‘Sleep-dependent’ memory consolidation? Brief periods of post-training rest and sleep provide an equivalent benefit for both declarative and procedural memory

Sleep following learning facilitates the consolidation of memories. This effect has often been attributed to sleep-specific factors, such as the presence of sleep spindles or slow waves in the electroencephalogram (EEG). However, recent studies suggest that simply resting quietly while awake could confer a similar memory benefit. In the current study, we examined the effects of sleep, quiet rest, and active wakefulness on the consolidation of declarative and procedural memory. We hypothesized that sleep and eyes-closed quiet rest would both benefit memory compared with a period of active wakefulness. After completing a declarative and a procedural memory task, participants began a 30-min retention period with PSG (polysomnographic) monitoring, in which they either slept (n = 24), quietly rested with their eyes closed (n = 22), or completed a distractor task (n = 29). Following the retention period, participants were again tested on their memory for the two learning tasks. As hypothesized, sleep and quiet rest both led to better performance on the declarative and procedural memory tasks than did the distractor task. Moreover, the performance advantages conferred by rest were indistinguishable from those of sleep. These data suggest that neurobiology specific to sleep might not be necessary to induce the consolidation of memory, at least across very short retention intervals. Instead, offline memory consolidation may function opportunistically, occurring during either sleep or stimulus-free rest, provided a favorable neurobiological milieu and sufficient reduction of new encoding.

