A sleep spindle framework for motor memory consolidation

Sleep spindle activity has repeatedly been found to contribute to brain plasticity and consolidation of both declarative and procedural memories. Here we propose a framework for motor memory consolidation that outlines the essential contribution of the hierarchical and multi-scale periodicity of spindle activity, as well as of the synchronization and interaction of brain oscillations during this sleep-dependent process. We posit that the clustering of sleep spindles in ‘trains', together with the temporally organized alternation between spindles and associated refractory periods, is critical for efficient reprocessing and consolidation of motor memories. We further argue that the long-term retention of procedural memories relies on the synchronized (functional connectivity) local reprocessing of new information across segregated, but inter-connected brain regions that are involved in the initial learning process. Finally, we propose that oscillatory synchrony in the spindle frequency band may reflect the cross-structural reactivation, reorganization and consolidation of motor, and potentially declarative, memory traces within broader subcortical–cortical networks during sleep. This article is part of the Theo Murphy meeting issue ‘Memory reactivation: replaying events past, present and future'.

Download Full-text

Pharmacologically Increasing Sleep Spindles Enhances Recognition for Negative and High-arousal Memories

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00433 ◽

2013 ◽

Vol 25 (10) ◽

pp. 1597-1610 ◽

Cited By ~ 65

Author(s):

Erik J. Kaestner ◽

John T. Wixted ◽

Sara C. Mednick

Keyword(s):

Rem Sleep ◽

Memory Consolidation ◽

Declarative Memory ◽

Memory Performance ◽

Emotional Memory ◽

Limited Range ◽

Sleep Spindles ◽

Sleep Spindle ◽

Emotional Stimuli ◽

Valence And Arousal

Sleep affects declarative memory for emotional stimuli differently than it affects declarative memory for nonemotional stimuli. However, the interaction between specific sleep characteristics and emotional memory is not well understood. Recent studies on how sleep affects emotional memory have focused on rapid eye movement sleep (REM) but have not addressed non-REM sleep, particularly sleep spindles. This is despite the fact that sleep spindles are implicated in declarative memory as well as neural models of memory consolidation (e.g., hippocampal neural replay). Additionally, many studies examine a limited range of emotional stimuli and fail to disentangle differences in memory performance because of variance in valence and arousal. Here, we experimentally increase non-REM sleep features, sleep spindle density, and SWS, with pharmacological interventions using zolpidem (Ambien) and sodium oxybate (Xyrem) during daytime naps. We use a full spread of emotional stimuli to test all levels of valence and arousal. We find that increasing sleep spindle density increases memory discrimination (da) for highly arousing and negative stimuli without altering measures of bias (ca). These results indicate a broader role for sleep in the processing of emotional stimuli with differing effects based on arousal and valence, and they raise the possibility that sleep spindles causally facilitate emotional memory consolidation. These findings are discussed in terms of the known use of hypnotics in individuals with emotional mood disorders.

Download Full-text

Acoustic Stimulation Following Sleep Spindle Activity May Enhance Procedural Memory Consolidation During a Nap

IEEE Access ◽

10.1109/access.2019.2913457 ◽

2019 ◽

Vol 7 ◽

pp. 56297-56307

Author(s):

Jinyoung Choi ◽

Kyungho Won ◽

Sung Chan Jun

Keyword(s):

Memory Consolidation ◽

Acoustic Stimulation ◽

Procedural Memory ◽

Sleep Spindle ◽

Spindle Activity

Download Full-text

Dysfunctional Overnight Memory Consolidation in Patients with Schizophrenia in Comparison to Healthy Controls: Disturbed Slow-Wave Sleep as Contributing Factor?

Neuropsychobiology ◽

10.1159/000517858 ◽

2021 ◽

pp. 1-12

Author(s):

Sara Lena Weinhold ◽

Julia Lechinger ◽

Jasper Ittel ◽

Romina Ritzenhoff ◽

Henning Johannes Drews ◽

...

