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Our ability to recall memories is improved when sleep follows learning, suggesting that sleep facilitates memory consolidation. A number of factors are thought to influence the impact of sleep on newly learned information, such as whether or not we rehearse that information (e.g. via restudy or retrieval practice), or the extent to which the information is consistent with our pre-existing schematic knowledge. In this pre-registered, online study, we examined the effects of both rehearsal and schematic congruency on overnight consolidation. Participants learned noun-colour pairings (e.g. elephant-red) and rated each pairing as plausible or implausible before completing a baseline memory assessment. Afterwards, participants engaged in a period of restudy or retrieval practice for the pairings, and then entered a 12 h retention interval of overnight sleep or daytime wakefulness. Follow-up assessments were completed immediately after sleep or wake, and again 24 h after learning. Our data indicated that overnight consolidation was amplified for restudied relative to retested noun-colour pairings, but only when sleep occurred soon after learning. Furthermore, whereas plausible (i.e. schematically congruent) pairings were generally better remembered than implausible (i.e. schematically incongruent) pairings, the benefits of sleep were stronger for implausible relative to plausible memories. These findings challenge the notion that schema-conformant memories are preferentially strengthened during post-learning sleep.

Overnight consolidation processes are thought to operate in a selective manner, such that important (i.e. future-relevant) memories are strengthened ahead of irrelevant information. Using an online protocol, we sought to replicate the seminal finding that the memory benefits of sleep are enhanced when people expect a future test [Wilhelm et al., 2011]. Participants memorised verbal paired associates to a criterion of 60 percent (Experiment 1) or 40 percent correct (Experiment 2) before a 12-hour delay containing overnight sleep (sleep group) or daytime wakefulness (wake group). Critically, half of the participants were informed that they would be tested again the following day, whereas the other half were told that they would carry out a different set of tasks. We observed a robust memory benefit of overnight consolidation, with the sleep group outperforming the wake group in both experiments. However, knowledge of an upcoming test had no impact on sleep-associated consolidation in either experiment, suggesting that overnight memory processes were not enhanced for future-relevant information. These findings, together with other failed replication attempts, show that sleep does not provide selective support to memories that are deemed relevant for the future.

Auditory closed-loop stimulation has gained traction in recent years as a means of enhancing slow oscillatory activity and, consequently, sleep-associated memory consolidation. Previous studies on this topic have primarily focused on the consolidation of semantically-congruent associations. In this study, we investigated the effect of auditory closed-loop stimulation on the overnight retention of semantically-incongruent associations. Twelve healthy males (age: M=20.06, SD=2.02 years) participated in two experimental conditions (simulation and sham). In the stimulation condition, clicks were delivered in phase with slow oscillation up-states, whereas in the sham condition no auditory stimuli were applied. Corroborating earlier work, stimulation (vs. sham) enhanced the slow oscillation rhythm, phase-coupled spindle activity and slow oscillation power. However, there was no benefit of stimulation on overnight memory retention. These findings suggest that closed-loop stimulation does not benefit semantically-incongruent associations.

We propose a framework in which top-down inhibitory control networks are impaired by sleep deprivation, giving rise to intrusive thoughts and, consequently, emotion dysregulation. This process leads to a vicious cycle of sleeplessness, persistent unwanted thoughts, and heightened anxiety; ultimately increasing the risk of mental illness.

Auditory closed-loop stimulation is a non-invasive technique that has been widely used to augment slow oscillations during non-rapid eye movement sleep. Based on the principles of closed-loop stimulation, we developed a novel protocol for manipulating theta activity (3-7 Hz) in rapid eye movement (REM) sleep. Sixteen healthy young adults were studied in two overnight conditions: Stimulation and Sham. In the Stimulation condition, 1 s of 5 Hz amplitude-modulated white noise was delivered upon detection of two supra-threshold theta cycles throughout REM sleep. In the Sham condition, corresponding time points were marked but no stimulation was delivered. Auditory stimulation entrained EEG activity to 5 Hz and evoked a brief (~0.5 s) increase in theta power. Interestingly, this initial theta surge was immediately followed by a prolonged (~3 s) period of theta suppression. Stimulation also induced a prolonged (~2 s) increase in beta power. Our results provide the first demonstration that the REM sleep theta rhythm can be manipulated in a targeted manner via auditory stimulation. Accordingly, auditory stimulation might offer a fruitful avenue for investigating REM sleep electrophysiology and its relationship to behaviour.

