Sleep promotes lasting changes in selective memory for emotional scenes

Abstract

Although we know that emotional events enjoy a privileged status in our memories, we still have much to learn about how emotional memories are processed, stored, and how they change over time. Here we show a positive association between REM sleep and the selective consolidation of central, negative aspects of complex scenes. Moreover, we show that the placement of sleep is critical for this selective emotional memory benefit. When testing occurred 24 h post-encoding, subjects who slept soon after learning (24 h Sleep First group) had superior memory for emotional objects compared to subjects whose sleep was delayed for 16 h post-encoding following a full day of wakefulness (24 h Wake First group). However, this increase in memory for emotional objects corresponded with a decrease in memory for the neutral backgrounds on which these objects were placed. Furthermore, memory for emotional objects in the 24 h Sleep First group was comparable to performance after just a 12 h delay containing a night of sleep, suggesting that sleep soon after learning selectively stabilizes emotional memory. These results suggest that the sleeping brain preserves in long-term memory only what is emotionally salient and perhaps most adaptive to remember.

Keywords: emotion; emotional memory enhancement; emotional memory formation; memory; memory consolidation; sleep; sleep and memory.

Figures

Figure 1

Experimental timeline. The 30 min (n = 40), 12 h wake (n = 24) and 12 h sleep (n = 24) groups (labeled “a”) are from Payne et al. (2008). Note: Because there were no differences in performance in the 30 min groups (30 min am, n = 20 and 30 min pm, n = 20), they were combined into a single 30 min variable for analyses reported in the current paper. The overnight polysomnography study reported here (Experiment 1, n = 27) follows the 12 h Sleep protocol (labeled “a”), with the addition of overnight sleep monitoring in the laboratory. The 24 h delay study (Experiment 2, labeled “b”) follows the 24 h Wake 1st (n = 22) and 24 h Sleep 1st (n = 22) protocols.

Figure 2

The emotional memory trade-off effect. Top—Sample stimuli with the identical neutral backgrounds and either a neutral (left) or negative emotional (right) object in the foreground; Bottom—Emotional trade-off (following a 30 min delay, from Payne et al., 2008) is seen on right as increased recognition of emotional objects with impaired recognition of neutral backgrounds. Figure adapted from Payne and Kensinger (2010).

Figure 3

REM sleep correlations. Specific recognition of negative objects is selectively positively correlated with time spent in REM sleep (REM Sleep Min) and with percent of the night spent in REM sleep (REM Sleep %).

Figure 4

Twenty-four hours delay memory performance overall. The emotional memory trade-off effect is preserved following a 24 h delay. Note that object memory is superior for negative, compared to neutral, scenes (p < 0.001), while scene backgrounds are more poorly remembered if they are paired with negative, compared to neutral, objects (p < 0.001).

Figure 5

Twenty-four hours delay memory performance is modulated by the placement of sleep. (A) Negative objects are better remembered in the Sleep First (p < 0.05), compared to the Wake First, condition, but the opposite is true for associated backgrounds (p < 0.05). (B) The Sleep First and Wake First groups do not differ on memory for any component of the neutral scenes.

Figure 6

(A) Change in memory across time. Relative to the 30 min condition, negative object memory was preserved 12 h later provided that subjects slept in the delay interval (Sleep 12 h group). Moreover, there was no further deterioration in negative object memory over the next 12 h (comparison between the Sleep 12 and 24 h Sleep First group). However, the backgrounds associated with these negative objects continued to deteriorate across these delay intervals, suggesting that sleeping soon after learning is key for protecting memory for emotional components of scenes. In the wake groups, on the other hand, memory for negative objects continued to deteriorate from the 30 min to Wake 12 h and from Wake 12 to 24 h Wake First delays, which depicts a pattern of increasing memory deterioration for negative objects in the wake groups. Note also the absence of the trade-off effect in the 24 h Wake First group (no difference in memory for objects vs. backgrounds), as well as the increased magnitude of the trade-off effect in the two sleep conditions (sleep 12 and 24 h Sleep First—see brackets). **p < 0.01. (B) Memory for neutral scenes shows a net decline over time, but note that the groups groups do not differ in memory for objects vs. backgrounds at any of the delay intervals.