Emotional learning retroactively enhances item memory but distorts source attribution

Abstract

An adaptive memory system should prioritize information surrounding a powerful learning event that may prove useful for predicting future meaningful events. The behavioral tagging hypothesis provides a mechanistic framework to interpret how weak experiences persist as durable memories through temporal association with a strong experience. Memories are composed of multiple elements, and different mnemonic aspects of the same experience may be uniquely affected by mechanisms that retroactively modulate a weakly encoded memory. Here, we investigated how emotional learning affects item and source memory for related events encoded close in time. Participants encoded trial-unique category exemplars before, during, and after Pavlovian fear conditioning. Selective retroactive enhancements in 24-h item memory were accompanied by a bias to misattribute items to the temporal context of fear conditioning. The strength of this source memory bias correlated with participants’ retroactive item memory enhancement, and source misattribution to the emotional context predicted whether items were remembered overall. In the framework of behavioral tagging: Memory attribution was biased to the temporal context of the stronger event that provided the putative source of memory stabilization for the weaker event. We additionally found that fear conditioning selectively and retroactively enhanced stimulus typicality ratings for related items, and that stimulus typicality also predicted overall item memory. Collectively, these results provide new evidence that items related to emotional learning are misattributed to the temporal context of the emotional event and judged to be more representative of their semantic category. Both processes may facilitate memory retrieval for related events encoded close in time.

Mood-congruent memory revisited.

“…Their findings demonstrated memory enhancement for the neutral items at encoding that were conceptually congruent with whichever category was reinforced after encoding, but only if memory was tested at least 6 hr later or the next day. These effects were also observed in Hennings et al (2021) and were recently shown to be mediated by postencoding hippocampal–cortical functional connectivity (Clewett et al, 2022). Moreover, similar retroactive effects that selectively strengthen memory consolidation have been demonstrated with postencoding reward manipulations (Braun et al, 2018; Patil et al, 2017).…”

Dynamic music-induced emotions shape the episodic structure of memory

“…Additionally, attempts to investigate the role of emotion on temporal memory neglect the role of continuously shifting emotional states on memory for event structure within temporally extended sequences. Namely, most studies use individual emotional stimuli to elicit moments of emotional reactivity [38][39][40] as well as memory metrics that fail to capture how complex memories take form. For example, prior work has tested temporal source memory for information encountered during, but not surrounding, emotional events 41 .…”

“…For example, prior work has tested temporal source memory for information encountered during, but not surrounding, emotional events 41 . Other studies have tested temporal source judgments for longertimescale events 39,[42][43][44][45] . Further still, memory for the temporal order of image sequences or frames from naturalistic film clips are typically queried by presenting items one at a time 46,47 or all at once during retrieval 41 .…”

Negative emotion enhances memory for the sequential unfolding of a naturalistic experience.

“…Another paradigm used to study memory for time involves making source-memory judgments for sequentially encoded lists, which perhaps represents a coarser appraisal of temporal-order memory (Palombo & Cocquyt, 2020). Most such studies indicate that emotion improves temporal source-memory judgments (e.g., D'Argembeau & Van der Linden, 2005;Rimmele et al, 2012; but also see Hennings et al, 2021), and this effect is somewhat more consistent for negative stimuli (see Petrucci & Palombo, 2021). Still, it is unclear whether source-memory judgments rely solely upon temporal information, as there may be other modulatory factors influencing task performance.…”