Sleep Satisfaction, Sleep–Wake Pattern, and Aging

Sleep Satisfaction, Sleep–Wake Pattern, and Aging

C H A P T E R 8 Sleep Satisfaction, SleepeWake Pattern, and Aging Arcady A. Putilov Laboratory of Sleep/Wake Neurobiology, The Institute of Higher Ne...

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C H A P T E R

8 Sleep Satisfaction, SleepeWake Pattern, and Aging Arcady A. Putilov Laboratory of Sleep/Wake Neurobiology, The Institute of Higher Nervous Activity and Neurophysiology of the Russian Academy of Sciences, Moscow, Russia hypothesis, Zilli et al.10 compared two groups of healthy people aged between 65 and 99 and between 19 and 28 years. They were not different in level of sleep satisfaction despite clear perception of worsening of night sleep characteristics demonstrated by people from the former group. The conclusion was made that, when these people rate their sleep satisfaction, they can rely more on the perceived freshness after awakening rather than on high frequency of nighttime awakenings that they also can clearly perceive.10 In other words, these people heed the perceived freshness after awakening not paying much attention to frequent nighttime awaken˚ kerstedt et al.11 showed that ings.10 More recently, A the values of the polysomnographic sleep characteristics for good sleep in older women (>51.5 years) were similar to the values for poor sleep in the younger women (<51.5 years). They concluded that age is an important factor in the relation between subjective and objective sleep and, in particular, objective criteria for good sleep are adjusted downward by older women. In addition to the worsening of objectively measured characteristics of night sleep quality, the normal aging process is also accompanied by the shifts of various behavioral, physiological, and hormonal rhythms at earlier clock times.12,13 Evidence for the age-associated advance of the daily sleepewake cycle was, in particular, provided by numerous epidemiological studies. They revealed the shifts toward morning preference on morningnesseeveningness scales14 and to earlier selfreported times for going to bed and awakening at free days.15 Such an advance might, at least partly, explain the perceived freshness after awakening but a possibility of significant link between sleep satisfaction and age-

INTRODUCTION It is believed that good sleep is absolutely crucial for health, but it is not excluded that good night sleep is the exception rather than the norm for elderly people. Approximately a half of them experience sleep disturbances.1 Moreover, the worsening of objective characteristics of sleep quality was documented for healthy noncomplaining elderly people.2 Middle-aged adults and elderly people often complain about difficulty of falling asleep and nighttime awakenings, unsatisfactory nocturnal sleep quality and disturbed or “light” sleep, insufficient sleep duration and unwanted early morning awakenings, reduced level of daytime alertness, and undesired daytime drowsiness.1,3 Such self-reports were corroborated by results of the vast majority of polysomnographic studies. They revealed significant worsening of objectively determined characteristics of sleep quality with advancing of age.4e6 Amazingly, such worsening was also detected in healthy, noncomplaining, and carefully screened elderly people.2 Therefore, complaints about poor sleep quality can be secondary to health problems, whereas the sleep aging process seems not to be the major reason for such complaints.7,8 Do elderly people fail to get the good sleep they really need? The answer is not evident because the sleep literature indicates that a perceived level of sleep satisfaction is not necessarily linked to age-associated deterioration of objective and subjective indicators of night sleep quality. Buysse et al.9 hypothesized healthy people with objectively deteriorated sleep are able to adjust expectations about their night sleep to what they accept as being its age-related changes. To provide support for this

Neurological Modulation of Sleep https://doi.org/10.1016/B978-0-12-816658-1.00008-9

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8. SLEEP SATISFACTION, SLEEP-WAKE PATTERN, AND AGING

associated changes in sleepewake timing has not been tested yet. Therefore, the following fraction contains the attempt to test whether a higher level of sleep satisfaction can be associated with typical for a given age characteristics of human sleepewake pattern.

