Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization

Abstract

Neutral events preceding emotional experiences can be better remembered, likely by assigning them as significant to guide possible use in future. Yet, the neurobiological mechanisms of how emotional learning enhances memory for past mundane events remain unclear. By two behavioral studies and one functional magnetic resonance imaging study with an adapted sensory preconditioning paradigm, we show rapid neural reactivation and connectivity changes underlying emotion-charged retroactive memory enhancement. Behaviorally, emotional learning enhanced initial memory for neutral associations across the three studies. Neurally, emotional learning potentiated trial-specific reactivation of overlapping neural traces in the hippocampus and stimulus-relevant neocortex. It further induced rapid hippocampal-neocortical functional reorganization supporting such retroactive memory benefit, as characterized by enhanced hippocampal-neocortical coupling modulated by the amygdala during emotional learning, and a shift of hippocampal connectivity from stimulus-relevant neocortex to transmodal prefrontal-parietal areas at post-learning rests. Together, emotional learning retroactively promotes memory integration for past neutral events through stimulating trial-specific reactivation of overlapping representations and reorganization of associated memories into an integrated network to foster its priority for future use.

Emotional information facilitates or disrupts memory integration through distinct hippocampal processes of reactivation and connectivity

“…This result suggests a rapid and trial-specific facilitation for integrating related neutral and emotional memories, supporting the view of "associative facilitation" (Kuhl et al, 2010;Schlichting and Preston, 2014;Wimmer and Shohamy, 2012). It is also in line with previous studies, showing that linking a neutral mundane event to emotionally salient information can enhance memory for the neutral event due to its gained value and significance for the future (Holmes et al, 2022;Li et al, 2008;Sharpe et al, 2017;Zhu et al, 2022). However, we did not find any facilitation effect on non-integrated memories, which differs from the delayed and generalized emotional enhancement for weak memories encoded closely in time, as proposed in synaptic tagging-and-capture models (Ballarini et al, 2009;Dunsmoor et al, 2015;Frey and Morris, 1997).…”

“…The SMA and MCC are also thought to regulate emotion generalization to target events along integrated memory traces but not to other irrelevant events (Kohn et al, 2014;Wager et al, 2008). The emotional involvement in memory processes promotes information transmission and communication between the hippocampus and neocortex (Battaglia et al, 2011;Hermans et al, 2014;Hofstetter et al, 2012;Zhu et al, 2022). Indeed, we found strengthened hippocampal connectivity with the TPJ and precuneus, which are core regions of the default mode network (DMN) (Hyatt et al, 2015;Schacter and Addis, 2007;Schacter et al, 2011).…”

“…Through memory integration, emotional arousal not only strengthens memory for an emotional event (LaBar and Cabeza, 2006;LeDoux, 1994;Schacter, 1999), but also has a broader impact on related, other events. Despite considerable efforts, a general consensus on the emotional modulation of related events has not been reached, as both facilitation and interference effects reported in divergent studies (Bravo-Rivera and Sotres-Bayon, 2020;Li et al, 2008;Mather and Sutherland, 2011;Wimmer and Shohamy, 2012;Zhu et al, 2022). In this study, we manipulated the emotional composition of to-be-integrated stimuli to elucidate the circumstances under which facilitation and interference effects occur, as well as their potentially distinct neural mechanisms.…”

“…One prominent view, "facilitation theory", has proposed that emotion facilitates memory integration (Holmes et al, 2022;Shohamy and Daw, 2015). Recent studies have shown that an emotionally salient experience enhances memory for related neutral events, indicating a tighter memory integration with strengthened associations among these pieces of information (Wang and Kahnt, 2021;Wimmer and Shohamy, 2012;Wong et al, 2019;Zhu et al, 2022). However, an "interference theory" suggests that emotion disrupts memory integration (Bravo-Rivera and Sotres-Bayon, 2020; Mather, 2007).…”

Cognitive neuroscience perspective on memory: overview and summary

“…BT explains how it is possible for event episodes with low-strength inputs or engagements can be converted into lasting memories ( Lynch, 2004 ; Moncada et al, 2015 ). Similarly, the emotional tagging hypothesis posits that the activation of the amygdala in emotionally arousing events helps to mark experiences as necessary, thus enhancing synaptic plasticity and facilitating transformation from transient into more permanent forms for encoding long-term memories ( Richter-Levin and Akirav, 2003 ; Zhu et al, 2022 ).…”