Yuksel Cagri, Denis Dan, Coleman James, Ren Boyu, Oh Angela, Cox Roy, Morgan Alexandra, Sato Erina, Stickgold Robert
bioRxiv. 2023 Jun 29:2023.03.01.530661. doi: 10.1101/2023.03.01.530661.
Sleep supports memory consolidation. However, it is not completely clear how different sleep stages contribute to this process. While rapid eye movement sleep (REM) has traditionally been implicated in the processing of emotionally charged material, recent studies indicate a role for slow wave sleep (SWS) in strengthening emotional memories. Here, to directly examine which sleep stage is primarily involved in emotional memory consolidation, we used targeted memory reactivation (TMR) in REM and SWS during a daytime nap. Contrary to our hypothesis, reactivation of emotional stimuli during REM led to impaired memory. Consistent with this, REM% was correlated with worse recall in the group that took a nap without TMR. Meanwhile, cueing benefit in SWS was strongly correlated with the product of times spent in REM and SWS (SWS-REM product), and reactivation significantly enhanced memory in those with high SWS-REM product. Surprisingly, SWS-REM product was associated with better memory for reactivated items and poorer memory for non-reactivated items, suggesting that sleep both preserved and eliminated emotional memories, depending on whether they were reactivated. Notably, the emotional valence of cued items modulated both sleep spindles and delta/theta power. Finally, we found that emotional memories benefited from TMR more than did neutral ones. Our results suggest that emotional memories decay during REM, unless they are reactivated during prior SWS. Furthermore, we show that active forgetting complements memory consolidation, and both take place across SWS and REM. In addition, our findings expand upon recent evidence indicating a link between sleep spindles and emotional processing.
睡眠有助于记忆巩固。然而,目前尚不完全清楚不同的睡眠阶段如何促成这一过程。虽然传统上认为快速眼动睡眠(REM)与处理充满情感的材料有关,但最近的研究表明慢波睡眠(SWS)在强化情感记忆方面也发挥作用。在此,为了直接探究哪个睡眠阶段主要参与情感记忆巩固,我们在白天小睡期间对REM和SWS阶段使用了定向记忆再激活(TMR)。与我们的假设相反,在REM阶段对情感刺激进行再激活导致记忆受损。与此一致的是,在没有进行TMR的小睡组中,REM占比与较差的回忆能力相关。同时,SWS阶段的线索获益与REM和SWS阶段的时长乘积(SWS-REM乘积)密切相关,并且再激活显著增强了具有高SWS-REM乘积者的记忆。令人惊讶的是,SWS-REM乘积与对再激活项目的更好记忆以及对未再激活项目的较差记忆相关,这表明睡眠既保留又消除情感记忆,这取决于它们是否被再激活。值得注意的是,线索项目的情感效价调节了睡眠纺锤波以及δ/θ波功率。最后,我们发现情感记忆比中性记忆从TMR中获益更多。我们的研究结果表明,情感记忆在REM阶段会衰退,除非它们在之前的SWS阶段被再激活。此外,我们表明主动遗忘补充了记忆巩固,并且两者都发生在SWS和REM阶段。此外,我们的发现扩展了最近表明睡眠纺锤波与情感处理之间存在联系的证据。