Sleep spindle characteristics in healthy subjects of different age groups

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Abstract

Objectives: Few studies have quantified the various characteristics of sleep spindles (SS) in groups of normal human subjects. The aim of the present study was to look at the effects of age on the number, density, duration, intra-spindle frequency, and periodicity of SS during stage 2 sleep in normal subjects of different age groups.

Methods: Thirty-six healthy subjects participated in the study. They were divided into 6 age groups: 10–19, 20–29, 30–39, 40–49, 50–59 and 60–69 years.

Results: The results show that there is a progressive decrease in SS number, density, duration and a progressive increase in intra-spindle frequency with age. These changes occur mainly in the first 4 decades, except for SS number and density, for which the changes seem to continue until the sixth decade. The present study also reveals a clear periodicity of SS in human sleep. SS occur every 3–6 s, and the modal value of inter-spindle intervals increases with aging.

Conclusions: The progressive decrease in the number of SS and slow-wave sleep time with age suggests that SS are part of sleep promoting mechanisms. The negative correlation found between SS density and sleep efficiency in the present study is congruent with the sleep maintenance role of SS.

Introduction

Sleep spindles (SS) were first described by Hans Berger in 1933 (Berger, 1933), but the term was coined by Loomis et al. in 1935 (Loomis et al., 1935). SS are a hallmark of stage 2 sleep, and have been used in the standard scoring method of Rechtschaffen and Kales (1968). Few studies, however, have quantified the various characteristics of SS in groups of normal human subjects. The SS density has been reported to be drastically decreased in Parkinson's disease (Puca et al., 1973, Mouret, 1975), Alzheimer's disease (Montplaisir et al., 1995, Prinz et al., 1982, Reynolds et al., 1985), Creutzfeldt–Jacob disease (Donnet et al., 1992), progressive supranuclear palsy (Montplaisir et al., 1997) and fatal familial insomnia (Sforza et al., 1995). Therefore, normative data are needed to differentiate normal aging from pathological conditions.

Since scoring SS across the night is a time-consuming task, most of these studies have been carried out using computer-based SS detection (Declerck et al., 1986, Gaillard and Blois, 1981, Principe and Smith, 1982). This approach encounters several difficulties due to the great variability of spindle morphology and of intra-spindle frequency. More recent studies have used pattern-recognition techniques (Dijk et al., 1993, Dijk, 1995) which are more powerful, but which still require further validation with visual detection methods.

Age has been shown to produce a decrease in the number and density (number/h of stage 2 sleep) of SS (Feinberg et al., 1967, Guazzelli et al., 1986, Kubicki et al., 1989, Nicolas et al., 1997, Wei et al., 1999), but the temporal pattern of the aging process is unknown since most of these studies have compared groups of young and elderly subjects. Most of these studies raise methodological concerns. Principe and Smith (1982) restricted their analysis to the first half of the night, while the density of SS increases from the beginning to the end of the night (Guazzelli et al., 1986). Therefore, their results may not be representative of the entire SS population. Other authors have included spindles detected in stages 2, 3 and 4 sleep (Gaillard and Blois, 1981, Declerck et al., 1986). It is virtually impossible to detect all SS in the presence of large amplitude delta waves, and even with computerized methods of detection, it is often impossible to correlate SS detected in stages 3 and 4 sleep with the presence of SS on visual examination. Two studies have looked at the intra-spindle frequency in relation to age, and found a decrease and a increase, respectively, of that inner frequency with advancing age (Feinberg et al., 1967, Principe and Smith, 1982). More recently, Evans and Richardson (1995) showed, during nap recording, the presence of a periodicity of approximately one every 3–5 s for SS. This finding was confirmed by Achermann and Borbély (1997) during nocturnal sleep, but no study was carried out with respect to the effects of age.

The aim of the present study was to look at the effects of age on the number, density, duration, intra-spindle frequency, and periodicity of SS during stage 2 sleep in normal subjects of different age groups. SS were counted for the entire night; they were visually selected since the aim of the study was to establish a standard database for further comparisons with automatic detection techniques and with pathological conditions.

Section snippets

Subjects and procedure

Thirty-six subjects participated in the present study. They were divided into 6 age groups: group 1, 10–19 years (14.1±0.2 years); group 2, 20–29 years (24.1±1.0 years); group 3, 30–39 years (35.1±2.9 years); group 4, 40–49 years (45.5±3.5 years); group 5, 50–59 years (54.7±2.9 years); and group 6, 60–69 years (64.8±3.4 years). Each group was comprised of 3 women and 3 men, except for group 6, for which there were two men and 4 women. Menstrual phase was not controlled for women. All subjects

Macrostructure of sleep

Table 1 shows results of PSG obtained in the 6 age groups. The total sleep time (TST), sleep efficiency, and percentage of slow-wave sleep (SWS) decreased with age. Conversely, the percentages of stage 1 sleep, stage 2 sleep increased with advancing age. The percentage of rapid eye movement (REM) sleep remained stable across the 6 age groups.

Number and density of SS

As shown in Table 2, there is a progressive decrease in the mean number and density of SS (number/h of stage 2 sleep) with age. Significant negative

Discussion

This is the first study in which a large number of SS characteristics, namely number, density, duration, frequency and periodicity, were studied, not only in young and elderly subjects, but in normal subjects of several age groups. This study is the first step in obtaining normative data for further studies on different populations of normal subjects, patients afflicted with different medical or psychiatric conditions, subjects treated with various pharmacological agents, or under experimental

Acknowledgements

This research was supported by the Medical Research Council of Canada and the ‘Fonds de la Recherche en Santé du Québec’. The authors would like to thank Jean Paquet, PhD, who helped with statistical analyses.

References (40)

  • C.F Reynolds et al.

    EEG sleep in elderly depressed, demented, and healthy subjects

    Biol Psychiatry

    (1985)
  • E Sforza et al.

    Sleep–wake cycle abnormalities in fatal familial insomnia. Evidence of the thalamus in sleep regulation

    Electroenceph clin Neurophysiol

    (1995)
  • S Uchida et al.

    Sigma (12–15 Hz) and delta (0.3–3 Hz) EEG oscillate reciprocally within NREM sleep

    Brain Res Bull

    (1991)
  • H.G Wei et al.

    Attenuated amplitude of circadian and sleep-dependent modulation of electroencephalographic sleep spindle characteristics in elderly human subjects

    Neurosci Lett

    (1999)
  • E Werth et al.

    Spindle frequency activity in the sleep EEG: individual differences and topographic distribution

    Electroenceph clin Neurophysiol

    (1997)
  • H Berger

    Über das elektroenkephalogramm des menschen

    Sechste Mitteilung Arch Psychiatr Nervenkr

    (1933)
  • A Bové et al.

    Relationship between sleep spindles and hypersomnia

    Sleep

    (1994)
  • D Contreras et al.

    Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm

    J Physiol (Lond)

    (1996)
  • A.C Declerck et al.

    Sleep spindle detection and its clinical relevance

    Eur Neurol

    (1986)
  • A Donnet et al.

    Sleep electroencephalogram at the early stage of Creutzfeldt–Jacob disease

    Clin Electroencephalogr

    (1992)
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