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.

Electroencephalogram oscillations recorded both within and over the medial frontal cortex have been linked to a range of cognitive functions, including positive and negative feedback processing. Medial frontal oscillatory characteristics during decision making remain largely unknown. Here, we examined oscillatory activity of the human medial frontal cortex recorded while subjects played a competitive decision-making game. Distinct patterns of power and cross-trial phase coherence in multiple frequency bands were observed during different decision-related processes (e.g., feedback anticipation vs. feedback processing). Decision and feedback processing were accompanied by a broadband increase in cross-trial phase coherence at around 220 msec, and dynamic fluctuations in power. Feedback anticipation was accompanied by a shift in the power spectrum from relatively lower (delta and theta) to higher (alpha and beta) power. Power and cross-trial phase coherence were greater following losses compared to wins in theta, alpha, and beta frequency bands, but were greater following wins compared to losses in the delta band. Finally, we found that oscillation power in alpha and beta frequency bands were synchronized with the phase of delta and theta oscillations (“phase–amplitude coupling”). This synchronization differed between losses and wins, suggesting that phase–amplitude coupling might reflect a mechanism of feedback valence coding in the medial frontal cortex. Our findings link medial frontal oscillations to decision making, with relations among activity in different frequency bands suggesting a phase-utilizing coding of feedback valence information.

Up to now, two conflicting theories have tried to explain the genesis of averaged event-related potentials (ERPs): Whereas one hypothesis claims that ERPs originate from an event-related activation of neural assemblies distinct from background dynamics, the other hypothesis states that ERPs are produced by phase resetting of ongoing oscillatory activity. So far, this question has only been addressed for early ERP components. Late ERP components, however, are generally thought to represent superimposed activities of several anatomically distinct brain areas. Thus, the question of which mechanism underlies the genesis of late ERP components cannot be easily answered based on scalp recordings. In contrast, two well-investigated late ERP components recorded invasively from within the human medial temporal lobe (MTL) in epilepsy patients, the so-called MTL-P300 and the anterior MTL-N400 (AMTL-N400), are based on single source activity. Hence, we investigated whether the MTL-P300 and the AMTL-N400 are based on an event-related activity increase, a phase reset of ongoing oscillatory activity or both. ERPs were recorded from the hippocampus and rhinal cortex in subjects performing a visual oddball paradigm and a visual word recognition paradigm. With wavelet techniques, stimulus-related phase-locking and power changes were analyzed in a frequency range covering 2 to 48 Hz. We found that the MTLP300 is accompanied by both phase reset and power increase and that both effects overlap partly in time. In contrast, the AMTL-N400 is initially associated with phase locking without power increase and only later during the course of the AMTL-N400 we observed an additional power increase. In conclusion, both aspects, event-related activation of neural assemblies and phase resetting of ongoing activity seem to be involved in the generation of late ERP components as recorded in cognitive tasks. Therefore, separate analysis of event-related power and phase-locking changes might reveal specific insights into the mechanisms underlying different cognitive functions.