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Laminar analysis of slow wave activity in humans
Open accessAbstract
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.
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“At the neocortical level, the slow oscillation in terms of EEG rhythms strongly modulates the amplitude of faster beta and gamma frequencies which is reduced to a minimum during the hyperpolarizing down-phase of the slow oscillation (224,240,828,829).”
From About Sleep's Role in Memory (2013) · cites this paper as [240]
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Metadata
- Authors
- Csercsa, R., Dombovári, B., Fabó, D., Wittner, L., Erőss, L., Entz, L., Sólyom, A., Rásonyi, G., Szűcs, A., Kelemen, A., Jakus, R., Juhos, V., Grand, L., Magony, A., Halász, P., Freund, T. F., Maglóczky, Z., Cash, S. S., Papp, L., Karmos, G., Halgren, E., & Ulbert, I.
- Affiliations
- Hungarian Academy of Sciences (HU)
- Pázmány Péter Catholic University (HU)
- Országos Idegsebészeti Tudományos Intézet (HU)
- Unified Szent István and Szent László Hospital (HU)
- HUN-REN Institute of Experimental Medicine (HU)
- Massachusetts General Hospital (US)
- University of California San Diego (US)
- ORCID
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-07-23
- Volume
- 133
- Issue
- 9
- Pages
- 2814-2829
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC3105490
- OpenAlex
- W2125813953
- Cited by
- 239
- References
- 96
- Citations by year
- 2026: 5 · 2025: 14 · 2024: 18 · 2023: 13 · 2022: 16 · 2021: 9 · 2020: 13 · 2019: 16 · 2018: 10 · 2017: 10 · 2016: 9 · 2015: 18 · 2014: 17 · 2013: 28 · 2012: 21
- FWCI
- 13.77
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Danish Cancer Society Research Center
- Agence Nationale de la Recherche
- Hungarian Scientific Research Fund
- Nemzeti Kutatási és Technológiai Hivatal
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- slow-wave activity, sleep spindles, slow-wave sleep, cortical oscillations, supragranular layers, intracortical recording, drug-resistant epilepsy, seizure localization, membrane currents, current source density, electrocorticography
- MeSH terms
- Action Potentials, Analysis of Variance, Animals, Brain, Brain Mapping, Electroencephalography, Electrophysiology, Epilepsy, Humans, Neurons, Periodicity, Spectrum Analysis
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