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.It is well established that sleep has a facilitating effect on memory formation in animals and humans (e.g., Jenkins and Dallenbach 1924;Smith 1985Smith , 1995Stickgold et al. 2000). However, the physiological mechanisms of this effect are still unclear. Specifically, there is an ongoing controversy concerning the differential contribution of rapid eye movement (REM) sleep and slow wave sleep (SWS) to memory consolidation. In particular, human studies provided mixed results, some indicating a beneficial effect of REM sleep on memory (Empson and Clarke 1970;Lewin and Glaubman 1975;Tilley and Empson 1978) whereas others suggested SWS to be critical for memory formation (Yaroush et al. 1971;Barrett and Ekstrand 1972;Fowler et al. 1973;Ekstrand 1977). The divergent outcomes appear to reflect differences in the methods used for investigating memory formation during sleep and in the type of memory examined. The most commonly used approach in the study of sleepassociated memory formation is the REM sleep deprivation paradigm, in which subjects are awakened whenever polysomnographic recordings indicate signs of REM sleep. In control conditions, awakenings are induced in nonREM sleep. Yet the REM sleep-deprivation paradigm has been subject to profound criticism (Horne and McGrath 1984; Vertes and Eastman, in press). Compared with other sleep stages, frequent arousal from REM sleep induces serious emotional and cognitive disturbances. These disturbances impa...

The ‘affect tagging and consolidation’ (ATaC) model of depression vulnerability

“…Importantly, the two groups did not differ in their recognition performance for neutral images. This emotion-specific effect of REM sleep corroborates earlier work which found that three hours of late night REM dominant sleep facilitates the consolidation of negative images (Groch, Zinke, Wilhelm, & Born, 2015) and information within negative stories (Wagner, Gais, & Born, 2001), relative to three hours of sleep obtained in the first half of the night where REM sleep is less abundant. Correlational analyses have yielded similar results, finding that the amount of time spent in REM sleep across a 12-hour retention interval correlates positively with recall performance for negative but not neutral objects within complex images (Payne et al, 2012).…”

“…Research which demonstrates that many compounds with antidepressant properties suppress REM sleep (Mayers & Baldwin, 2005;Steiger & Kimura, 2010; also see: Murck et al, 2003;Nofzinger et al, 1995;Sonntag et al, 1996), considered alongside evidence that REM sleep duration and density is associated with the consolidation of negative memories (Gilson et al, 2015;Groch et al, 2015;Nishida et al, 2009;Payne et al, 2012;Wagner et al, 2001;Wiesner et al, 2015), has led researchers to speculate that REM sleep alterations may underlie the emotional memory bias observed in depressed patients (Walker & van der Helm, 2009;Walker, 2009). However, the majority of studies directly investigating the effect of REM sleep on emotional memory consolidation focus exclusively on comparisons between recognition performance for neutral and negatively salient stimuli (however see : Cairney, Durrant, Power, & Lewis, 2015), ignoring the possibility that REM sleep may also play a role in the consolidation of positive memories.…”

“…The ATaC model predicts that the excessive emotional tagging of negative material associated with negatively-biased amygdala activity may not manifest as a clinically significant memory bias if REM sleep, which stabilises negative experiences in long-term memory (Groch et al, 2015;Nishida et al, 2009;Payne et al, 2012;Wagner et al, 2001;Wiesner et al, 2015;also see: Wagner, Hallschmid, Rasch, & Born, 2006), is adequately regulated. As we have seen, REM sleep propensity is tightly regulated by circadian rhythms (Pace-Schott & Hobson, 2002) which are thought to be disturbed in depression (Bunney & Bunney, 2013;Etain et al, 2011;Kronfeld-Schor & Einat, 2012).…”

Cognitive and emotional processes during dreaming: A neuroimaging view

“…Activation in these regions suggest that memory consolidation processes, in particular emotional memories, may occur during REM sleep (Hu, Stylos-Allan, & Walker, 2006;Nishida, Pearsall, Buckner, & Walker, 2009;Sterpenich et al, 2009;Wagner, Gais, & Born, 2001;Wagner, Hallschmid, Rasch, & Born, 2006;Walker, 2009). While a large body of data support the involvement of sleep in memory (for review, see Dang-Vu, Desseilles, Peigneux, & Maquet, 2006), the relationship between processes related to memory consolidation and those underlying dream experience is still poorly understood (e.g.…”

Rem sleep, early experience, and the development of reproductive strategies

“…There is now abundant evidence that the amygdala specializes in processing of emotion, particularly negative emotions, and functions as the "decisional" or "appraisal organ" of the mind (Bechara et al 1999;Davidson and Irwin 1999;LeDoux 1996). In addition, along with hippocampal sites, it apparently supports both emotional memory formation and reactivation of emotional memories during REM (Wagner et al 2001;Wilson and McNaughton 1994). It also contributes to regulation of other brain structures such as the hypothalamus that, in turn, regulate ongoing neuroendocrine processes in the developing organism (LeDoux 2002;Davis and Whalen 2001).…”