The architecture of reward value coding in the human orbitofrontal cortex

Abstract

To ensure their survival, animals exhibit a number of reward-directed behaviors, such as foraging for food or searching for mates. This suggests that a core set of brain regions may be shared by many species to process different types of rewards. Conversely, many new brain areas have emerged over the course of evolution, suggesting potential specialization of specific brain regions in the processing of more recent rewards such as money. Here, using functional magnetic resonance imaging in humans, we identified the common and distinct brain systems processing the value of erotic stimuli and monetary gains. First, we provide evidence that a set of neural structures, including the ventral striatum, anterior insula, anterior cingulate cortex, and midbrain, encodes the subjective value of rewards regardless of their type, consistent with a general hedonic representation. More importantly, our results reveal reward-specific representations in the orbitofrontal cortex (OFC): whereas the anterior lateral OFC, a phylogenetically recent structure, processes monetary gains, the posterior lateral OFC, phylogenetically and ontogenetically older, processes more basic erotic stimuli. This dissociation between OFC representations of primary and secondary rewards parallels current views on lateral prefrontal cortex organization in cognitive control, suggesting an increasing trend in complexity along a postero-anterior axis according to more abstract representations. Together, our results support a modular view of reward value coding in the brain and propose that a unifying principle of postero-anterior organization can be applied to the OFC.

Figure 1.

Paradigm and behavior. A, Sequence of events during a typical trial. Subjects first saw a cue informing them about the type, probability, and intensity of an upcoming reward (supplemental Fig. 1, available at www.jneurosci.org as supplemental material). Three cases are represented here: a 75% chance of receiving a high amount of money (top), a 25% chance of seeing a low erotic content picture (middle), and a sure chance of getting nothing (control trials; bottom). After a short delay and a target discrimination task, subjects saw the outcome, which was contingent on both the announced probability and their performance on the discrimination task. Reward outcomes consisted either in a monetary amount displayed on a safe (top) or an erotic picture (middle) and were followed by the rating of their subjective value on a continuous scale. Non-rewarded and control trials displayed a scrambled picture at outcome (bottom). B, Behavioral results on the discrimination task: mean reaction times according to reward intensity (left) and probability (middle) and mean hit rates according to reward intensity (right). C, Mean subjective ratings according to reward intensity, on a 1-to-9 scale. Error bars indicate SEM. *p < 0.05; **p < 0.01; ***p < 0.001 by Tukey's HSD tests.

Figure 2.

Functional postero-anterior dissociation in the orbitofrontal cortex depending on reward type. Brain regions responding specifically to monetary reward outcomes are displayed in blue–green, and those responding specifically to erotic reward outcomes are displayed in red–yellow. Plots of mean percent signal change, which are not independent of the whole-brain analysis, are shown only to illustrate the double dissociation between monetary/erotic rewards and anterior (Ant.)/posterior (Post.) OFC. Activations are overlaid on an average anatomical scan of all subjects (p < 0.05 FWE whole-brain corrected). Error bars indicate SEM.

Figure 3.

Specific response of amygdala to erotic rewards. Activations are overlaid on an average anatomical scan of all subjects (p < 0.05 FWE whole-brain corrected). Left and right plots of mean percent signal change, which are not independent of the whole-brain analysis, are shown only to illustrate the specificity of amygdalar response. Error bars indicate SEM.

Figure 4.

Response pattern of the reward-specific brain regions as a function of reward intensity. Percent signal change is plotted in the circled ROIs for monetary and erotic rewards according to the following conditions: high intensity, low intensity, and no reward. In each region, brain activity increases with reward intensity only for the reward for which it is specific. Error bars indicate SEM. The signal is averaged across the right and left hemispheres in each brain region (similar patterns of activity were observed in each hemisphere). Ant., Anterior; Post., posterior.

Figure 5.

Brain regions reflecting hedonic ratings regardless of reward type. Activations show the brain areas in which activity positively correlates with both monetary and erotic ratings (intersection of T-maps thresholded at p < 0.01 FDR whole-brain corrected shown in yellow or thresholded at p < 0.05 FDR whole-brain corrected shown in red). The regions displayed in red were used as an inclusive mask in the analysis of Figure 6. Activations are overlaid on an average anatomical scan of all subjects.

Figure 6.

Common reward brain regions. A, T-map showing the brain regions encoding experienced reward value for both monetary and erotic reward outcomes. Activations are overlaid on an average anatomical scan of all subjects (p < 0.05 FWE whole-brain corrected). B, Percent signal change is plotted in the circled ROIs for monetary and erotic rewards according to the following conditions: high intensity, low intensity, and no reward. Note that these plots are not independent of the whole-brain analysis and are only shown as an illustration for easier visual comparison with Figure 4. Error bars indicate SEM. The signal is averaged across the right and left hemispheres in each brain region (similar patterns of activity were observed in each hemisphere). Ant., Anterior.

Figure 7.

Brain regions reflecting prediction errors regardless of reward type. Activations result from a conjunction analysis showing the brain regions in which activity positively correlates with both monetary and erotic prediction errors (p < 0.001 uncorrected). Activations are overlaid on an average anatomical scan of all subjects.