Dataset Information

Infraslow coordination of slow wave activity through altered neuronal synchrony.

ABSTRACT: Slow wave activity (SWA; the EEG power between 0.5 and 4 Hz during non-rapid eye movement sleep [NREM]) is the best electrophysiological marker of sleep need; SWA dissipates across the night and increases following sleep deprivation. In addition to these well-documented homeostatic SWA trends, SWA exhibits extensive variability across shorter timescales (seconds to minutes) and between local cortical regions. The physiological underpinnings of SWA variability, however, remain poorly characterized. In male Sprague-Dawley rats, we observed that SWA exhibits pronounced infraslow fluctuations (~40- to 120-s periods) that are coordinated across disparate cortical locations. Peaks in SWA across infraslow cycles were associated with increased slope, amplitude, and duration of individual slow waves and a reduction in the total number of waves and proportion of multipeak waves. Using a freely available data set comprised of extracellular unit recordings during consolidated NREM episodes in male Long-Evans rats, we further show that infraslow SWA does not appear to arise as a consequence of firing rate modulation of putative excitatory or inhibitory neurons. Instead, infraslow SWA was associated with alterations in neuronal synchrony surrounding "On"/"Off" periods and changes in the number and duration of "Off" periods. Collectively, these data provide a mechanism by which SWA can be coordinated across disparate cortical locations and thereby connect local and global expression of this patterned neuronal activity. In doing so, infraslow SWA may contribute to the regulation of cortical circuits during sleep and thereby play a critical role in sleep function.

SUBMITTER: Dash MB

PROVIDER: S-EPMC6930134 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Infraslow coordination of slow wave activity through altered neuronal synchrony.

Dash Michael B MB

Sleep 20191201 12

Slow wave activity (SWA; the EEG power between 0.5 and 4 Hz during non-rapid eye movement sleep [NREM]) is the best electrophysiological marker of sleep need; SWA dissipates across the night and increases following sleep deprivation. In addition to these well-documented homeostatic SWA trends, SWA exhibits extensive variability across shorter timescales (seconds to minutes) and between local cortical regions. The physiological underpinnings of SWA variability, however, remain poorly characterize ...[more]

PMID: 31353415

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Project description:Brain electrical activity is largely composed of oscillations at characteristic frequencies. These rhythms are hierarchically organized and are thought to perform important pathological and physiological functions. The slow wave is a fundamental cortical rhythm that emerges in deep non-rapid eye movement sleep. In animals, the slow wave modulates delta, theta, spindle, alpha, beta, gamma and ripple oscillations, thus orchestrating brain electrical rhythms in sleep. While slow wave activity can enhance epileptic manifestations, it is also thought to underlie essential restorative processes and facilitate the consolidation of declarative memories. Animal studies show that slow wave activity is composed of rhythmically recurring phases of widespread, increased cortical cellular and synaptic activity, referred to as active- or up-state, followed by cellular and synaptic inactivation, referred to as silent- or down-state. However, its neural mechanisms in humans are poorly understood, since the traditional intracellular techniques used in animals are inappropriate for investigating the cellular and synaptic/transmembrane events in humans. To elucidate the intracortical neuronal mechanisms of slow wave activity in humans, novel, laminar multichannel microelectrodes were chronically implanted into the cortex of patients with drug-resistant focal epilepsy undergoing cortical mapping for seizure focus localization. Intracortical laminar local field potential gradient, multiple-unit and single-unit activities were recorded during slow wave sleep, related to simultaneous electrocorticography, and analysed with current source density and spectral methods. We found that slow wave activity in humans reflects a rhythmic oscillation between widespread cortical activation and silence. Cortical activation was demonstrated as increased wideband (0.3-200 Hz) spectral power including virtually all bands of cortical oscillations, increased multiple- and single-unit activity and powerful inward transmembrane currents, mainly localized to the supragranular layers. Neuronal firing in the up-state was sparse and the average discharge rate of single cells was less than expected from animal studies. Action potentials at up-state onset were synchronized within +/-10 ms across all cortical layers, suggesting that any layer could initiate firing at up-state onset. These findings provide strong direct experimental evidence that slow wave activity in humans is characterized by hyperpolarizing currents associated with suppressed cell firing, alternating with high levels of oscillatory synaptic/transmembrane activity associated with increased cell firing. Our results emphasize the major involvement of supragranular layers in the genesis of slow wave activity.

Project description:Slow wave activity (SWA) during sleep is associated with synaptic regulation and memory processing functions. Each cycle of non-rapid-eye-movement (NREM) sleep demonstrates a waxing and waning amount of SWA during the transitions between stages N2 and N3 sleep, and the deeper N3 sleep is associated with an increased density of SWA. Further, SWA is an amalgam of different types of slow waves, each identifiable by their temporal coupling to spindle subtypes with distinct physiological features. The objectives of this study were to better understand the neurobiological properties that distinguish different slow wave and spindle subtypes, and to examine the composition of SWA across cycles of NREM sleep. We further sought to explore changes in the composition of NREM cycles that occur among aging adults. To address these goals, we analyzed subsets of data from two well-characterized cohorts of healthy adults: (1) The DREAMS Subjects Database (n = 20), and (2) The Cleveland Family Study (n = 60). Our analyses indicate that slow wave/spindle coupled events can be characterized as frontal vs. central in their relative distribution between electroencephalography (EEG) channels. The frontal predominant slow waves are identifiable by their coupling to late-fast spindles and occur more frequently during stage N3 sleep. Conversely, the central-associated slow waves are identified by coupling to early-fast spindles and favor occurrence during stage N2 sleep. Together, both types of slow wave/spindle coupled events form the composite of SWA, and their relative contribution to the SWA rises and falls across cycles of NREM sleep in accordance with depth of sleep. Exploratory analyses indicated that older adults produce a different composition of SWA, with a shift toward the N3, frontal subtype, which becomes increasingly predominant during cycles of NREM sleep. Overall, these data demonstrate that subtypes of slow wave/spindle events have distinct cortical propagation patterns and differ in their distribution across lighter vs. deeper NREM sleep. Future efforts to understand how slow wave sleep and slow wave/spindle coupling impact memory performance and neurological disease may benefit from examining the composition of SWA to avoid potential confounds that may occur when comparing dissimilar neurophysiological events.

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Infraslow coordination of slow wave activity through altered neuronal synchrony.

Publications

Infraslow coordination of slow wave activity through altered neuronal synchrony.

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