A better comprehension of age-related changes in sleep regulation will aid in the design of preventive and therapeutic programs adapted to older individuals
The North American population is aging rapidly. We predict that in 2020, more than 40% of the population will be over 40 and more than 25% will be over 55 (US Census Bureau, 2000). There is no doubt that aging is associated with an important increase in sleep-wake cycle complaints, which has important individual, social, and economic consequences.
Multiple factors, including medical problems, side effects of medications, and specific sleep disorders, account for this age-related increase in sleep difficulties.1 For example, the prevalence of sleep apnea disorder and periodic leg movement in sleep (PLMS) starts to increase significantly during the middle years of life.2,3 The National Sleep Foundation estimates that 35% or more of people aged 65 years and older experience PLMS. Others have estimated that 4% of men and 2% of women over the age of 50 have sleep apnea in addition to excessive daytime sleepiness.4
It is important to point out that notable modifications of the sleep-wake cycle are also observed in “optimal aging” (in people who do not suffer from medical, psychiatric, or specific sleep disorders). These age-related changes occur quite early and they may have important repercussions for older individuals, especially when their sleep-wake system faces challenges such as those related to stress, jet lag, and shift work.
The middle years of life
The modification of sleep organization is a hallmark of the normal aging process.5 Elderly people go to bed and wake up earlier than younger people and their sleep is shorter, shallower (less deep sleep), and more fragmented (more awakenings during the night). Although these changes are well known, the question of how and when sleep deteriorates over the adult life span has received less attention in literature. Until now, our understanding of the mechanisms by which sleep deteriorates with age has come almost exclusively from comparisons of young and elderly subjects. However, subjective sleep complaints begin to increase in the middle years of life and almost all sleep parameters show significant changes between the ages of 20 and 60.6-8,9-11
The extent to which sleep patterns change between the ages of 20 and 59 years in a group of 110 men and women was studied9 and even in this restricted age range, we found fairly important age effects on sleep. At home, middle-aged subjects (40-60 years old) went to bed earlier, woke up earlier, spent less time in bed, and reported better mood and alertness at waketime than did the young (20-39 years old).9 In the sleep laboratory, the deepest sleep stages displayed the most dramatic age-related changes. Middle-aged subjects had on average half the amount of slow-wave sleep (SWS) than the young subjects did. In addition, people in their 40s and 50s spent less time asleep and woke up more often during sleep, spent less time in rapid-eye movement (REM) sleep, and had higher percentages of stage 1 and stage 2 sleep than did younger subjects.9
Quantitative analysis of sleep electroencephalography (EEG) across the night is a powerful and sensitive tool for evaluating changes in sleep regulatory processes with advancing age. For example, slow-wave activity (spectral power between 0.75 Hz and 4.5 Hz during non-REM [NREM]) increases proportionally with the number of hours of wakefulness preceding sleep; it is also an indicator of sleep intensity.12 Recent studies13,14 in both depressed and insomniac populations also suggest that elevated fast frequency activity during NREM sleep might be an indicator of hyperarousal and that it could be related to lower sleep quality. Experimental results of quantitative sleep EEG analysis point out important modifications between 20 and 60 years of age. The most consistent of these age-related changes is a decrease in slow-wave activity, which corroborates that sleep of middle-aged subjects is less intense than sleep of younger subjects.8,10 Interestingly, middle-aged subjects also show elevated fast frequency activity during NREM sleep. These sleep EEG changes may underlie the aging sleep-wake cycle system’s greater difficulty adapting to challenges that ordinarily disrupt sleep.
Early Rising and Age
Biological clocks regulate the timing of psychological and physiological functions so they are in tune within the individual and with the 24-hour environment. For example, the biological clock will tell your body when it is time to go to bed and when it is time to be awake. In order to work well, biological clocks should emit a strong signal at the right time. Since it is not possible in humans to measure the activity of the biological clock directly, robust circadian (24-hour) rhythms such as body temperature are used as markers of its activity. People can easily experience the biological clock modulation of sleep propensity (the ability to initiate or maintain sleep) in situations of jet lag or shift work, when they try to sleep at circadian times of low sleep propensity during the day (which leads to fragmented sleep) and to stay awake and productive at circadian times of high sleep propensity at night (which leads to low levels of alertness).