Supplemental material, Harrington_Supplemental_Material for Losing Control: Sleep Deprivation Impairs the Suppression of Unwanted Thoughts by Marcus O. Harrington, Jennifer E. Ashton, Subbulakshmi Sankarasubramanian, Michael C. Anderson and Scott A. Cairney in Clinical Psychological Science

We propose a framework for the memory function of spindle oscillations during sleep. In this framework, memories are reinstated by spindle events, and further reprocessed during subsequent spindle refractory periods. We posit that spindle refractoriness is crucial for protecting memory reprocessing from interference. We further argue that temporally-coordinated spindle refractory periods across local networks facilitate the consolidation of rich, multimodal representations, and that localized spindle refractoriness optimizes oscillatory interactions that support systems consolidation in the sleeping brain.

Retrieval facilitates the long-term retention of memories, but may also enable stored representations to be updated with new information that is available at the time of retrieval. However, if information integrated during retrieval is erroneous, future recall can be impaired: a phenomenon known as retrieval-induced distortion (RID). Whether RID causes an “overwriting” of existing memory traces or leads to the co-existence of original and distorted memory traces is unknown. Because sleep enhances memory consolidation, the effects of sleep after RID can provide novel insights into the structure of updated memories. As such, we investigated the effects of sleep on memory consolidation following RID. Participants encoded word locations and were then tested before (T1) and after (T2) an interval of sleep or wakefulness. At T2, the majority of words were placed closer to the locations retrieved at T1 than to the studied locations, consistent with RID. After sleep compared with after wake, the T2-retrieved locations were closer to both the studied locations and the T1-retrieved locations. These findings suggest that RID leads to the formation of an additional memory trace that corresponds to a distorted variant of the same encoding event, which is strengthened alongside the original trace during sleep. More broadly, these data provide evidence for the importance of sleep in the preservation and adaptive updating of memories.

Study Objectives: Memories are strengthened during sleep. The benefits of sleep for memory can be enhanced by re-exposing the sleeping brain to auditory cues; a technique known as targeted memory reactivation (TMR). Prior studies have not assessed the nature of the retrieval mechanisms underpinning TMR: the matching process between auditory stimuli encountered during sleep and previously encoded memories. We carried out two experiments to address this issue. Methods: In Experiment 1, participants associated words with verbal and non-verbal auditory stimuli before an overnight interval in which subsets of these stimuli were replayed in slow-wave sleep. We repeated this paradigm in Experiment 2 with the single difference that the gender of the verbal auditory stimuli was switched between learning and sleep. Results: In Experiment 1, forgetting of cued (vs. non-cued) associations was reduced by TMR with verbal and non-verbal cues to similar extents. In Experiment 2, TMR with identical non-verbal cues reduced forgetting of cued (vs. non-cued) associations, replicating Experiment 1. However, TMR with non-identical verbal cues reduced forgetting of both cued and non-cued associations. Conclusions: These experiments suggest that the memory effects of TMR are influenced by the acoustic overlap between stimuli delivered at training and sleep. Our findings hint at the existence of two processing routes for memory retrieval during sleep. Whereas TMR with acoustically identical cues may reactivate individual associations via simple episodic matching, TMR with non-identical verbal cues may utilise linguistic decoding mechanisms, resulting in widespread reactivation across a broad category of memories. Keywords: Sleep, Memory, Reactivation

