Scott A. Cairney

Sleep-dependent consolidation of statistical learning.

The importance of sleep for memory consolidation has been firmly established over the past decade. Recent work has extended this by suggesting that sleep is also critical for the integration of disparate fragments of information into a unified schema, and for the abstraction of underlying rules. The question of which aspects of sleep play a significant role in integration and abstraction is, however, currently unresolved. Here, we examined the role of sleep in abstraction of the implicit probabilistic structure in sequential stimuli using a statistical learning paradigm, and tested for its role in such abstraction by searching for a predictive relationship between the type of sleep obtained and subsequent performance improvements using polysomnography. In our experiments, participants were exposed to a series of tones in a probabilistically determined sequential structure, and subsequently tested for recognition of novel short sequences adhering to this same statistical pattern in both immediate- and delayed-recall sessions. Participants who consolidated over a night of sleep improved significantly more than those who consolidated over an equivalent period of daytime wakefulness. Similarly, participants who consolidated across a 4-h afternoon delay containing a nap improved significantly more than those who consolidated across an equivalent period without a nap. Importantly, polysomnography revealed a significant correlation between the level of improvement and the amount of slow-wave sleep obtained. We also found evidence of a time-based consolidation process which operates alongside sleep-specific consolidation. These results demonstrate that abstraction of statistical patterns benefits from sleep, and provide the first clear support for the role of slow-wave sleep in this consolidation.

Overnight Consolidation Aids the Transfer of Statistical Knowledge from the Medial Temporal Lobe to the Striatum

Sleep is important for abstraction of the underlying principles (or gist) which bind together conceptually related stimuli, but little is known about the neural correlates of this process. Here, we investigate this issue using overnight sleep monitoring and functional magnetic resonance imaging (fMRI). Participants were exposed to a statistically structured sequence of auditory tones then tested immediately for recognition of short sequences which conformed to the learned statistical pattern. Subsequently, after consolidation over either 30 min or 24h, they performed a delayed test session in which brain activity was monitored with fMRI. Behaviorally, there was greater improvement across 24h than across 30 min, and this was predicted by the amount of slow wave sleep (SWS) obtained. Functionally, we observed weaker parahippocampal responses and stronger striatal responses after sleep. Like the behavioral result, these differences in functional response were predicted by the amount of SWS obtained. Furthermore, connectivity between striatum and parahippocampus was weaker after sleep, whereas connectivity between putamen and planum temporale was stronger. Taken together, these findings suggest that abstraction is associated with a gradual shift from the hippocampal to the striatal memory system and that this may be mediated by SWS.

Complementary Roles of Slow-Wave Sleep and Rapid Eye Movement Sleep in Emotional Memory Consolidation

Although rapid eye movement sleep (REM) is regularly implicated in emotional memory consolidation, the role of slow-wave sleep (SWS) in this process is largely uncharacterized. In the present study, we investigated the relative impacts of nocturnal SWS and REM upon the consolidation of emotional memories using functional magnetic resonance imaging (fMRI) and polysomnography (PSG). Participants encoded emotionally positive, negative, and neutral images (remote memories) before a night of PSG-monitored sleep. Twenty-four hours later, they encoded a second set of images (recent memories) immediately before a recognition test in an MRI scanner. SWS predicted superior memory for remote negative images and a reduction in right hippocampal responses during the recollection of these items. REM, however, predicted an overnight increase in hippocampal-neocortical connectivity associated with negative remote memory. These findings provide physiological support for sequential views of sleep-dependent memory processing, demonstrating that SWS and REM serve distinct but complementary functions in consolidation. Furthermore, these findings extend those ideas to emotional memory by showing that, once selectively reorganized away from the hippocampus during SWS, emotionally aversive representations undergo a comparably targeted process during subsequent REM.