Of the myriad new experiences we encode each day, only a fraction are remembered over the long-term. The formation of long-term memory is crucial for optimal functioning in our everyday lives and for building knowledge across days, weeks, and years. Such enduring memories require not only the effective encoding of new information, but also a set of postencoding processes, termed “consolidation,” that function to stabilize and transform new memory traces over time (McGaugh 2000; Frankland and Bontempi 2005; Genzel and Wixted 2017).Consolidation of memory is better supported by some states of consciousness than others. For example, sleep has long been known to optimize memory consolidation, purportedly due to specific neurobiology that actively promotes the consolidation process (Diekelmann and Born 2010). Numerous studies have demonstrated that sleep facilitates the consolidation of both declarative and procedural memories. Slow oscillations (Huber et al. 2004; Marshall et al. 2006) and slow wave sleep (SWS) (Alger et al. 2012; Diekelmann et al. 2012) are thought to especially benefit hippocampus-dependent, declarative memory. Meanwhile, various forms of implicit and procedural memory have been linked to rapid eye movement (REM) sleep (Plihal and Born 1997; Mednick et al. 2009) or non-REM stage 2 (N2) sleep (Walker et al. 2002; Tucker and Fishbein 2009).A potential mechanism of offline memory consolidation during sleep is memory “reactivation,” in which patterns of neural activity in the hippocampus and cortex associated with awake experience are reiterated after learning. For example, when rats sleep after being trained on a spatial learning task, hippocampal “place cells” fire again in the same order as when the animals were being trained on the task during wake (Lee and Wilson 2002; Ji and Wilson 2007). Such neural reactivation not only occurs in the hippocampus, but also concurrently in a variety of cortical areas (Ji and Wilson 2007; Peyrache et al. 2009; Kaefer et al. 2020). The recent advent of optogenetics has allowed experimental investigation of memory reactivation in animal models. Experimentally disrupting the hippocampal ripple oscillations during which reactivation occurs impairs memory (Girardeau et al. 2009; Ego-Stengel and Wilson 2010). Conversely, selectively reactivating neural ensembles related to a particular memory appears to induce consolidation, particularly when this manipulation is applied during sleep or light amnesia (de Sousa et al. 2019).But is sleep the only brain state that facilitates memory consolidation in this way? It has been argued that sleep-specific neurobiology, including sleep slow waves (Alger et al. 2012), sleep spindles (Wamsley et al. 2012; Mednick et al. 2013; Laventure et al. 2016), and/or REM sleep (Karni et al. 1994; Stickgold et al. 2000; McDevitt et al. 2015; Boyce et al. 2016), is required for offline memory reactivation and consolidation to occur, or at least to occur optimally. However, a growing body of literature indicates that stimulus-free waking rest can similarly facilitate consolidation (Wamsley 2019). In two influential experiments, Dewar et al. (2012) demonstrated that compared with participants who completed a nonverbal distractor task, those who rested quietly with their eyes closed in a darkened room for 10 min after learning showed better memory for short stories encoded prior to the retention period. The rest group significantly outperformed the wake group after 15 min, 30 min, and 7 d (experiment 1), even in the absence of retrieval practice during the 7-d period (experiment 2).This effect of post-training rest on memory retention has been reported in an increasing number of papers across the last decade (Gottselig et al. 2004; Mercer 2015; Martini et al. 2018; Wamsley 2019; Martini and Sachse 2020). Brokaw et al. (2016) replicated the behavioral observations of Dewar et al. (2012) and showed that this memory benefit was associated with EEG slow oscillation activity, which is thought to facilitate hippocampal–cortical communication and concomitant memory consolidation during sleep (Marshall et al. 2006; Mölle and Born 2011). A recent study by Sattari et al. (2019) also linked improved memory performance to waking EEG slow oscillations, suggesting that the memory-enhancing effects of rest and sleep may share a common mechanism.Of course, it has been known for decades that at least some consolidation must occur during wakefulness. Local, cellular level consolidation begins to stabilize memory immediately following encoding (Bailey and Kandel 2008; Redondo and Morris 2011), enabling us to recall the events of the previous hours in the absence of intervening sleep. The novel suggestion of these more recent studies is that consolidation does not occur equivalently during all types of wakefulness (Dewar et al. 2012; Brokaw et al. 2016). Instead, stimulus-free rest periods appear to have features that are especially suited to facilitate memory.Reduced sensory processing during eyes-closed rest may be one factor accounting for the memory facilitation effect. However, even internally generated stimuli can also function to block consolidation, as demonstrated by the fact that mental tasks such as retrieval of autobiographical memory and focused meditation are also associated with a reduction in rest''s memory benefit (Craig et al. 2014; Collins and Wamsley 2020). Similarly, we reported in two previous studies that individuals with a high propensity for daydreaming show less memory benefit following a period of rest, presumably because intense internally generated mental activity inhibits consolidation (Humiston et al. 2019; Wamsley and Summer 2020).Together, these observations suggest that consolidation occurs during wakefulness when sensory processing is reduced, when low-frequency EEG oscillations are increased, and when internally generated cognition is at a minimum. Therefore, consolidation may not depend on neural mechanisms specific to sleep, instead opportunistically occurring across multiple states of consciousness whenever the correct conditions are met (Mednick et al. 2011). According to the opportunistic theory of memory consolidation, the processes of encoding and consolidation are mutually exclusive: During any brain state in which we are not currently encoding new information, existing memories consolidate as the neural milieu becomes favorable (Mednick et al. 2011; Wamsley 2019). Unoccupied quiet rest, like sleep, is a state in which the encoding of new stimuli is reduced. In addition, quiet rest and sleep also share a number of neurobiological features that are thought to actively promote memory consolidation, including overall slower EEG in comparison with active wakefulness, increased activation of default-mode network brain structures (Buckner and Vincent 2007), and decreased levels of acetylcholine in the brain (Hasselmo and McGaughy 2004). Additionally, the cellular-level offline reactivation of memory occurs not only during sleep, but also during quiet rest (Foster and Wilson 2006; Karlsson and Frank 2009; Carr et al. 2011; Staresina et al. 2013). At the same time, it must be noted that eyes-closed rest does not replicate all aspects of sleep neurobiology proposed to facilitate memory. For example, sleep spindle oscillations and sleep-specific neurohormonal changes are not present during eyes-closed rest.While sleep and rest both benefit memory in comparison with active wakefulness, it is not known whether they do so equivalently. With few studies directly comparing the size of rest''s memory benefit with that of sleep, it remains possible that sleep provides some benefit above and beyond that conferred by waking rest. The limited number of prior studies in this area have shown mixed results. As opposed to the type of truly task-free condition used in the waking rest studies reviewed above, most experiments comparing active wakefulness, rest, and sleep have used a “rest” condition in which participants are asked to complete an undemanding activity such as listening to music or books on tape. This approach sacrifices complete sensory restriction in return for allowing rest condition participants to maintain wakefulness for longer periods of time. For example, Mednick and colleagues have used quiet rest conditions in which participants listen to music or audiobooks, finding that this form of quiet rest facilitates memory equivalently to sleep for some forms of learning (Mednick et al. 2009; Sattari et al. 2019), but not for others (Mednick et al. 2002; McDevitt et al. 2014). Keeping rest participants awake via verbal instructions to alternately open and close their eyes, Simor et al. (2018) found no effect of post-training rest or sleep on performance of a serial reaction time task, relative to an active wake control. While these observations might indicate that only selected forms of memory can be consolidated during resting wakefulness, it is possible that the encoding of meaningful auditory stimuli during these rest conditions prevents optimal consolidation.Only a few prior studies have compared the memory effects of sleep with those of an equivalent duration of eyes-closed, entirely task-free rest. For example, Gottselig et al. (2004) successfully compared the effects of sleep, quiet rest, and active wakefulness on memory consolidation using a carefully controlled rest condition without any stimuli presented to the participants. Using a statistical auditory sequence learning task, they reported that both sleep and rest equivalently facilitated retention. In contrast, using a declarative memory task, Piosczyk et al. (2013) found that neither quiet rest nor sleep improved memory more than active wakefulness. A recent study from our own laboratory directly compared sleep, rest, and active wakefulness using declarative and procedural tasks commonly used in studies of sleep and memory (Tucker et al. 2020). However, high rates of attrition (due to rest participants inadvertently falling asleep and sleep participants failing to obtain sleep) prevented a robust test of our hypothesis that sleep and quiet rest would equivalently benefit memory, relative to active wakefulness.The goal of the current study was to directly compare the memory benefit of a brief nap (<30 min) with that of an equivalent duration of task-free quiet rest. We hypothesized that a brief period of sleep and quiet rest would have an equivalent effect on the consolidation of both declarative and procedural memories, significantly boosting memory retention compared with an equivalent duration of active wakefulness. Following our previous work, we expected that memory retention across sleep and quiet rest would be associated with slow oscillation EEG power in the <1-Hz range, but that participants with high trait daydreaming propensity would show less improvement across quiet rest.     

Lights,camera, action: the role of editing and framing on the processing of filmed events

ABSTRACT

Filmmakers use various cinematic techniques in an effort to guide attention to certain aspects of these events. The present study was conducted to investigate how framing and editing can guide viewers’ attention toward character actions during event segmentation. Participants watched and segmented a movie that simultaneously showed two actors engaged in two related activities. Participants watched one of three versions of the movie: Static center version that did not foreground any character; Static off-center version that foregrounding one of the characters, and an edited version with a mix of shots that foregrounding both characters. Participants engaged in an event partonomy task in which they were asked to identify the boundaries between the events that were depicted in the movie. After watching the movie, they were asked to recall the events. The results showed converging evidence between the event segmentation and recall data, which both indicated that cinematic devices affect the perception and memory of the event structure depicted in the film.