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

Significance Frontal pole cortex (FPC) refers to the most anterior part of prefrontal cortex, a region that is highly developed in anthropoid primates. However, because of technical difficulties in studying this area, its role in primate cognition had remained largely unknown. We studied effects of selective bilateral lesions within FPC on monkeys’ cognitive flexibility. FPC lesion did not impair the performance in well-learned cognitively demanding tasks. However, FPC-lesioned monkeys remained more focused than control monkeys in exploiting the current task when they faced newly introduced interruptions by a simple secondary task or free rewards. This unique pattern of behavioral changes in FPC-lesioned monkeys suggests that FPC is involved in redistribution of cognitive resources from the current task to novel opportunities. 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.