Keyword(s):

Linear Relationship ◽

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Declarative Memory ◽

Sleep Spindles ◽

Sleep Spindle ◽

Delta Power ◽

Sleep Parameters ◽

Spindle Power

Introduction: Memory deficiency has been shown in schizophrenia patients, but results on the role of sleep parameters in overnight consolidation of associative verbal memory are still missing. Therefore, the aim of our study was to elucidate underlying processes of impaired sleep-related consolidation of associative word pairs in schizophrenia including standard sleep parameters as well as sleep spindle counts and spectral analysis. Methods: Eighteen stably medicated schizophrenia patients and 24 healthy age-matched controls performed an associative declarative memory task before and after polysomnographic recordings. Part of the participants expected verbal associative memory testing in the morning, while the others did not. Furthermore, participants filled in self-rating questionnaires of schizophrenia-typical experiences (Eppendorf Schizophrenia Inventory [ESI] and Psychotic Symptom Rating Scale). Results: Schizophrenia patients performed worse in verbal declarative memory in the evening as well as in overnight consolidation (morning compared to evening performance). While duration of slow-wave sleep was nearly comparable between groups, schizophrenia patients showed lower sleep spindle count, reduced delta power during slow-wave sleep, and reduced spindle power during the slow oscillation (SO) up-state. In healthy but not in schizophrenia patients, a linear relationship between overnight memory consolidation and slow-wave sleep duration as well as delta power was evident. No significant effect with respect to the expectation of memory retrieval was evident in our data. Additionally, we observed a negative linear relationship between total number of sleep spindles and ESI score in healthy participants. Discussion/Conclusion: As expected, schizophrenia patients showed deficient overnight verbal declarative memory consolidation as compared to healthy controls. Reduced sleep spindles, delta power, and spindle power during the SO up-state may link sleep and memory deficiency in schizophrenia. Additionally, the absence of a linear relationship between sleep-related memory consolidation and slow-wave sleep as well as delta power suggests further functional impairments in schizophrenia. Note that this conclusion is based on observational data. Future studies should investigate if stimulation of delta waves during sleep could improve memory performance and thereby quality of life in schizophrenia.

Download Full-text

Sleep spindles and cognition in depression

10.31219/osf.io/waz3d ◽

2017 ◽

Author(s):

Leonore Bovy ◽

Martin Dresler ◽

Frederik D Weber

Keyword(s):

Memory Consolidation ◽

Cognitive Abilities ◽

Declarative Memory ◽

Critical Role ◽

Antidepressant Medication ◽

Sleep Spindles ◽

Sleep Spindle ◽

Preliminary Model ◽

Patient Groups ◽

Medication Selection

Sleep plays a critical role in orchestrating several cognitive functions. Sleep spindles are particularly at the forefront of studies on the consolidation of cognitive abilities, such as procedural and declarative memory. Despite that major depressive disorder (MDD) has been linked to sleep spindle alterations, their role in MDD pathogenesis and symptomatology (including memory deficits) is still scarcely investigated. Here, we first provide an overview of sleep and sleep spindle alterations in MDD and their potential effects on memory and cognition. Secondly, limited data suggest that sleep spindles deficits in severe MDD might not only lead to cognitive impairments but primarily affect memory consolidation processes during sleep. Furthermore, it seems likely that many sleep spindle related effects are masked by interacting (antidepressant) medication, selection of mixed patient groups with mild symptomatology as well as use of incomprehensive methodology in analyzing sleep. We propose a preliminary model predicting that impairments in sleep spindle related activity during sleep are mainly responsible for memory consolidation deficits in depressed patients, but that medication augmenting sleep spindle activity can enhance and restore sleep-mediated consolidation. Future studies thus need to scrutinize previous findings on sleep spindle effects in MDD.

