Memory consolidation is linked to spindle-mediated information processing during sleep

AbstractHow 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. More recently, experimental manipulations have demonstrated that NREM sleep provides a window of opportunity to selectively strengthen particular memory traces via the delivery of sensory cues. It has remained unclear, however, whether experimental memory cueing triggers the brain’s endogenous consolidation mechanisms (linked to SOs and/or spindles) and whether those mechanisms in turn mediate effective processing of the cue information. Here we devised a novel paradigm in which associative memories (adjective-object and adjective-scene pairs) were selectively cued during a post-learning nap, successfully stabilising next-day retention relative to non-cued memories. First, we found that compared to novel control adjectives, memory cues were accompanied by an increase in fast spindles coupled to SO up states. Critically, EEG pattern decodability of the associated memory category (object vs. scene) was temporally linked to cue-induced spindles and predicted next-day retrieval performance across participants. These results provide highly controlled empirical evidence for an information processing role of sleep spindles in service of memory consolidation.

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Bidirectional Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Spiking Activity During NREM Sleep

Cerebral Cortex ◽

10.1093/cercor/bhaa228 ◽

2020 ◽

Vol 31 (1) ◽

pp. 324-340

Author(s):

Pavel Sanda ◽

Paola Malerba ◽

Xi Jiang ◽

Giri P Krishnan ◽

Jorge Gonzalez-Martinez ◽

...

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Nrem Sleep ◽

Slow Waves ◽

Slow Oscillation ◽

Cortical Input ◽

Sharp Wave ◽

Up States ◽

Intracranial Recordings

Abstract The dialogue between cortex and hippocampus is known to be crucial for sleep-dependent memory consolidation. During slow wave sleep, memory replay depends on slow oscillation (SO) and spindles in the (neo)cortex and sharp wave-ripples (SWRs) in the hippocampus. The mechanisms underlying interaction of these rhythms are poorly understood. We examined the interaction between cortical SO and hippocampal SWRs in a model of the hippocampo–cortico–thalamic network and compared the results with human intracranial recordings during sleep. We observed that ripple occurrence peaked following the onset of an Up-state of SO and that cortical input to hippocampus was crucial to maintain this relationship. A small fraction of ripples occurred during the Down-state and controlled initiation of the next Up-state. We observed that the effect of ripple depends on its precise timing, which supports the idea that ripples occurring at different phases of SO might serve different functions, particularly in the context of encoding the new and reactivation of the old memories during memory consolidation. The study revealed complex bidirectional interaction of SWRs and SO in which early hippocampal ripples influence transitions to Up-state, while cortical Up-states control occurrence of the later ripples, which in turn influence transition to Down-state.

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Hippocampal Theta Activity and Learning: A Reply to Douglas

Psychological Reports ◽

10.2466/pr0.1969.24.2.580 ◽

1969 ◽

Vol 24 (2) ◽

pp. 580-582 ◽

Cited By ~ 1

Author(s):

Thomas L. Bennett

Keyword(s):

Decision Making ◽

Information Processing ◽

Electrical Activity ◽

Memory Consolidation ◽

Theta Activity ◽

Hippocampal Theta Activity ◽

And Performance ◽

Hippocampal Theta ◽

Learning And Performance

Adey and his associates have asserted that theta electrical activity recorded from the hippocampus during learning and performance reflects the role of this structure in information processing, decision making and memory consolidation. This notion was recently questioned by Douglas (1967) who concluded that the tasks employed by Adey and his associates to assess theta activity were tasks which the lesion literature indicated do not requite hippocampal functioning to be learned. The present paper questions Douglas' assertion by describing studies in the lesion literature which demonstrate that the tasks used by Adey and his co-workers may actually require hippocampal functioning to be learned.

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Endogenous memory reactivation during sleep in humans is clocked by slow oscillation-spindle complexes

10.1101/2020.09.16.299545 ◽

2020 ◽

Author(s):

Thomas Schreiner ◽

Marit Petzka ◽

Tobias Staudigl ◽

Bernhard P. Staresina

Keyword(s):

Memory Function ◽

Nrem Sleep ◽

Learning Material ◽

Associative Memories ◽

Brain Areas ◽

Slow Oscillations ◽

Memory Reactivation ◽

Function Of Sleep ◽

Prior Experiences

ABSTRACTSleep is thought to support memory consolidation via reactivation of prior experiences, with particular electrophysiological sleep signatures (slow oscillations (SOs) and sleep spindles) gating the information flow between relevant brain areas. However, empirical evidence for a role of endogenous memory reactivation (i.e., without experimentally delivered memory cues) for consolidation in humans is lacking. Here, we devised a paradigm in which participants acquired associative memories before taking a nap. Multivariate decoding was then used to capture endogenous memory reactivation during non-rapid eye movement (NREM) sleep. Results revealed reactivation of learning material during SO-spindle complexes, with the precision of SO-spindle coupling predicting reactivation strength. Critically, reactivation strength in turn predicted the level of consolidation across participants. These results elucidate the memory function of sleep in humans and emphasize the importance of SOs and spindles in clocking endogenous consolidation processes.

