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

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.

Keywords: cognition; emotional memory; heart rate variability (HRV); rapid eye movement sleep (REM); sleep; sleep spindles.

Figure 1

Experimental design schematic. (A) Participants completed the encoding session of the Emotional Picture Task in the morning, followed by an initial test in the evening. Before polysomnographically recorded sleep, participants were administered either zolpidem or placeo. Participants completed a second test the following morning. (B) This study employed a double-blind, within-subject, placebo-controlled, cross-over design. Participants were randomized to receive placebo during visit 1 and zolpidem during visit 2, or vice versa. This figure was created using BioRender.com.

Figure 2

Emotional picture task paradigm.

Figure 3

Correlations between vagal activity and the overnight performance change in emotional and neutral memory. (A) In the placebo condition, overnight performance change for neutral images positively correlated with HRV during SWS (r = 0.520, p_adj = 0.011) and with HRV during REM (r = 0.550, p_adj = 0.010). However, no significant associations were found between negative images and HRV during SWS (r = −0.057, p_adj = 1) or with HRV during REM (r = −0.099, p_adj = 1). (B) In the zolpidem condition, there were no significant correlations between overnight performance change for neutral or negative images and HRV during SWS (all p_adj = 1) or with HRV during REM (all p_adj = 1).

Figure 4

Correlations between vagal activity and the emotional memory tradeoff effect. (A) There were no significant correlations between the emotional memory tradeoff effect and HRV during SWS for either the placebo (r = −0.36, p_adj = 0.069) or zolpidem condition (r = −0.26, p_adj = 0.38). (B) In the placebo condition, the emotional memory tradeoff effect negatively correlated with HRV during REM (r = −0.46, p_adj = 0.034), but this association was eliminated by zolpidem (r = −0.17, p_adj = 0.38).