Download Full-text

Direct electrical stimulation of the amygdala enhances declarative memory in humans

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1714058114 ◽

2017 ◽

Vol 115 (1) ◽

pp. 98-103 ◽

Cited By ~ 32

Author(s):

Cory S. Inman ◽

Joseph R. Manns ◽

Kelly R. Bijanki ◽

David I. Bass ◽

Stephan Hamann ◽

...

Keyword(s):

Electrical Stimulation ◽

Memory Consolidation ◽

Emotional Response ◽

Declarative Memory ◽

Perirhinal Cortex ◽

Memory Systems ◽

Brain Regions ◽

Memory Test ◽

Depth Electrodes ◽

Emotional Events

Emotional events are often remembered better than neutral events, a benefit that many studies have hypothesized to depend on the amygdala’s interactions with memory systems. These studies have indicated that the amygdala can modulate memory-consolidation processes in other brain regions such as the hippocampus and perirhinal cortex. Indeed, rodent studies have demonstrated that direct activation of the amygdala can enhance memory consolidation even during nonemotional events. However, the premise that the amygdala causally enhances declarative memory has not been directly tested in humans. Here we tested whether brief electrical stimulation to the amygdala could enhance declarative memory for specific images of neutral objects without eliciting a subjective emotional response. Fourteen epilepsy patients undergoing monitoring of seizures via intracranial depth electrodes viewed a series of neutral object images, half of which were immediately followed by brief, low-amplitude electrical stimulation to the amygdala. Amygdala stimulation elicited no subjective emotional response but led to reliably improved memory compared with control images when patients were given a recognition-memory test the next day. Neuronal oscillations in the amygdala, hippocampus, and perirhinal cortex during this next-day memory test indicated that a neural correlate of the memory enhancement was increased theta and gamma oscillatory interactions between these regions, consistent with the idea that the amygdala prioritizes consolidation by engaging other memory regions. These results show that the amygdala can initiate endogenous memory prioritization processes in the absence of emotional input, addressing a fundamental question and opening a path to future therapies.

Download Full-text

Schema and Motor-Memory Consolidation

Psychological Science ◽

10.1177/0956797619847164 ◽

2019 ◽

Vol 30 (7) ◽

pp. 963-978

Author(s):

Bradley R. King ◽

Nina Dolfen ◽

Mareike A. Gann ◽

Zenzi Renard ◽

Stephan P. Swinnen ◽

...

Keyword(s):

Sequence Learning ◽

Memory Consolidation ◽

Motor Memory ◽

Motor Sequence Learning ◽

Motor Sequence ◽

Learning Paradigm ◽

New Information ◽

Motor Information ◽

Schema Model ◽

Perceptual Systems

Recent research has demonstrated that memory-consolidation processes can be accelerated if newly learned information is consistent with preexisting knowledge. Until now, investigations of this fast integration of new information into memory have focused on the declarative and perceptual systems. We employed a unique manipulation of a motor-sequence-learning paradigm to examine the effect of experimentally acquired memory on the learning of new motor information. Results demonstrate that new information is rapidly integrated into memory when practice occurs in a framework that is compatible with the previously acquired memory. This framework consists of the ordinal representation of the motor sequence. This enhanced integration cannot be explained by differences in the explicit awareness of the sequence and is observed only if the previously acquired motor memory was consolidated overnight. Results are consistent with the schema model of memory consolidation and offer insights into how previous motor experience can accelerate learning and consolidation processes.

Download Full-text

Slow Sleep Spindle Activity, Declarative Memory, and General Cognitive Abilities in Children

SLEEP ◽

10.5665/sleep.4000 ◽

2014 ◽

Vol 37 (9) ◽

pp. 1501-1512 ◽

Cited By ~ 59

Author(s):

Kerstin Hoedlmoser ◽

Dominik P.J. Heib ◽

Judith Roell ◽

Philippe Peigneux ◽

Avi Sadeh ◽

...