Recent work has suggested that the benefits of sleep for memory consolidation are enhanced for highly salient (vs. non-salient) memories. Using a technique known as targeted memory reactivation (TMR) it is possible to selectively strengthen newly learned memories by re-exposing the sleeping brain to auditory cues. The aim of the current study was to examine whether emotionally salient memories are also more responsive to TMR in slow-wave sleep (SWS) than neutral memories. In an initial training phase participants memorised emotionally negative and neutral pictures, which were each paired with a semantically related sound. Recognition for the pictures was assessed before and after a 90 minute nap opportunity, during which half the sounds were re-presented during SWS (as assessed via online polysomnographic sleep monitoring). We observed no effect of TMR on the recognition of emotionally negative or neutral memories. Our results highlight the importance of the memory paradigm used to assess TMR and suggest that the robust and durable nature of recognition memory may make it an insensitive measure of behavioural TMR benefits. To fully assess the impacts of TMR on emotional memory processing in sleep, future studies should adopt experimental paradigms that maximise the salience of emotional stimuli while also providing a sensitive index of memory accuracy.

Previous research has indicated that emotionally affective memory representations are preferentially consolidated over their neutral counterparts across time and sleep. While compelling, two broad research questions remain unanswered: 1) what are the neural mechanisms underpinning time- and sleep-dependent emotional memory processing and, 2) are focal and contextual elements of emotional and neutral memory influenced in different manners by post-learning sleep? Accordingly, the research described in this thesis makes use of behavioural experimentation, polysomnography (PSG) and functional magnetic resonance imaging (fMRI), with the principal aim of refining contemporary knowledge regarding the mechanisms and specificity of memory consolidation processes occurring over time and sleep. In chapter 2, we used event-related fMRI to compare the neural correlates of emotional image memories that had undergone 1 week (remote memory) or 30 minutes (recent memory) of consolidation. Our findings suggested that remote image memories, irrespective of emotional valence, were more dependent upon neocortical brain regions than recent image memories. In addition, strongly consolidated remote image memories appeared to be more reliant upon the precuneus, whereas weakly consolidated remote image memories were associated with increased activity in several occipital areas. In chapter 3, we used overnight PSG and event-related fMRI to expand upon the findings of chapter 2 and investigate how different stages of post-learning sleep influenced the reorganisation of emotional image memories over 24 hours (remote memory), as compared to 30 minutes (recent memory), of consolidation. We observed a slow-wave sleep (SWS)-related reduction in right hippocampal activity, and rapid eye movement sleep (REM)-related increase in hippocampal-cortical connectivity, associated with the retrieval of negative remote image memories, suggesting a complimentary role of SWS and REM in emotional memory processing. In chapter 4, we investigated how replaying learning associated sounds during diurnal SWS impacted upon the consolidation of emotionally negative and neutral picture-location memories. Our findings indicated that sound re-exposure primed memories for a targeted but dissociative consolidation process, whereby a concomitant enhancement and suppression of respective negative and neutral memories took place during the ensuing SWS period. In chapter 5, we used a napping paradigm with PSG to explore the properties of sleep that play a decisive role in the consolidation of emotionally negative and neutral context memories. The results were suggestive of a paradoxical sleep-dependent mechanism, whereby stage two sleep mediates a strengthening of negative context memories and sleep spindles support a suppression of their neutral counterparts. A potential SWS-related suppression of negative memories however, may have prevented emotion-related memory enhancements from occurring over sleep in the contextual domain. Finally, in chapter 6, we examined how environmental context-dependent memory effects were influenced by a period of post-learning sleep or wakefulness. We observed a sleep-related reduction in the extent to which environmental cues impacted upon retrieval, suggesting that sleep may mediate an active decontextualisation of declarative memories. Overall, these studies have provided new insights regarding the role of time and sleep in emotional and non-emotional memory processing.

