Network Homeostasis and State Dynamics of Neocortical Sleep

Watson, Brendon O.; Levenstein, Daniel; Greene, Jeremy A.; Gelinas, Jennifer N.; Buzsáki, György

doi:10.1016/j.neuron.2016.03.036

Cited by 289 publications

(505 citation statements)

References 70 publications

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“…However, selectively after learning, a bimodality of cortical IEG expression was revealed as a sustained relative increase in gene expression during sleep, analogous to reported firing rate changes [35]. These bimodal changes are consistent with the concept of a selective strengthening of synapses involved in engrams—which most likely includes only a small percentage of neurons—and the general downscaling of all other synapses in mPFC during sleep, with a consequential enhancement of signal-to-noise ratio in the cortex as a signature of systems consolidation [16,17].…”

Section: Discussionmentioning

confidence: 65%

“…We predicted that novelty would lead to a learning-independent increase in immediate early gene (IEG) mRNA expression in the hippocampus related to the production of plasticity-related proteins implicated in synaptic tagging and capture [32] and the consequent consolidation of hippocampal traces [29]. In contrast, sleep should trigger a relatively selective increase in cortical consolidation after learning but against the background of a time-dependent down-regulation of IEG expression unrelated to memory consolidation, resembling findings recently reported for firing-rate changes [16,17,33–35]. …”

Section: Introductionmentioning

confidence: 75%

“…This time-related decrease—possibly a “wash-out” of gene expression–related products—may be related to “downscaling” [34,60]. Downscaling is a type of cortical resetting process that is not yet well understood mechanistically [35,61–64]. The important idea is that within engram cells with potentiated synapses, synapses that are recently inactive are selectively downscaled, while the potentiated synapses of a new memory trace may be left intact [33,34,60].…”

Section: Discussionmentioning

confidence: 99%

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The Yin and Yang of Memory Consolidation: Hippocampal and Neocortical

et al. 2017

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While hippocampal and cortical mechanisms of memory consolidation have long been studied, their interaction is poorly understood. We sought to investigate potential interactions with respect to trace dominance, strengthening, and interference associated with postencoding novelty or sleep. A learning procedure was scheduled in a watermaze that placed the impact of novelty and sleep in opposition. Distinct behavioural manipulations—context preexposure or interference during memory retrieval—differentially affected trace dominance and trace survival, respectively. Analysis of immediate early gene expression revealed parallel up-regulation in the hippocampus and cortex, sustained in the hippocampus in association with novelty but in the cortex in association with sleep. These findings shed light on dynamically interacting mechanisms mediating the stabilization of hippocampal and neocortical memory traces. Hippocampal memory traces followed by novelty were more dominant by default but liable to interference, whereas sleep engaged a lasting stabilization of cortical traces and consequent trace dominance after preexposure.

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Section: Discussionmentioning

confidence: 65%

Section: Introductionmentioning

confidence: 75%

Section: Discussionmentioning

confidence: 99%

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The Yin and Yang of Memory Consolidation: Hippocampal and Neocortical

et al. 2017

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“…The obtained clusters were manually controlled in the ‘KlustaViewa’ environment. Clusters containing multiple single units (evident from the lack of a >1 ms absolute refractory period in the autocorrelogram48) were manually split and only kept if splitting resulted in single-units with clear refractory period. Individual clusters belonging to the same unit (evident from a symmetric drop in the cross-correlogram at short time lags) were merged.…”

Section: Methodsmentioning

confidence: 99%

Organization of prefrontal network activity by respiration-related oscillations

Biskamp

Bartos

Sauer

2017

Sci Rep

182

206

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The medial prefrontal cortex (mPFC) integrates information from cortical and sub-cortical areas and contributes to the planning and initiation of behaviour. A potential mechanism for signal integration in the mPFC lies in the synchronization of neuronal discharges by theta (6–12 Hz) activity patterns. Here we show, using in vivo local field potential (LFP) and single-unit recordings from awake mice, that prominent oscillations in the sub-theta frequency band (1–5 Hz) emerge during awake immobility in the mPFC. These oscillation patterns are distinct from but phase-locked to hippocampal theta activity and occur synchronized with nasal respiration (hence termed prefrontal respiration rhythm [PRR]). PRR activity modulates the amplitude of prefrontal gamma rhythms with greater efficacy than theta oscillations. Furthermore, single-unit discharges of putative pyramidal cells and GABAergic interneurons are entrained by prefrontal PRR and nasal respiration. Our data thus suggest that PRR activity contributes to information processing in the prefrontal neuronal network.

