Neural Substrates of Reward Processing and Emotion

National Institute Of Mental Health

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Abstract

Lesion studies suggest dissociable functions of medial prefrontal cortex (MFC) and orbitofrontal cortex (OFC), with MFC being essential for social cognition and OFC being essential for value-based decision making. Although bilateral amygdala damage also results in impairments in these domains, it is not known whether the dissociable functional roles of MFC and OFC critically depend on interactions with the amygdala. To test this possibility, we compared the performance of animals with crossed surgical disconnection of the prelimbic cortex, a subregion of MFC, and amygdala (MFC x AMY) and animals with surgical disconnection of the OFC and amygdala (OFC x AMY), to a group of controls (CON). All animals were assessed for food-retrieval latency while viewing videos of social stimuli (a test of social interest) and object choices based on current food value (devaluation task, a test of value-based decision making). Compared to the CON group, group MFC x AMY, but not group OFC x AMY, showed significantly reduced latencies to reach for a reward in the presence of videos of conspecifics, indicating reduced social valuation and/or reduced social interest. In a test of value-based decision making, however, the opposite pattern was observed; group OFC x AMY, but not group MFC x AMY, displayed severe deficits on object choice following selective satiation. These data indicate that MFC and OFC interact with the amygdala to subserve distinct behavioral contributions in the domains of social valuation and object valuation, respectively. That these prefrontal-amygdala circuits are functionally dissociable lends support to the idea that MFC and OFC make independent contributions to cognitive appraisals of the environment. As indicated above, the MFC, together with the amygdala and cortex near the temporal-parietal junction is implicated in social cognition. This network of brain regions is specialized for processing social information. For example, neurons in the MFC encode not only reward value but also features of conspecifics and of oneself. Our previous research has demonstrated that MFC damage blunts learning of prosocial preferences. It has been difficult, however, to disentangle MFC contributions to social attention, social preference, and social reward, as measured by vicarious reinforcement (i.e., the willingness to give reward to others). To further investigate the role of the MFC in social cognition, we measured the influence of MFC damage on animals preferences for viewing images with social (conspecific faces) or nonsocial (inanimate objects) content. Both intact animals and those with MFC damage were allowed to choose between two neutral antecedent stimuli: one predicting the onset of a social image and the other predicting the onset of a nonsocial image. All animals exhibited a slight but statistically significant preference for choosing the antecedent that predicted social images. MFC damage did not reduce preferences for viewing social images; however, animals with MFC lesions tended to make more looks at the antecedent stimuli before making a choice compared to controls. These findings suggest that animals with MFC damage experience greater difficulty than controls evaluating deliberate actions associated with social outcomes but have no difficulty assessing the inherent value of social stimuli per se.