About sleep's role in memory Rasch, Björn; Born, Jan
Physiological reviews,
04/2013, Letnik:
93, Številka:
2
Journal Article
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Over more than a century of research has established the fact that sleep benefits the retention of memory. In this review we aim to comprehensively cover the field of "sleep and memory" research by ...providing a historical perspective on concepts and a discussion of more recent key findings. Whereas initial theories posed a passive role for sleep enhancing memories by protecting them from interfering stimuli, current theories highlight an active role for sleep in which memories undergo a process of system consolidation during sleep. Whereas older research concentrated on the role of rapid-eye-movement (REM) sleep, recent work has revealed the importance of slow-wave sleep (SWS) for memory consolidation and also enlightened some of the underlying electrophysiological, neurochemical, and genetic mechanisms, as well as developmental aspects in these processes. Specifically, newer findings characterize sleep as a brain state optimizing memory consolidation, in opposition to the waking brain being optimized for encoding of memories. Consolidation originates from reactivation of recently encoded neuronal memory representations, which occur during SWS and transform respective representations for integration into long-term memory. Ensuing REM sleep may stabilize transformed memories. While elaborated with respect to hippocampus-dependent memories, the concept of an active redistribution of memory representations from networks serving as temporary store into long-term stores might hold also for non-hippocampus-dependent memory, and even for nonneuronal, i.e., immunological memories, giving rise to the idea that the offline consolidation of memory during sleep represents a principle of long-term memory formation established in quite different physiological systems.
Memory consolidation refers to the transformation over time of experience-dependent internal representations and their neurobiological underpinnings. The process is assumed to be embodied in synaptic ...and cellular modifications at brain circuits in which the memory is initially encoded and to proceed by recurrent reactivations, both during wakefulness and during sleep, culminating in the distribution of information to additional locales and integration of new information into existing knowledge. We present snapshots of our current knowledge and gaps in knowledge concerning the progress of consolidation over time and the cognitive architecture that supports it and shapes our long-term memories.
Memories, like people, undergo transformations in life. Dudai, Karni, and Born present snapshots of our knowledge and gaps in knowledge concerning the consolidation and transformation of memory over time and the cognitive architecture that supports it and shapes long-term recollections.
Sleep is known to support memory consolidation. Here we review evidence for an active system consolidation occurring during sleep. At the beginning of this process is sleep's ability to preserve ...episodic experiences preferentially encoded in hippocampal networks. Repeated neuronal reactivation of these representations during slow-wave sleep transforms episodic representations into long-term memories, redistributes them toward extrahippocampal networks, and qualitatively changes them to decontextualized schema-like representations. Electroencephalographic (EEG) oscillations regulate the underlying communication: Hippocampal sharp-wave ripples coalescing with thalamic spindles mediate the bottom-up transfer of reactivated memory information to extrahippocampal regions. Neocortical slow oscillations exert a supraordinate top-down control to synchronize hippocampal reactivations of specific memories to their excitable up-phase, thus allowing plastic changes in extrahippocampal regions. We propose that reactivations during sleep are a general mechanism underlying the abstraction of temporally stable invariants from a flow of input that is solely structured in time, thus representing a basic mechanism of memory formation.
There is now compelling evidence that sleep promotes the long-term consolidation of declarative and procedural memories. Behavioral studies suggest that sleep preferentially consolidates explicit ...aspects of these memories, which during encoding are possibly associated with activation in prefrontal–hippocampal circuitry. Hippocampus-dependent declarative memory benefits particularly from slow-wave sleep (SWS), whereas rapid-eye-movement (REM) sleep seems to benefit procedural aspects of memory. Consolidation of hippocampus-dependent memories relies on a dialog between the neocortex and hippocampus. Crucial features of this dialog are the neuronal reactivation of new memories in the hippocampus during SWS, which stimulates the redistribution of memory representations to neocortical networks; and the neocortical slow (<1 Hz) oscillation that synchronizes hippocampal-to-neocortical information transfer to activity in other brain structures.
Slow-wave sleep (SWS) facilitates the consolidation of hippocampus-dependent declarative memory. Based on the standard two-stage memory model, we propose that memory consolidation during SWS ...represents a process of system consolidation which is orchestrated by the neocortical <1Hz electroencephalogram (EEG) slow oscillation and involves the reactivation of newly encoded representations and their subsequent redistribution from temporary hippocampal to neocortical long-term storage sites. Indeed, experimental induction of slow oscillations during non-rapid eye movement (non-REM) sleep by slowly alternating transcranial current stimulation distinctly improves consolidation of declarative memory. The slow oscillations temporally group neuronal activity into up-states of strongly enhanced neuronal activity and down-states of neuronal silence. In a feed-forward efferent action, this grouping is induced not only in the neocortex but also in other structures relevant to consolidation, namely the thalamus generating 10-15Hz spindles, and the hippocampus generating sharp wave-ripples, with the latter well known to accompany a replay of newly encoded memories taking place in hippocampal circuitries. The feed-forward synchronizing effect of the slow oscillation enables the formation of spindle-ripple events where ripples and accompanying reactivated hippocampal memory information become nested into the single troughs of spindles. Spindle-ripple events thus enable reactivated memory-related hippocampal information to be fed back to neocortical networks in the excitable slow oscillation up-state where they can induce enduring plastic synaptic changes underlying the effective formation of long-term memories.
