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Grouping of Spindle Activity During Slow Oscillations in Human Non-Rapid Eye Movement Sleep

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Grouping of Spindle Activity During Slow Oscillations in Human Non-Rapid Eye Movement Sleep The Journal of Neuroscience, December 15, 2002, 22(24):10941–10947 Grouping of Spindle Activity during Slow Oscillations in Human Non-Rapid Eye Movement Sleep Matthias Mo¨ lle, Lisa Marshall, Steffen Gais, and Jan Born Institute of Neuroendocrinology, University of Lu¨ beck, 23538 Lu¨ beck, Germany Based on findings primarily in cats, the grouping of spindle spindle activity 400–500 msec after negative half-waves was activity and fast brain oscillations by slow oscillations during more than twofold the increase during slow positive half-waves slow-wave sleep (SWS) has been proposed to represent an ( p Ͻ 0.001). A similar although less pronounced dynamic was essential feature in the processing of memories during sleep. observed for beta activity, but not for alpha and theta frequen- We examined whether a comparable grouping of spindle and cies. Discrete spindles identified during stages 2 and 3 of fast activity coinciding with slow oscillations can be found in non-rapid eye movement (REM) sleep coincided with a discrete human SWS. For negative and positive half-waves of slow slow positive half-wave-like potential preceded by a pro- oscillations (dominant frequency, 0.7–0.8 Hz) identified during nounced negative half-wave ( p Ͻ 0.01). These results provide SWS in humans (n ϭ 13), wave-triggered averages of root mean the first evidence in humans of grouping of spindle and beta square (rms) activity in the theta (4–8 Hz), alpha (8–12 Hz), activity during slow oscillations. They support the concept that spindle (12–15 Hz), and beta (15–25 Hz) range were formed. phases of cortical depolarization during slow oscillations, re- Slow positive half-waves were linked to a pronounced and flected by surface-positive (depth-negative) field potentials, widespread increase in rms spindle activity, averaging 0.63 Ϯ drive the thalamocortical spindle activity. The drive is particu- 0.065 ␮V (23.4%; p Ͻ 0.001, with reference to baseline) at the larly strong during cortical depolarization, expressed as midline central electrode (Cz). In contrast, spindle activity was surface-positive field potentials. suppressed during slow negative half-waves, on average by Key words: slow oscillations; spindle activity; human; sleep; Ϫ0.65 Ϯ 0.06 ␮VatCz(Ϫ22%; p Ͻ 0.001). An increase in EEG; cortical depolarization In recent years, studies in humans and animals have accumulated ization of cortical pyramidal neurons, with the depolarization converging evidence for the hypothesis that a reprocessing of associated with depth-negative and surface-positive EEG field events acquired during previous wakefulness occurs during non- potentials and, conversely, the hyperpolarizing phase associated rapid eye movement (REM) sleep, which eventually supports with a depth-positive, surface-negative EEG potential (Steriade long-term storage of respective neuronal representations (Plihal et al., 1994; Contreras and Steriade, 1995). Spindle activity orig- and Born, 1997; Buzsa´ki, 1998; Gais et al., 2000; Sutherland and inating within thalamo-neocortical loops and also faster frequen- McNaughton, 2000). At the level of rhythmic activity in the brain, cies were found to be driven during the depolarizing (surface- spindle activity (12–15 Hz) and faster oscillatory activity have positive) phase of slow waves, during which the firing of both been linked to aspects of the consolidation process (Siapas pyramidal cells is increased. In contrast, the hyperpolarizing and Wilson, 1998; Steriade and Amzica, 1998; Destexhe et al., (surface-negative) phase is associated with neuronal silence 1999; Sejnowski and Destexhe, 2000; Gais et al., 2002). Spindle (Buzsa´ki et al., 1988; Contreras and Steriade, 1995; Steriade et 2ϩ oscillations provoke a massive Ca entry into the spindling al., 1996; Destexhe et al., 1999). cortical cells, and thus could set the stage for plastic synaptic A grouping of spindle activity by slow oscillations has been changes that are supposed to be induced during subsequent suggested also to be present in the human EEG (Achermann and slow-wave activity. Notably, spindle and fast oscillatory activity in Borbe´ly, 1997; Amzica and Steriade, 1997). However, distinct Ͻ cats have been found to be distinctly grouped by slow ( 1Hz) slow rhythms for spindles were revealed at a periodicity of ϳ4 sec oscillations (Contreras and Steriade, 1995, 1996; Contreras et al., and slower (i.e., at a much longer periodicity than that of the slow 1997; Steriade and Amzica, 1998; Steriade, 1999). Moreover, the oscillations displaying an obvious peak in humans and cats at grouping by slow oscillations has been considered relevant for the ϳ0.7–0.8 Hz) (Achermann and Borbe´ly, 1997; Marshall et al., effective generation in particular of spindle activity and for es- 2000). Also, spindle activity is known to be generally decreased tablishing reiterative