Effect of cognitive load on time spent offline during wakefulness.

Humans continuously alternate between online attention to the current environment and offline attention to internally generated thought and imagery. This may be a fundamental feature of the waking brain, but remains poorly understood. Here, we took a data-driven approach to defining online and offline states of wakefulness, using machine learning methods applied to measures of sensory responsiveness, subjective report, electroencephalogram (EEG), and pupil diameter. We tested the effect of cognitive load on the structure and prevalence of online and offline states, hypothesizing that time spent offline would increase as cognitive load of an ongoing task decreased. We also expected that alternation between online and offline states would persist even in the absence of a cognitive task. As in prior studies, we arrived at a three-state model comprised of one online state and two offline states. As predicted, when cognitive load was high, more time was spent online. Also as predicted, the same three states were present even when participants were not performing a task. These observations confirm our method is successful at isolating seconds-long periods of offline time. Varying cognitive load may be a useful way to manipulate time spent in at least one of these offline states in future experimental studies.

Consolidation of emotional memory during waking rest depends on trait anxiety.

A short period of eyes-closed waking rest improves long-term memory for recently learned information, including declarative, spatial, and procedural memory. However, the effect of rest on emotional memory consolidation remains unknown. This preregistered study aimed to establish whether post-encoding rest affects emotional memory and how anxiety levels might modulate this effect. Participants completed a modified version of the dot-probe attention task that involved reacting to and encoding word stimuli appearing underneath emotionally negative or neutral photos. We tested the effect of waking rest on memory for these words and pictures by manipulating the state that participants entered just after this task (rest vs. active wake). Trait anxiety levels were measured using the State-Trait Anxiety Inventory and examined as a covariate. Waking rest improved emotional memory consolidation for individuals high in trait anxiety. These results suggest that the beneficial effect of waking rest on memory extends into the emotional memory domain but depends on individual characteristics such as anxiety.

Memory Consolidation during Ultra-short Offline States.

Traditionally, neuroscience and psychology have studied the human brain during periods of "online" attention to the environment, while participants actively engage in processing sensory stimuli. However, emerging evidence shows that the waking brain also intermittently enters an "offline" state, during which sensory processing is inhibited and our attention shifts inward. In fact, humans may spend up to half of their waking hours offline [Wamsley, E. J., & Summer, T. Spontaneous entry into an "offline" state during wakefulness: A mechanism of memory consolidation? Journal of Cognitive Neuroscience, 32, 1714-1734, 2020; Killingsworth, M. A., & Gilbert, D. T. A wandering mind is an unhappy mind. Science, 330, 932, 2010]. The function of alternating between online and offline forms of wakefulness remains unknown. We hypothesized that rapidly switching between online and offline states enables the brain to alternate between the competing demands of encoding new information and consolidating already-encoded information. A total of 46 participants (34 female) trained on a memory task just before a 30-min retention interval, during which they completed a simple attention task while undergoing simultaneous high-density EEG and pupillometry recording. We used a data-driven method to parse this retention interval into a sequence of discrete online and offline states, with a 5-sec temporal resolution. We found evidence for three distinct states, one of which was an offline state with features well-suited to support memory consolidation, including increased EEG slow oscillation power, reduced attention to the external environment, and increased pupil diameter (a proxy for increased norepinephrine). Participants who spent more time in this offline state following encoding showed improved memory at delayed test. These observations are consistent with the hypothesis that even brief, seconds-long entry into an offline state may support the early stages of memory consolidation.

'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.

Effect of postlearning meditation on memory consolidation: level of focused attention matters.

Recent studies demonstrate that eyes-closed rest benefits memory consolidation, perhaps due to reduced attention to environmental stimuli. Here, we asked whether focusing attention to internal thoughts and feelings after learning similarly blocks memory consolidation. Verbal memory was tested following an eyes-closed consolidation period filled with either focused attention to breath or quiet rest. Although breath-focus did not impair memory relative to quiet rest overall, participants who reported being more successful in maintaining breath-focus during this condition showed increased forgetting. We interpret these findings as incompatible with a simple sensory-interference-based account of rest's effect on memory.

Spontaneous Entry into an "Offline" State during Wakefulness: A Mechanism of Memory Consolidation?

