Direct Electrophysiological Evidence for Prefrontal Control of Hippocampal Processing during Voluntary Forgetting

Forgetting does not necessarily reflect failure to encode information but can, to some extent, also be voluntarily controlled. Previous studies have suggested that voluntary forgetting relies on active inhibition of encoding processes in the hippocampus by the dorsolateral prefrontal cortex (DLPFC) [1-4]. During attentional and sensorimotor processing, enhanced DLPFC theta power alongside increased alpha/beta oscillations are a neural signature of an inhibitory top-down mechanism, with theta oscillations reflecting prefrontal control and alpha/beta oscillations occurring in areas targeted by inhibition [5-12]. Here, we used intracranial EEG recordings in presurgical epilepsy patients implanted in DLPFC (n = 13) and hippocampus (n = 15) during an item-method directed forgetting paradigm. We found that voluntary forgetting is associated with increased neural oscillations in the low theta band (3-5 Hz) in DLPFC and in a broad theta/alpha/beta (6-18 Hz) frequency range in hippocampus. Combining time-lagged correlation analysis, phase synchronization, and Granger causality in 6 patients with electrodes in both DLPFC and hippocampus, we obtained converging evidence for a top-down control of hippocampal activity by the DLPFC. Together, our results provide strong support for a model in which voluntary forgetting relies on enhanced inhibition of the hippocampus by the DLPFC.