Events that violate predictions are thought to not only modulate activity within the hippocampus and PFC but also enhance communication between the two regions. Scalp and intracranial EEG studies have shown that oscillations in the theta frequency band are enhanced during processing of contextually unexpected information. Some theories suggest that the hippocampus and PFC interact during processing of unexpected events, and it is possible that theta oscillations may mediate these interactions. Here, we had the rare opportunity to conduct simultaneous electrophysiological recordings from the human hippocampus and PFC from two patients undergoing presurgical evaluation for pharmacoresistant epilepsy. Recordings were conducted during a task that involved encoding of contextually expected and unexpected visual stimuli. Across both patients, hippocampal–prefrontal theta phase synchronization was significantly higher during encoding of contextually unexpected study items, relative to contextually expected study items. Furthermore, the hippocampal–prefrontal theta phase synchronization was larger for contextually unexpected items that were later remembered compared with later forgotten items. Moreover, we did not find increased theta synchronization between the PFC and rhinal cortex, suggesting that the observed effects were specific to prefrontal–hippocampal interactions. Our findings are consistent with the idea that theta oscillations orchestrate communication between the hippocampus and PFC in support of enhanced encoding of contextually deviant information.

Adapting behavior based on category knowledge is a fundamental cognitive function, which can be achieved via different learning strategies relying on different systems in the brain. Whereas the learning of typical category members has been linked to implicit, prototype abstraction learning, which relies predominantly on prefrontal areas, the learning of exceptions is associated with explicit, exemplar-based learning, which has been linked to the hippocampus. Stress is known to foster implicit learning strategies at the expense of explicit learning. Procedural, prefrontal learning and cognitive control processes are reflected in frontal midline theta (4–8 Hz) oscillations during feedback processing. In the current study, we examined the effect of acute stress on feedback-based category learning of typical category members and exceptions and the oscillatory correlates of feedback processing in the EEG. A computational modeling procedure was applied to estimate the use of abstraction and exemplar strategies during category learning. We tested healthy, male participants who underwent either the socially evaluated cold pressor test or a nonstressful control procedure before they learned to categorize typical members and exceptions based on feedback. The groups did not differ significantly in their categorization accuracy or use of categorization strategies. In the EEG, however, stressed participants revealed elevated theta power specifically during the learning of exceptions, whereas the theta power during the learning of typical members did not differ between the groups. Elevated frontal theta power may reflect an increased involvement of medial prefrontal areas in the learning of exceptions under stress.

The nucleus accumbens is critical for reward-guided learning and decision-making. It is thought to “gate” the flow of a diverse range of information (e.g., rewarding, aversive, and novel events) from limbic afferents to basal ganglia outputs. Gating and information encoding may be achieved via cross-frequency coupling, in which bursts of high-frequency activity occur preferentially during specific phases of slower oscillations. We examined whether the human nucleus accumbens engages such a mechanism by recording electrophysiological activity directly from the accumbens of human patients undergoing deep brain stimulation surgery. Oscillatory activity in the gamma (40–80 Hz) frequency range was synchronized with the phase of simultaneous alpha (8–12 Hz) waves. Further, losing and winning small amounts of money elicited relatively increased gamma oscillation power prior to and following alpha troughs, respectively. Gamma–alpha synchronization may reflect an electrophysiological gating mechanism in the human nucleus accumbens, and the phase differences in gamma–alpha coupling may reflect a reward information coding scheme similar to phase coding.