Moments of inattention to our surroundings may be essential to optimal cognitive functioning. Here, we investigated the hypothesis that humans spontaneously switch between two opposing attentional states during wakefulness-one in which we attend to the external environment (an "online" state) and one in which we disengage from the sensory environment to focus our attention internally (an "offline" state). We created a data-driven model of this proposed alternation between "online" and "offline" attentional states in humans, on a seconds-level timescale. Participants (n = 34) completed a sustained attention to response task while undergoing simultaneous high-density EEG and pupillometry recording and intermittently reporting on their subjective experience. "Online" and "offline" attentional states were initially defined using a cluster analysis applied to multimodal measures of (1) EEG spectral power, (2) pupil diameter, (3) RT, and (4) self-reported subjective experience. We then developed a classifier that labeled trials as belonging to the online or offline cluster with >95% accuracy, without requiring subjective experience data. This allowed us to classify all 5-sec trials in this manner, despite the fact that subjective experience was probed on only a small minority of trials. We report evidence of statistically discriminable "online" and "offline" states matching the hypothesized characteristics. Furthermore, the offline state strongly predicted memory retention for one of two verbal learning tasks encoded immediately prior. Together, these observations suggest that seconds-timescale alternation between online and offline states is a fundamental feature of wakefulness and that this may serve a memory processing function.

Dreaming of a learning task is associated with enhanced memory consolidation: Replication in an overnight sleep study.

Sleep following learning benefits memory. One model attributes this effect to the iterative "reactivation" of memory traces in the sleeping brain, demonstrated in animal models. Although technical limitations prohibit using the same methods to observe memory reactivation in the human brain, the study of mental activity during sleep provides an alternative method of observing memory activation during sleep. In fact, the content of dream experience may reflect the process of memory reactivation and consolidation in the sleeping brain. In line with this hypothesis, we previously reported that dreaming about a spatial learning task during a nap strongly predicts subsequent performance improvements. Here, we replicate this observation in an overnight sleep study, for the first time demonstrating that pre-sleep training on a virtual maze navigation task is reflected in dreams reported from all phases of sleep, with unambiguous representation of the task in dream content associated with improved next-morning performance. These observations are consistent with reactivation-based models of memory consolidation in sleep, confirming our earlier finding that the cognitive-level activation of recent experience during sleep is associated with subsequent performance gains.

A brief period of eyes-closed rest enhances motor skill consolidation.

Post-training sleep benefits both declarative and procedural memory consolidation. However, recent research suggests that eyes-closed waking rest may provide a similar benefit. Brokaw et al. (2016), for example, recently demonstrated that verbal declarative memory improved more following a 15 min period of waking rest, in comparison to 15 min of active wake. Here, we used the same procedures to test whether procedural memory similarly benefits from waking rest. Participants were trained on the Motor Sequence Task (MST), followed by a 15 min retention interval during which they either rested with their eyes closed or completed a distractor task. Rest significantly enhanced MST performance, mirroring the effect observed in Brokaw et al. (2016) and demonstrating that waking rest benefits the early stages of procedural memory. An additional group of participants tested 4 h later displayed no effect of rest. Overall, these results suggest that the early MST performance "boost" described in prior studies may depend on post-learning state.

The impact of sleep on novel concept learning.

Prior research demonstrates that sleep benefits memory consolidation. But beyond its role in memory retention, sleep may also facilitate the reorganization and flexible use of new information. In the present study, we investigated the effect of sleep on conceptual knowledge. Participants classified abstract dot patterns into novel categories, and were later tested on both previously seen dot patterns as well as on new patterns. A Wake group (n=17) trained at 9AM, continued with their daily activities, and then tested at 9PM that evening. A Sleep group (n=20) trained at 9PM, went home to sleep, and was tested the following morning at 9AM. Two Immediate Test control groups completed testing immediately following training in either the morning (n=18) or evening (n=18). Post-training sleep led to superior classification of all stimulus types, including the specific exemplars learned during training, novel patterns that had not previously been seen, and "prototype" patterns from which the exemplars were derived. However, performance did not improve significantly above baseline after a night of sleep. Instead, sleep appeared to maintain performance, relative to a performance decline across a day of wakefulness. There was additionally evidence of a time of day effect on performance. Together with prior observations, these data support the notion that sleep may be involved in an important process whereby we extract commonalities from our experiences to construct useful mental models of the world around us.

Resting state EEG correlates of memory consolidation.

Numerous studies demonstrate that post-training sleep benefits human memory. At the same time, emerging data suggest that other resting states may similarly facilitate consolidation. In order to identify the conditions under which non-sleep resting states benefit memory, we conducted an EEG (electroencephalographic) study of verbal memory retention across 15min of eyes-closed rest. Participants (n=26) listened to a short story and then either rested with their eyes closed, or else completed a distractor task for 15min. A delayed recall test was administered immediately following the rest period. We found, first, that quiet rest enhanced memory for the short story. Improved memory was associated with a particular EEG signature of increased slow oscillatory activity (<1Hz), in concert with reduced alpha (8-12Hz) activity. Mindwandering during the retention interval was also associated with improved memory. These observations suggest that a short period of quiet rest can facilitate memory, and that this may occur via an active process of consolidation supported by slow oscillatory EEG activity and characterized by decreased attention to the external environment. Slow oscillatory EEG rhythms are proposed to facilitate memory consolidation during sleep by promoting hippocampal-cortical communication. Our findings suggest that EEG slow oscillations could play a significant role in memory consolidation during other resting states as well.