ASSOCIATIONS BETWEEN SLEEPeWAKE PATTERN, SLEEP SATISFACTION, AND AGE In total, 178 participants of sleep deprivation experiments self-reported sleep satisfaction along with a set of characteristics of sleepewake pattern. Data on their objective (electroencephalographic) and subjective measures of sleepiness obtained in the course of sleep deprivation were published elsewhere16e18 and some preliminary results based on a smaller sample were briefly reported in Putilov.19 Each of the participants included in experiment denied a history of psychiatric or sleep disorders, any current health problems, and involvement in shift work or transmeridian flights during the preceding month. The experiments were performed in accordance with the ethical standards laid down in the Declaration of Helsinki. Their protocols were approved by the Ethics Committee of the Institute. Informed written consent was obtained from each of the participants studied as paid volunteers. The ages of 76 male and 102 female participants ranged from 15 to 67 years (mean  standard deviation ¼ 31.4  12.8). Each morning during a week prior to the experiment, the participants reported duration of their nap, sleep latency, and times for going to bed and awakening. Total sleep duration was calculated as difference between these times minus sleep latency. Sleep Satisfaction was Scored (SSS) as a response to a single question: “Did you have a good sleep? (No ¼ 1 . [I slept] Very well ¼ 5)”. In Russian this question sounds as “Vispalis’? (Net ¼ 1 . Otlichno [vispalsya/as’] ¼ 5)”. Everyday self-reports were averaged over preexperimental week with exception of duration of nap that was transformed into a nap frequency score (1 ¼ no, 2 ¼ once, and 3 ¼ more than once). The 72-item Sleep-Wake Pattern Assessment Questionnaire20,21 was administered for self-assessment of anytime and daytime wakeability, anytime and nighttime sleepability, and evening and morning lateness (W, V, F, S, E, and M, respectively). The scales were earlier validated against objective or subjective measures of circadian phase position, wave forms of diurnal variations in sleepiness, etc.16,17,22,23 The last of analyzed self-reports was subjective sleepiness scored with the 9-step Karolinska Sleepiness Scale (KSS)24 at 9:00 after the first night of sleep deprivation.

The whole list of these self-reports is given in each of Tables 8.1e8.3. The sample was subdivided into three age groups and three SSS groups (Table 8.1). The participants of SSS groups reported throughout the pre-experimental week that they, on average, slept very well (SSS > 4.0), well (SSS between 3.6 and 4.0), and not so well (SSS  3.5). To test significance of relationship between sleep satisfaction and sleepewake pattern in the whole sample and in subsamples of participants with different ages and SSS, we performed regression and correlation analyses (Table 8.1), three- and two-way MANOVAs (Table 8.2), and factor analysis (Table 8.3). Main effects and interactions between factors “Age” and “SSS” (Table 8.2, central column) are illustrated in Figs. 8.1 and 8.2. Significance level was fixed at P ¼ .05. The results presented in Tables 8.1 and 8.2 and in Figs. 8.1 and 8.2 suggest that the self-reported characteristics of sleepewake pattern exhibited significant changes across ages and that any of these changes was in expected direction. Particularly, age of study participants correlated with advance shift of times for going to bed and awakening, morning earliness, shortening of sleep duration, and reduction of nighttime sleep ability. SSS did not correlate significantly with age (Table 8.1). A set of characteristics of sleepewake pattern that correlated with SSS differed from the set of correlates of age. Some of the correlations and predictors revealed in analyses of the whole sample were intuitively expected, e.g., the correlations suggesting associations of higher SSS with longer nighttime sleep (Table 8.1). However, higher SSS was additionally associated with both morning earliness and late awakening (Table 8.1). Results of analyses performed separately on three age subsamples provided an explanation for these contradictive relationships. In the group of youngest participants (25 years) the significant correlates were, as expected, lateness, lateness traits, and longer sleep duration whereas in the group of oldest participants (46e67 years) higher SSS was, also as expected, associated with morning earliness and earlier time for going to bed (Table 8.1). If the strongest predictor of this score in the group of youngest participants was late awakening, such a predictor in the groups of older participants (26 years) was morning earliness. These results were further confirmed by results of three-way MANOVA of the whole dataset. They yielded significant interaction between factors “Age” and “SSS” for times for going to bed and awakening (Table 8.2). As can be seen in Fig. 8.1, sleep satisfaction was linked to agetypical characteristics of sleepewake pattern, such as long sleep duration and lateness in young adults and earliness in older adults. The results of MANOVAs and factor analysis additionally revealed significant relationship between sleep

