Effects of emotion and stress on mnemonic binding of contextual information: Brain dynamics and neural substrates
Human Cognitive and Systems Neuroscience
Final Report Abstract
Emotional memories can be extremely robust and long-lasting, which in extreme circumstances can contribute to the development of mood, anxiety, and stress-related disorders. Despite abundant evidence showing enhanced memory for emotional aspects of events, less is known about the underlying mechanisms of memory for associated contextual information. This is of particular interest, because dysfunctional integration of item-context information in memory traces may play a critical role in the symptomatology of affective disturbances (e.g., intrusive memory reactivations in post-traumatic stress disorder, PTSD). In a series of event-related potential (ERP) and functional brain imaging (fMRI) experiments with healthy participants, we investigated temporal dynamics and neural substrates related to long-term item-context binding using neutral objects that were actively and passively associated with emotionally arousing or neutral scenes. Across studies, we reliably found that contextual memory tested after one week was enhanced for objects encoded with emotional scenes (emotional associates) compared to objects encoded with neutral scenes (neutral associates). We also found evidence that enhanced memory for emotional and neutral associates was mediated by distinct episodic memory representations (familiarity and recollection). Particularly, information about emotional associates with contextual details was recollection-based remembered and related to a pronounced parietal ERP old/new effect (around 500 ms) during retrieval, a putative correlate of recollection memory. In addition, enhanced functional activity was found during retrieval of objects from emotional scene contexts in brain regions previously linked to episodic memory and context retrieval (recollection), such as prefrontal cortex, parietal cortex and MTL (hippocampus, parahippcampal cortex). Further ERP results showed that enhanced retrieval of emotional associates is also triggered automatically (without explicit memory task) and that enhanced retrieval for emotional associates may result from heightened attention and elaborative processing during encoding (indexed by enhanced P100 and LPP amplitudes). The project also investigated the role of acute stress (also taking into account rapid and slow corticosteroid actions) on emotional and neutral item-context binding. Results are preliminary (elaborated analyses are currently in progress) but showed stress effects on context-binding in our paradigm. Contrary to our predictions that rapid cortisol would disrupt binding we found enhanced enhanced (but not diminished) MTL activity during retrieval of emotional associates, compared to controls. Furthermore, when slow cortisol actions were considered, we specifically found that acute stress applied 180 minutes before encoding result in a familiarity-based memory for emotional context information (parietal ERP old/new effect was also absent), which could be interpreted as impaired contextual memory binding. The results may give support for recent models suggesting that rapid stress (via catecholamine and non-genomic cortisol action) facilitates encoding (and later retrieval) of prioritized information. Slower longlasting genomic cortisol actions, on the other hand, may facilitate restorative processes, which includes diminished acquirement of new recollective information to promote undisturbed processing of prior experiences. Taken together, the project provided new neuroscientific insights into the binding mechanisms of emotional and neutral context information, which could also be relevant in understanding mechanisms, e.g. involved in the activation of trauma-related memories by neutral environmental cues in clinical disorders.
Publications
- (2016). Binding neutral information to emotional contexts: Brain dynamics of long-term recognition memory. Cognitive, Affective, and Behavioral Neuroscience, 2, 234-247
Ventura-Bort, C., Löw, A., Wendt, J., Molto, J., Poy, R., Dolcos, F., Hamm, A.O., & Weymar, M.
(See online at https://doi.org/10.3758/s13415-015-0385-0) - (2016). When context matters: Electrophysiological correlates of associative learning and memory for neutral items bound to emotional contextual information. sixth ICOM (International Conference on Memory, Budapest (Hungary), July 17-22, 2016
Ventura-Bort, C., Löw, A., Wendt, J., Dolcos, F., Hamm, A.O., Weymar, M.
- (2016). When neutral turns significant: Brain dynamics of rapidly formed associations between neutral stimuli and emotional contexts. European Journal of Neuroscience, 44, 2176-2183
Ventura-Bort, C., Löw, A., Wendt, J., Dolcos, F., Hamm, A.O., & Weymar, M.
(See online at https://doi.org/10.1111/ejn.13319) - (2017). Current Issues and Emerging Directions in the Impact of Emotion on Memory: A Review of Evidence from Brain Imaging Investigations. Memory in Social Context. Edited by Takashi Tsukiura and Satoshi Umeda. Springer
Dolcos, F., Katsumi, Y., Denkova, E., Weymar, M., & Dolcos, S.
(See online at https://doi.org/10.1007/978-4-431-56591-8_5) - (2017). Emerging Directions in Emotional Episodic Memories. Frontiers in Psychology, 8:1867
Dolcos, F., Katsumi, Y., Weymar, M., Moore, M., Tsukiura, T., & Dolcos, S.
(See online at https://doi.org/10.3389/fpsyg.2017.01867) - (2017). Enhanced voluntary and spontaneous memory retrieval of emotional associates: An ERP study. SPR (Society for Psychophysiological Research) conference in Wien (A). Psychophysiology, 54 (Suppl.), S129. October 11-15, 2017
Ventura-Bort, C., Hamm, A., & Weymar, M.
- (2017). Item and source memory for emotional associates is mediated by different retrieval processes: An ERP study. Neuropsychologia. (December 12, 2017)
Ventura-Bort, C., Dolcos, F., Wendt, J., Wirkner, J., Hamm, A.O., & Weymar, M.
(See online at https://doi.org/10.1016/j.neuropsychologia.2017.12.015) - (2017). Transcutaneous vagus nerve stimulation modulates attentional allocation processes: an ERP study. ESCoP (European Society for Cognitive Psychology) conference in Potsdam. September 3-6, 2017
Ventura-Bort, C., Genheimer, H., Wirkner, J., Wendt, J., Hamm, A.O., & Weymar, M.
- (2018). Current research and emerging directions in emotional memory: Evidence from healthy functioning, psychopathology, and interventions. ESCAN (European Society for Cognitive and Affective Neuroscience) conference in Leiden (NL)
Weymar, M., & Dolcos, F.
- (2018). Effects of transcutaneous vagus nerve stimulation (tVNS) on the P300 and alpha-amylase level: A pilot study. Frontiers in Human Neuroscience 12:202
Ventura-Bort, C., Wirkner, J., Genheimer, H., Wendt, J., Hamm, A.O., & Weymar, M.
(See online at https://doi.org/10.3389/fnhum.2018.00202) - (2018). Neural substrates of item and source memory for emotional associates: an fMRI study. ESCAN (European Society for Cognitive and Affective Neuroscience) conference in Leiden (NL)
Ventura-Bort, C., Katsumi, Y., Wendt, J., Wirkner, J, König, J., Lotze, M., Hamm, A., Dolcos, F., & Weymar, M.
- (2019). Chronic stress and emotion: Differential effects on attentional processing and recognition memory. Psychoneuroendocrinology, 107, 93-97
Wirkner, J., Ventura-Bort, C., Schwabe, L., Hamm, A.O., & Weymar, M.
(See online at https://doi.org/10.1016/j.psyneuen.2019.05.008) - (2019). Emotion and motivation as context: New evidence for biased processing in perception, learning and memory. „Gehirn und Psychologie 2019“ conference of the DGPs und DGPA in Dresden
Schacht, A., & Weymar, M.
- (2019). Enhanced spontaneous retrieval cues from emotional events: An ERP study. Biological Psychology, 148, 107742
Ventura-Bort, C., Wirkner, J., Dolcos, F., Wendt, J., Hamm, A.O., & Weymar, M.
(See online at https://doi.org/10.1016/j.biopsycho.2019.107742)