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“…We suggest however, that the results of the current study may open a window on the organization of cortical networks to serve diverse sleep functions. Normal memory processing can involve both REM and NREM sleep-dependent mechanisms (50) and the processes of sleep homeostasis seen after sleep loss may represent compensatory mechanisms to maintain sleep-dependent memory consolidation. Specifically, synaptic potentiation in REM sleep was proposed as part of a two-stage process of memory consolidation (7,51) in which neuronal circuits reactivated in SWS (52)(53)(54) are primed for long-term potentiation (LTP) which occurs in the ensuing REM sleep supported by enhanced plasticity-related gene expression (55,56) and high-frequency "desynchronized" activity, characteristic for this state.…”

Section: The Pattern Of Rem Sleep Rebound Is Mirrored In Eeg Slowmentioning

confidence: 99%

Differential modulation of global and local neural oscillations in REM sleep by homeostatic sleep regulation

Kim

Kocsis

Hwang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Homeostatic rebound in rapid eye movement (REM) sleep normally occurs after acute sleep deprivation, but REM sleep rebound settles on a persistently elevated level despite continued accumulation of REM sleep debt during chronic sleep restriction (CSR). Using highdensity EEG in mice, we studied how this pattern of global regulation is implemented in cortical regions with different functions and network architectures. We found that across all areas, slow oscillations repeated the behavioral pattern of persistent enhancement during CSR, whereas high-frequency oscillations showed progressive increases. This pattern followed a common rule despite marked topographic differences. The findings suggest that REM sleep slow oscillations may translate top-down homeostatic control to widely separated brain regions whereas fast oscillations synchronizing local neuronal ensembles escape this global command. These patterns of EEG oscillation changes are interpreted to reconcile two prevailing theories of the function of sleep, synaptic homeostasis and sleep dependent memory consolidation. There has been substantial recent progress in understanding the neuronal mechanisms of two seemingly unrelated but, more likely, complementary functions of sleep. The first, conceptualized as the synaptic homeostasis theory (1), produced experimental evidence for a global downscaling of synaptic strength during sleep to offset the unsustainable upscaling associated with neuronal activation during the preceding period of wakefulness (2). The second line of research keeps accumulating data to support an active role of sleep in offline memory processing (3) and argues that certain synapses not only escape global downscaling in sleep but instead are potentiated; firing rate and synchrony in select neuronal ensembles representing newly acquired and deemed relevant information are increased. The mechanisms of how these two proposed functions of sleep are reconciled on the network or ensemble level are poorly understood.From the very beginning, both processes were linked to specific oscillatory patterns of neuronal activity. The synaptic homeostasis hypothesis, and sleep homeostatic regulation in general, was correlated with EEG delta power (4) and memory consolidation was associated with episodic fast oscillations during non-REM (NREM) sleep (5). Recent evidence from network level investigations concur. On the one hand, different measures of homeostatic downscaling on the neuronal level (synaptic depotentiation, decrease in firing rate, decreased synchrony, etc.) were shown to correlate with the global decrease in delta power (6). On the other hand, reactivation of memory traces primarily occur during spindle-ripple events (7) and requires the temporal organization provided by local fast oscillations for coordination of firing within local neuronal ensembles.Slow and fast oscillations, respectively, support global and local processing, not only in NREM sleep but also in any brain state, in general. Slow oscillations (delta, theta, alpha, beta1) all...

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Network Homeostasis and State Dynamics of Neocortical Sleep

Cited by 289 publications

References 70 publications

The Yin and Yang of Memory Consolidation: Hippocampal and Neocortical

The Yin and Yang of Memory Consolidation: Hippocampal and Neocortical

Organization of prefrontal network activity by respiration-related oscillations

Differential modulation of global and local neural oscillations in REM sleep by homeostatic sleep regulation

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