Neural mechanisms underlying contextual dependency of subjective values: converging evidence from monkeys and humans

Abstract

A major challenge for decision theory is to account for the instability of expressed preferences across time and context. Such variability could arise from specific properties of the brain system used to assign subjective values. Growing evidence has identified the ventromedial prefrontal cortex (VMPFC) as a key node of the human brain valuation system. Here, we first replicate this observation with an fMRI study in humans showing that subjective values of painting pictures, as expressed in explicit pleasantness ratings, are specifically encoded in the VMPFC. We then establish a bridge with monkey electrophysiology, by comparing single-unit activity evoked by visual cues between the VMPFC and the orbitofrontal cortex. At the neural population level, expected reward magnitude was only encoded in the VMPFC, which also reflected subjective cue values, as expressed in Pavlovian appetitive responses. In addition, we demonstrate in both species that the additive effect of prestimulus activity on evoked activity has a significant impact on subjective values. In monkeys, the factor dominating prestimulus VMPFC activity was trial number, which likely indexed variations in internal dispositions related to fatigue or satiety. In humans, prestimulus VMPFC activity was externally manipulated through changes in the musical context, which induced a systematic bias in subjective values. Thus, the apparent stochasticity of preferences might relate to the VMPFC automatically aggregating the values of contextual features, which would bias subsequent valuation because of temporal autocorrelation in neural activity.

Keywords: decision making; electrophysiology; fMRI; neuroeconomics; reward; ventromedial prefrontal cortex.

Figure 1.

Graphical explanation of how contextual factor impacts subjective value. As usually assumed, a change of stimulus (stim B in black vs stim A in blue) modulates the magnitude of the VMPFC evoked response and, therefore, the subjective value assigned to the stimulus. The original hypothesis is that a difference in context (context 2 in blue vs context 1 in red) induces a shift in VMPFC baseline activity (Pre-stim), which would persist into poststimulus activity. This would impact the subjective value given to a same stimulus A because subjective value is encoded in the absolute peak of the evoked response, and not in the differential from baseline.

Figure 2.

Behavioral tasks and models. Tasks are illustrated with the successive screenshots displayed during a given trial. The links in the models below represent significant linear dependency. a, Once the monkey touched the bar, one of three visual cues (checkerboards) appeared, indicating reward size. Then a go signal appeared on screen (image not shown), and the monkey released the bar and received the reward accompanied by a visual feedback (blue square). b, After a long interval accompanied by a random musical context, a new painting was displayed on screen. Then subjects moved a cursor on an analog scale to indicate how much they liked the painting (regardless of musical context).

Figure 3.

Behavioral expression of subjective value. a, Proportion of accepted trials (full lines, left axis) and lipping index (dashed lines, right axis) as a function of reward level. Error bars indicate intertrial SEM. b, Lipping index as a function of trial number. Trial number was z-scored, ranked over all recording sessions and binned into data points representing 773 trials each. Straight line indicates linear regression fit. c, Probability of choosing painting A over painting B as a function of the differential between their in-scanner ratings (all choices pooled). Dots indicate 20 choices per subject, ranked according to pleasantness rating difference. Error bars indicate intersubject SEM. Sigmoid line indicates logistic regression fit. d, Correlation between painting and music pleasantness. Dots indicate 10 trials per subject, ranked according to music rating.

Figure 4.

Encoding of value-related factors in the VMPFC. a, Localization of recorded neurons (red represents VMPFC; blue represents OFC) in Monkey 1 (left) and Monkey 2 (right). Numbers indicate the distance in millimeters from the interaural line in the rostrocaudal axis. b, Evolution of prestimulus activity (number of spikes in the last 500 ms before cue onset) as trial number increases. Dots indicates 773 trials, ranked according to z-scored trial number. Error bars indicate intertrial SEM. c, Encoding of reward level over time around cue onset. At each time point, graph represents the average number of spikes over the last 500 ms. Solid and dashed lines indicate cue onset and reward delivery, respectively. d, Correlation between lipping index and poststimulus activity (number of spikes in the first 500 ms after cue onset). Dots indicate 773 trials, ranked according to lipping index. Error bars indicate intertrial SEM. e, Encoding of pleasantness rating in the VMPFC. x, y, z coordinates of the maxima refer to the MNI space. Color scales on the right indicate t values. A voxelwise threshold of p < 0.005 was used for displaying purposes. Top, Sagittal glass brain. Bottom, Frontal slice. Left, Correlation with music pleasantness over the duration of music display. Middle, Correlation with painting pleasantness 4 s after painting onset. Right, Conjunction between painting and music pleasantness. f, Correlation of painting pleasantness with poststimulus activity in independently defined ROI for VMPFC. Dots indicate 10 trials per subject, ranked according to painting rating. Error bars indicate intersubject SEM.

Figure 5.

Value encoding in individual neurons or voxels from medial to lateral prefrontal cortex. Top, Graphs represent, for individual neurons (red represents VMPFC; blue represents OFC), the regression coefficients obtained for encoding trial number in prestimulus activity (a), reward level in poststimulus activity (b), and the correlation between the two (c). **p < 0.01, when the distribution of regression coefficients is significantly shifted away from zero. All recorded neurons are shown according to their x-coordinate (distance along a line orthogonal to the medial wall). Bottom, Graphs represent, for individual voxels (red represents ROI showing significant effect at the group level; blue represents not significant), the regression coefficients (averaged across subjects) obtained for encoding music pleasantness in prestimulus activity (d), painting pleasantness in poststimulus activity (e), and the correlation between the two (f). Voxels were selected by moving the VMPFC ROI along a line orthogonal to the medial wall. For any given distance of x to the medial wall, we represent all voxels of coordinate x = x in an 8-mm-diameter sphere centered on x = x, y = 44, and z = −10 in the MNI space. Trend lines show robust regression fit across VMPFC neurons or voxels. Light red area represents 95% confidence interval of regression estimates.

Figure 6.

Time course of value encoding in the VMPFC. a, Time course of peristimulus electrophysiological signal (number of spikes over the last 500 ms) in the VMPFC, shown separately for slow and fast lipping trials. Solid and dashed lines indicate cue onset and reward delivery, respectively. b, Correlation between prestimulus activity (spikes in the last 500 ms before cue onset) and lipping index. Dots indicate 773 trials, ranked according to lipping index. Error bars indicate intertrial SEM. c, Time course of peristimulus fMRI activity in the VMPFC ROI, shown separately for high and low rating trials. Black vertical line indicates painting onset. d, Correlation between painting ratings and regression coefficients (betas) extracted in the ROI at painting onset. Dots indicate 10 trials, ranked according to painting rating and averaged across subjects. Error bars indicate intersubject SEM.