In this issue of Neuron, Helfrich et al. (2017) demonstrate that phase-amplitude coupling (PAC) between slow oscillations and spindles is crucial for memory consolidation, and shifts in its phase ...relationship may explain age-related deficits in memory performance. These results also suggest a more general function of PAC in synaptic plasticity.
In this issue of Neuron, Helfrich et al. (2017) demonstrate that phase-amplitude coupling (PAC) between slow oscillations and spindles is crucial for memory consolidation, and shifts in its phase relationship may explain age-related deficits in memory performance. These results also suggest a more general function of PAC in synaptic plasticity.
Slow oscillations and sleep spindles are hallmarks of the EEG during slow-wave sleep (SWS). Both oscillatory events, especially when co-occurring in the constellation of spindles nesting in the slow ...oscillation upstate, are considered to support memory formation and underlying synaptic plasticity. The regulatory mechanisms of this function at the circuit level are poorly understood. Here, using two-photon imaging in mice, we relate EEG-recorded slow oscillations and spindles to calcium signals recorded from the soma of cortical putative pyramidal-like (Pyr) cells and neighboring parvalbumin-positive interneurons (PV-Ins) or somatostatin-positive interneurons (SOM-Ins). Pyr calcium activity was increased more than threefold when spindles co-occurred with slow oscillation upstates compared with slow oscillations or spindles occurring in isolation. Independent of whether or not a spindle was nested in the slow oscillation upstate, the slow oscillation downstate was preceded by enhanced calcium signal in SOM-Ins that vanished during the upstate, whereas spindles were associated with strongly increased PV-In calcium activity. Additional wide-field calcium imaging of Pyr cells confirmed the enhanced calcium activity and its widespread topography associated with spindles nested in slow oscillation upstates. In conclusion, when spindles are nested in slow oscillation upstates, maximum Pyr activity appears to concur with strong perisomatic inhibition of Pyr cells via PV-Ins and low dendritic inhibition via SOM-Ins (i.e., conditions that might optimize synaptic plasticity within local cortical circuits).
Sleep shapes cortical network activity, fostering global homeostatic downregulation of excitability while maintaining or even upregulating excitability in selected networks in a manner that supports ...memory consolidation. Here, we used two-photon calcium imaging of cortical layer 2/3 neurons in sleeping male mice to examine how these seemingly opposing dynamics are balanced in cortical networks. During slow-wave sleep (SWS) episodes, mean calcium activity of excitatory pyramidal (Pyr) cells decreased. Simultaneously, however, variance in Pyr population calcium activity increased, contradicting the notion of a homogenous downregulation of network activity. Indeed, we identified a subpopulation of Pyr cells distinctly upregulating calcium activity during SWS, which were highly active during sleep spindles known to support mnemonic processing. Rapid eye movement (REM) episodes following SWS were associated with a general downregulation of Pyr cells, including the subpopulation of Pyr cells active during spindles, which persisted into following stages of sleep and wakefulness. Parvalbumin-positive inhibitory interneurons (PV-In) showed an increase in calcium activity during SWS episodes, while activity remained unchanged during REM sleep episodes. This supports the view that downregulation of Pyr calcium activity during SWS results from increased somatic inhibition via PV-In, whereas downregulation during REM sleep is achieved independently of such inhibitory activity. Overall, our findings show that SWS enables upregulation of select cortical circuits (likely those which were involved in mnemonic processing) through a spindle-related process, whereas REM sleep mediates general downregulation, possibly through synaptic re-normalization.
Sleep is thought to globally downregulate cortical excitability and, concurrently, to upregulate synaptic connections in neuron ensembles with newly encoded memory, with upregulation representing a function of sleep spindles. Using
two-photon calcium imaging in combination with surface EEG recordings, we classified cells based on their calcium activity during sleep spindles. Spindle-active pyramidal (Pyr) cells persistently increased calcium activity during slow-wave sleep (SWS) episodes while spindle-inactive cells decreased calcium activity. Subsequent rapid eye movement (REM) sleep episodes profoundly reduced calcium activity in both cell clusters. Results indicate that SWS allows for a spindle-related differential upregulation of ensembles whereas REM sleep functions to globally downregulate networks.
Brain rhythms regulate information processing in different states to enable learning and memory formation. The <1 Hz sleep slow oscillation hallmarks slow-wave sleep and is critical to memory ...consolidation. Here we show in sleeping humans that auditory stimulation in phase with the ongoing rhythmic occurrence of slow oscillation up states profoundly enhances the slow oscillation rhythm, phase-coupled spindle activity, and, consequently, the consolidation of declarative memory. Stimulation out of phase with the ongoing slow oscillation rhythm remained ineffective. Closed-loop in-phase stimulation provides a straight-forward tool to enhance sleep rhythms and their functional efficacy.
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► Sounds in phase with slow oscillations enhance brain slow oscillatory activity. ► In-phase stimulation enhances spindle activity phase coupled to slow oscillations. ► In-phase stimulation promotes sleep-dependent memory consolidation. ► Closed-loop stimulation provides a new tool for probing the function of EEG rhythms
Ngo et al. show that the slow oscillation, a hallmark of slow-wave sleep, can be enhanced by low volume sounds presented repeatedly in phase with the oscillatory rhythm. This enhancement strengthened the consolidation of word-pair memories during sleep.
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