The behavioural adjustment that follows the experience of conflict has been extensively studied in humans, leading to influential models of executive-control adjustment. Recent studies have revealed striking similarities in conflict-induced behavioural adjustment between humans and monkeys, indicating that monkeys can provide a model to study the underlying neural substrates and mechanisms of such behaviour. These studies have advanced our knowledge about the role of different prefrontal brain regions, including the anterior cingulate cortex (ACC) and the dorsolateral prefrontal cortex (DLPFC), in executive-control adjustment and suggest a pivotal role for the DLPFC in the dynamic tuning of executive control and, consequently, in behavioural adaptation to changing environments.

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.

Our cognitive abilities in performing tasks are influenced by experienced competition/conflict between behavioral choices. To determine the role of the anterior cingulate cortex (ACC) and dorsolateral prefrontal cortex (DLPFC) in the conflict detection-resolution process, we conducted complementary lesion and single-cell recording studies in monkeys that were resolving a conflict between two rules. We observed conflict-induced behavioral adjustment that persisted after lesions within the ACC but disappeared after lesions within the DLPFC. In the DLPFC, activity was modulated in some cells by the current conflict level and in other cells by the conflict experienced in the previous trial. These results show that the DLPFC, but not the ACC, is essential for the conflict-induced behavioral adjustment and suggest that encoding and maintenance of information about experienced conflict is mediated by the DLPFC.

Humans are set apart from other animals by many elements of advanced cognition and behaviour, including language, judgement and reasoning. What is special about the human brain that gives rise to these abilities? Could the foremost part of the prefrontal cortex (the frontopolar cortex), which has become considerably enlarged in humans during evolution compared with other animals, be important in this regard, especially as, in primates, it contains a unique cytoarchitectural field, area 10? The first studies of the function of the frontopolar cortex in monkeys have now provided critical new insights about its precise role in monitoring the significance of current and alternative goals. In human evolution, the frontopolar cortex may have acquired a further role in enabling the monitoring of the significance of multiple goals in parallel, as well as switching between them. Here, we argue that many other forms of uniquely human behaviour may benefit from this cognitive ability mediated by the frontopolar cortex.

The cognitive flexibility to select appropriate rules in a changing environment is essential for survival and is assumed to depend on the integrity of prefrontal cortex (PFC). To explore the contribution of the dorsolateral PFC to flexible rule-based behavior, we recorded the activity of cells in this region of monkeys performing a Wisconsin Card Sorting Test (WCST) analog. The monkey had to match a sample to one of three test items by either color or shape. Liquid reward and a discrete visual signal (error signal) were given as feedback to correct and incorrect target selections, respectively. The relevant rule and its frequent changes were not cued, and the monkeys could find it only by interpreting the feedback. In one-third of cells, cellular activity was modulated by the relevant rule, both throughout the trial and between trials. The magnitude of the modulation correlated with the number of errors that the monkeys committed after each rule change in the course of reestablishing high performance. Activity of other cells differed between correct and error trials independently from the rule-related modulation. This difference appeared during actual responses and before the monkeys faced the problems. Many PFC cells responded to the error-signal presentation, and, in some of them, the magnitude of response depended on the relevant rule. These results suggest that the dorsolateral PFC contributes to WCST performance by maintaining the relevant rule across trials, assessing behavioral outcomes, and monitoring the processes that could lead to success and failure in individual trials.

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. frontal pole cortex | posterior cingulate cortex | executive control

Fifteen years ago, an influential model proposed that the human dorsal anterior cingulate cortex (dACC) detects conflict and induces adaptive control of behavior. Over the years support for this model has been mixed, in particular due to divergent findings in human versus nonhuman primates. We here review recent findings that suggest greater commonalities across species. These include equivalent behavioral consequences of conflict and similar neuronal signals in the dACC, but also a common failure of dACC lesions to reliably abolish conflict-driven behavior. We conclude that conflict might be one among many drivers of adjustments in executive control and that the ACC might be just one component of overlapping distributed systems involved in context-dependent learning and behavioral control.

Imaging and neural activity recording studies have shown activation in the primate prefrontal cortex when shifting attention between visual dimensions is necessary to achieve goals. A fundamental unanswered question is whether representations of these dimensions emerge from top-down attentional processes mediated by prefrontal regions or from bottom-up processes within visual cortical regions. We hypothesized a causative link between prefrontal cortical regions and dimension-based behavior. In large cohorts of humans and macaque monkeys, performing the same attention shifting task, we found that both species successfully shifted between visual dimensions, but both species also showed a significant behavioral advantage/bias to a particular dimension; however, these biases were in opposite directions in humans (bias to color) versus monkeys (bias to shape). Monkeys’ bias remained after selective bilateral lesions within the anterior cingulate cortex (ACC), frontopolar cortex, dorsolateral prefrontal cortex (DLPFC), orbitofrontal cortex (OFC), or superior, lateral prefrontal cortex. However, lesions within certain regions (ACC, DLPFC, or OFC) impaired monkeys’ ability to shift between these dimensions. We conclude that goal-directed processing of a particular dimension for the executive control of behavior depends on the integrity of prefrontal cortex; however, representation of competing dimensions and bias toward them does not depend on top-down prefrontal-mediated processes.