Awake reactivation of emotional memory traces through hippocampal-neocortical interactions

Awake reactivation of emotional memory traces through hippocampal-neocortical interactions
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DOI:
10.1016/j.neuroimage.2016.04.026
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发表时间:
2016-07-01
期刊:
影响因子:
5.7
通讯作者:
Hermans, Erno J.
Hermans, Erno J.
中科院分区:
医学1区
文献类型:
--
作者:
de Voogd, Lycia D.;Fernandez, Guillen;Hermans, Erno J.

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唤起记忆的经历通常会被很好地记住,这不仅是因为编码的即时效果,而且还通过进一步加强随后的巩固过程。大量的研究表明神经调节系统如何促进突触巩固。然而,情绪唤起的经历如何改变系统水平的相互作用,可能是突触水平的修改的结果,仍然不清楚。动物模型预测,记忆痕迹是通过在学习后休息等“离线”时期跨大脑皮层-新皮层回路的自发再激活来维持的,并表明这可能对情感记忆更强。本研究旨在使用功能性磁共振成像在人类中测试这一假设。参与者经历了两个类别的定位器范式,其次是分类差分延迟恐惧条件反射范式与清醒休息块交错。在参与者之间进行平衡,一个类别(CS+)的样本,而不是另一个(CS-),与轻度电击配对。24小时后测试恐惧回忆(差异性条件性瞳孔扩张)。定位器范式的分析复制了早期的工作,显示了新皮层高阶视觉区域的类别特异性反应模式。至关重要的是,我们表明,在学习后休息,自发再激活这些新皮层模式是强的CS+比CS-类。此外,海马连接的区域表现出这些再激活预测强度的恐惧回忆24小时后。我们的结论是,学习过程中的情绪唤醒促进了自发的学习后再激活的新皮层表示最近的经验,这导致更好的记忆时,恰逢海马连接。我们的研究结果揭示了一种系统水平的机制,可以解释长期记忆对情感体验的持久性。(C)2016 Elsevier Inc. All rights reserved.
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 24 h 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 24 h 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. (C) 2016 Elsevier Inc. All rights reserved.