Traumatic experiences are associated with increased emotional arousal. Overnight consolidation strengthens the episodic content of emotional memories, but it is still unclear how sleep influences the associated arousal response. To investigate this question, we compared the effects of sleep and wake on psychophysiological and subjective reactivity during emotional memory retrieval. Participants provided affective ratings for negative and neutral images while heart rate deceleration (HRD) and skin conductance responses (SCRs) were monitored. Following a 12-hour delay of sleep or wakefulness, participants completed an image recognition task where HRD, SCRs and affective ratings were recorded again. HRD responses to previously-encoded (“old”) negative images were preserved after sleep but diminished after wakefulness. No between-group difference in HRD was observed for novel negative images at recognition, indicating that the effects of sleep for old images were not driven by a generalised overnight increase in visceral activity, or circadian factors. No significant effects of sleep were observed for SCRs or subjective ratings. Our data suggest that cardiac arousal experienced at the time of encoding is sensitive to plasticity-promoting processes during sleep in a similar manner to episodic aspects of emotional memory.

New vocabulary is consolidated offline, particularly during sleep; however, the parameters that influence consolidation remain unclear. Two experiments investigated effects of exposure level and delay between learning and sleep on adults' consolidation of novel competitors (e.g. BANARA) to existing words (e.g. BANANA). Participants made speeded semantic decisions (i.e. a forced choice: natural versus man-made) to the existing words, with the expectation that novel word learning would inhibit responses due to lexical competition. This competition was observed, particularly when assessed after sleep, for both standard and high exposure levels (10 and 20 exposures per word; Experiment 1). Using a lower exposure level (five exposures; Experiment 2), no post-sleep enhancement of competition was observed, despite evidence of consolidation when explicit knowledge of novel word memory was tested. Thus, when encoding is relatively weak, consolidation-related lexical integration is particularly compromised. There was no evidence that going to bed soon after learning is advantageous for overnight consolidation; however, there was some preliminary suggestion that longer gaps between learning and bed-onset were associated with better explicit memory of novel words one week later, but only at higher levels of exposure. These findings suggest that while lexical integration can occur overnight, weaker lexical traces may not be able to access overnight integration processes in the sleeping brain. Furthermore, the finding that longer-term explicit memory of stronger (but not weaker) traces benefit from periods of wake following learning deserves examination in future research.

People make inferences about the trustworthiness of others based on their observed gaze behaviour. Faces that consistently look towards a target location are rated as more trustworthy than those that look away from the target. Representations of trust are important for future interactions; yet little is known about how they are consolidated in long-term memory. Sleep facilitates memory consolidation for incidentally-learned information and may therefore support the retention of trust representations. We investigated the consolidation of trust inferences across periods of sleep or wakefulness. In addition, we employed a memory cueing procedure (targeted memory reactivation, TMR) in a bid to strengthen certain trust memories over others. We observed no difference in the retention of trust inferences following delays of sleep or wakefulness, and there was no effect of TMR in either condition. Interestingly, trust inferences remained stable one week after learning, irrespective of the initial post-learning delay. A second experiment showed that this implicit learning occurs despite participants’ being unable to explicitly recall the gaze behaviour of specific faces immediately after encoding. Together, these results suggest that gist-like, social inferences are formed at the time of learning without retaining the original episodic memory and thus do not benefit from offline consolidation through replay. We discuss our findings in the context of a novel framework whereby trust judgements reflect an efficient, powerful, and adaptable storage device for social information.

Sleep supports memory consolidation as well as next-day learning. The influential Active Systems account of offline consolidation suggests that sleep-associated memory processing paves the way for new learning, but empirical evidence in support of this idea is scarce. Using a within-subjects (N = 30), crossover design, we assessed behavioural and electrophysiological indices of episodic encoding after a night of sleep or total sleep deprivation in healthy adults (aged 18-25 years), and investigated whether behavioural performance was predicted by the overnight consolidation of episodic associations formed the previous day. Sleep supported memory consolidation and next-day learning, as compared to sleep deprivation. However, the magnitude of this sleep-associated consolidation benefit did not significantly predict the ability to form novel memories after sleep. Interestingly, sleep deprivation prompted a qualitative change in the neural signature of encoding: whereas 12-20 Hz beta desynchronization – an established marker of successful encoding – was observed after sleep, sleep deprivation disrupted beta desynchrony during successful learning. Taken together, these findings suggest that effective learning depends on sleep, but not necessarily sleep-associated consolidation.