{"title":"Phase consistency dynamics of memory encoding.","authors":"Ryan A Colyer, Michael J Kahana","doi":"10.1523/JNEUROSCI.2077-24.2025","DOIUrl":null,"url":null,"abstract":"<p><p>Human and animal studies implicate theta and alpha oscillations in memory function. We tested whether theta, alpha, and beta phase consistency predicts memory encoding dynamics in neurosurgical patients performing delayed free recall tasks with either unrelated (N=188: 99 male, 89 female) or categorized words (N=157: 88 male, 69 female). We observed widespread post-stimulus phase consistency (3-21 Hz) and, crucially, identified distinct frequency-specific patterns predictive of successful encoding. Specifically, increased early-list item recall was significantly correlated across subjects with increased theta (3-7 Hz) phase consistency. Subsequent recall analyses, controlling for serial position, revealed distinct frequency signatures for successfully encoded items: theta (3-6 Hz) and alpha (9-14 Hz) for unrelated lists, and theta (3-6 Hz) and beta (14-19 Hz) for categorized lists. Regional analyses for unrelated lists highlighted the lateral temporal cortex for theta effects and the prefrontal cortex for both theta and alpha consistency. These findings provide novel evidence for the frequency-specific presence of increased phase consistency during episodic encoding, revealing its sensitivity to both item context and temporal position within a learning sequence.<b>Significance statement</b> Neural oscillations are implicated in memory encoding, but their precise roles are still being defined. Our study leverages large-scale intracranial EEG from participants undergoing word recall experiments, and introduces analytical innovations for robustly quantifying phase consistency with differing numbers of recalled versus forgotten items. This methodology reveals that phase consistency across different frequency bands (theta, alpha, beta) predicts memory formation. We demonstrate a role for theta consistency in encoding early list items and show that the brain recruits different oscillatory patterns (alpha or beta alongside theta) depending on item context (unrelated vs. categorized lists). These findings advance our understanding of the frequency-specific neural mechanisms supporting human episodic memory, revealing how the brain adapts its encoding strategies based on informational structure.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0000,"publicationDate":"2025-07-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/JNEUROSCI.2077-24.2025","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Human and animal studies implicate theta and alpha oscillations in memory function. We tested whether theta, alpha, and beta phase consistency predicts memory encoding dynamics in neurosurgical patients performing delayed free recall tasks with either unrelated (N=188: 99 male, 89 female) or categorized words (N=157: 88 male, 69 female). We observed widespread post-stimulus phase consistency (3-21 Hz) and, crucially, identified distinct frequency-specific patterns predictive of successful encoding. Specifically, increased early-list item recall was significantly correlated across subjects with increased theta (3-7 Hz) phase consistency. Subsequent recall analyses, controlling for serial position, revealed distinct frequency signatures for successfully encoded items: theta (3-6 Hz) and alpha (9-14 Hz) for unrelated lists, and theta (3-6 Hz) and beta (14-19 Hz) for categorized lists. Regional analyses for unrelated lists highlighted the lateral temporal cortex for theta effects and the prefrontal cortex for both theta and alpha consistency. These findings provide novel evidence for the frequency-specific presence of increased phase consistency during episodic encoding, revealing its sensitivity to both item context and temporal position within a learning sequence.Significance statement Neural oscillations are implicated in memory encoding, but their precise roles are still being defined. Our study leverages large-scale intracranial EEG from participants undergoing word recall experiments, and introduces analytical innovations for robustly quantifying phase consistency with differing numbers of recalled versus forgotten items. This methodology reveals that phase consistency across different frequency bands (theta, alpha, beta) predicts memory formation. We demonstrate a role for theta consistency in encoding early list items and show that the brain recruits different oscillatory patterns (alpha or beta alongside theta) depending on item context (unrelated vs. categorized lists). These findings advance our understanding of the frequency-specific neural mechanisms supporting human episodic memory, revealing how the brain adapts its encoding strategies based on informational structure.
期刊介绍:
JNeurosci (ISSN 0270-6474) is an official journal of the Society for Neuroscience. It is published weekly by the Society, fifty weeks a year, one volume a year. JNeurosci publishes papers on a broad range of topics of general interest to those working on the nervous system. Authors now have an Open Choice option for their published articles