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1. Spontaneous Entry into an “Offline” State during Wakefulness: A Mechanism of Memory Consolidation?

   https://doi.org/10.1162/jocn_a_01587  

   Wamsley, Erin J.; Summer, Theodore (September 2020, Journal of Cognitive Neuroscience)

   null (Ed.)

   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. 

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2. Effect of cognitive load on time spent offline during wakefulness

   https://doi.org/10.1093/cercor/bhae022  

   Wamsley, Erin_J; Collins, Megan (January 2024, Cerebral Cortex)

   Abstract 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. 

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

   https://doi.org/10.1101/lm.053330.120  

   Wang, Serene Y.; Baker, Kirsten C.; Culbreth, Jessica L.; Tracy, Olivia; Arora, Madison; Liu, Tingtong; Morris, Sydney; Collins, Megan B.; Wamsley, Erin J. (May 2021, Learning & 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. 

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4. Spontaneous slow oscillation—slow spindle features predict induced overnight memory retention

   https://doi.org/10.1093/sleep/zsab127  

   Dehnavi, Fereshteh; Koo-Poeggel, Ping Chai; Ghorbani, Maryam; Marshall, Lisa (May 2021, Sleep)

   Abstract Study Objectives Synchronization of neural activity within local networks and between brain regions is a major contributor to rhythmic field potentials such as the EEG. On the other hand, dynamic changes in microstructure and activity are reflected in the EEG, for instance slow oscillation (SO) slope can reflect synaptic strength. SO-spindle coupling is a measure for neural communication. It was previously associated with memory consolidation, but also shown to reveal strong interindividual differences. In studies, weak electric current stimulation has modulated brain rhythms and memory retention. Here, we investigate whether SO-spindle coupling and SO slope during baseline sleep are associated with (predictive of) stimulation efficacy on retention performance. Methods Twenty-five healthy subjects participated in three experimental sessions. Sleep-associated memory consolidation was measured in two sessions, in one anodal transcranial direct current stimulation oscillating at subjects individual SO frequency (so-tDCS) was applied during nocturnal sleep. The third session was without a learning task (baseline sleep). The dependence on SO-spindle coupling and SO-slope during baseline sleep of so-tDCS efficacy on retention performance were investigated. Results Stimulation efficacy on overnight retention of declarative memories was associated with nesting of slow spindles to SO trough in deep nonrapid eye movement baseline sleep. Steepness and direction of SO slope in baseline sleep were features indicative for stimulation efficacy. Conclusions Findings underscore a functional relevance of activity during the SO up-to-down state transition for memory consolidation and provide support for distinct consolidation mechanisms for types of declarative memories. 

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5. Replay-based consolidation governs enduring memory storage

   Paller, Ken A; Mayes, Andrew R; Antony, James W; Norman, Ken A (January 2020, The Cognitive Neurosciences, Sixth Edition, MIT Press.)

   null; Mangun, G.R.; Gazzaniga, M.S. (Ed.)

   The human ability to remember unique experiences from many years ago comes so naturally that we often take it for granted. It depends on three stages: (1) encoding, when new information is initially registered, (2) storage, when encoded information is held in the brain, and (3) retrieval, when stored information is used. Historically, cognitive neuroscience studies of memory have emphasized encoding and retrieval. Yet, the intervening stage may hold the most intrigue, and has become a major research focus in the years since the last edition of this book. Here we describe recent investigations of post-acquisition memory processing in relation to enduring storage. This evidence of memory processing belies the notion that memories stored in the brain are held in stasis, without changing. Various methods for influencing and monitoring brain activity have been applied to study offline memory processing. In particular, memories can be reactivated during sleep and during resting periods, with distinctive physiological correlates. These neural signals shed light on the contribution of hippocampal-neocortical interactions to memory consolidation. Overall, results converge on the notion that memory reactivation is a critical determinant of systems-level consolidation, and thus of future remembering, which in turn facilitates future planning and problem solving. 

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