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On the Role of Exact and Nonexact Associative Memories in Human and Machine Information Processing

Computer and Information Sciences–1969 - SEN Report Series Software Engineering ◽

10.1016/b978-0-12-696202-4.50016-4 ◽

1971 ◽

pp. 141-153

Author(s):

Nicholas V. Findler

Keyword(s):

Information Processing ◽

Associative Memories

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p75NTR as a Molecular Memory Switch

10.20944/preprints201912.0333.v1 ◽

2019 ◽

Author(s):

Shen Ning ◽

Mehdi Jorfi

Keyword(s):

Memory Consolidation ◽

Sleep Disturbances ◽

Biological Function ◽

Neurological Diseases ◽

Molecular Memory ◽

Sleep Research ◽

Memory Traces ◽

The Impact ◽

Synaptic Circuitry

In recent years, many molecular and environmental factors have been studied to understand how synaptic plasticity is modulated. Sleep, as an evolutionary conserved biological function, has shown to be a critical player for the consolidation and filtering of synaptic circuitry underlying memory traces. Although sleep disturbances do not alter normal memory consolidation, they may reflect fundamental circuit malfunctions that can play a significant role in exacerbating diseases, such as autism and Alzheimer’s disease. Very recently, scientists sought to answer part of this enigma and they identified p75 neurotrophic receptor (p75NTR) as a critical player in mediating impairments in hippocampal-dependent associative plasticity upon sleep deprivation. This paper will review the role of the p75NTR, critically discuss the impact and implications of this research as the bridge for sleep research and neurological diseases.

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Stimulation augments spike sequence replay and memory consolidation during slow-wave sleep

10.1101/670091 ◽

2019 ◽

Author(s):

Yina Wei ◽

Giri P Krishnan ◽

Lisa Marshall ◽

Thomas Martinetz ◽

Maxim Bazhenov

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Temporal Pattern ◽

Slow Wave Sleep ◽

Sensory Stimulation ◽

Slow Waves ◽

Memory Traces ◽

Spatio Temporal ◽

Synaptic Level

AbstractNewly acquired memory traces are spontaneously reactivated during slow-wave sleep (SWS), leading to the consolidation of recent memories. Empirical studies found that sensory stimulation during SWS selectively enhances memory consolidation and the effect depends on the phase of stimulation. In this new study, we aimed to understand the mechanisms behind the role of sensory stimulation on memory consolidation using computational models implementing effects of neuromodulators to simulate transitions between awake and SWS sleep, and synaptic plasticity to allow the change of synaptic connections due to the training in awake or replay during sleep. We found that when closed-loop stimulation was applied during the Down states (900-2700) of sleep slow oscillation, particularly right before transition from Down to Up state, it significantly affected the spatio-temporal pattern of the slow-waves and maximized memory replay. In contrast, when the stimulation was presented during the Up states (2700-3600 and 00-900), it did not have a significant impact on the slow-waves or memory performance after sleep. For multiple memories trained in awake, presenting stimulation cues associated with specific memory trace could selectively augment replay and enhance consolidation of that memory and interfere with consolidation of the others (particularly weak) memories. Our study proposes a synaptic level mechanism of how memory consolidation is affected by sensory stimulation during sleep.Significance statementStimulation, such as training-associated cues or auditory stimulation, during sleep can augment consolidation of the newly encoded memories. In this study, we used a computational model of the thalamocortical system to describe the mechanisms behind the role of stimulation in memory consolidation during slow-wave sleep. Our study suggested that stimulation preferentially strengthens the memory traces when delivered at specific phase of slow oscillations just before Down to Up state transition when it makes the largest impact on the spatio-temporal pattern of sleep slow waves. In the presence of multiple memories, presenting sensory cues during sleep could selectively strengthen selected memories. Our study proposes a synaptic level mechanism of how memory consolidation is affected by sensory stimulation during sleep.

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Memory quality modulates the effect of aging on memory consolidation during sleep: Reduced maintenance but intact gain

10.1101/547448 ◽

2019 ◽

Cited By ~ 1

Author(s):

Beate E. Muehlroth ◽

Myriam C. Sander ◽

Yana Fandakova ◽

Thomas H. Grandy ◽

Björn Rasch ◽

...

Keyword(s):

Memory Consolidation ◽

Brain Structure ◽

Nrem Sleep ◽

Structure Characteristic ◽

Multivariate Techniques ◽

Associative Memories ◽

Age Related ◽

Sleep Physiology ◽

Permanent Memory ◽

Effects Of Aging

AbstractSuccessful consolidation of associative memories relies on the coordinated interplay of slow oscillations and sleep spindles during non-rapid eye movement (NREM) sleep, enabling the transfer of labile information from the hippocampus to permanent memory stores in the neocortex. During senescence, the decline of the structural and functional integrity of the hippocampus and neocortical regions is paralleled by changes of the physiological events that stabilize and enhance associative memories during NREM sleep. However, the currently available evidence is inconclusive if and under which circumstances aging impacts memory consolidation. By tracing the encoding quality of single memories in individual participants, we demonstrate that previous learning determines the extent of age-related impairments in memory consolidation. Specifically, the detrimental effects of aging on memory maintenance were greatest for mnemonic contents of medium encoding quality, whereas memory gain of weakly encoded memories did not differ by age. Using multivariate techniques, we identified profiles of alterations in sleep physiology and brain structure characteristic for increasing age. Importantly, while both ‘aged’ sleep and ‘aged’ brain structure profiles were associated with reduced memory maintenance, inter-individual differences in neither sleep nor structural brain integrity qualified as the driving force behind age differences in sleep-dependent consolidation in the present study.

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