An individual’s tendency to be more of a morning type or an evening type can be measured with standardized questionnaires.15 These questionnaires assess the times of day that people feel their best in addition to when they prefer to wake up, go to bed, and engage in intellectual and physical activity. Older people report that they are more morning types than young people. This difference starts during the middle years of life.9 Research on the habitual sleep-wake patterns of young and elderly subjects using sleep diaries corroborates this age-related tendency toward morningness. Elderly subjects go to bed and wake up on average 1 hour earlier than young subjects. Furthermore, physiological markers of their biological clock, such as temperature circadian rhythm, are also advanced by about 1 hour compared to the young.16.17 We have just reported that these changes may occur as early as the middle years of life.18 Middle-aged subjects go to bed and wake up on average 1 hour earlier than young subjects. Interestingly, their temperature circadian rhythm is also advanced by 1 hour compared to the young. Thus, an advanced signal from the biological clock seems to appear quite early in the aging process. This earlier biological signal is associated with earlier bedtime and waketime. The mechanisms underlying the advance of the biological clock still have to be determined.
Adapting to the Sleep-wake Cycle
Middle-aged people not only show sleep modifications, but they also appear to be more sensitive to challenges imposed on their sleep-wake cycle. For example, middle-aged people have more problems adjusting to shift work than younger individuals do and they adapt more slowly to jet lag.19 At least two mechanisms may explain their lower tolerance in these situations, which include:
• Recuperating From Sleep Deprivation. Sleep deepens following longer waketimes. SWS and slow-wave activity during NREM sleep increase proportionally with the number of hours of wakefulness that precede sleep.12 Thus, the longer people are awake, the more SWS and slow-wave activity they will have in their sleep. Very few studies to date have assessed the effects of sleep deprivation in aging. Are aged subjects as able as younger subjects to react to sleep deprivation with an increase in sleep intensity? Two very recent animal studies20,21 have shown that aged animals exhibited reduced sleep responses following acute sleep deprivation. In human studies, elderly individuals have been subject to 1 or 2 nights of sleep deprivation or to sleep fragmentation. Although elderly adults respond to sleep deprivation with an increase in sleep intensity, they tend nonetheless to show lower levels of deep sleep than younger subjects do after this challenge.22,23 We recently investigated the different effects of 1 night of complete sleep deprivation (25 hours of constant wakefulness) in young (20-39 years) and middle-aged subjects (40-60 years).24 As measured with SWS and slow-wave activity, sleep was more intense in both groups of subjects following sleep deprivation. However, the increase of sleep intensity following sleep deprivation was less pronounced in the middle-aged than in the young. Therefore, it appears that even though the sleep of middle-aged subjects has the ability to respond to an acute sleep deprivation with an increase of deep sleep, its overall capacity to respond diminishes.
• Maintaining Sleep When Biological Clocks Are Ticking. Some authors25,26 have suggested that older subjects might be particularly vulnerable when they try to sleep while their biological clocks are giving a strong signal for wakefulness (during the day). In our study24 of the effects of a total night of sleep deprivation in young and middle-aged subjects, recovery sleep took place during the day. This experimental situation was similar to what night workers experience when they sleep during the day following their first night shift. In our study, both groups of subjects had more awakenings during their daytime recovery sleep than at their normal sleep times despite the fact that they experienced 1 night of complete sleep deprivation. Importantly, however, middle-aged subjects had even more problems sleeping during the day than the young subjects did. They showed a more substantial increase in awakenings during daytime sleep. These results indicate that as early as their 40s and 50s, people’s ability to sleep decreases while their biological clock is promoting wakefulness, as is the case in situations of jet lag and shift work.
Differences in Gender and Sleep
It is well recognized that there are gender differences in sleep in the elderly population. Compared to older men of the same age, older women usually sleep more deeply and wake up less often during the night despite the fact that they complain more often of insomnia.6,7 These results led to the hypothesis that the sleep of men and women may age at different rates.
