Using a nap paradigm, here we demonstrate the selective offline benefit of sleep on the consolidation of negative emotional memories. Furthermore, this offline emotional memory advantage correlated with the amount of REM sleep, and specifically the extent of right-dominant prefrontal theta power during REM.
To date, a number of studies have investigated the interaction between offline time and sleep on affective memory consolidation. For example, Hu et al. (2006)
compared the offline consolidation of emotionally arousing and nonarousing picture-stimuli following a 12 h period across the day or across a night containing sleep. A selective emotional memory benefit was observed only across a night containing sleep and not simply across the simple passage of time, as evidenced by inferior neutral and
emotional memory performance across the day. Wagner and colleagues (Wagner et al. 2001
) have also shown that sleep selectively favors the retention of previously learned emotional texts relative to neutral texts, and that this affective memory benefit is only present following late-night sleep (a time period rich in stage-2 NREM and REM sleep), an effect that can persist for several years (Wagner et al. 2006
). Most recently, it has been shown that sleep preferentially and selectively consolidates emotional objects embedded within a scene, rather than the image as a whole (Payne et al. in press).
Here we similarly describe an offline sleep benefit for emotional memory consolidation but also demonstrate that this effect is evident even following an interval containing a short (90 min) sleep epoch, relative to an equivalent time period awake. Importantly, this effect is revealed when comparing memory performance at identical circadian study-test time points. An alternative explanation for these offline improvements could be attributed to interference from continued waking activities in the No-Nap group, not present during the sleep period in the Nap group, resulting in a passive rather than proactive sleep-state favoring consolidation. However, we find this explanation to be unlikely for several reasons. The lack of interference in the Nap group should result in global consolidation benefits for both emotional and neutral memory categories. Contrary, the sleep benefit was only seen for emotional stimuli. Indeed, one may predict that affective stimuli, being more emotional and potent, should be less susceptible to interference across the day, and result in more similar consolidation benefits to those observed in the No-Nap group. Instead, the opposite was found. Furthermore, the advantage in emotional memory was not proportional to total sleep duration (indexing the total interference-free time in the Nap group), but instead, with a specific type of sleep (REM; incidentally, the stage associated with the greatest amount of potentially interfering mental activity (Hobson and Pace-Schott 2002
). Most compelling, however, was that the emotional memory benefit correlated with a specific electrophysiological oscillation, strongly suggesting an active mechanistic role for sleep in consolidation (and not simply a passive state, lacking interference).
The current findings go beyond demonstrating that emotional memory is preferentially modulated across periods of sleep, and to our knowledge, provide the first demonstration that the extent of emotional memory consolidation is associated with REM-sleep characteristics—both amount and speed of entry. Importantly, this REM relationship was specific to emotional memory with no detectable relationship observed for neutral memory. Furthermore, the emotional memory benefit was selective to REM, with no other sleep-stage measure demonstrating an association with offline performance improvement.
Corroborating these correlations, it has previously been hypothesized that REM sleep represents a brain-state particularly amenable to emotional memory consolidation, based on its unique biology (Pare et al. 2002
; Hu et al. 2006
). Neurochemically, levels of limbic and forebrain ACh are markedly elevated during REM (Vazquez and Baghdoyan 2001
), reportedly quadruple those seen during NREM and double those measured in quite waking (Marrosu et al. 1995
). Considering the known importance of ACh in the long-term consolidation of emotional learning (McGaugh 2004
), this procholinergic REM state may result in a selective memory facilitation of affective memories, similar to that reported using experimental manipulations of ACh (Power 2004
). Moreover, by processing such memories in a brain-state that is largely devoid of aminergic tone (Pace-Schott and Hobson 2002
), particularly noradrenergic input from the locus coeruleus, the modulation of negative emotional experiences during REM may help depotentiate and ultimately ameliorate the autonomic charge originally acquired at the time of learning, negating a long-term state of chronic anxiety.
