Phase reset dynamics of memory encoding

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Abstract

Human and animal studies have implicated oscillatory reset following a behaviorally relevant stimulus in learning and memory function. Here we asked whether phase reset predicts the dynamics of memory encoding for subsequently recalled and forgotten items. Our dataset comprised 188 neurosurgical patients (99 male, 89 female) who studied lists of common words for a subsequent delayed free recall test. We observed significant 3–21 Hz overall phase reset widespread throughout the brain in the 125–500 ms interval following stimulus presentation for both subsequently recalled and forgotten items. We found that the increased recalls of the primacy effect correlated significantly and exclusively with theta phase reset from 3–7 Hz throughout the brain. When controlling for serial position effects and examining the phase consistency differences of subsequently recalled and forgotten items, we identified both a theta (3–6 Hz) and an alpha (9–14 Hz) component of phase reset. Examined separately, early list items revealed a significant theta phase reset difference, while later list items revealed a significant alpha phase reset difference for subsequently recalled items. In regional analyses, the lateral temporal cortex exhibited a significant theta phase reset difference, while the prefrontal cortex revealed both a significant theta and a significant alpha phase reset difference for subsequently recalled items. These findings support the view that oscillatory reset serves an important role in encoding new episodic associations, and reveal differing oscillatory mechanisms across theta and alpha bands for serial position effects of phase reset versus serial position controlled subsequent recall.

Significance Statement

In 188 neurosurgical patients we examined the relationship of memory function with oscillatory phase consistency in response to word encoding events in a delayed free recall task. We innovated a new approach to computing a phase consistency score with robustness across sample size differences. Using this method, we showed a significant serial position correlate across subjects with primacy regions exhibiting a clear increase in theta phase consistency (3–7 Hz). After controlling for serial position effects, we also observed a significant effect of both increased theta phase consistency (3–6 Hz) and increased alpha phase consistency (9–14 Hz) for subsequently recalled versus forgotten items. This improves our understanding of the multi-faceted role of frequency-specific phase resetting in episodic memory encoding.

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