Negative reinforcement impairs overnight memory consolidation.

Post-learning sleep is beneficial for human memory. However, it may be that not all memories benefit equally from sleep. Here, we manipulated a spatial learning task using monetary reward and performance feedback, asking whether enhancing the salience of the task would augment overnight memory consolidation and alter its incorporation into dreaming. Contrary to our hypothesis, we found that the addition of reward impaired overnight consolidation of spatial memory. Our findings seemingly contradict prior reports that enhancing the reward value of learned information augments sleep-dependent memory processing. Given that the reward followed a negative reinforcement paradigm, consolidation may have been impaired via a stress-related mechanism.

Dreaming and offline memory consolidation.

Converging evidence suggests that dreaming is influenced by the consolidation of memory during sleep. Following encoding, recently formed memory traces are gradually stabilized and reorganized into a more permanent form of long-term storage. Sleep provides an optimal neurophysiological state to facilitate this process, allowing memory networks to be repeatedly reactivated in the absence of new sensory input. The process of memory reactivation and consolidation in the sleeping brain appears to influence conscious experience during sleep, contributing to dream content recalled on awakening. This article outlines several lines of evidence in support of this hypothesis, and responds to some common objections.

A meta-analysis of the relation between dream content and memory consolidation.

The frequent appearance of newly learned information in dreams suggests that dream content is influenced by memory consolidation. Many studies have tested this hypothesis by asking whether dreaming about a learning task is associated with improved memory, but results have been inconsistent. We conducted a meta-analysis to determine the strength of the association between learning-related dreams and post-sleep memory improvement. We searched the literature for studies that (1) trained participants on a pre-sleep learning task and then tested their memory after sleep, and (2) associated post-sleep memory improvement with the extent to which dreams incorporated learning task content. Sixteen studies qualified for inclusion, which together reported 45 effects. Integrating across effects, we report a strong and statistically significant association between task-related dreaming and memory performance (SMD = 0.51 [95% CI 0.28, 0.74], p < 0.001). Among studies using polysomnography, this relationship was statistically significant for dreams collected from non-rapid eye movement (NREM) sleep (n = 10) but not for dreams collected from rapid eye movement (REM) sleep (n = 12). There was a significant association between dreaming and memory for all types of learning tasks studied. This meta-analysis provides further evidence that dreaming about a learning task is associated with improved memory performance, suggesting that dream content may be an indication of memory consolidation. Furthermore, we report preliminary evidence that the relationship between dreaming and memory may be stronger in NREM sleep compared to REM.

Constructive episodic simulation in dreams.

Memories of the past help us adaptively respond to similar situations in the future. Originally described by Schacter & Addis in 2007, the "constructive episodic simulation" hypothesis proposes that waking thought combines fragments of various past episodes into imagined simulations of events that may occur in the future. This same framework may be useful for understanding the function of dreaming. N = 48 college students were asked to identify waking life sources for a total of N = 469 dreams. Participants frequently traced dreams to at least one past or future episodic source (53.5% and 25.7% of dreams, respectively). Individual dreams were very often traced to multiple waking sources (43.9% of all dreams with content), with fragments of past memory incorporated into scenarios that anticipated future events. Waking-life dream sources are described in terms of their phenomenology and distribution across time and sleep stage, providing new evidence that dreams not only reflect the past, but also utilize memory in simulating potential futures.

Sleep spindle activity is associated with the integration of new memories and existing knowledge.

Sleep spindle activity has been associated with improvements in procedural and declarative memory. Here, for the first time, we looked at the role of spindles in the integration of newly learned information with existing knowledge, contrasting this with explicit recall of the new information. Two groups of participants learned novel spoken words (e.g., cathedruke) that overlapped phonologically with familiar words (e.g., cathedral). The sleep group was exposed to the novel words in the evening, followed by an initial test, a polysomnographically monitored night of sleep, and a second test in the morning. The wake group was exposed and initially tested in the morning and spent a retention interval of similar duration awake. Finally, both groups were tested a week later at the same circadian time to control for possible circadian effects. In the sleep group, participants recalled more words and recognized them faster after sleep, whereas in the wake group such changes were not observed until the final test 1 week later. Following acquisition of the novel words, recognition of the familiar words was slowed in both groups, but only after the retention interval, indicating that the novel words had been integrated into the mental lexicon following consolidation. Importantly, spindle activity was associated with overnight lexical integration in the sleep group, but not with gains in recall rate or recognition speed of the novel words themselves. Spindle activity appears to be particularly important for overnight integration of new memories with existing neocortical knowledge.

