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. 2024 May 30;11(5):ENEURO.0285-23.2024.
doi: 10.1523/ENEURO.0285-23.2024. Print 2024 May.

Targeted Memory Reactivation during Nonrapid Eye Movement Sleep Enhances Neutral, But Not Negative, Components of Memory

Dan Denis  1 , Jessica D Payne  2
Affiliations

Targeted Memory Reactivation during Nonrapid Eye Movement Sleep Enhances Neutral, But Not Negative, Components of Memory

Dan Denis et al. eNeuro. .

Abstract

Emotionally salient components of memory are preferentially remembered at the expense of accompanying neutral information. This emotional memory trade-off is enhanced over time, and possibly sleep, through a process of memory consolidation. Sleep is believed to benefit memory through a process of reactivation during nonrapid eye movement sleep (NREM). Here, targeted memory reactivation (TMR) was used to manipulate the reactivation of negative and neutral memories during NREM sleep. Thirty-one male and female participants encoded composite scenes containing either a negative or neutral object superimposed on an always neutral background. During NREM sleep, sounds associated with the scene object were replayed, and memory for object and background components was tested the following morning. We found that TMR during NREM sleep improved memory for neutral, but not negative scene objects. This effect was associated with sleep spindle activity, with a larger spindle response following TMR cues predicting TMR effectiveness for neutral items only. These findings therefore do not suggest a role of NREM memory reactivation in enhancing the emotional memory trade-off across a 12 h period but do align with growing evidence of spindle-mediated memory reactivation in service of neutral declarative memory.

Keywords: emotion; memory; reactivation; sleep; sleep spindles.

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Figures

Figure 1.
Figure 1.
Experimental design. In the evening, participants incidentally encoded 92 scenes containing either a negative or neutral object superimposed on an always neutral background. Each scene was accompanied by a sound naturally linked to the object. During the first hour of nonrapid eye movement sleep, half of the sounds were replayed. A surprise memory test was administered the following morning. Participants viewed scene components individually and had to indicate whether the component was old or new.
Figure 2.
Figure 2.
Behavioral results. A, Corrected recognition scores for cued (dark blue) and uncued (light blue) items. **p < 0.01. B, Cueing benefit (cued minus uncued corrected recognition). **p < 0.01 (cueing benefit significantly different from 0). All error bars indicate 95% confidence intervals.
Figure 3.
Figure 3.
Cue-elicited EEG activity during sleep. A, EEG response to memory and control cues. Time 0 indicates cue onset. Left, Time-frequency representation (TFR) of cue-elicited neural activity following memory-related cues. Middle, TFR of response to control sounds. Significant differences between memory and control cues (cluster corrected) highlighted with black contour. Right, Spindle probability following either memory (pink) or control (green) cues. Significant difference (cluster corrected) highlighted in gray. Shaded area depicts the 95% confidence interval. B, Same as A, but for either negative (left) or neutral (middle) cues. Right, Plot shows spindle probability following either negative (orange) or neutral (green) cues. Shaded area depicts the 95% confidence interval.
Figure 4.
Figure 4.
Cue-evoked time-frequency power in the spindle (A) and theta (B) frequencies bands are associated with cueing benefit of neutral, but not negative, object memory. *p < 0.05.
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