The hippocampus as the switchboard between perception and memory

Matthias S Treder,Ramesh Chelvarajah,Fernando Carceller-Benito,María Carmen Martín-Buro,David T Rollings,Sebastian Michelmann,Maria Wimber,Simon Hanslmayr,Frédéric Roux,Ian Charest,Arturo Ugalde-Canitrot,Vijay Sawlani,Bernhard P Staresina

doi:10.1073/pnas.2114171118

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 (55 to 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 to 12 Hz). Intriguingly, the hippocampal gamma power increase marked the moment at which extrahippocampal activation patterns shifted from perceptual cue toward mnemonic target representations. In parallel, source-localized 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.

Highlights

Adaptive memory recall requires a rapid and flexible switch from external perceptual reminders to internal mnemonic representations
While these results indicate that successful memory relies on intricate hippocampal–cortical interactions, the temporal dynamics within the cortical retrieval network” (CRN) are challenging to resolve with functional MRI (fMRI) alone, hampering understanding of different CRN regions’ contributions [16]
Our study elucidates the role of the hippocampus as a switchboard from perception to memory and unveils the ensuing cortical dynamics supporting the recall process

Summary

Introduction

Adaptive memory recall requires a rapid and flexible switch from external perceptual reminders to internal mnemonic representations. It retains pointers to the cortical sites involved in the initial experience [3, 4] such that presenting a partial reminder prompts reinstatement of the entire association via hippocampal pattern completion [5, 6] In support of these models, human functional MRI (fMRI) studies linked hippocampal activation with cortical reinstatement of mnemonic target representations during successful recall [7,8,9,10,11,12,13]. 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-localized and time-resolved EEG alpha power. Together, these results unveil the hippocampal–cortical dynamics supporting rapid and flexible memory recall

Methods

Results

Conclusion