Theta rhythmicity governs human behavior and hippocampal signals during memory-dependent tasks

Marije Ter Wal,Hajo Hamer,Stephanie Gollwitzer,Vijay Sawlani,Johannes Lang,David Rollings,Bernhard Staresina,Julia Lifanov,Maria Wimber,Juan Linde-Domingo,Frédéric Roux,Ramesh Chelvarajah,Simon Hanslmayr,Luca D Kolibius

doi:10.1038/s41467-021-27323-3

Abstract

Memory formation and reinstatement are thought to lock to the hippocampal theta rhythm, predicting that encoding and retrieval processes appear rhythmic themselves. Here, we show that rhythmicity can be observed in behavioral responses from memory tasks, where participants indicate, using button presses, the timing of encoding and recall of cue-object associative memories. We find no evidence for rhythmicity in button presses for visual tasks using the same stimuli, or for questions about already retrieved objects. The oscillations for correctly remembered trials center in the slow theta frequency range (1-5 Hz). Using intracranial EEG recordings, we show that the memory task induces temporally extended phase consistency in hippocampal local field potentials at slow theta frequencies, but significantly more for remembered than forgotten trials, providing a potential mechanistic underpinning for the theta oscillations found in behavioral responses.

Highlights

Memory formation and reinstatement are thought to lock to the hippocampal theta rhythm, predicting that encoding and retrieval processes appear rhythmic themselves
In this study we demonstrated that oscillations can be detected in behavioral responses from associative memory tasks
Using the Oscillation score[43], we showed that button presses that indicate the timing of memory encoding and retrieval were rhythmically modulated, i.e. periodically more or less likely to occur, predominantly in the 1–5 Hz frequency band

Summary

Introduction

Memory formation and reinstatement are thought to lock to the hippocampal theta rhythm, predicting that encoding and retrieval processes appear rhythmic themselves. Using intracranial EEG recordings, we show that the memory task induces temporally extended phase consistency in hippocampal local field potentials at slow theta frequencies, but significantly more for remembered than forgotten trials, providing a potential mechanistic underpinning for the theta oscillations found in behavioral responses. During retrieval, cues trigger the completion of existing patterns encoded in hippocampus, eliciting reinstatement of the memory in associated cortical regions. Both memory encoding and retrieval have been associated with changes in oscillatory patterns in hippocampal local field potentials (LFPs). Spiking activity of hippocampal neurons was reported to lock to the LFP at theta frequencies[17] during successful encoding[18]

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