Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization
- Beijing Normal University, China
- Radboud University Nijmegen Medical Centre, Netherlands
- Xinyang Normal University, China
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.
Data availability
All fMRI data collected in this study are available on OpenNeuro under the accession number ds004109 (https://openneuro.org/datasets/ds004109/versions/1.0.0).All code used for analysis are available on GitHub (https://github.com/QinBrainLab/2017_EmotionLearning.git).
Article and author information
Author details
Funding
National Natural Science Foundation of China (32130045)
- Shaozheng Qin
National Natural Science Foundation of China (31522028)
- Shaozheng Qin
National Natural Science Foundation of China (81571056)
- Shaozheng Qin
Open Research Fund of the State Key Laboratory of Cognitive Neuroscience and Learning (CNLZD1503)
- Shaozheng Qin
Chinese Scholarship Council (201806040186)
- Yannan Zhu
The funders have no role in study design, data collection, interpretation, and decision to submit the work for publication.
Ethics
Human subjects: Informed written consent was obtained from each participant before the experiment. The Institutional Review Board for Human Subjects at Beijing Normal University (ICBIR_A_0098_002), Xinyang Normal University (same as above) and Peking University (IRB#2015-09-04) approved the procedures for Study 1, 2 and 3 respectively.
Copyright
© 2022, Zhu et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization
eLife 11:e60190.
https://doi.org/10.7554/eLife.60190
Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
