Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices

Abstract

The precise role of orbitofrontal cortex (OFC) in affective processing is still debated. One view suggests OFC represents stimulus reward value and supports learning and relearning of stimulus-reward associations. An alternate view implicates OFC in behavioral control after rewarding or punishing feedback. To discriminate between these possibilities, we used event-related functional magnetic resonance imaging in subjects performing a reversal task in which, on each trial, selection of the correct stimulus led to a 70% probability of receiving a monetary reward and a 30% probability of obtaining a monetary punishment. The incorrect stimulus had the reverse contingency. In one condition (choice), subjects had to choose which stimulus to select and switch their response to the other stimulus once contingencies had changed. In another condition (imperative), subjects had simply to track the currently rewarded stimulus. In some regions of OFC and medial prefrontal cortex, activity was related to valence of outcome, whereas in adjacent areas activity was associated with behavioral choice, signaling maintenance of the current response strategy on a subsequent trial. Caudolateral OFC-anterior insula was activated by punishing feedback preceding a switch in stimulus in both the choice and imperative conditions, indicating a possible role for this region in signaling a change in reward contingencies. These results suggest functional heterogeneity within the OFC, with a role for this region in representing stimulus-reward values, signaling changes in reinforcement contingencies and in behavioral control.

Figure 1.

Illustration of task display for choice and imperative reversal task. Subjects were presented with two abstract visual stimuli. At the beginning, one stimulus was designated the correct stimulus and the other the incorrect stimulus. In the choice task, subjects selected a stimulus, which then increased in brightness and was followed by a monetary outcome (winning or losing 10 or 20 pence). In the imperative task, subjects did not select the stimulus, but instead this selection was made by computer. Subjects had to respond to indicate which of the two stimuli had been selected and then received rewarding and punishing feedback.

Figure 2.

Areas of ventral PFC showing reward-related responses in the choice task. A, Group random effects results are shown superimposed on coronal and sagittal slices from the subject-averaged structural MRI image [at the Montreal Neurological Institute (MNI) coordinates indicated in the top right corner of each image]. Significant effects are shown at p < 0.001 in yellow, and to show the full extent of the activations, at p < 0.01 in red. A plot of effect sizes from medial PFC (the area circled) is shown for each trial type (reward, pun_noswch and pun_swch). B, Results from the same contrast are shown for a subset of single subjects superimposed on each subject's individual structural MRI. The threshold is set at p < 0.01 for illustration.

Figure 3.

Areas activated in conjunction of reward-pun_noswch contrast between the choice and imperative tasks. Group random effects results are shown superimposed on coronal slices at the MNI coordinates indicated (top right corner of each image). Significant effects are shown at p < 0.001 in yellow and at p < 0.01 in red (to show the full extent of the activations). mPFC, Medial PFC; mOFC, medial OFC; lOFC, lateral OFC; nACC, nucleus accumbens; Amyg, amygdaloid area.

Figure 4.

Areas related to response maintenance in the choice task. A, Group random effects results are shown superimposed on coronal and sagittal slices from the subject-averaged structural MRI image (at the MNI coordinates indicated in the top right corner of each image). Significant effects are shown at p < 0.001 in yellow and at p < 0.01 in red (to show the full extent of the activations). A plot of effect sizes from medial OFC (the area circled) is shown for each trial type (reward, pun_noswch, and pun_swch). B, Results from the same contrast are shown for a subset of single subjects superimposed on each subject's individual structural MRI. The threshold is set at p < 0.01 for illustration. C, Plots of fitted event-related responses obtained from peak voxels in medial OFC of each single subject shown in B.

Figure 5.

Valence (reward-punishment) and response maintenance-related effects in the choice task. Activations related to rewarding outcomes and response maintenance are shown superimposed on the same coronal and sagittal slices. Reward-related effects are shown in red (at p < 0.01) and yellow (at p < 0.001), and response maintenance-related effects are shown in blue (at p < 0.01) and cyan (at p < 0.001).

Figure 6.

Areas related to response switching in the choice task. A, Group random effects results of the contrast of pun_swch - [rewacq + pun_noswch]/2 are shown superimposed on coronal and sagittal slices from the subject-averaged MRI image (at the MNI coordinates indicated in the top right corner of each image). Significant effects are shown at p < 0.001 in yellow and at p < 0.01 in red (to show the full extent of the activations). A plot of effect sizes from anterior insula/caudolateral OFC (the area circled) is shown for each trial type (reward, pun_noswch, and pun_swch). B, Results from the contrast of pun_swch-pun_noswch at the group random effects level, showing a separate locus of activity in caudolateral OFC. C, Results from the contrast pun_swch - [rewacq + punacq]/2 are shown for a subset of single subjects superimposed on each subject's individual structural MRI. The threshold is set at p < 0.01 for illustration.

Figure 7.

Response switching or contingency change detection? Effects of a conjunction of the contrast of pun_swch - [rewacq + punacq]/2 between the choice and imperative tasks is shown superimposed on a coronal slice from the subject averaged MRI image (at the MNI coordinate shown top right). This result illustrates that anterior insula/caudolateral OFC is recruited during both the choice and imperative tasks, suggesting that this area may be more related to detection of contingency changes than response inhibition per se. Significant effects are shown at p < 0.001 in yellow and at p < 0.01 in red (to show the full extent of the activations).