Morehouse Allison B, Simon Katharine C, Chen Pin-Chun, Mednick Sara C
Department of Cognitive Science, University of California, Irvine, CA, United States.
Department of Pediatrics, Irvine, CA, United States.
Front Behav Neurosci. 2025 Feb 24;19:1513655. doi: 10.3389/fnbeh.2025.1513655. eCollection 2025.
Emotional memories change over time, but the mechanisms supporting this change are not well understood. Sleep has been identified as one mechanism that supports memory consolidation, with sleep selectively benefitting negative emotional consolidation at the expense of neutral memories, with specific oscillatory events linked to this process. In contrast, the consolidation of neutral and positive memories, compared to negative memories, has been associated with increased vagally mediated heart rate variability (HRV) during wakefulness. However, how HRV during sleep contributes to emotional memory consolidation remains unexplored. We investigated how sleep oscillations (i.e., sleep spindles) and vagal activity during sleep contribute to the consolidation of neutral and negative memories. Using a double-blind, placebo-controlled, within-subject, cross-over design, we examined the impact of pharmacological vagal suppression using zolpidem on overnight emotional memory consolidation. Thirty-three participants encoded neutral and negative pictures in the morning, followed by picture recognition tests before and after a night of sleep. Zolpidem or placebo was administered in the evening before overnight sleep, and participants were monitored with electroencephalography and electrocardiography. In the placebo condition, greater overnight improvement for neutral pictures was associated with higher vagal HRV in both Non-Rapid Eye Movement Slow Wave Sleep (NREM SWS) and REM. Additionally, the emotional memory tradeoff (i.e., difference between consolidation of neutral versus negative memories) was associated with higher vagal HRV during REM, but in this case, neutral memories were remembered better than negative memories, indicating a potential role for REM vagal HRV in promoting a positive memory bias overnight. Zolpidem, on the other hand, reduced vagal HRV during SWS, increased NREM spindle activity, and eliminated the positive memory bias. Lastly, we used stepwise linear mixed effects regression to determine how NREM spindle activity and vagal HRV during REM independently explained the variance in the emotional memory tradeoff effect. We found that the addition of vagal HRV in combination with spindle activity significantly improved the model's fit. Overall, our results suggest that sleep brain oscillations and vagal signals synergistically interact in the overnight consolidation of emotional memories, with REM vagal HRV critically contributing to the positive memory bias.
情绪记忆会随时间变化，但其背后的机制尚未完全明晰。睡眠被认为是支持记忆巩固的一种机制，睡眠会选择性地促进负面情绪记忆的巩固，而以中性记忆为代价，特定的振荡事件与这一过程相关。相比之下，与负面记忆相比，中性和正面记忆的巩固与清醒时迷走神经介导的心率变异性（HRV）增加有关。然而，睡眠期间的HRV如何促进情绪记忆巩固仍未得到探索。我们研究了睡眠振荡（即睡眠纺锤波）和睡眠期间的迷走神经活动如何促进中性和负面记忆的巩固。采用双盲、安慰剂对照、受试者内交叉设计，我们研究了使用唑吡坦进行药理学迷走神经抑制对夜间情绪记忆巩固的影响。33名参与者在早上对中性和负面图片进行编码，然后在一夜睡眠前后进行图片识别测试。在夜间睡眠前的晚上给予唑吡坦或安慰剂，并通过脑电图和心电图对参与者进行监测。在安慰剂条件下，中性图片在夜间的更大改善与非快速眼动慢波睡眠（NREM SWS）和快速眼动睡眠（REM）中更高的迷走神经HRV相关。此外，情绪记忆权衡（即中性记忆与负面记忆巩固之间的差异）与REM期间更高的迷走神经HRV相关，但在这种情况下，中性记忆比负面记忆记忆得更好，表明REM迷走神经HRV在促进夜间积极记忆偏差方面可能发挥作用。另一方面，唑吡坦降低了SWS期间的迷走神经HRV，增加了NREM纺锤波活动，并消除了积极记忆偏差。最后，我们使用逐步线性混合效应回归来确定REM期间的NREM纺锤波活动和迷走神经HRV如何独立解释情绪记忆权衡效应的方差。我们发现，将迷走神经HRV与纺锤波活动相结合能显著改善模型的拟合度。总体而言，我们的结果表明，睡眠脑振荡和迷走神经信号在情绪记忆的夜间巩固中协同相互作用，REM迷走神经HRV对积极记忆偏差起着关键作用。
