Sleep spindles provide indirect support to the consolidation of emotional encoding contexts

Abstract

Emotional memories tend to be strengthened ahead of neutral memories during sleep-dependent consolidation. In recent work, however, we found that this is not the case when emotion pertains to the contextual features of a memory instead of its central constructs, suggesting that emotional contexts are influenced by distinct properties of sleep. We therefore examined the sleep-specific mechanisms supporting representations of emotional context and asked whether these differ to those already implicated in central emotional memory processing, such as rapid eye movement sleep (REM). Participants encoded neutral foreground images that were each associated with an emotionally negative or neutral background (context) image. Immediate and delayed tests for the emotionality of the foreground/background image association were separated by a 4-h consolidation period, which consisted of either total wakefulness or included a 2-h polysomnographically monitored nap. Although memory for negative contexts was not associated with REM, or any other parameter of sleep, sleep spindles (12-15 Hz) predicted increased forgetting and slowed response times for neutral contexts. Together with prior work linking spindles to emotional memory processing, our data may suggest that spindles provide multi-layered support to emotionally salient memories in sleep, with the nature of such effects depending on whether the emotionality of these memories pertains to their central or contextual features. Therefore, whereas spindles may mediate a direct strengthening of central emotional information, as suggested in prior work, they may also provide concurrent indirect support to emotional contexts by working to suppress non-salient neutral contexts.

Sleep before and after learning promotes the consolidation of both neutral and emotional information regardless of REM presence

“…As summarized by Cellini and Parma (2015), re-exposing participants during SWS to a cue previously matched with a threatening stimulus, successfully enhances fear extinction in humans. Other studies showed direct (Kaestner, et al, 2013) or indirect evidence (Cairney, Durrant, Hulleman, & Lewis, 2014a;Cairney, et al, 2014b) of a relationship between sleep spindles and emotional memory. Notably, Cairney and colleagues (2015) reported a positive association between the proportion of SWS and the consolidation of unpleasant pictures.…”

“…For example, in two recent studies, human participants were selectively re-exposed during NREM to sounds or odors previously matched with a threatening stimulus and, as a result, fear extinction was successfully enhanced (Ai, Chen, Liu, He, Xue, Bao et al, 2015;Hauner, Howard, Zelano, & Gottfried, 2013;He, Sun, Li, Zhang, Shi, Ai et al, 2015). Furthermore, studies found associations between sleep spindles and the consolidation of emotional information (Cairney, Durrant, Jackson, & Lewis, 2014b;Kaestner, Wixted, & Mednick, 2013). Moreover, in another study, Cairney and colleagues (2015) showed a positive relationship between the proportion of SWS and memory consolidation of unpleasant pictures.…”

Exploring the nap paradox: are mid-day sleep bouts a friend or foe?

“…Although originally implicated in procedural learning, sleep spindles have been linked with the consolidation of a host of memory types, including emotional and declarative memory. For example, higher spindle activity in a mid-day nap was linked to enhanced consolidation of an associative task [17] and was also shown to moderate emotional memory consolidation [73]. In preschool-aged children, we demonstrated that higher spindle density in habitual nappers was correlated with enhanced consolidation of a visuo-spatial task [31].…”

Sleep’s impact on emotional memory: A meta-analysis of whole-night, nap, and REM sleep effects

“…Despite these converging findings, several studies failed to establish associations between REMS physiology and emotional memory performance [33][34][35][36], leaving ambiguities regarding the role of REMS in emotional memory consolidation. Critically, a considerable number of studies did not even replicate selective retention benefits of emotional memories across sleep [37][38][39].…”