It is not clear when gender differences emerge over the aging process. Gender differences in quantitative sleep EEG measures have been reported among subjects as young as 20-29 years of age.27 Young women already show higher slow-wave activity than young men. In subjects between the ages of 20 years and 60 years, we found differences between men and women for a few parameters.9 Women spent more time in bed than did men, as their sleep diaries indicated. In the laboratory, women showed more SWS and fewer awakenings. Importantly, however, age did not influence the sleep of men and women between 20 years and 60 years differently. We also recently studied the ways in which age and gender influence quantitative sleep EEG between 20 years and 60 years.10 Women showed elevated activity in the slow frequencies (0.25-9.00 Hz), but also in some of the faster frequencies (14.25-16.00 Hz). Again, however, the aging process had a similar influence on both men and women.
We know that sleep and quantitative sleep EEG vary with the level of reproductive hormones across the menstrual cycle,28 during pregnancy,29 and following hormonal replacement therapy in menopausal women.30 No studies to date have carefully evaluated these influences when determining if the sleep-wake cycles of men and women age at a different rate. The discrepancy between objective and subjective gender differences in sleep also needs to be addressed. Further research should evaluate the influence of hormonal status on gender differences in sleep, as well as its interaction with the aging process.
Conclusion
There are several theoretical and clinical reasons to study the mechanisms that underlie the effects of age on the sleep-wake cycle in the middle-aged population. First, in the middle-aged population it is possible to evaluate the mechanisms that underlie age-related modifications to the sleep-wake cycle when they first start to appear. This gives important insight into the sequence of events articulating age-related changes. In addition, studies that sample elderly subjects have to exclude an important proportion of subjects because of strict research criteria. Our knowledge of age-related changes to the sleep-wake cycle is therefore almost entirely based on supra-normal aging. Because middle-aged subjects are less affected by the confound variables associated with aging than the elderly are, it is possible to study a larger segment of the population.
Members of the middle-aged population are also particularly at risk of suffering from perturbations to the sleep-wake cycle. Their multiple social, familial, and professional responsibilities not only limit the strategies they may adopt to alleviate their sleep and alertness problems (fewer opportunities to nap, and change sleep-wake schedules), but also enhance the consequences of such problems (lower productivity level, higher risk for accidents, and irritability). A better comprehension of age-related changes in sleep regulation will aid in the design of preventive and therapeutic programs adapted to older individuals. With increasing numbers of the middle-aged population now facing night work and jet lag, these questions are of more than simply academic interest.
Julie Carrier, PhD, is assistant professor in the Department of Psychology, University of Montreal, and a researcher at the Centre d’etude du sommeil et des rythmes biologiques, Hôpital du Sacré-Coeur de Montreal, both in Quebec, Canada.
References
1. Ancoli-Israel S. Sleep problems in older adults: putting myths to bed. Geriatrics. 1997;52:20-30.
2. Bixler EO, Kales A, Vela-Bueno A, Jacoby JA, Scarone S, Soldatos CR. Nocturnal myoclonus and nocturnal myoclonic activity. Research Communications in Chemical Pathology and Pharmacology. 1982;36:129-140.
3. Kripke DF, Ancoli-Israel S, Klauber MR, Wingard DL, Mason WJ, Mullaney DJ. Prevalence of sleep-disordered breathing in ages 40-64 years: a population-based survey. Sleep. 1997;20:65-76.
4. Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med. 1993;328:1230-1235.
5. Bliwise DL. Sleep and circadian rhythm disorders in aging and dementia. In: Turek FW, Zee PC, eds. Regulation of Sleep and Circadian Rhythms. New York: Marcel Dekker; 1999:487-526.
6. Webb WB. The measurement and characteristics of sleep in older persons. Neurobiol Aging. 1982;3:311-319.
7. Williams RL, Karacan I, Hursch CJ. EEG of Human Sleep: Clinical Applications. New York: John Wiley & Sons; 1974.
8. Landolt HP, Dijk DJ, Achermann P, Borbely AA. Effect of age on the sleep EEG: slow-wave activity and spindle frequency activity in young and middle-aged men. Brain Res. 1996;738:205-212.
9. Carrier J, Monk TH, Buysse DJ, Kupfer DJ. Sleep and morningness-eveningness in the “middle” years of life (20y-59y). J Sleep Res. 1997;6:230-237.
