Laminar analysis of slow wave activity in humans

Richárd Csercsa, Balázs Dombovári, Dániel Fabó, L. Wittner, L. Erőss, László Entz, András Sólyom, G. Rásonyi, Anna Szcs, A. Kelemen, R. Jakus, Vera Juhos, László Grand, Andor Magony, P. Halász, T. Freund, Z. Maglóczky, Sydney S. Cash, László Papp, G. KarmosEric Halgren, I. Ulbert

Research output: Contribution to journalArticle

120 Citations (Scopus)

Abstract

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 (0.3-200Hz) 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±10ms 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.

Original languageEnglish
Pages (from-to)2814-2829
Number of pages16
JournalBrain
Volume133
Issue number9
DOIs
Publication statusPublished - 2010

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Human Activities
Sleep
Partial Epilepsy
Brain
Microelectrodes
Eye Movements
Action Potentials
Seizures

Keywords

  • current source density
  • laminar recording
  • sleep
  • slow wave activity
  • unit activity

ASJC Scopus subject areas

  • Clinical Neurology
  • Medicine(all)

Cite this

Laminar analysis of slow wave activity in humans. / Csercsa, Richárd; Dombovári, Balázs; Fabó, Dániel; Wittner, L.; Erőss, L.; Entz, László; Sólyom, András; Rásonyi, G.; Szcs, Anna; Kelemen, A.; Jakus, R.; Juhos, Vera; Grand, László; Magony, Andor; Halász, P.; Freund, T.; Maglóczky, Z.; Cash, Sydney S.; Papp, László; Karmos, G.; Halgren, Eric; Ulbert, I.

In: Brain, Vol. 133, No. 9, 2010, p. 2814-2829.

Research output: Contribution to journalArticle

Csercsa, R, Dombovári, B, Fabó, D, Wittner, L, Erőss, L, Entz, L, Sólyom, A, Rásonyi, G, Szcs, A, Kelemen, A, Jakus, R, Juhos, V, Grand, L, Magony, A, Halász, P, Freund, T, Maglóczky, Z, Cash, SS, Papp, L, Karmos, G, Halgren, E & Ulbert, I 2010, 'Laminar analysis of slow wave activity in humans', Brain, vol. 133, no. 9, pp. 2814-2829. https://doi.org/10.1093/brain/awq169
Csercsa R, Dombovári B, Fabó D, Wittner L, Erőss L, Entz L et al. Laminar analysis of slow wave activity in humans. Brain. 2010;133(9):2814-2829. https://doi.org/10.1093/brain/awq169
Csercsa, Richárd ; Dombovári, Balázs ; Fabó, Dániel ; Wittner, L. ; Erőss, L. ; Entz, László ; Sólyom, András ; Rásonyi, G. ; Szcs, Anna ; Kelemen, A. ; Jakus, R. ; Juhos, Vera ; Grand, László ; Magony, Andor ; Halász, P. ; Freund, T. ; Maglóczky, Z. ; Cash, Sydney S. ; Papp, László ; Karmos, G. ; Halgren, Eric ; Ulbert, I. / Laminar analysis of slow wave activity in humans. In: Brain. 2010 ; Vol. 133, No. 9. pp. 2814-2829.
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AU - Csercsa, Richárd

AU - Dombovári, Balázs

AU - Fabó, Dániel

AU - Wittner, L.

AU - Erőss, L.

AU - Entz, László

AU - Sólyom, András

AU - Rásonyi, G.

AU - Szcs, Anna

AU - Kelemen, A.

AU - Jakus, R.

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AU - Grand, László

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AU - Halgren, Eric

AU - Ulbert, I.

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N2 - 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 (0.3-200Hz) 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±10ms 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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