Napping and the selective consolidation of negative aspects of scenes.

Abstract

After information is encoded into memory, it undergoes an offline period of consolidation that occurs optimally during sleep. The consolidation process not only solidifies memories, but also selectively preserves aspects of experience that are emotionally salient and relevant for future use. Here, we provide evidence that an afternoon nap is sufficient to trigger preferential memory for emotional information contained in complex scenes. Selective memory for negative emotional information was enhanced after a nap compared to wakefulness in two control conditions designed to carefully address interference and time-of-day confounds. Although prior evidence has connected negative emotional memory formation to rapid eye movement (REM) sleep physiology, we found that non-REM delta activity and the amount of slow wave sleep (SWS) in the nap were robustly related to the selective consolidation of negative information. These findings suggest that the mechanisms underlying memory consolidation benefits associated with napping and nighttime sleep are not always the same. Finally, we provide preliminary evidence that the magnitude of the emotional memory benefit conferred by sleep is equivalent following a nap and a full night of sleep, suggesting that selective emotional remembering can be economically achieved by taking a nap.

The differential effects of emotional salience on direct associative and relational memory during a nap

“…More specifically, we predicted that because of the emotional salience of the negative pairs, sleep would preferentially benefit these associations over neutral pairs and promote greater relational associations for faces related through negative objects. We did not predict group differences for neutral information, consistent with previous findings using intermixed negative and neutral stimuli (e.g., Payne et al, 2015;Payne et al, 2008). We also hypothesized that REM sleep, specifically, would benefit memory for the pairs associated with negative objects, and particularly for relational memory formation, based on prior literature demonstrating a role for REM sleep in both emotional memory consolidation (e.g., Nishida et al, 2009;Payne et al, 2015;Wagner et al, 2001), and memory reorganization (e.g., Landmann et al, 2015).…”

“…When we originally considered predictions about how adding emotional salience to the A-B/B-C task would impact memory and interact with sleep-based consolidation processes, we first reflected on previous work from our lab demonstrating selective preservation of emotional components of scenes in the emotional memory trade-off task (Payne et al, 2008;Payne & Kensinger, 2011;Payne et al, 2015). In these experiments, emotional objects are better remembered than neutral objects, but at the expense of memory for neutral information in the background, and sleep magnifies this trade-off effect, boosting memory specifically for the emotional images.…”

“…We anticipated one of two possible outcomes to pairing negative and neutral stimuli together in our study, using an A-B, B-C design, as described above. Previous evidence from our lab examining memory for complex emotional stimuli has found that, even within stimuli, memory for emotionally salient components is enhanced, but at the expense of memory for the neutral contextual details, an effect known as the emotional memory trade-off effect (Kensinger, Garoff-Eaton, & Schacter, 2006;Kensinger, 2009;Payne & Kensinger, 2010;Payne et al, 2015;Payne, Stickgold, Swanberg, & Kensinger, 2008). A real-life example of this effect is the weapon-focus effect (Loftus, Loftus, & Messo, 1987), in which the victims of a robbery report superior memory for the details of the weapon that had been present, but at the expense for memory for the face of the assailant.…”

“…Sleep has been repeatedly shown to preferentially benefit emotional memories over neutral ones (Hu, Stylos-Allan, & Walker, 2006;Nishida, Pearsall, Buckner, & Walker, 2009;Payne & Kensinger, 2010;Wagner, Gais, & Born, 2001), although evidence of this effect is not conclusive (Baran, Pace-Schott, Ericson, & Spencer, 2012), as well as to selectively benefit the emotional components of a memory over the neutral contextual details (Cunningham et al, 2014;Payne, Chambers, & Kensinger, 2012;Payne et al, 2015;Payne et al, 2008). REM sleep, specifically oscillations in the theta frequency range, has been most often linked to emotional memory consolidation (Nishida et al, 2009).…”

Setting the alarm: Word emotional attributes require consolidation to be operational.

“…Sleep is known to specifically promote consolidation of emotionally salient memories (for reviews, see Goldstein & Walker, 2014;Payne & Kensinger, 2010 Kensinger (2008), sleep modifies emotional memories by enhancing the negative aspects of the scene (e.g., a damaged car) at the expense of its neutral aspects (e.g., pedestrians on the pavement; see also Cunningham et al, 2014;Payne, Chambers, & Kensinger, 2012;Payne et al, 2015). In view of this overnight memory trade-off, a straightforward prediction is that negative memories should be even more negative once sleep has occurred.…”