A brief nap is beneficial for human route-learning: The role of navigation experience and EEG spectral power.

Here, we examined the effect of a daytime nap on changes in virtual maze performance across a single day. Participants either took a short nap or remained awake following training on a virtual maze task. Post-training sleep provided a clear performance benefit at later retest, but only for those participants with prior experience navigating in a three-dimensional (3D) environment. Performance improvements in experienced players were correlated with delta-rich stage 2 sleep. Complementing observations that learning-related brain activity is reiterated during post-navigation NREM sleep in rodents, the present data demonstrate that NREM sleep confers a performance advantage for spatial memory in humans.

Cognitive replay of visuomotor learning at sleep onset: temporal dynamics and relationship to task performance.

STUDY OBJECTIVES: Studies of neural activity in animals and humans suggest that experiences are "replayed" in cortical and hippocampal networks during NREM sleep. Here, we examine whether memory reactivation in sleeping humans might also be evident within reports of concomitant subjective experience (i.e., dreaming). DESIGN: Participants were trained on an engaging visuomotor learning task across a period of one or more days, and sleep onset mentation was collected at variable intervals using the "Nightcap" home-monitoring device. Verbal reports of sleep onset mentation were obtained either at the beginning of the night, or following 2 h of initial sleep. SETTING: Data were collected in participants' home environments, via the Nightcap monitoring system, and at The Center for Sleep and Cognition, Beth Israel Deaconess Medical Center, Boston MA. PARTICIPANTS: 43 healthy, medication-free college students (16 males, age 18-25 years). INTERVENTIONS: N/A. MEASUREMENTS AND RESULTS: The learning task exerted a powerful, direct effect on verbal reports of mentation during light NREM sleep (stages 1 and 2). On post-training nights, a full 30% of all verbal reports were related to the task. The nature of this cognitive "replay" effect was altered with increasing durations of sleep, becoming more abstracted from the original experience as time into sleep increased. CONCLUSIONS: These observations are interpreted in light of memory consolidation theory, and demonstrate that introspective reports can provide a valuable window on cognitive processing in the sleeping brain.

How the brain constructs dreams.

Deep inside the temporal lobe of the brain, the hippocampus has a central role in our ability to remember, imagine and dream.

Does sleep protect memories against interference? A failure to replicate.

Across a broad spectrum of memory tasks, retention is superior following a night of sleep compared to a day of wake. However, this result alone does not clarify whether sleep merely slows the forgetting that would otherwise occur as a result of information processing during wakefulness, or whether sleep actually consolidates memories, protecting them from subsequent retroactive interference. Two influential studies suggested that sleep protects memories against the subsequent retroactive interference that occurs when participants learn new yet overlapping information (interference learning). In these studies, interference learning was much less detrimental to memory following a night of sleep compared to a day of wakefulness, an indication that sleep supports this important aspect of memory consolidation. In the current replication study, we repeated the protocol of and, additionally, we examined the impact of intrinsic motivation on performance in sleep and wake participants. We were unable to replicate the finding that sleep protects memories against retroactive interference, with the detrimental effects of interference learning being essentially the same in wake and sleep participants. We also found that while intrinsic motivation benefitted task acquisition it was not a modulator of sleep-wake differences in memory processing. Although we cannot accept the null hypothesis that sleep has no role to play in reducing the negative impact of interference, the findings draw into question prior evidence for sleep's role in protecting memories against interference. Moreover, the current study highlights the importance of replicating key findings in the study of sleep's impact on memory processing before drawing strong conclusions that set the direction of future research.

The expression of trace conditioning during non-REM sleep and its relation to subjective experience.

Research in animals has demonstrated that patterns of neural activity first seen during waking experience are later "replayed" during sleep, in hippocampal and cortical networks. The characteristics of memory reactivation during human sleep, however, have not yet been fully described. Meanwhile, the possible relationship of dreaming to this "replay" of memories in the sleeping brain is entirely unknown. In the present study, we induced hippocampus-dependent memory retrieval during human sleep using a "trace conditioning" procedure. Prior to sleep, subjects underwent either trace (hippocampus-dependent) or delay (hippocampus-independent) auditory fear conditioning. Conditioned stimuli were then presented to subjects during non-REM sleep. Both delay-conditioned and trace-conditioned subjects exhibited conditioned EEG responses during post-training sleep. However, selectively in trace-conditioned subjects, fear-conditioned cues also affected the valence of dreamed emotions. These findings suggest that hippocampus-dependent learning is accessible during non-REM sleep, and that hippocampus-mediated memory reactivation may be expressed, not only through neural activity in the sleeping brain, but also within concomitant subjective experience.