I. INTRODUCTION AND BACKGROUND OF SLEEP DISRUPTION

TABLE 8.1 Correlations of Age and Sleep Satisfaction Score (SSS) With Other Variables. Correlation of

Age (For All and Three SSS Groups)

SSS (For All and Three Age Groups)

Grouping

SSS

£3.5

3.6e4.0

>4.0

Age

£25

26e45

>45

Group Size, N

178

52

57

69

178

88

54

36

CORRELATION WITH Gender#

0.069

0.086

0.083

0.186

0.026

0.101

0.006

0.003

Age

e

e

e

e

0.002

0.187

0.073

0.263

SSS

0.002

0.063

0.218

0.13

e

e

e

e

Go to bed

0.241***

0.031

0.399**

0.430***

0.012

0.246*

0.055

0.375*

Sleep latency

0.077

0.044

0.188

0.210

0.091

0.157

0.140

0.166

Awakening

0.280***

0.061

0.438**

0.522***

0.149**

0.404***

0.168

0.232

0.163**

0.048

0.213

0.366**

0.208***

0.354**

0.264

0.265

Napping score

0.003

0.145

0.017

0.132

0.090

0.180

0.172

0.146

KSS at 9:00

0.082

0.125

0.077

0.219

0.125*

0.136

0.141

0.241

W

0.071

0.009

0.035

0.149

0.088

0.177

0.215

0.037

V

0.012

0.041

0.095

0.072

0.132*

0.197

0.257

0.070

F

0.126

0.042

0.318*

0.237*

0.018

0.105

0.217

0.138

S

0.229***

0.281*

0.332*

0.504***

0.092

0.159

0.222

0.186

E

0.120

0.008

0.224

0.119

0.068

0.303**

0.097

0.167

M

0.172**

0.037

0.415**

0.353**

0.141**

0.018

0.327*

0.524**

Total sleep time #

Notes: Total sleep time: Difference between time of Awakening and time of sleep onset (calculated by adding Sleep latency to time to Go to bed); Napping score: 0 ¼ none, 1 ¼ once, and 2 ¼ more than once a week; KSS at 9:00: Self-reported score on the Karolinska Sleepiness Scale at 9:00 after sleepless night; #A Kendall’s tau, otherwise a Pearson coefficient of correlation. Level of significance for correlation coefficient: *** (P < .001), ** (P < .01), * (P < .05).

TABLE 8.2 F-ratios From Three- and Two-Way MANOVAs With Factors Age and/or SSS. MANOVA Factor

