skip to main content

Title: Memory reactivation and suppression modulate integration of the semantic features of related memories in hippocampus

Encoding an event that overlaps with a previous experience may involve reactivating an existing memory and integrating it with new information or suppressing the existing memory to promote formation of a distinct, new representation. We used fMRI during overlapping event encoding to track reactivation and suppression of individual, related memories. We further used a model of semantic knowledge based on Wikipedia to quantify both reactivation of semantic knowledge related to a previous event and formation of integrated memories containing semantic features of both events. Representational similarity analysis revealed that reactivation of semantic knowledge related to a prior event in posterior medial prefrontal cortex (pmPFC) supported memory integration during new learning. Moreover, anterior hippocampus (aHPC) formed integrated representations combining the semantic features of overlapping events. We further found evidence that aHPC integration may be modulated on a trial-by-trial basis by interactions between ventrolateral PFC and anterior mPFC, with suppression of item-specific memory representations in anterior mPFC inhibiting hippocampal integration. These results suggest that PFC-mediated control processes determine the availability of specific relevant memories during new learning, thus impacting hippocampal memory integration.

more » « less
Author(s) / Creator(s):
; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Cerebral Cortex
Medium: X Size: p. 9020-9037
p. 9020-9037
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    We investigated how the human brain integrates experiences of specific events to build general knowledge about typical event structure. We examined an episodic memory area important for temporal relations, anterior-lateral entorhinal cortex, and a semantic memory area important for action concepts, middle temporal gyrus, to understand how and when these areas contribute to these processes. Participants underwent functional magnetic resonance imaging while learning and recalling temporal relations among novel events over two sessions 1 week apart. Across distinct contexts, individual temporal relations among events could either be consistent or inconsistent with each other. Within each context, during the recall phase, we measured associative coding as the difference of multivoxel correlations among related vs unrelated pairs of events. Neural regions that form integrative representations should exhibit stronger associative coding in the consistent than the inconsistent contexts. We found evidence of integrative representations that emerged quickly in anterior-lateral entorhinal cortex (at session 1), and only subsequently in middle temporal gyrus, which showed a significant change across sessions. A complementary pattern of findings was seen with signatures during learning. This suggests that integrative representations are established early in anterior-lateral entorhinal cortex and may be a pathway to the later emergence of semantic knowledge in middle temporal gyrus.

    more » « less
  2. Consolidating memories for long-term storage depends on reactivation. Reactivation occurs both consciously, during wakefulness, and unconsciously, during wakefulness and sleep. While considerable work has examined conscious awake and unconscious sleep reactivation, in this study, we directly compare the consequences of conscious and unconscious reactivation during wakefulness. Forty-one participants learned associations consisting of adjective–object–position triads. Objects were clustered into distinct semantic groups (e.g., fruits, vehicles) such that we could examine consequences of reactivation on semantically related memories. After an intensive learning protocol, we systematically reactivated some of the triads by presenting the adjective as a cue. Reactivation was done so that it was consciously experienced for some triads, and only unconsciously processed for others. Memory for spatial positions, the most distal part of the association, was affected by reactivation in a consciousness-dependent and memory-strength-dependent manner. Conscious reactivation resulted in weakening of semantically related memories that were strong initially, resonating with prior findings of retrieval-induced forgetting. Unconscious reactivation, on the other hand, selectively benefited weak reactivated memories, as previously shown for reactivation during sleep. Semantically linked memories were not impaired, but rather were integrated with the reactivated memory. These results taken together demonstrate that conscious and unconscious reactivation have qualitatively different consequences. Results support a consciousness-dependent inhibition account, whereby unconscious reactivation entails less inhibition than conscious reactivation, thus allowing more liberal spread of activation. Findings set the stage for additional exploration into the role of conscious experience in memory storage and structuring.

    more » « less
  3. null (Ed.)
    Abstract Memory consolidation involves the reactivation of memory traces during sleep. If different memories are reactivated each night, how much do they interfere with one another? We examined whether reactivating multiple memories incurs a cost to sleep-related benefits by contrasting reactivation of multiple memories versus single memories during sleep. First, participants learned the on-screen location of different objects. Each object was part of a semantically coherent group comprised of either one, two, or six items (e.g., six different cats). During sleep, sounds were unobtrusively presented to reactivate memories for half of the groups (e.g., “meow”). Memory benefits for cued versus non-cued items were independent of the number of items in the group, suggesting that reactivation occurs in a simultaneous and promiscuous manner. Intriguingly, sleep spindles and delta-theta power modulations were sensitive to group size, reflecting the extent of previous learning. Our results demonstrate that multiple memories may be consolidated in parallel without compromising each memory’s sleep-related benefit. These findings highlight alternative models for parallel consolidation that should be considered in future studies. 
    more » « less
  4. Humans are adept in simultaneously following multiple goals, but the neural mechanisms for maintaining specific goals and distinguishing them from other goals are incompletely understood. For short time scales, working memory studies suggest that multiple mental contents are maintained by theta-coupled reactivation, but evidence for similar mechanisms during complex behaviors such as goal-directed navigation is scarce. We examined intracranial electroencephalography recordings of epilepsy patients performing an object-location memory task in a virtual environment. We report that large-scale electrophysiological representations of objects that cue for specific goal locations are dynamically reactivated during goal-directed navigation. Reactivation of different cue representations occurred at stimulus-specific hippocampal theta phases. Locking to more distinct theta phases predicted better memory performance, identifying hippocampal theta phase coding as a mechanism for separating competing goals. Our findings suggest shared neural mechanisms between working memory and goal-directed navigation and provide new insights into the functions of the hippocampal theta rhythm. 
    more » « less
  5. null ; Mangun, G.R. ; Gazzaniga, M.S. (Ed.)
    The human ability to remember unique experiences from many years ago comes so naturally that we often take it for granted. It depends on three stages: (1) encoding, when new information is initially registered, (2) storage, when encoded information is held in the brain, and (3) retrieval, when stored information is used. Historically, cognitive neuroscience studies of memory have emphasized encoding and retrieval. Yet, the intervening stage may hold the most intrigue, and has become a major research focus in the years since the last edition of this book. Here we describe recent investigations of post-acquisition memory processing in relation to enduring storage. This evidence of memory processing belies the notion that memories stored in the brain are held in stasis, without changing. Various methods for influencing and monitoring brain activity have been applied to study offline memory processing. In particular, memories can be reactivated during sleep and during resting periods, with distinctive physiological correlates. These neural signals shed light on the contribution of hippocampal-neocortical interactions to memory consolidation. Overall, results converge on the notion that memory reactivation is a critical determinant of systems-level consolidation, and thus of future remembering, which in turn facilitates future planning and problem solving. 
    more » « less