Donders Institute for Brain, Cognition and Behaviour, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands; Department for Cognitive Neuroscience, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands.
Donders Institute for Brain, Cognition and Behaviour, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands; Department for Cognitive Neuroscience, Radboud university medical center, 6500 HB, Nijmegen, The Netherlands.
Neuroimage. 2016 Jul 1;134:563-572. doi: 10.1016/j.neuroimage.2016.04.026. Epub 2016 Apr 16.
Emotionally arousing experiences are typically well remembered not only due to immediate effects at encoding, but also through further strengthening of subsequent consolidation processes. A large body of research shows how neuromodulatory systems promote synaptic consolidation. However, how emotionally arousing experiences alter systems-level interactions, presumably a consequence of modifications at a synaptic level, remains unclear. Animal models predict that memory traces are maintained by spontaneous reactivations across hippocampal-neocortical circuits during "offline" periods such as post-learning rest, and suggest this might be stronger for emotional memories. The present study was designed to test this hypothesis in humans using functional Magnetic Resonance Imaging. Participants underwent a two-category localizer paradigm followed by a categorical differential delay fear conditioning paradigm interleaved with blocks of awake rest. Counterbalanced across participants, exemplars of one category (CS+), but not the other (CS-), were paired with mild electrical shocks. Fear recall (differential conditioned pupil dilation) was tested 24h later. Analyses of the localizer paradigm replicate earlier work showing category-specific response patterns in neocortical higher-order visual regions. Critically, we show that during post-learning rest, spontaneous reactivation of these neocortical patterns was stronger for the CS+ than the CS- category. Furthermore, hippocampal connectivity with the regions exhibiting these reactivations predicted strength of fear recall 24h later. We conclude that emotional arousal during learning promotes spontaneous post-learning reactivation of neocortical representations of recent experiences, which leads to better memory when coinciding with hippocampal connectivity. Our findings reveal a systems-level mechanism that may explain the persistence of long-term memory for emotional experiences.
情感体验通常不仅由于编码时的即时效应而被很好地记住，而且还通过进一步加强随后的巩固过程来增强。大量研究表明神经调节系统如何促进突触巩固。然而，情感体验如何改变系统水平的相互作用，推测是突触水平修饰的结果，目前仍不清楚。动物模型预测，记忆痕迹通过在“离线”期间（例如学习后休息）跨海马-新皮层回路的自发再激活来维持，并且对于情绪记忆来说，这可能更强。本研究旨在使用功能磁共振成像在人类中测试这一假设。参与者接受了两个类别定位器范式，然后进行了类别差异延迟恐惧条件范式，其间穿插清醒休息块。在参与者之间平衡，一个类别的范例（CS+），但不是另一个（CS-）与轻度电击配对。24 小时后测试恐惧回忆（差异条件瞳孔扩张）。定位器范式的分析复制了早期工作，表明新皮层高级视觉区域存在类别特异性反应模式。至关重要的是，我们表明，在学习后的休息期间，这些新皮层模式的自发再激活对于 CS+比 CS-类别更强。此外，海马与表现出这些再激活的区域的连接性预测了 24 小时后恐惧回忆的强度。我们得出结论，学习期间的情感唤醒促进了最近经历的新皮层表示的自发学习后再激活，当与海马连接性同时发生时，会导致更好的记忆。我们的发现揭示了一种系统水平的机制，该机制可能解释了情绪体验的长期记忆的持久性。