Keyword(s):

Cognitive Abilities ◽

Declarative Memory ◽

Sleep Spindle ◽

Spindle Activity ◽

Slow Sleep

Download Full-text

Electrophysiological Indicators of Sleep-associated Memory Consolidation in 5- to 6-year-old Children

10.1101/2020.09.04.283606 ◽

2020 ◽

Author(s):

Ann-Kathrin Joechner ◽

Sarah Wehmeier ◽

Markus Werkle-Bergner

Keyword(s):

Young Adults ◽

School Children ◽

Memory Consolidation ◽

Declarative Memory ◽

Slow Oscillation ◽

Sleep Spindles ◽

Sleep Spindle ◽

Slow Oscillations ◽

Slow Sleep ◽

Temporal Coupling

ABSTRACTIn young adults, memory consolidation during sleep is supported by a time-coordinated interplay of sleep spindles and slow oscillations. However, given tremendous developmental changes in sleep spindle and slow oscillation morphology, it remains elusive whether the same mechanisms as identified in young adults are comparably functional across childhood. Here, we characterise slow and fast sleep spindles and their temporal coupling to slow oscillations in 24 pre-school children. Further, we ask whether slow and fast sleep spindles and their modulation during slow oscillations are similarly associated with behavioural indicators of declarative memory consolidation as suggested from adult literature. Employing a development-sensitive, individualised approach, we reliably identify an inherent, development-specific fast sleep spindle type, though nested in the adult-like slow sleep spindle frequency range, along with a dominant slow sleep spindle type. Further, we provide evidence for the modulation of fast sleep spindles during slow oscillations, already in pre-school children. However, the temporal coordination between fast sleep spindles and slow oscillations is weaker and less precise than expected from adult research. While we do not find evidence for a critical contribution of the pattern of fast sleep spindle modulation during slow oscillations for memory consolidation, crucially, both inherent slow and fast sleep spindles separately are differentially related to sleep-associated consolidation of items of varying quality. While a higher number of slow sleep spindles is associated with stronger maintenance of medium-quality memories, more fast sleep spindles are linked to higher gain of low-quality items. Our results provide evidence for two functionally relevant inherent sleep spindle types in pre-school children despite not fully matured sleep spindle – slow oscillation coupling.

Download Full-text

Beta-tACS does not impact the dynamics of motor memory consolidation

10.1101/2020.05.25.114850 ◽

2020 ◽

Author(s):

Liliia Roshchupkina ◽

Whitney Stee ◽

Philippe Peigneux

Keyword(s):

Memory Consolidation ◽

Primary Motor Cortex ◽

Brain Plasticity ◽

Critical Time ◽

Specific Effect ◽

Oscillatory Activity ◽

Motor Memory ◽

Training Time ◽

Time Points ◽

Transcranial Alternating Current Stimulation

AbstractThe consolidation of motor memory is a non-linear temporal dynamic. There are critical time points at which post-training performance can improve (e.g., 30 min and 24 h) or merely stabilize (e.g., 4 h). Besides, neuronal plasticity is supported by synchronized oscillatory activity in and between brain areas at play during the acquisition and consolidation of motor skills. Transcranial alternating current stimulation (tACS) can entrain cortical oscillatory activity, which may eventually modulate brain plasticity-related processes. Previous reports suggest that 20 Hz electrical stimulation over the primary motor cortex (M1) following training facilitates the consolidation of motor memories. To the best of our knowledge, the effect of tACS was not investigated when applied at critical post-training time points, nor its impact at longer time scales. In the present study, we investigated the effect of 20 Hz tACS applied over M1 within critical time periods (25min vs. 4h) on motor memory consolidation at immediate and delayed (24h) retrieval. Performance similarly evolved over time in all conditions, independently from the stimulation type (20 Hz tACS vs. Sham tACS) or the stimulation time point. As it stands, our results do not support the proposal that 20 Hz tACS exerts a positive, specific effect on the consolidation of motor memories.

Download Full-text