Vagal heart rate variability during rapid eye movement sleep reduces negative memory bias.

IF 2.6 3区 医学 Q2 BEHAVIORAL SCIENCES
Frontiers in Behavioral Neuroscience Pub Date : 2025-02-24 eCollection Date: 2025-01-01 DOI:10.3389/fnbeh.2025.1513655
Allison B Morehouse, Katharine C Simon, Pin-Chun Chen, Sara C Mednick
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引用次数: 0

Abstract

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.

快速眼动睡眠时的迷走心率变异可减少负性记忆偏差。
随着时间的推移,情绪记忆会发生变化,但支持这种变化的机制还没有得到很好的理解。睡眠已被确定为支持记忆巩固的一种机制,睡眠选择性地有利于负面情绪巩固,以牺牲中性记忆为代价,特定的振荡事件与这一过程有关。相反,与消极记忆相比,中性记忆和积极记忆的巩固与清醒时迷走神经介导的心率变异性(HRV)的增加有关。然而,睡眠期间的心率波动如何促进情绪记忆巩固仍未得到研究。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消极记忆的巩固。采用双盲、安慰剂对照、受试者内交叉设计,我们研究了唑吡坦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消极的图片进行编码,然后在睡眠前后进行图片识别测试。在晚上睡觉前给予唑吡坦或安慰剂,并用脑电图和心电图监测参与者。在安慰剂组中,中性图片的夜间改善与非快速眼动慢波睡眠(NREM SWS)和快速眼动睡眠(REM)中较高的迷走神经HRV有关。此外,情绪记忆权衡(即中性记忆巩固与消极记忆巩固之间的差异)与快速眼动睡眠期间较高的迷走神经HRV有关,但在这种情况下,中性记忆比消极记忆更容易被记住。这表明快速眼动迷走神经HRV在促进夜间积极记忆偏差中的潜在作用。另一方面,唑吡坦降低了SWS期间迷走神经HRV,增加了NREM纺锤体活动,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非快速眼动期间的纺锤体活动和迷走神经HRV如何独立解释情绪记忆权衡效应的差异。我们发现迷走HRV与纺锤体活动的结合显著改善了模型的拟合。总的来说,我们的研究结果表明,睡眠时的大脑振荡和迷走神经信号在情绪记忆的夜间巩固中协同作用,快速眼动期迷走神经HRV对积极记忆偏差起着关键作用。
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来源期刊
Frontiers in Behavioral Neuroscience
Frontiers in Behavioral Neuroscience BEHAVIORAL SCIENCES-NEUROSCIENCES
CiteScore
4.70
自引率
3.30%
发文量
506
审稿时长
6-12 weeks
期刊介绍: Frontiers in Behavioral Neuroscience is a leading journal in its field, publishing rigorously peer-reviewed research that advances our understanding of the neural mechanisms underlying behavior. Field Chief Editor Nuno Sousa at the Instituto de Pesquisa em Ciências da Vida e da Saúde (ICVS) is supported by an outstanding Editorial Board of international experts. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics, clinicians and the public worldwide. This journal publishes major insights into the neural mechanisms of animal and human behavior, and welcomes articles studying the interplay between behavior and its neurobiological basis at all levels: from molecular biology and genetics, to morphological, biochemical, neurochemical, electrophysiological, neuroendocrine, pharmacological, and neuroimaging studies.
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