Behavioral consequences of selective damage to frontal pole and posterior cingulate cortices.

Frontal pole cortex (FPC) and posterior cingulate cortex (PCC) have close neuroanatomical connections, and imaging studies have shown coactivation or codeactivation of these brain regions during performance of certain tasks. However, they are among the least well-understood regions of the primate brain. One reason for this is that the consequences of selective bilateral lesions to either structure have not previously been studied in any primate species. We studied the effects of circumscribed bilateral lesions to FPC or PCC on monkeys' ability to perform an analog of Wisconsin Card Sorting Test (WCST) and related tasks. In contrast to lesions in other prefrontal regions, neither posttraining FPC nor PCC lesions impaired animals' abilities to follow the rule switches that frequently occurred within the WCST task. However, FPC lesions were not without effect, because they augmented the ability of animals to adjust cognitive control after experiencing high levels of conflict (whereas PCC lesions did not have any effect). In addition, FPC-lesioned monkeys were more successful than controls or PCC-lesioned animals at remembering the relevant rule across experimentally imposed distractions involving either an intervening secondary task or a surprising delivery of free reward. Although prefrontal cortex posterior to FPC is specialized for mediating efficient goal-directed behavior to maximally exploit reward opportunities from ongoing tasks, our data led us to suggest that FPC is, instead, specialized for disengaging executive control from the current task and redistributing it to novel sources of reward to explore new opportunities/goals.

Dissociable components of rule-guided behavior depend on distinct medial and prefrontal regions.

Much of our behavior is guided by rules. Although human prefrontal cortex (PFC) and anterior cingulate cortex (ACC) are implicated in implementing rule-guided behavior, the crucial contributions made by different regions within these areas are not yet specified. In an attempt to bridge human neuropsychology and nonhuman primate neurophysiology, we report the effects of circumscribed lesions to macaque orbitofrontal cortex (OFC), principal sulcus (PS), superior dorsolateral PFC, ventrolateral PFC, or ACC sulcus, on separable cognitive components of a Wisconsin Card Sorting Test (WCST) analog. Only the PS lesions impaired maintenance of abstract rules in working memory; only the OFC lesions impaired rapid reward-based updating of representations of rule value; the ACC sulcus lesions impaired active reference to the value of recent choice-outcomes during rule-based decision-making.