Electrophysiological correlates of sleep delta waves1

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Abstract

Recent studies have disclosed several oscillations occurring during resting sleep within the frequency range of the classical delta band (0.5–4 Hz). There are at least 3 oscillations with distinct mechanisms and sites of origin: a slow (<1 Hz) cortically-generated oscillation, a clock-like thalamic oscillation (1–4 Hz), and a cortical oscillation (1–4 Hz). The present paper reviews data on these oscillations and the possible mechanisms which coalesce them into the polymorphic waves of slow wave sleep. Data stem from intracellular (over 500 single cell and 50 double impalements) and field potentials recorded from the cortex and thalamus of cats (120 animals) under ketamine and xylazine anesthesia. Other experiments were based on whole night EEG recordings from humans (5 subjects). The frequency of the slow oscillation both in anesthetized animals and in naturally sleeping humans ranged between 0.1 and 1 Hz (89% of the cases being between 0.5 and 0.9 Hz). The slow (<1 Hz) oscillation is reflected in the EEG as rhythmic sequences of surface-negative waves (associated with hyperpolarizations of deeply-lying neurons) and surface-positive K-complexes (representing excitation in large pools of cortical neurons). Through its long-range synchronization, the slow oscillation has the ability to trigger and to group thalamically-generated spindles and two delta (1–4 Hz) oscillations. Finally, it is argued that the analysis of the electroencephalogram should transcend the spectral analyses, by taking into account the shape of the waves and, when possible, the basic mechanisms that generate those waves.

Section snippets

Oscillations or waves?

One of the major sources of confusion stems from the undiscriminated use of terms such as oscillations or waves. From the spectral point of view there is no reliable border between the two, both contributing to the power spectrum. However, from the electrophysiological point of view, waves and oscillations may reflect different phenomena. The term oscillation may have various meanings according to the context. In its most general form, it is a variation of a parameter (e.g. current, voltage)

Slow cortical oscillation (<1 Hz) during sleep

A slow oscillation (<1 Hz) has been described in intracellular recordings of cortical neurons in anesthetized cats (Steriade et al., 1993d). This cellular oscillation is marked by a continuous alternation of the membrane potential between two voltage levels (Fig. 1): a depolarized and a hyperpolarized one. The membrane depolarization lasts for about 0.4–0.8 s, is due to synchronous synaptic activities in the cortical network (Amzica and Steriade, 1995b), and is made mainly of excitatory and

Slow (<1 Hz) glial activities

It has long been known that glial cells of the cerebral cortex exhibit electrical activity related to the physiological behavior of the brain. The contribution of glial cells to the genesis of delta waves has been repeatedly hypothesized (see Elul, 1972; Ball et al., 1977), but never demonstrated. The relationship between glial and neural activities has been mostly investigated through non-electric methods which did not disclose the basic mechanisms that underlie the communication between

Integration of activities below 4 Hz in corticothalamic networks

Several types of activities in the 0.5–4 Hz frequency band have been presented here. They have different sites and mechanisms of genesis, and may contribute together or separately to the delta activity recorded in the EEG. The slow (<1 Hz) oscillation has a distinct nature from other slow (1–4 Hz) rhythms. It should be therefore regarded as a distinct activity, not only because of its frequency range, but mostly because of its electrophysiologic features and because it has the ability to

Methodological issues for electroencephalographers

We believe that analyses of EEG data should take into consideration the actual aspect of waves and, if possible, their relationship with the state of the cellular aggregates of the corticothalamic network. Obviously this is not possible by merely a spectral approach. Fourier spectra are not able to discriminate between periodic phenomena and waves with a given shape, i.e. with a given spectral content. During quiet sleep, the slow oscillation provokes rhythmic KCs (see above) every 1 s or more.

Conclusions

Several electrophysiological phenomena are responsible for the genesis of <4 Hz activities (Fig. 9). Depending on the weight of synaptic linkages, on local circuit configurations and on the general behavioral state of the network, the slow oscillation, the thalamically generated clock-like delta oscillation and cortical delta waves may coalesce to produce the intricate electrographic pattern of slow wave sleep. The use of a more specific language (slow oscillation, thalamic clock-like delta,

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