Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep

Abstract

Recent studies indicated a selective activation during rapid eye movement (REM) sleep of the amygdala known to play a decisive role in the processing of emotional stimuli. This study compared memory retention of emotional versus neutral text material over intervals covering either early sleep known to be dominated by nonREM slow wave sleep (SWS) or late sleep, in which REM sleep is dominant. Two groups of men were tested across 3-h periods of early and late sleep (sleep group) or corresponding retention intervals filled with wakefulness (wake group). Sleep was recorded polysomnographically. Cortisol concentrations in saliva were monitored at acquisition and retrieval testing. As expected, the amount of REM sleep was about three times greater during late than during early retention sleep, whereas a reversed pattern was observed for SWS distribution (P < 0.001). Sleep improved retention, compared with the effects of wake intervals (P < 0.02). However, this effect was substantial only in the late night (P < 0.005), during which retention was generally worse than during the early night (P < 0.02). Late sleep particularly enhanced memory for emotional texts. This effect was highly significant in comparison with memory for neutral texts (P < 0.01) and in comparison with memory after late and early wake intervals (P < 0.001). Cortisol concentration differed between early and late retention intervals but not between sleep and wake conditions. Results are consonant with a supportive function of REM sleep predominating late sleep for the formation of emotional memory in humans.

Figure 1

Memory retention across the early (left panel) and late night (right panel) for neutral and emotional texts over 3-h retention intervals filled with sleep (black) or wakefulness (grey). Retention is indicated by the percentage of content words correctly recalled at retrieval testing with reference to performance at learning before the retention interval. Note the superior retention of emotional texts after late sleep compared to late wakefulness and to retention of neutral texts. In comparison with early night conditions, retention of emotional texts during late sleep was also significantly superior to that during early wakefulness. ***P < 0.001, **P < 0.01.

Figure 2

Study design. Subjects were tested on two nights (early versus late retention condition), with the order balanced across subjects. On the early retention condition, learning of the texts took place between 2215–2300 h, followed by a retention interval of ∼3 h. On the late retention condition, subjects first slept between 2300–0200 h (to “consume” SWS). Learning took place between 0215–0300 h, followed by a 3-h retention interval with subsequent retrieval testing. The experimental sleep group slept during the retention interval, and retrieval was tested 15 min after awakening. The control group remained awake in the retention intervals.