processing of memories in non-REM sleep. with increasing delta activity in humans, which could mask a At the cellular level, the slow oscillations are built up by the grouping of this activity present during slow-wave sleep (SWS) rhythmic sequence of membrane depolarization and hyperpolar- (Aeschbach and Borbe´ly, 1993; Dijk et al., 1993; De Gennaro et al., 2000a,b). Given the importance that has been ascribed to the Received June 17, 2002; revised Sept. 23, 2002; accepted Sept. 27, 2002. regulation of spindle and fast oscillatory activity by slow oscilla- This work was supported by a grant from the Deutsche Forschungsgemeinschaft. We thank Dr. D. Contreras for helpful comments on a previous version of this tions during SWS for the possibility of memory processing during manuscript. this seemingly quiet period of sleep, we examined the temporal Correspondence should be addressed to Dr. M. Mo¨lle, Institute of Neuroendo- dynamics between these faster rhythmic activities and slow oscil- crinology, University of Lu¨beck, Ratzeburger Allee 160, Haus 23a, 23538 Lu¨beck, Germany. E-mail: [email protected]. lations during non-REM sleep and SWS in the human EEG, with Copyright © 2002 Society for Neuroscience 0270-6474/02/2210941-07$15.00/0 particular reference to spindle activity. As in animals, we ex- 10942 J. Neurosci., December 15, 2002, 22(24):10941–10947 Mo¨ lle et al. • Spindle Activity during Slow Oscillations Figure 1. Selection of slow-oscillation half-waves. From top to bottom, Sleep hypnogram for the first cycle from an individual night (W, wake; R, REM sleep; S1–S4, non-REM sleep stages 1–4). Dots underneath indicate time points of the largest slow-positive and negative-oscillation half-waves chosen for analysis (see Materials and Methods for details). DC-recorded (0–30 Hz) original EEG signal, slow-oscillation sig- nal (bandpass, 0.16–4 Hz), spindle activ- ity (12–15 Hz), and spindle rms signal are shown. Parallel vertical bars indicate a critical 20 sec time interval used for the analyses as depicted in Figure 3A. pected enhanced spindle activity during the depolarizing phase (i.e., surface-positive compared with surface-negative half-waves of slow oscillations). MATERIALS AND METHODS Subjects and EEG recordings. Direct current (DC) EEG signals were recorded from 13 young, healthy subjects (six females, seven males, aged 18–25 years) displaying regular sleep–wake rhythms and identified by interview as good sleepers. Because the present analyses relied on DC- recorded EEG signals and because restrained head movement is a necessary prerequisite for proper artifact-free recordings of this kind, subjects were asked to practice at home sleeping through two nights on their back wearing a cervical collar before the experiment proper. Only data from subjects who displayed normal sleep patterns on the experi- mental night were included in the analyses. In particular, care was taken that the first sleep cycle was well pronounced, revealed a minimum of artifacts, and possessed a minimum of at least 20 min of time spent in SWS [i.e., stages 3 and 4 according to the standard criteria by Rechtschaffen and Kales (1968)]. Recording of the DC potentials was as Figure 2. Averaged spectral power density for the slow oscillation described previously (Marshall et al., 1998, 2000). In brief, recordings frequency band (0.16–4 Hz) at Fz (solid line) and Cz (dashed line). Note were obtained from electrodes located at F3, the midline frontal elec- the peak power density at 0.7–0.8 Hz. trode (Fz), F4, C3, the midline central electrode (Cz), and C4 (interna- tional 10–20 system) referenced to linked mastoid electrodes. To attach the electrodes, clip-on sockets were fixed with collodion to the scalp filter of 4 Hz (Ϫ3dBat4.7Hz;Ϫ96 dB at Ն6 Hz). This bandpass (Bauer et al., 1989). Before filling sockets and electrodes with electrode filtering (0.16–4 Hz) was done after spectral power analysis of the EEG gel (Electrode Electrolyte; TECA Corp., Pleasantville, NY), the under- in all individuals; it revealed a single broad peak indicating maximum lying scalp was punctured with a sterile hypodermic needle, to eliminate power at ϳ0.7 Hz (see Fig. 2). Exploratory analyses performed on a possible skin potential artifacts (Picton and Hillyard, 1972). Electrode more narrow frequency band of slow oscillation of Ͻ1 Hz revealed impedance was always Ͻ5 kohm. EEG signals were amplified (2000-fold) essentially identical results. and analog-filtered (0–30 Hz) with a DC amplifier (Toennies DC/AC To produce the spindle activity signal, a bandpass FIR filter of 12–15 amplifier; Jaeger GmbH and Co., KG, Hoechberg, Germany). The DC Hz (Ϫ3 dB at 11.3 and 15.7 Hz; Ϫ96 dB from 0 to 10 Hz and at Ն17 Hz) offset was automatically corrected at a threshold of Ϯ4 mV. With short- was applied. After bandpass filtering, a root mean square (rms) signal circuited input, the amplifier drift, if present, was Ͻ3 ␮V/hr. Analog was calculated with a time resolution of 0.05 sec using a time window of DC/EEG signals were digitized at 100 Hz (CED 1401; Cambridge 0.1 sec (see Fig.
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