An Optimal Oscillatory Phase for Pattern Reactivation During Memory Retrieval

Abstract

Computational models and in vivo studies in rodents suggest that the hippocampal system is not always in an optimal state for retrieval. We here show that the phase of a theta oscillation modulates neural memory reactivation in humans. EEG was recorded while participants were cued to recall previously learned word-picture associations, and multivariate pattern classifiers were trained to detect neural reactivation of the target memory. We found that classifier fidelity rhythmically fluctuated at 7-8Hz across the entire recall period. Inspired by animal work, we then computed “classifier-locked averages” to analyse how ongoing theta oscillations behaved around the time points at which the classifier indicated memory retrieval. We found strong theta (7-8Hz) phase consistency approximately 300ms before the time points of maximal neural reactivation of a memory, originating from medial temporal and occipital sources. Our findings provide important evidence that the neural signatures of memory retrieval fluctuate and are time-locked to the phase of an ongoing theta oscillation.