Dissociating the role of the orbitofrontal cortex and the striatum in the computation of goal values and prediction errors

Abstract

To make sound economic decisions, the brain needs to compute several different value-related signals. These include goal values that measure the predicted reward that results from the outcome generated by each of the actions under consideration, decision values that measure the net value of taking the different actions, and prediction errors that measure deviations from individuals' previous reward expectations. We used functional magnetic resonance imaging and a novel decision-making paradigm to dissociate the neural basis of these three computations. Our results show that they are supported by different neural substrates: goal values are correlated with activity in the medial orbitofrontal cortex, decision values are correlated with activity in the central orbitofrontal cortex, and prediction errors are correlated with activity in the ventral striatum.

Figure 1.

Task design. a, Subjects were presented with a high-resolution image of a food item or a yellow square with a price shown above and an action independent gain/loss shown below. Positive values indicated a gain and negative values indicated a cost or loss. Subjects indicated with a button press whether or not they would pay the price above the image for the right to eat the food item shown and the end of the experiment. The gain/loss below the image occurred regardless of the subject's choice. b, Trials including only food items, only price, and only gain where included to help separate the values for GV, DV, and PE. Trial order, food items, price, and gain were randomized within subjects. c, Percentage of “yes” responses as a function of decision value. The y-axis represents the percentage of trials on which subjects responded “yes” to purchase the food item shown. The x-axis represents the decision value of the trial. Decision value was calculated as the amount the subject bid for the food item minus the cost for that food item in the current trial. Error bars represent SEM.

Figure 2.

Regions associated with goal value, decision value, and prediction error. For time courses in a–c, high values are shown with circular markers connected by solid lines. Low values are marked by triangles connected by dotted lines. Markers represent the mean β value from a finite impulse response model at each time point. Error bars represent the SEM. Asterisks indicate points in time where there is a significant difference between high and low based on paired t tests at p < 0.05. Activation maps in d, e, and f are shown at a threshold of p < 0.005 uncorrected and an extent threshold of 10 voxels. Voxels in red are significant at p < 0.005 uncorrected, whereas voxels in yellow remain significant at p < 0.0001 uncorrected. d, Activity in the OFC and anterior cingulate cortex correlated with goal value. e, Activity in the central OFC correlated with decision value. f, Activity in the ventral striatum correlated with prediction error. g–o, Bar graphs represent the mean β value ± SE at high (HH), medium high (MH), medium low (ML), and low (LL) levels of GV, DV, and PE. The p values displayed in the bar graphs were determined based on paired t tests between high and low trials. Bars in black show the value that best fits each region.

Figure 3.

Fit of each value computation to activity in medial OFC, central OFC, and ventral striatum. The y-axis shows the mean β for GV, DV, and PE. The error bars represent the 95% confidence interval of the mean. The different value computations (GV, DV, PE) are shown on the x-axis. Dark gray bars highlight value computations for which the fit to activity is greater than zero. The effects of GV, DV, and PE were compared in each region using Wilcoxon signed rank tests and those results are represented by the p values on each graph.

Figure 4.

Fit for GV, DV, and PE to activity in the ventral striatum. The β values in this figure come from a secondary fMRI analysis model where PE was entered as the first parametric regressor for response giving it the maximum explanatory power. The y-axis shows the mean β for GV, DV, and PE. The error bars represent the 95% confidence interval of the mean. The different value computations (GV, DV, PE) are shown on the x-axis. Dark gray bars highlight value computations for which the fit to activity is greater than zero. The effects of GV, DV, and PE were compared using paired t tests and those results are represented by the p values on the graph.

Figure 5.

Comparison of the fits for GV, DV, and PE in mOFC, cOFC, and VS The y-axis shows the mean β for value specified in the graph title. The error bars represent the 95% confidence interval of the mean. The regions of interest (mOFC, cOFC, and VS) are shown on the x-axis. Dark gray bars highlight regions where the fit to activity is greater than zero. The effects fits were compared between regions using Wilcoxon signed rank tests and those results are represented by the p values on each graph.

Figure 6.

Selectivity of medial OFC, central OFC, and ventral striatum to bid, price, and random gain. Bar graphs represent the mean β value ± SE on the y-axis and high (HH), medium high (MH), medium low (ML), and low (LL) levels of bid, price or random gain on the x-axis. Positive prices represented compensations to the subject whereas negative prices represented subtractions from the subject's endowment. a–c, Activity in medial OFC for the different levels of bid, price, and gain. d–f, Activity in central OFC for the different levels of bid, price, and gain. g–i, Activity in ventral striatum for the different levels of bid, price, and gain. The p values displayed in the bar graphs were determined based on paired t tests between high and low trials. Bars in black show values with a significant effect.

Figure 7.

Combined activation maps for GV, DV, and PE. Activation maps are shown at an uncorrected threshold of p < 0.001. Activity correlated with GVs in the mOFC is shown in red, activity correlated with DVs in the cOFC is shown in yellow, and activity correlated with PEs in the ventral striatum is shown in green.