Coordination of high gamma activity in anterior cingulate and lateral prefrontal cortical areas during adaptation.

The anterior cingulate cortex (ACC) and the lateral prefrontal cortex (LPFC) process complementary information for planning and evaluating behavior. This suggests at least that processes in these two areas are coordinated during behavioral adaptation. We analyzed local field potentials recorded in both regions in two monkeys performing a problem-solving task that alternated exploration and repetitive behaviors with the specific prediction that neural activity should reveal interareal coordination mainly during exploration. Both areas showed increased high gamma power after errors in exploration and after rewards in exploitation. We found that high gamma (60-140 Hz) power increases in ACC were followed by a later increase in LPFC only after negative feedback (errors) or first positive feedback (correct) during the exploration period. The difference in latencies between the two structures disappeared in repetition period. Simultaneous recordings revealed correlations between high gamma power in the two areas around feedback; however, correlations were observed in both exploration and repetition. In contrast, postfeedback beta (10-20 Hz) power in ACC and LPFC correlated more frequently during repetition. Together, our data suggest that the coordination between ACC and LPFC activity is expressed during adaptive as well as stable behavioral periods but with different modes depending on the behavioral period.

Behavioral shifts and action valuation in the anterior cingulate cortex.

Rapid optimization of behavior requires decisions about when to explore and when to exploit discovered resources. The mechanisms that lead to fast adaptations and their interaction with action valuation are a central issue. We show here that the anterior cingulate cortex (ACC) encodes multiple feedbacks devoted to exploration and its immediate termination. In a task that alternates exploration and exploitation periods, the ACC monitored negative and positive outcomes relevant for different adaptations. In particular, it produced signals specific of the first reward, i.e., the end of exploration. Those signals disappeared in exploitation periods but immediately transferred to the initiation of trials-a transfer comparable to learning phenomena observed for dopaminergic neurons. Importantly, these were also observed for high gamma oscillations of local field potentials shown to correlate with brain imaging signal. Thus, mechanisms of action valuation and monitoring of events/actions are combined for rapid behavioral regulation.

Expectations, gains, and losses in the anterior cingulate cortex.

The anterior cingulate cortex (ACC) participates in evaluating actions and outcomes. Little is known on how action-reward values are processed in ACC and if the context in which actions are performed influences this processing. In the present article, we report ACC unit activity of monkeys performing two tasks. The first task tested whether the encoding of reward values is co ntext dependent-that is, dependent on the size of theother rewards that are available in the current block of trials. The second task tested whether unexpected events signaling a change in reward are represented. We show that the context created by a block design (i.e., the context of possible alternative rewards) influences the encoding of reward values, even if no decision or choice is required. ACC activity encodes the relative and not absolute expected reward values. Moreover, cingulate activitysignals and evaluates when reward expectations are violated by unexpected stimuli, indicating reward gains or losses.