Neurophysiologically, these alterations may be reflected in (or caused by) changes of synchronized oscillatory activity between limbic (including amygdala and hippocampal) and neocortical regions during REM sleep (Pare et al. 2002
; Jones and Wilson 2005
). Cooperation between these structures plays a role in the modulation of affective experiences (Pare et al. 2002
), leading to the possibility that synchronous activity within these networks during REM sleep may modulate plastic changes essential to emotional memory consolidation. Complimentary to such a model, it has also been demonstrated that learning and later successful recollection of human emotional episodic memories rely on interactions between the hippocampus and amygdala—the degree to which accurately predicts the extent of latent memory retention (Kilpatrick and Cahill 2003
; Dolcos et al. 2004
; Dolcos et al. 2005
Here we demonstrate that the offline facilitation of emotional memory is not simply correlated with the amount and latency of REM sleep, but specifically with an electrophysiological signature of REM sleep—spectral activity in the theta-band range. Furthermore, this relationship was topographically organized, with the biased extent of right-dominant theta power being most predictive of the amount of emotional memory improvement, a relationship consistent with the right-sided anatomical distribution of object (vs. verbal) memory (Kelley et al. 1998
; Wagner et al. 1998
; McDermott et al. 1999
) and also the right-frontal dominant relationship with negative affective processing (Davidson 2002
). Although the functional association between emotional memory and REM-sleep electrophysiology remains unclear, coordinated theta oscillations have been proposed to constitute a mechanism allowing disparate brain regions that initially encoded information to selectively interact offline, in a coupled relationship, and by doing so, promote the strengthening of specific memory representations across distributed networks (Buzsaki 2002
; Jones and Wilson 2005
). It is therefore interesting to speculate whether surface EEG theta correlations observed in the current study, complimentary to those recorded at a cellular level (Jones and Wilson 2005
), may represent the large-scale cooperation between connected subcortical limbic structures and prefrontal regions (Sotres-Bayon et al. 2004
; Jones and Wilson 2005
), the extent of which predicts the amount of offline emotional memory processing and postsleep benefit.
It should be noted, however, that theta activity is not exclusive to REM sleep, and has been observed during periods of sleep–wake transition as well as during quite wakefulness (e.g., Cantero et al. 2003
). We did not record EEG activity in the no-nap group, and therefore do not have an index of theta activity during wakefulness in these participants. Although it is likely that an amount of theta activity will have been present, it does not appear to benefit emotional memory consolidation in a similar manner to that observed during REM, because no emotional memory advantage was observed in those that remained awake. Therefore, although these findings in no way dismiss the possibility that theta activity may be present across brain-states, they do suggest that theta activity, in combination with the REM-sleep state, preferentially facilitates emotional memory consolidation.
Although neutral memory was not enhanced following the nap, we are not suggesting that nonemotional declarative memories do not benefit from sleep. There is now substantial evidence indicating that a full night of nocturnal sleep modulates emotion-free declarative memories, and is most commonly associated with NREM SWS characteristics (Marshall and Born 2007
). Furthermore, our current study focused principally on a short epoch of sleep (but see data in Supplemental Fig. 1
), which, although containing NREM SWS, may not have been sufficient to trigger robust neutral memory consolidation benefits.
In the broader context, this REM-sleep modulation of negative aversive memories may hold implications for the mechanistic understanding and treatment of mood disorders, including major depression. Depression is commonly associated with alterations in REM sleep, including a faster progression into REM (reduced REM latency) and an increase in the amount of REM (Tsuno et al. 2005
; Armitage 2007
). Considering the REM association with negative emotional memory reported here, such REM abnormalities in depression may represent a maladaptive consolidation process of prior negative affective experiences, which, due to the increased REM amount and faster speed of entry into REM, could selectively and disproportionately reinforce negative memories at night, thereby potentiating the mood disorder. Likewise, post-traumatic stress disorder (PTSD) is also associated with a dysregulation of REM sleep, with reports of increased sympathetic autonomic tone (Harvey et al. 2003
; Mellman and Hipolito 2006
). There may similarly be an adverse consequence to such trauma-induced REM-sleep changes in PTSD, which if they persist, could counter-productively amplify, rather than ameliorate, the acquired affective experience. Such basic research findings may help the growing translational appreciation of the interaction between affective mood disorders and sleep physiology.