Emotional learning retroactively enhances item memory but distorts source attribution

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.

Emotional experiences gain privileged access to the neurobehavioral mechanisms of long-term memory (LaBar and Cabeza 2006; Kensinger 2009; McGaugh 2015; Yonelinas and Ritchey 2015; Mather et al. 2016). Importantly, this emotional enhancement of memory can spread to seemingly mundane details encoded close in time to the emotional experience. Through this temporal association, affectively neutral information retroactively acquires the capacity to predict emotional events, allowing us to better avoid or seek out those outcomes. However, what aspects of memory are modulated via temporal proximity to an emotional event? Episodic memories, for instance, are composed of stimulus information (e.g., item memory) embedded with contextual details (e.g., source memory) (Johnson et al. 1993; Tulving 2002). Emotion enhances item memory (Sharot and Phelps 2004; LaBar and Cabeza 2006; Mather 2007) but has inconsistent effects on contextual details associated with emotional stimuli (Yonelinas and Ritchey 2015). While there is evidence that episodic memory is selectively prioritized for related information encoded before (Dunsmoor et al. 2015) and after (Dunsmoor et al. 2015, 2018; Tambini et al. 2017; Keller and Dunsmoor 2020) an emotional experience, retroactive and proactive effects of emotional learning on source memory for this same information is unknown. Here, we investigated how temporal proximity to an emotional learning event influences both item memory and contextual details for related information.Enhancement in memory via a temporal association between mundane and salient events is consistent with neurobiological models of long-term memory. For example, the behavioral tagging hypothesis (derived from the synaptic tagging hypothesis; Frey and Morris 1997) proposes that weak learning is strengthened in memory if it is encoded within a critical time window of a more salient event and if the two events share overlapping neural ensembles (Moncada and Viola 2007; Ballarini et al. 2009; Wang et al. 2010; Takeuchi et al. 2016). As emotion is a powerful learning event, information encoded within temporal proximity may be strengthened in memory via a mechanism of behavioral tagging. The behavioral tagging hypothesis has been translated to humans using novelty (Fenker et al. 2008; Ballarini et al. 2013; Ramirez Butavand et al. 2020), threat (Dunsmoor et al. 2015), and reward (Patil et al. 2017) to induce memory enhancements for weakly encoded information encoded close in time. However, it is unclear whether and how this mechanism may affect memory for the contextual details associated with the weak event.Emotion can sometimes improve memory accuracy for information directly associated with an emotional stimulus, such as the spatial and temporal context in which the emotional stimulus was encoded (Kensinger and Schacter 2006; Schmidt et al. 2011; Rimmele et al. 2012; Talmi et al. 2019). Therefore, one possibility is that emotional learning improves both item and source memory for information in temporal proximity to an emotional event. In this case, we might expect item memory to be accompanied by source memory accuracy, such that items are appropriately organized in time relative to the emotional event. Alternatively, emotional learning might have no effect (Sharot and Yonelinas 2008; Wang and Fu 2010) or even impair memory for contextual information. Indeed, it may be simpler to remember a trivial item by virtue of associating the item with the salient context (Takashima et al. 2016). It is therefore plausible that linking weak and strong events by temporal proximity might improve item memory at the cost of source memory. Consequently, we may expect a relationship between the strength of item memory for related events encoded close in time and the strength of a misallocation bias to source the item to the more salient temporal context. This might suggest that retroactive memory enhancement for weakly encoded items relies in part on misattribution to the more salient emotional context.In addition to our exploration of how emotional learning impacts item and source memory for proximal events, we tested a parallel hypothesis that emotional learning alters abstract stimulus properties that may indirectly facilitate memory retrieval for those items as well. Previous work demonstrates that emotional learning is sensitive to how well an item represents its broader category; that is, typicality (Dunsmoor and Murphy 2014, 2015; Dunsmoor et al. 2014; Struyf et al. 2018; Lei et al. 2019). Whether emotional learning has the power to alter an abstract stimulus property such as subjective typicality is unknown, but stimulus memorability may be an underappreciated factor contributing to item memory (Bainbridge 2019). For instance, the hippocampus plays a role in both episodic memory and concept representations (Quiroga 2012; Davis and Poldrack 2014; Mack et al. 2016). Moreover, typical category members used as conditioned stimuli in Pavlovian fear conditioning preferentially engage the hippocampus and hippocampal-amygdala functional connectivity (Dunsmoor et al. 2014), which is a substrate for emotional memory enhancement (Murty et al. 2010).In the present study participants underwent a 2-d Pavlovian fear conditioning task that included trial-unique (i.e., nonrepeating) pictures of animals and tools as conditioned stimuli (CSs), based on the protocol from Dunsmoor et al. (2015). Items were encoded before, during, and after Pavlovian fear conditioning. We predicted that emotional learning would have divergent effects on 24-h episodic memory accuracy for CS items and the encoding temporal context. Specifically, we predicted that CSs semantically related to the fear conditioned category would be selectively remembered regardless of their temporal context (Dunsmoor et al. 2015), but that participants would have a bias to attribute these related CSs to the temporal context of fear conditioning. We also investigated whether emotional learning enhances subjective typicality for CS category members related to the fear conditioning category, and whether long-term memory would be influenced by how strongly an item was deemed to represent its superordinate category. Such findings might indicate that weak memories formed in temporal proximity to an emotional experience our bound to the more salient temporal context, and that emotional learning can alter abstract stimulus properties of weakly encoded information to make this information more memorable.