Simon J. Durrant

Overlapping memory replay during sleep builds cognitive schemata.

Sleep enhances integration across multiple stimuli, abstraction of general rules, insight into hidden solutions and false memory formation. Newly learned information is better assimilated if compatible with an existing cognitive framework or schema. This article proposes a mechanism by which the reactivation of newly learned memories during sleep could actively underpin both schema formation and the addition of new knowledge to existing schemata. Under this model, the overlapping replay of related memories selectively strengthens shared elements. Repeated reactivation of memories in different combinations progressively builds schematic representations of the relationships between stimuli. We argue that this selective strengthening forms the basis of cognitive abstraction, and explain how it facilitates insight and false memory formation.

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.

Neural prediction of higher-order auditory sequence statistics

During auditory perception, we are required to abstract information from complex temporal sequences such as those in music and speech. Here, we investigated how higher-order statistics modulate the neural responses to sound sequences, hypothesizing that these modulations are associated with higher levels of the peri-Sylvian auditory hierarchy. We devised second-order Markov sequences of pure tones with uniform first-order transition probabilities. Participants learned to discriminate these sequences from random ones. Magnetoencephalography was used to identify evoked fields in which second-order transition probabilities were encoded. We show that improbable tones evoked heightened neural responses after 200 ms post-tone onset during exposure at the learning stage or around 150 ms during the subsequent test stage, originating near the right temporoparietal junction. These signal changes reflected higher-order statistical learning, which can contribute to the perception of natural sounds with hierarchical structures. We propose that our results reflect hierarchical predictive representations, which can contribute to the experiences of speech and music.

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.

GLM and SVM analyses of neural response to tonal and atonal stimuli: new techniques and a comparison

This paper gives both general linear model (GLM) and support vector machine (SVM) analyses of an experiment concerned with tonality in music. The two forms of analysis are both contrasted and used to complement each other, and a new technique employing the GLM as a pre-processing step for the SVM is presented. The SVM is given the task of classifying the stimulus conditions (tonal or atonal) on the basis of the blood oxygen level-dependent signal of novel data, and the prediction performance is evaluated. In addition, a more detailed assessment of the SVM performance is given in a comparison of the similarity in the identification of voxels relevant to the classification of the SVM and a GLM. A high level of similarity between SVM weight and GLM t-maps demonstrate that the SVM is successfully identifying relevant voxels, and it is this that allows it to perform well in the classification task in spite of very noisy data and stimuli that involve higher-order cognitive functions and considerably inter-subject variation in neural response.

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.

Memory Consolidation: Tracking Transfer with Functional Connectivity

Every day we store memories of innumerable new experiences. Our extraordinary ability to retrieve so many of them at a later time is due in no small part to the consolidation of these memories, a process that continues offline long after the experiences themselves are over.