The role of frontopolar cortex in adjusting the balance between response execution and action inhibition in anthropoids

Executive control of behaviour entails keeping a fine balance between response execution and action inhibition. The most anterior part of the prefrontal cortex (frontopolar cortex) is highly developed in anthropoids; however, no previous study has examined its essential (indispensable) role in regulating the interplay between action execution and inhibition. In this cross-species study, we examine the performance of humans and macaque monkeys in the context of a stop-signal task and then assess the consequence of selective and bilateral damage to frontopolar cortex on monkeys’ behaviour. Humans and monkeys showed significant within-session practice-related adjustments in both response execution (increase in response time (RT) and decrease in response variabilities) and action inhibition (enhanced inhibition). Furthermore, both species expressed context-dependent (post-error and post-stop) behavioral adjustments. In post-lesion testing, frontopolar-damaged monkeys had a longer RT and lower percentage of timeout trials, compared to their pre-lesion performance. The practice-related changes in mean RT and in RT variability were significantly heightened in frontopolar-damaged monkeys. They also showed attenuated post-error, but exaggerated post-stop, behavioural adjustments. Importantly, frontopolar damage had no significant effects on monkeys’ inhibition ability. Our findings indicate that frontopolar cortex plays a critical role in allocation of control to response execution, but not action inhibition. • In both humans and monkeys, practice-related and context-dependent behavioural adjustment occurred within a testing session. • Selective lesions within frontopolar cortex led to a significant increase in response time and timeout errors. • Selective lesions within frontopolar cortex significantly affected the within-session adaptive changes in response execution. • Selective lesions within frontopolar cortex had no significant effect on monkeys’ inhibition ability. • The exploitation drive might dominate in frontopolar-lesioned monkeys and enhance adaptive changes in response execution.