Similarity of brain activity patterns during learning and subsequent resting state predicts memory consolidation

Abstract

Long-term memory depends on memory consolidation that seems to rely on learning-induced changes in the brain activity. Here, we introduced a novel approach analyzing continuous EEG data to study learning-induced changes as well as trait-like characteristics in brain activity underlying consolidation. Thirty-one healthy young adults performed a learning task and their performance was retested after a short (~1h) delay, that enabled us to investigate the consolidation of serial-order and probability information simultaneously. EEG was recorded during a pre- and post-learning rest period and during learning. To investigate the brain activity associated with consolidation performance, we quantified similarities in EEG functional connectivity of learning and pre-learning rest (baseline similarity) as well as learning and post-learning rest (post-learning similarity). While comparable patterns of these two could indicate trait-like similarities, changes in similarity from baseline to post-learning could indicate learning-induced changes, possibly spontaneous reactivation. Individuals with higher learning-induced changes in alpha frequency connectivity (8.5-9.5 Hz) showed better consolidation of serial-order information. This effect was stronger for more distant channels, highlighting the role of long-range centro-parietal networks underlying the consolidation of serial-order information. The consolidation of probability information was associated with learning-induced changes in delta frequency connectivity (2.5-3 Hz) and seemed to be dependent on more local, short-range connections. Beyond these associations with learning-induced changes, we also found substantial overlap between the baseline and post-learning similarity and their associations with consolidation performance, indicating that stable (trait-like) differences in functional connectivity networks may also be crucial for memory consolidation. Significance statementWe studied memory consolidation in humans by characterizing how similarity in neural oscillatory patterns during learning and rest periods supports consolidation. Previous studies on similarity focused on learning-induced changes (including reactivation) and neglected the stable individual characteristics that are present over resting periods and learning. Moreover, learning-induced changes are predominantly studied invasively in rodents or with neuroimaging or event-related electrophysiology techniques in humans. Here, we introduced a novel approach that enabled us 1) to reveal both learning-induced changes and trait-like individual differences in brain activity and 2) to study learning-induced changes in humans by analyzing continuous EEG. We investigated the consolidation of two types of information and revealed distinct learning-induced changes and trait-like characteristics underlying the different memory processes.