Targeted Memory Reactivation During Slow Wave Sleep Facilitates Emotional Memory Consolidation

STUDY OBJECTIVES To investigate the mechanisms by which auditory targeted memory reactivation (TMR) during slow wave sleep (SWS) influences the consolidation of emotionally negative and neutral memories. DESIGN Each of 72 (36 negative, 36 neutral) picture-location associations were encoded with a semantically related sound. During a subsequent nap, half of the sounds were replayed in SWS, before picture-location recall was examined in a final test. SETTING Manchester Sleep Laboratory, University of Manchester. PARTICIPANTS 15 adults (3 male) mean age = 20.40 (standard deviation ± 3.07). INTERVENTIONS TMR with auditory cues during SWS. MEASUREMENTS AND RESULTS Performance was assessed by memory accuracy and recall response times (RTs). Data were analyzed with a 2 (sound: replayed/not replayed) × 2 (emotion: negative/neutral) repeated measures analysis of covariance with SWS duration, and then SWS spindles, as the mean-centered covariate. Both analyses revealed a significant three-way interaction for RTs but not memory accuracy. Critically, SWS duration and SWS spindles predicted faster memory judgments for negative, relative to neutral, picture locations that were cued with TMR. CONCLUSIONS TMR initiates an enhanced consolidation process during subsequent SWS, wherein sleep spindles mediate the selective enhancement of reactivated emotional memories.

Schema-conformant memories are preferentially consolidated during REM sleep

Memory consolidation is most commonly described by the standard model, which proposes an initial binding role for the hippocampus which diminishes over time as intracortical connections are strengthened. Recent evidence suggests that slow wave sleep (SWS) plays an essential role in this process. Existing animal and human studies have suggested that memories which fit tightly into an existing knowledge framework or schema might use an alternative consolidation route in which the medial prefrontal cortex takes on the binding role. In this study we sought to investigate the role of sleep in this process using a novel melodic memory task. Participants were asked to remember 32 melodies, half of which conformed to a tonal schema present in all enculturated listeners, and half of which did not fit with this schema. After a 24-h consolidation interval, participants were asked to remember a further 32 melodies, before being given a recognition test in which melodies from both sessions were presented alongside some previously unheard foils. Participants remembered schema-conformant melodies better than non-conformant ones. This was much more strongly the case for consolidated melodies, suggesting that consolidation over a 24-h period preferentially consolidated schema-conformant items. Overnight sleep was monitored between the sessions, and the extent of the consolidation benefit for schema-conformant items was associated with both the amount of REM sleep obtained and EEG theta power in frontal and central regions during REM sleep. Overall our data suggest that REM sleep plays a crucial role in the rapid consolidation of schema-conformant items. This finding is consistent with previous results from animal studies and the SLIMM model of Van Kesteren, Ruiter, Fernández, and Henson (2012), and suggest that REM sleep, rather than SWS, may be involved in an alternative pathway of consolidation for schema-conformant memories.

Sleep spindles provide indirect support to the consolidation of emotional encoding contexts

Emotional memories tend to be strengthened ahead of neutral memories during sleep-dependent consolidation. In recent work, however, we found that this is not the case when emotion pertains to the contextual features of a memory instead of its central constructs, suggesting that emotional contexts are influenced by distinct properties of sleep. We therefore examined the sleep-specific mechanisms supporting representations of emotional context and asked whether these differ to those already implicated in central emotional memory processing, such as rapid eye movement sleep (REM). Participants encoded neutral foreground images that were each associated with an emotionally negative or neutral background (context) image. Immediate and delayed tests for the emotionality of the foreground/background image association were separated by a 4-h consolidation period, which consisted of either total wakefulness or included a 2-h polysomnographically monitored nap. Although memory for negative contexts was not associated with REM, or any other parameter of sleep, sleep spindles (12-15 Hz) predicted increased forgetting and slowed response times for neutral contexts. Together with prior work linking spindles to emotional memory processing, our data may suggest that spindles provide multi-layered support to emotionally salient memories in sleep, with the nature of such effects depending on whether the emotionality of these memories pertains to their central or contextual features. Therefore, whereas spindles may mediate a direct strengthening of central emotional information, as suggested in prior work, they may also provide concurrent indirect support to emotional contexts by working to suppress non-salient neutral contexts.

