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Reconciling the Impact of Emotion on Episodic Relational Memory

Symposium Session 4: Sunday, April 14, 2024, 1:30 – 3:30 pm EDT, Sheraton Hall EF

Chairs: Florin Dolcos¹, Deborah Talmi²; ¹University of Illinois at Urbana-Champaign, USA, ²University of Cambridge, UK
Presenters: Florin Dolcos, Paul Christian Bogdan, Yuta Katsumi, Alexandru Daniel Iordan, Simona Buetti2, Alejandro Lleras, Hillary Schwarb, Kara Federmeier, Kelly Freeman Bost, Sanda Dolcos, Deborah Talmi, Emilie De Montpellier, Rik Henson, Hannah Bernhard, Mathias Weymar, Janine Wirkner, Julia Wendt, Lars Schwabe, Florin Dolcos, Alfons O. Hamm, Carlos Ventura-Bort, Daniela Palombo, Omran Safi, Chantelle Cocquyt, Victoria Victoria Wardell

The effects of emotion on memory are wide-ranging and powerful, but they are not uniform. Although there is agreement that emotion enhances memory for individual items, how it influences memory for associated contextual details (relational memory, RM) remains debated, and the factors influencing these discrepant findings are not clear. Clarifying the circumstances in which emotion enhances or impairs RM has game-changing practical benefits for improving RM in healthy functioning and for alleviating RM declines associated with psychopathology and aging. Capturing the richness or RM is a significant challenge. Studies identifying impaired RM by emotion typically measure accuracy in recognizing spatially-based relations between pictorial items and associated contexts, such as between the picture of an accident and the background where it occurred. However, assessments that capture more fully the richness of RM (e.g., by probing participants to recollect specific contextual details surrounding emotional stimuli – what, where, when) often identify enhancing effects of emotion on RM. Adding to this controversy, emerging studies specifically investigating the impact of emotion on memory for associated temporal details of events also point to inconsistent findings. Benefitting researchers, practitioners, and educators alike, this comprehensive symposium addresses central open issues: Dolcos will provide reconciling evidence from behavioral, eye-tracking, and functional neuroimaging investigations, Talmi will discuss evidence disproving the prevalent view that emotion impairs RM, Weymar will present brain imaging, electrophysiological, and neurostimulation evidence regarding the impact of emotion on RM, and Palombo will pinpoint the circumstances in which emotion enhances or impairs memory for temporal associations.

Presentations

Reconciling Opposing Effects of Emotion on Relational Memory: Behavioral, Eye-Tracking, and Brain Imaging Evidence

Florin Dolcos¹, Paul Christian Bogdan^1,2, Yuta Katsumi^1,3, Alexandru Daniel Iordan^1,4, Simona Buetti2¹, Alejandro Lleras¹, Hillary Schwarb^1,5, Kara Federmeier¹, Kelly Freeman Bost¹, Sanda Dolcos¹; ¹University of Illinois at Urbana-Champaign, ²Duke University, ³Harvard Medical School, ⁴University of Michigan, ⁵University of Nebraska

Available evidence suggests that emotion impairs relational memory (RM), but there is also evidence that emotion enhances RM. To reconcile these diverging findings, we performed three main studies incorporating the following features: (1) increased specificity of testing RM, by distinguishing between subjective (recollection-based) and objective (item-context match) RM accuracy, (2) accounted for emotion-attention interactions via eye-tracking and task manipulation, and (3) used stimuli with integrated item-context content. Challenging the view that emotion impairs RM, we identified both enhancing and impairing effects. First, emotion enhanced subjective RM, separately and when confirmed by accurate objective RM. Second, emotion impaired objective RM through attention-capturing, but it enhanced RM accuracy when attentional effects were statistically accounted for using eye-tracking data. Importantly, these two sets of findings were replicated and extended in two larger online studies. Third, emotion also enhanced RM when participants were specifically cued to focus on contextual details during encoding, likely by increasing item-context binding. Finally, challenging models of emotion-RM interactions, fMRI data recorded from a subset of participants showed that enhanced RM by emotion was associated with increased activation within and functional connectivity among regions involved in emotion (amygdala) and context (parahippocampal cortex) processing, and in item-context binding (hippocampus). These results challenge the prevalent view that emotion impairs RM by inhibiting the hippocampal engagement in binding operations. Overall, these findings reconcile evidence regarding opposing effects of emotion on RM and inform training interventions to increase RM specificity in healthy functioning, PTSD, and aging, by promoting item-context binding and diminishing memory decontextualization.

