Abstract
Lesion studies in macaques suggest dissociable functions of the orbitofrontal cortex (OFC) and medial frontal cortex (MFC), with OFC being essential for goal-directed decision making and MFC supporting social cognition. Bilateral amygdala damage results in impairments in both of these domains. There are extensive reciprocal connections between these prefrontal areas and the amygdala; however, it is not known whether the dissociable roles of OFC and MFC depend on functional interactions with the amygdala. To test this possibility, we compared the performance of male rhesus macaques (Macaca mulatta) with crossed surgical disconnection of the amygdala and either MFC (MFC x AMY, n=4) or OFC (OFC x AMY, n=4) to a group of unoperated controls (CON, n=5). All monkeys were assessed for their performance on two tasks to measure: (1) food-retrieval latencies while viewing videos of social and nonsocial stimuli in a test of social interest, and (2) object choices based on current food value using reinforcer devaluation in a test of goal-directed decision making. Compared to the CON group, the MFC x AMY group, but not the OFC x AMY group, showed significantly reduced food-retrieval latencies while viewing videos of conspecifics, indicating reduced social valuation and/or interest. By contrast, on the devaluation task, group OFC x AMY, but not group MFC x AMY, displayed deficits on object choices following changes in food value. These data indicate that the MFC and OFC must functionally interact with the amygdala to support normative social and nonsocial valuation, respectively.
Significance Statement
Ascribing value to conspecifics (social) vs. objects (nonsocial) may be supported by distinct but overlapping brain networks. Here we test whether two nonoverlapping regions of the prefrontal cortex, the medial frontal cortex and the orbitofrontal cortex, must causally interact with the amygdala to sustain social valuation and goal-directed decision making, respectively. We found that these prefrontal-amygdala circuits are functionally dissociable, lending support for the idea that medial frontal and orbital frontal cortex make independent contributions to cognitive appraisals of the environment. These data provide a neural framework for distinct value assignment processes and may enhance our understanding of the cognitive deficits observed following brain injury or in the development of mental health disorders.
Footnotes
The authors declare no competing financial interests.
This work was supported by the Intramural Research Program of the National Institute of Mental Health (EAM, ZIAMH002887). MSP was supported by a National Institutes of Health Center for Compulsive Behavior Postdoctoral Fellowship. We thank Dawn Lundgren, Emily Moylan, and Emily Fiuzat for assistance with data collection; Richard Saunders and Emily Moylan for help performing surgery; and Ben Jung, Jakob Seidlitz, and Adam Messinger for assistance with the lesion assessments. We also thank the staff of the Nuclear Magnetic Resonance Facility, National Institute of Neurological Disorders and Stroke, and the Laboratory of Diagnostic and Radiology Research. Current author affiliations: MSP (Sarah Lawrence College, 1 Mead Way, Bronxville, NY 10708); NKC (Temple University, 1701 N Broad St, Philadelphia, PA 19122); SEVR (Division of Program Coordination, Planning, and Strategic Initiatives, National Institutes of Health, Bethesda, MD 20892).
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