gyrus−34−4434392.32
    • The following clusters survived the multiple-comparison correction in univariate voxel-wise conjunction analysis at the outcome phase [MNI coordinates, cluster size (k), inverse Bayes factors (BF01) values indicating the evidence in favor of null interaction effects].

    • View popup
    Table 5.

    Relationship between Emotion and Loss effects

    Brain regionxyzkr(33)p valueBF01
    vmPFC040−12110−0.0880.6144.21
    R. amygdala324−221750.0280.8754.69
    L. amygdala−26−4−201180.0880.6134.21
    R. caudate/ventral striatum6−8−8690.1530.3794.12
    L. caudate/ventral striatum−6−6−8520.1680.3363.72
    • Correlation between emotion and loss main effects in clusters of our primary ROIs (MNI coordinates, cluster size (k), Pearson's correlation (r) and the corresponding p value, inverse Bayes factors (BF01) values indicating the evidence in favor of null correlation effects).

    • View popup
    Table 6.

    Subjective ratings

    Outcome conditionMean ± SD
    Please rate how you felt when the NO-LOSS information was signaled by a POSITIVE image7.85 ± 1.33
    Please rate how you felt when the LOSS information was signaled by a POSITIVE image4.41 ± 2.14
    Please rate how you felt when the NO-LOSS information was signaled by a NEUTRAL image6.63 ± 1.86
    Please rate how you felt when the LOSS information was signaled by a NEUTRAL image3.89 ± 2.05
    • Average self-reported pleasantness ratings for the four outcome conditions on a scale of 1–9 (1 being unpleasant and 9 being pleasant), collected at the end of each phase.

    • View popup
    Table 7.

    Behavioral choice measures separately for two phases

    ConditionsPhase 1Phase 2
    Mean ± SD (%)t(34)p valueMean ± SD (%)t(34)p value
    Chair choices49.29 ± 13.69−0.310.7642.62 ± 14.27−2.060.004
    Plane choices49.37 ± 13.83−0.270.7955.99 ± 14.592.430.021
    Chair choices that led to Loss outcome51.03 ± 5.261.150.2653.28 ± 10.211.900.07
    Plane choices that led to Loss outcome48.86 ± 5.59−1.200.2448.51 ± 6.69−1.310.19
    • In Phase 1, positive stimulus signaled a loss outcome and neutral stimulus signaled a no-loss outcome. In Phase 2, neutral stimulus signaled a loss outcome, and positive stimulus signaled a no-loss outcome. The t(34) and corresponding p values are based on a one-sample t test against the chance value (50%).

    • View popup
    Table 8.

    Average estimated learning rates (α) for the different stimulus types, chair and plane and deemed high and low inherent value stimuli for the two phases separately

    StimulusPhase 1Phase 2
    Mean ± SD (%)t(34)p valueMean ± SD (%)t(34)p value
    Chair0.101 ± 0.1823.2640.0030.156 ± 0.2683.4660.002
    Plane0.199 ± 0.2514.692<0.0010.214 ± 0.2844.463<0.001
    High value0.139 ± 0.2014.382<0.0010.216 ± 0.2964.384<0.001
    Low value0.161 ± 0.2463.628<0.0010.154 ± 0.2553.518<0.001
    • In Phase 1, positive stimulus signaled a loss outcome and neutral stimulus signaled a no-loss outcome. In Phase 2, neutral stimulus signaled a loss outcome, and positive stimulus signaled a no-loss outcome. The t(34) and corresponding p values are based on a one-sample t test against zero.

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Additive Effects of Monetary Loss and Positive Emotion in the Human Brain
Sagarika Jaiswal, Lakshman N.C. Chakravarthula, Srikanth Padmala
eNeuro 2 April 2024, 11 (4) ENEURO.0374-23.2024; DOI: 10.1523/ENEURO.0374-23.2024

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Additive Effects of Monetary Loss and Positive Emotion in the Human Brain
Sagarika Jaiswal, Lakshman N.C. Chakravarthula, Srikanth Padmala
eNeuro 2 April 2024, 11 (4) ENEURO.0374-23.2024; DOI: 10.1523/ENEURO.0374-23.2024
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Keywords

  • additive integration
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  • monetary losses
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