No Evidence that Emotion Decreases Hippocampally-based Associative Binding: Results of an Emotional Variant of the Weather-Prediction Task

Deborah Talmi¹, Emilie De Montpellier¹, Rik Henson¹, Hannah Bernhard¹; ¹University of Cambridge

The weather-prediction task offers a well-established methodology to identify the contribution of the hippocampus to associative binding. This is achieved by comparing the ‘paired-associates’ condition, where participants memorise associations between patterns and outcomes, and the ‘feedback’ condition, where they learn them through trial-and-error. Neuroimaging and neuropsychology results suggest that the paired-associate condition relies on hippocampal mechanisms. Because conditions are well-matched, comparing them inference about hippocampal mechanisms is less vulnerable to measurement noise. We replaced traditional abstract patterns by negative or neutral scenes to test whether emotion impairs hippocampally-based associative binding. Two pre-registered experiments used a 2 (Emotion: negative/neutral) X 2 (Learning condition: feedback/paired-associates). Ratings suggested that the emotion manipulation was successful. We obtained no evidence that emotion impairs hippocampally-based associative binding. Analysis of participants’ learning strategy provided no evidence that emotion decreased deployment of hippocampally-based ‘simple’ strategies. Present results suggest that previous findings using paired-associate memory tests, where emotion decreased memory performance, may not be due to the effect of emotion on hippocampally-dependent associative binding. Our results add to evidence that the dual-representation account, originally developed to account for trauma memories in post-traumatic stress disorders, may not account for memory performance in laboratory settings where stimuli that are less personally traumatic.

Effects of Emotion and Stress on Item vs. Contextual Memory: Brain Dynamics and Neural Substrates

Mathias Weymar¹, Janine Wirkner², Julia Wendt¹, Lars Schwabe³, Florin Dolcos⁴, Alfons O. Hamm², Carlos Ventura-Bort¹; ¹University of Potsdam, Germany, ²University of Greifswald, Germany, ³Universität Hamburg, Germany, ⁴University of Illinois at Urbana-Champaign, USA

It is well known that single arousing emotional events are better remembered than neutral events, a mechanism mediated by the release of stress hormones. When emotional information is encoded as a part of a complex event, such as in the context of or in relation to other events, the beneficial effect of emotion on memory and the role of stress, however, has been less clear so far. In the present talk I present data from a series of studies, in which we found that non-invasive vagal nerve stimulation (taVNS), putatively targeting the LC/NA system, enhances recollection memory for emotional scenes. We further show that objects that have been encoded in the context of emotional compared to neutral scenes were better remembered (source memory). Using ERPs and functional neuroimaging (fMRI) we further demonstrate that correct recognition of these emotional associates (objects from emotional background scenes) produced enhanced parietal ERP Old/New differences as well as larger activation in parietal and prefrontal regions, as part of the recollection network for item and source memory. Interestingly, when acute stress was applied during item/context binding at encoding, opposing effects emerged with stronger brain activation in regions of the recollection network during item retrieval and impaired activation during context (particularly unpleasant) retrieval. Taken together, our line of research provides new insights into the binding mechanisms of emotional and neutral item/context information, which could also be important for better understanding memory abnormalities and neural changes that are typically observed in individuals suffering from stressor- and trauma-related disorders.

The Temporal Tapestry of Emotional Memory: Untangling the Threads

Daniela Palombo¹, Omran Safi¹, Chantelle Cocquyt¹, Victoria Victoria Wardell¹; ¹University of British Columbia

The events of our lives unfold in time. Later, when we remember those events, we can recall not only what transpired, but also their sequential unfolding and the amount of time that elapsed—namely, ‘remembered time.’ How does emotion, especially negative emotion, affect our ability to stitch together the elements of an event with correct temporal features? During my presentation, I will present an overview of recent studies from my laboratory that revolve around this question. Specifically, these studies utilize video, virtual reality, and other naturalistic stimuli to explore the influence of negative emotion on memory for temporal order and temporal duration. Our work—in combination with an established and growing body of literature—suggests that the effects of negative emotion on both aspects of temporal processing are intricate. They evidence enhancements, impairments, or no effects at all under different experimental circumstances. Seeking to reconcile the myriad of findings, I will provide a theoretical roadmap poised to steer future efforts in this domain of cognition. I will also delve briefly into the applied implications of this roadmap in the context of mental health and beyond.