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      Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples

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          Abstract

          Sleep is pivotal for memory consolidation. According to two-stage accounts, memory traces are gradually translocated from hippocampus to neocortex during non-rapid-eye-movement (NREM) sleep. Mechanistically, this information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. To test this hypothesis, we analyzed intracranial and scalp Electroencephalography sleep recordings from pre-surgical epilepsy patients. We first observed a concurrent spindle power increase in hippocampus (HIPP) and neocortex (NC) time-locked to individual hippocampal ripple events. Coherence analysis confirmed elevated levels of hippocampal-neocortical spindle coupling around ripples, with directionality analyses indicating an influence from NC to HIPP. Importantly, these hippocampal-neocortical dynamics were particularly pronounced during long-duration compared to short-duration ripples. Together, our findings reveal a potential mechanism underlying active consolidation, comprising a neocortical-hippocampal-neocortical reactivation loop initiated by the neocortex. This hippocampal-cortical dialogue is mediated by sleep spindles and is enhanced during long-duration hippocampal ripples.

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          Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration.

          Sleep is universal, tightly regulated, and its loss impairs cognition. But why does the brain need to disconnect from the environment for hours every day? The synaptic homeostasis hypothesis (SHY) proposes that sleep is the price the brain pays for plasticity. During a waking episode, learning statistical regularities about the current environment requires strengthening connections throughout the brain. This increases cellular needs for energy and supplies, decreases signal-to-noise ratios, and saturates learning. During sleep, spontaneous activity renormalizes net synaptic strength and restores cellular homeostasis. Activity-dependent down-selection of synapses can also explain the benefits of sleep on memory acquisition, consolidation, and integration. This happens through the offline, comprehensive sampling of statistical regularities incorporated in neuronal circuits over a lifetime. This Perspective considers the rationale and evidence for SHY and points to open issues related to sleep and plasticity. Copyright © 2014 Elsevier Inc. All rights reserved.
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            Measuring phase synchrony in brain signals

            This article presents, for the first time, a practical method for the direct quantification of frequency‐specific synchronization (i.e., transient phase‐locking) between two neuroelectric signals. The motivation for its development is to be able to examine the role of neural synchronies as a putative mechanism for long‐range neural integration during cognitive tasks. The method, called phase‐locking statistics (PLS), measures the significance of the phase covariance between two signals with a reasonable time‐resolution (<100 ms). Unlike the more traditional method of spectral coherence, PLS separates the phase and amplitude components and can be directly interpreted in the framework of neural integration. To validate synchrony values against background fluctuations, PLS uses surrogate data and thus makes no a priori assumptions on the nature of the experimental data. We also apply PLS to investigate intracortical recordings from an epileptic patient performing a visual discrimination task. We find large‐scale synchronies in the gamma band (45 Hz), e.g., between hippocampus and frontal gyrus, and local synchronies, within a limbic region, a few cm apart. We argue that whereas long‐scale effects do reflect cognitive processing, short‐scale synchronies are likely to be due to volume conduction. We discuss ways to separate such conduction effects from true signal synchrony. Hum Brain Mapping 8:194–208, 1999. © 1999 Wiley‐Liss, Inc.
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              Large-scale cortical correlation structure of spontaneous oscillatory activity.

              Little is known about the brain-wide correlation of electrophysiological signals. We found that spontaneous oscillatory neuronal activity exhibited frequency-specific spatial correlation structure in the human brain. We developed an analysis approach that discounts spurious correlation of signal power caused by the limited spatial resolution of electrophysiological measures. We applied this approach to source estimates of spontaneous neuronal activity reconstructed from magnetoencephalography. Overall, correlation of power across cortical regions was strongest in the alpha to beta frequency range (8–32 Hz) and correlation patterns depended on the underlying oscillation frequency. Global hubs resided in the medial temporal lobe in the theta frequency range (4–6 Hz), in lateral parietal areas in the alpha to beta frequency range (8–23 Hz) and in sensorimotor areas for higher frequencies (32–45 Hz). Our data suggest that interactions in various large-scale cortical networks may be reflected in frequency-specific power envelope correlations.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                13 July 2020
                2020
                : 9
                : e57011
                Affiliations
                [1 ]School of Psychology and Centre for Human Brain Health, University of Birmingham BirminghamUnited Kingdom
                [2 ]Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Centre NijmegenNetherlands
                [3 ]Department of Epileptology, University of Bonn BonnGermany
                University of Lübeck Germany
                University of Texas at Austin United States
                University of Lübeck Germany
                Max Planck Institute for Human Development Germany
                University of California, Irvine United States
                Author information
                https://orcid.org/0000-0001-5828-5588
                https://orcid.org/0000-0002-0558-9745
                Article
                57011
                10.7554/eLife.57011
                7363445
                32657268
                3aee52c5-3995-4291-8d39-6d26bf1a5959
                © 2020, Ngo et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 17 March 2020
                : 06 July 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome;
                Award ID: 107672/Z/15/Z
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: SFB1089
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                Triggered by (long-duration) hippocampal ripples, spindles facilitate communication between the hipppocampus and neocortex during natural sleep.

                Life sciences
                sleep,hippocampus,spindles,ripples,human
                Life sciences
                sleep, hippocampus, spindles, ripples, human

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