The benefits of targeted memory reactivation for consolidation in sleep are contingent on memory accuracy and direct cue-memory associations

STUDY OBJECTIVES To investigate how the effects of targeted memory reactivation (TMR) are influenced by memory accuracy prior to sleep and the presence or absence of direct cue-memory associations. METHODS 30 participants associated each of 50 pictures with an unrelated word and then with a screen location in two separate tasks. During picture-location training, each picture was also presented with a semantically related sound. The sounds were therefore directly associated with the picture locations but indirectly associated with the words. During a subsequent nap, half of the sounds were replayed in slow wave sleep (SWS). The effect of TMR on memory for the picture locations (direct cue-memory associations) and picture-word pairs (indirect cue-memory associations) was then examined. RESULTS TMR reduced overall memory decay for recall of picture locations. Further analyses revealed a benefit of TMR for picture locations recalled with a low degree of accuracy prior to sleep, but not those recalled with a high degree of accuracy. The benefit of TMR for low accuracy memories was predicted by time spent in SWS. There was no benefit of TMR for memory of the picture-word pairs, irrespective of memory accuracy prior to sleep. CONCLUSIONS TMR provides the greatest benefit to memories recalled with a low degree of accuracy prior to sleep. The memory benefits of TMR may also be contingent on direct cue-memory associations.

Eye-tracking the time-course of novel word learning and lexical competition in adults and children.

HighlightsNewly learned spoken words can compete for recognition soon after learning.Lexical competition effects were smaller for newly learned than existing words.Explicit memory was superior for words learned the day before testing.The sleep advantage for explicit memory correlated with sleep‐spindle density.Word learning seems boosted by sleep to a greater degree in children than adults. Abstract Lexical competition is a hallmark of proficient, automatic word recognition. Previous research suggests that there is a delay before a new spoken word becomes engaged in this process, with sleep playing an important role. However, data from one method – the visual world paradigm – consistently show competition without a delay. We trained 42 adults and 40 children (aged 7–8) on novel word‐object pairings, and employed this paradigm to measure the time‐course of lexical competition. Fixations to novel objects upon hearing existing words (e.g., looks to the novel object biscal upon hearing “click on the biscuit”) were compared to fixations on untrained objects. Novel word‐object pairings learned immediately before testing and those learned the previous day exhibited significant competition effects, with stronger competition for the previous day pairings for children but not adults. Crucially, this competition effect was significantly smaller for novel than existing competitors (e.g., looks to candy upon hearing “click on the candle”), suggesting that novel items may not compete for recognition like fully‐fledged lexical items, even after 24 h. Explicit memory (cued recall) was superior for words learned the day before testing, particularly for children; this effect (but not the lexical competition effects) correlated with sleep‐spindle density. Together, the results suggest that different aspects of new word learning follow different time courses: visual world competition effects can emerge swiftly, but are qualitatively different from those observed with established words, and are less reliant upon sleep. Furthermore, the findings fit with the view that word learning earlier in development is boosted by sleep to a greater degree.

Memory Consolidation Is Linked to Spindle-Mediated Information Processing during Sleep

Summary How are brief encounters transformed into lasting memories? Previous research has established the role of non-rapid eye movement (NREM) sleep, along with its electrophysiological signatures of slow oscillations (SOs) and spindles, for memory consolidation [1, 2, 3, 4]. In related work, experimental manipulations have demonstrated that NREM sleep provides a window of opportunity to selectively strengthen particular memory traces via the delivery of auditory cues [5, 6, 7, 8, 9, 10], a procedure known as targeted memory reactivation (TMR). It has remained unclear, however, whether TMR triggers the brain’s endogenous consolidation mechanisms (linked to SOs and/or spindles) and whether those mechanisms in turn mediate effective processing of mnemonic information. We devised a novel paradigm in which associative memories (adjective-object and adjective-scene pairs) were selectively cued during a post-learning nap, successfully stabilizing next-day retention relative to non-cued memories. First, we found that, compared to novel control adjectives, memory cues evoked an increase in fast spindles. Critically, during the time window of cue-induced spindle activity, the memory category linked to the verbal cue (object or scene) could be reliably decoded, with the fidelity of this decoding predicting the behavioral consolidation benefits of TMR. These results provide correlative evidence for an information processing role of sleep spindles in service of memory consolidation.

Mechanisms of Memory Retrieval in Slow-Wave Sleep

Abstract 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 nonverbal 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. noncued) associations was reduced by TMR with verbal and nonverbal cues to similar extents. In Experiment 2, TMR with identical nonverbal cues reduced forgetting of cued (vs. noncued) associations, replicating Experiment 1. However, TMR with nonidentical verbal cues reduced forgetting of both cued and noncued 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 nonidentical verbal cues may utilize linguistic decoding mechanisms, resulting in widespread reactivation across a broad category of memories.