The hippocampus as the switchboard between perception and memory
Matthias Sebastian TrederiD, Ian CharestiD, Sebastian MichelmanniD, María Carmen Martín-BuroiD, Frédéric RouxiD, Fernando Eliseo Carceller-Benito, Arturo Ugalde-CanitrotiD, David T. RollingsiD, Vijay SawlaniiD, Ramesh ChelvarajahiD, Maria WimberiD, Simon HanslmayriD, Bernhard P. StaresinaiD
Abstract
Adaptive memory recall requires a rapid and flexible switch from external perceptual reminders to internal mnemonic representations. However, owing to the limited temporal or spatial resolution of brain imaging modalities used in isolation, the hippocampal-cortical dynamics supporting this process remain unknown. We thus employed an object-scene cued recall paradigm across two studies, including intracranial Electroencephalography (iEEG) and high-density scalp EEG. First, a sustained increase in hippocampal high gamma power (60-110 Hz) emerged 500 ms after cue onset and distinguished successful vs. unsuccessful recall. This increase in gamma power for successful recall was followed by a decrease in hippocampal alpha power (8-12 Hz). Intriguingly, the hippocampal gamma power increase marked the moment at which extrahippocampal activation patterns shifted from perceptual cue towards mnemonic target representations. In parallel, source-localised EEG alpha power revealed that the recall signal progresses from hippocampus to posterior parietal cortex and then to medial prefrontal cortex. Together, these results identify the hippocampus as the switchboard between perception and memory and elucidate the ensuing hippocampal-cortical dynamics supporting the recall process. SignificanceHow do we adaptively switch from perceiving the external world to retrieving goal-relevant internal memories? To tackle this question, we used - in a cued-recall paradigm - direct intracranial recordings from the human hippocampus complemented by high-density scalp Electroencephalography (EEG). We found that a hippocampal signal ~500 ms after a perceptual cue marks the conversion from external (perceptual) to internal (mnemonic) representations. This sets in motion a recall cascade involving posterior parietal and medial prefrontal cortex, revealed via source-localised and time-resolved EEG alpha power. Together, these results unveil the hippocampal-cortical dynamics supporting rapid and flexible memory recall.
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