Three-Way Age

Two-Way Age 3 SSS

Age

SSS

3.3***

2.6**

3.7***

4.1***

SSS

MULTIVARIATE TEST (ROY’S LARGEST ROOT CRITERION) F-ratio

3.8***

F-RATIO FOR BETWEEN-GROUPS EFFECTS Age

e

e

e

e

0.2

SSS

e

e

e

0.3

e

Go to bed

9.6***

0.7

2.6*

10.6***

0.1

Sleep latency

0.7

2.1

1.0

0.9

1.9

Awakening

13.2***

1.0

2.7*

14.7***

2.2

Total sleep time

2.9

4.2*

0.5

3.7*

7.5**

Napping score

2.0

0.4

0.4

1.9

1.1

KSS at 9:00

0.9

2.7

0.1

1.1

3.8*

W

0.6

4.4*

0.3

0.7

6.4**

V

1.7

3.6*

0.4

1.6

4.1*

F

3.0

0.5

1.9

2.5

0.1

S

4.6*

2.8

1.1

4.9**

2.5

E

3.8*

0.4

1.4

4.5*

0.1

M

6.9**

9.2***

1.9

7.7**

5.8**

Notes: Gender was the third or second between-subjects factor in three- and two-way MANOVAs, respectively. Level of significance for F-ratio: *** (P < .001), ** (P < .01), * (P < .05). See also notes to Table 8.1.

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8. SLEEP SATISFACTION, SLEEP-WAKE PATTERN, AND AGING

TABLE 8.3

Loadings on Six Principal Components and Three Rotated Factors.

Analysis PCs or RFs Eigenvalue Cumulative %

Principal Components (PCs) 1

2 3.12

17.9

3 2.11

30.4

4

5

1.74 41.5

Rotated Factors (RFs)

1.54 52.7

MDE

6 1.19

63.4

1.00

2.68

71.3

WDV 2.24

FDS 2.04

17.9

32.8

46.4

LOADING ON 6 NONROTATED PRINCIPAL COMPONENTS AND 3 VARIMAX ROTATED FACTORS Gender

0.173

0.261

0.309

0.023

0.142

0.646

0.035

0.088

0.429

Age

L0.593

0.188

0.005

0.016

0.334

0.128

L0.524

0.068

0.327

SSS

0.034

0.549

0.104

0.365

0.409

0.191

0.203

0.500

0.154

Go to bed

0.697

0.028

0.310

0.330

0.080

0.344

0.741

0.174

0.049

0.249

0.312

0.544

0.268

0.172

0.455

0.015

0.045

L0.673

Awakening

0.787

0.143

0.465

0.116

0.233

0.047

0.923

0.07

Total sleep time

0.415

0.243

0.224

L0.645

0.240

0.281

0.512

0.106

0.089

Napping score

0.198

0.234

0.425

0.433

0.529

0.053

0.114

0.389

0.331

KSS at 9:00

0.425

0.399

0.001

0.071

0.304

0.186

0.261

L0.521

0.014

W

0.138

0.690

0.112

0.518

0.090

0.075

0.021

0.638

0.316

V

0.470

0.606

0.268

0.101

0.176

0.057

0.112

0.787

0.166

F

0.497

0.029

L0.553

0.117

0.374

0.139

0.121

0.305

0.668

S

0.447

0.465

0.470

0.092

0.372

0.082

0.220

0.121

0.758

E

0.221

0.403

0.401

0.542

0.051

0.116

0.481

0.368

0.070

M

0.662

0.304

0.158

0.093

0.215

0.181

0.560

0.491

0.022

Sleep latency

0.008

Notes: M þ E, W þ V, and F þ S: Only three largest factors (“Lateness”, “Wakeability”, and “Sleepability”) were extracted, rotated, and interpreted as corresponding to three pairs of questionnaire scales, respectively. The highest of loadings (either 0.5 < or >0.5) are printed in Bold. See also notes to Table 8.1.

satisfaction and wakeability characteristics of sleepe wake pattern (Table 8.3 and Fig. 8.2). For instance, high SSS was sorted into “Wakeability” (second) factor that also included a low level of sleepiness after sleepless night and higher scores on anytime and daytime wakeability scales (Table 8.3). Such results suggest that only relationship of higher sleep satisfaction with better wakeability (second factor) persisted across the life span whereas higher sleepability (third factor) and earlier or later phase of wakeesleep cycle (first factor) were important contributors to sleep satisfaction only in separate age groups (Fig. 8.2).

