Research ReportTheta activity in the waking EEG is a marker of sleep propensity in the rat
Introduction
Sleep propensity rises progressively during waking and declines monotonically during sleep. The level of EEG slow-wave activity (SWA; EEG power between 0.5 and 4.0 Hz) increases proportionally to the duration of prior wakefulness, and thus reflects the homeostatic aspect of sleep regulation [5], [11], [26]. This fundamental property of sleep has been demonstrated for a wide variety of different species [6], [25].
In the two-process model of sleep regulation, the time course of the rise of the homeostatic Process S was derived from the level of SWA in non-rapid eye movement (NREM) sleep preceding and following a waking episode [1], [5]. In humans, a marker of Process S was identified also in the waking EEG. Thus, an increase of delta or theta power occurred in the course of wakefulness [2], [3], [9], [12], [22], [28]. Further evidence for a link between theta activity in the waking EEG and sleep homeostasis was provided by a between-subject correlative study [12]. The rate of increase of theta power during 40 h of waking correlated positively with the increase of SWA in NREM sleep. Moreover, theta activity in the waking EEG paralleled subjective sleepiness [2], [12], [15], [20], [21], [24].
In animals, an EEG correlate for sleep pressure during waking has not been reported. Rodents exhibit a variety of waking behaviors including active exploration and quiescence with low locomotion. These differences in behavior are reflected in the EEG [29]. During active waking, associated with voluntary movements, the EEG is desynchronized, dominated by fast frequencies and regular theta activity, while quiet waking is characterized by a mixed pattern with slower waves [14], [16], [29].
The changes in arousal level and EEG activity are interrelated because both depend on the tonic depolarizing input from the brainstem [18], [23]. Several neurotransmitters play a major role in the “arousal brain system” [18]. The neurons comprising the ascending reticular activating system, as well as thalamocortical neurons, use glutamate as a transmitter; pontomesencephalic neurons use acetylcholine, while locus coeruleus neurons, projecting in a diffuse manner from the brainstem to the entire forebrain, are adrenergic [18]. Activation of these nuclei results in the blockage of synchronized low-frequency oscillations in the thalamocortical system that are typical for NREM sleep, and in the generation of fast activity, typical for wakefulness [23].
We hypothesized that an increase of sleep propensity could be manifested in the EEG during quiet wakefulness also in rodents in the course of prolonged wakefulness. To test this hypothesis, we subdivided the waking epochs during a 6-h sleep deprivation (SD) into quiet waking and active waking on the basis of EMG activity, analyzed the changes in the power spectrum, and investigated whether the changes were related to the increase of SWA during recovery sleep.
Section snippets
Animals
The local governmental commission for animal research approved the experiments. Adult male albino rats of the Sprague–Dawley strain (n = 14) with a mean body weight 277.5 ± 5.1 (SEM) g were used. The animals were kept individually in Macrolon cages (53 × 34 × 37 cm) with food and water available ad libitum, and maintained on a 12-h light–12-h dark cycle (light from 8.00 to 20.00 h; 7 W OSRAM Dulux EL energy saving lamp, approximately 30 lx). Ambient temperature was maintained at 21–22 °C. Under
The largest increase in EEG power during SD was in the theta band
The waking EEG spectrum during SD was characterized by a prominent peak at 7.5 Hz (Fig. 1, right panel, indicated by a vertical line). During SDL, EEG power computed for 2-h intervals increased significantly in the 1.5–6.5 Hz range in the course of SD, while power at the peak frequency did not change (1-way ANOVA for repeated measures, factor ‘2-h interval’: three intervals). Fig. 2 (left panel) illustrates the absolute EEG spectra of the first and last 2-h SD. The comparison of EEG power
Discussion
We demonstrate for the first time in a rodent that an EEG parameter during wakefulness reflects sleep propensity and is related to the subsequent increase in sleep intensity. EEG power in the theta band increased during SD, and correlated positively with the level of SWA in NREM sleep during recovery. The increase of EEG power at the theta-peak frequency was restricted to epochs of quiet waking. This effect was statistically significant for SDL and showed a trend for SDD.
The results are
Acknowledgments
We thank Drs. A.A. Borbély and P. Achermann for advice and comments on the manuscript. The study was supported by Swiss National Science Foundation grants 3100A0-100567, 3100-053005.97, and 3100.062112.00.
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Present address: University of Wisconsin-Madison, Psychiatric Institute and Clinics, 6001 Research Park Blvd., Madison, WI 53719, USA.