10. Carrier J, Land S, Buysse DJ, Kupfer DJ, Monk TH. The effects of age and gender on sleep EEG power spectral density in the “middle” years of life (20y-60y). Psychophysiology. 2001;38:232-242.
11. Van Cauter E, Leproult R, Plat L. Age-related changes in slow wave sleep and REM sleep and relationship with growth hormone and cortisol levels in healthy men. JAMA. 2000;284:861-868.
12. Achermann P, Dijk D-J, Brunner DP, Borbély A. A model of human sleep homeostasis based on EEG slow-wave activity: quantitative comparison of data and simulations. Brain Res Bull. 1993;31:97-113.
13. Armitage R, Hudson A, Trivedi M, Rush AJ. Sex difference in the distribution of EEG frequencies during sleep: unipolar depressed outpatients. J Affective Disord. 1995;34:121-129.
14. Merica H, Blois R, Gaillard JM. Spectral characteristics of sleep EEG in chronic insomnia. European Journal of Neurosciences. 1998;10:1826-1834.
15. Horne JA, Ostberg O. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol. 1976;4:97-110.
16. Carrier J, Monk TH, Reynolds CFI, Buysse DJ, Kupfer DJ. Are age differences in sleep due to phase differences in the output of the circadian timing system? Chronobiol Int. 1999;16:79-91.
17. Duffy JF, Dijk D-J, Klerman EB, Czeisler CA. Later endogenous circadian temperature nadir relative to an earlier wake time in older people. Am J Physiol. 1998;275:R1478-R1487.
18. Touchette E, Paquet J, Morettini J, Carrier J. Phase advance of habitual sleep timing and circadian temperature rhythm in middle-aged subjects. Sleep. In press.
19. Moline ML, Pollak CP, Monk TH, et al. Age-related differences in recovery from simulated jet lag. Sleep. 1992;15:28-40.
20. Shiromani PJ, Lu J, Wagner D, et al. Compensatory sleep response to 12 h wakefulness in young and old rats. Am J Physiol. 2000;278:R125-R133.
21. Mendelson WB, Bergmann BM. Age-dependent changes in recovery sleep after 48 hours of sleep deprivation in rats. Neurobiol Aging. 2000;21:689-693.
22. Brendel DH, Reynolds CF, Jennings JR, et al. Sleep stage physiology, mood, and vigilance responses to total sleep deprivation in healthy 80-year-olds and 20-year-olds. Psychophysiology. 1990;27:677-685.
23. Bonnet M. The effect of sleep fragmentation on sleep and performance in younger and older subjects. Neurobiol Aging. 1989;10:21-25.
24. Gaudreau H, Morettini J, Lavoie HB, Carrier J. Recuperating during the day: the effects of a 25-hour sleep deprivation in the middle years of life. Neurobiol Aging. In press.
25. Campbell SS, Dawson D. Aging young sleep: a test of the phase advance hypothesis of sleep disturbance in the elderly. J Sleep Res. 1992;1:205-210.
26. Dijk D-J, Duffy JF, Riel E, Shanahan TL, Czeisler CA. Ageing and the circadian and homeostatic regulation of human sleep during forced desynchrony of rest, melatonin and temperature rhythms. J Physiol. 1999;516:611-627.
27. Dijk D-J, Beersma DGM, Hoofdakker RH. Sex differences in the sleep EEG of young adults: visual scoring and spectral analysis. Sleep. 1989;12:500-507.
28. Driver HS, Dijk DJ, Werth E, Biedermann K, Borbely AA. Sleep and the sleep electroencephalogram across the menstrual cycle in young healthy women. J Clin Endocrinol Metab. 1996;81:728-735.
29. Brunner DP, Munch M, Biedermann K, Huch R, Huch A, Borbély AA. Changes in sleep and sleep electroencephalogram during pregnancy. Sleep. 1994;17:576-582.
30. Antonijevic IA, Stalla GK, Steiger A. Modulation of the sleep electroencephalogram by estrogen replacement in postmenopausal women. Am J Obstet Gynecol. 2000;182:277-282.
