Dissociable Effects of Subtotal Lesions within the Macaque Orbital Prefrontal Cortex on Reward-Guided Behavior

Abstract

The macaque orbital prefrontal cortex (PFo) has been implicated in a wide range of reward-guided behaviors essential for efficient foraging. The PFo, however, is not a homogeneous structure. Two major subregions, distinct by their cytoarchitecture and connections to other brain structures, compose the PFo. One subregion encompasses Walker's areas 11 and 13 and the other centers on Walker's area 14. Although it has been suggested that these subregions play dissociable roles in reward-guided behavior, direct neuropsychological evidence for this hypothesis is limited. To explore the independent contributions of PFo subregions to behavior, we studied rhesus monkeys (Macaca mulatta) with restricted excitotoxic lesions targeting either Walker's areas 11/13 or area 14. The performance of these two groups was compared to that of a group of unoperated controls on a series of reward-based tasks that has been shown to be sensitive to lesions of the PFo as a whole (Walker's areas 11, 13, and 14). Lesions of areas 11/13, but not area 14, disrupted the rapid updating of object value during selective satiation. In contrast, lesions targeting area 14, but not areas 11/13, impaired the ability of monkeys to learn to stop responding to a previously rewarded object. Somewhat surprisingly, neither lesion disrupted performance on a serial object reversal learning task, although aspiration lesions of the entire PFo produce severe deficits on this task. Our data indicate that anatomically defined subregions within macaque PFo make dissociable contributions to reward-guided behavior.