Medial prefrontal cell activity signaling prediction errors of action values.

To adapt behavior to a changing environment, one must monitor outcomes of executed actions and adjust subsequent actions accordingly. Involvement of the medial frontal cortex in performance monitoring has been suggested, but little is known about neural processes that link performance monitoring to performance adjustment. Here, we recorded from neurons in the medial prefrontal cortex of monkeys learning arbitrary action-outcome contingencies. Some cells preferentially responded to positive visual feedback stimuli and others to negative feedback stimuli. The magnitude of responses to positive feedback stimuli decreased over the course of behavioral adaptation, in correlation with decreases in the amount of prediction error of action values. Therefore, these responses in medial prefrontal cells may signal the direction and amount of error in prediction of values of executed actions to specify the adjustment in subsequent action selections. Organisms can survive in a changing environment by adapting their behavior. Behavioral adaptation is composed of two complementary processes: evaluating outcomes of an executed action (performance monitoring) and adjusting the subsequent action (performance adjustment). Through the alternation between performance monitoring and performance adjustment, the behavior adapts to the environmental circumstances 1-3 . The medial frontal cortex (MFC), located around the anterior cingulate sulcus 4 , is thought to be involved in performance monitoring, as the MFC is activated when an executed action is found to be inappropriate. A negative deflection (error-related negativity, ERN) has been repeatedly observed in human electroencephalogram (EEG) studies During behavioral adaptation, the detection of both failure and success is informative. An action that was not successful must be changed, whereas a successful action must be actively maintained. For the MFC to be involved in both the change and active maintenance of action, the representation of both failures and successes is necessary. However, it is controversial whether the MFC is involved in representing successes. Most EEG 5-7 and fMRI studies 9-11 have found that the MFC activity is stronger in response to failures than to successes, thus suggesting that the MFC is mainly involved in error detection. In some other EEG If it is the case that the MFC represents both failures and successes, another important question arises. Does the same group of cells represent the failure and success, or do different groups of cells represent them? The representations of failure and success by separate cells could facilitate determination of whether an action should be maintained or changed. Unless cells representing success are anatomically segregated from cells representing failure, EEG and fMRI measurements cannot address these questions, because cells responding to failures cannot be discriminated from those responding to successes. Instead, single-cell recording must be used to determine this important aspect of failure and success representation in the MFC. It has been proposed 19 that the MFC uses signals of reward prediction errors conveyed by dopamine cells 20 for performance adjustment (also see ref. 21). The magnitude of reward prediction error depends on the expected outcome as well as the actual outcome. In fact, a greater ERN is elicited by unexpected unfavorable outcomes than by expected unfavorable outcomes 22 , and a greater error-related activity is evoked in MFC cells when the monkey expects a larger amount of reward and misses it 23 . These findings imply that MFC activity is more correlated with reward prediction error than with negative outcomes themselves. To determine whether the MFC responses to action outcomes are associated with subsequent performance adjustments, the magnitude of responses should be compared with the reward prediction error