NEUROPHYSIOLOGICAL UNDERPINNING OF THE AGEMODULATING LINK BETWEEN SLEEPeWAKE PATTERN AND SLEEP SATISFACTION These results on association between sleep satisfaction, sleepewake pattern, and age supported and ˚ kerstedt extended the findings reported by Zilli et al.,10 A

et al.,11 and other authors. It seems that the self-assessed characteristics of the sleepewake pattern exhibited notable shifts already on the age interval from early to late adulthood. Moreover, those characteristics of this pattern that can be linked to quality of night sleep (e.g., score on S scale) also exhibited significant change. However, despite these changes sleep satisfaction did not decline in older study participants as compared to younger participants. It remained adjusted to what is considered to be the age-specific pattern of the sleepe wake cycle. Thus, the results suggested that (1) similarly to night sleep characteristics, a set of characteristics of sleepewake pattern is significantly linked to sleep satisfaction, (2) despite profound difference between ages in these characteristics, the link remains significant across the life span, and (3) sleep satisfaction is higher when the characteristics of sleepewake pattern are typical for this age. Elderly people were proposed to be able to adjust their expectations about sleep to the changes they accept as age-related.9 The present results indicate that such an adjustment is also notable in groups of people of younger ages (till 67 years), and that it persists across

I. INTRODUCTION AND BACKGROUND OF SLEEP DISRUPTION

83

NEUROPHYSIOLOGICAL UNDERPINNING OF THE AGE-MODULATING

Clock hour ± SEM

(A)

Go to bed

24

22

Age:

≤25

26-45

>45

Age:

≤25

SSS ≤3.5 Clock hour ± SEM

(B)

26-45

>45

Age:

≤25

SSS=3.6-4.0

26-45

>45

SSS>4.0

Awakening 9

7

5

Age:

≤25

26-45

>45

Age:

≤25

SSS ≤3.5

Hours ± SEM

(C )

26-45

>45

Age:

≤25

SSS=3.6-4.0

26-45

>45

SSS>4.0

Total sleep 8

7

6

Age:

≤25

26-45

>45

Age:

≤25

SSS ≤3.5

(D) Score ± SEM

10

26-45

>45

Age:

≤25

SSS=3.6-4.0

26-45

>45

SSS>4.0

M (Morning Lateness)

5 0 -5

-10

Age:

≤25

26-45

>45

Age:

≤25

SSS ≤3.5

26-45

>45

Age:

≤25

SSS=3.6-4.0

26-45

>45

SSS>4.0

FIGURE 8.1 Self-assessments of sleepewake times and lateness in groups with different age and SSS. Estimated marginal means  Standard Error of Mean (SEM, vertical lines) for participants subdivided into nine groups (three ranges of age x three rages of SSS) calculated in three-way MANOVA (Table 8.2, left).

the interval of ages from early to late adulthood. Can the sleep aging process underlie this ability in spite of biological rather than psychological nature of this process? In the following discussion I am arguing for possibility that age-associated changes in sleepewake regulating processes can determine people’s ability to adjust their perception of “sleep goodness” to typical for their age sleepewake pattern. Namely, I think that the effect of aging on relative strengths of the antagonistic wake and sleep drives can determine the ability of older people to adjust expectations about their night sleep quality to age-specific sleepewake pattern. According to the two-process conceptualization of the sleepewake regulating mechanisms, the sleep drive

(i.e., the sleep-promoting process) arises from combination of two major processes, homeostatic and circadian, and the strength of this drive is indicated by amplitude of slow-wave activity and percentage of slow-wave sleep.25 Factor analysis of data of longitudinal intraindi˚ kerstedt with covidual studies reported by A workers26,27 suggested that the items designed for subjective evaluation of “sleep goodness” were sorted into two major factors. The first factor was represented by subjective sleep quality, calmness of sleep, ease of falling asleep, number of awakenings, sleep latency, etc. This set of items predicted “better” sleep with longer sleep duration, lower number of awakenings, higher amount and percentage of slow wave sleep, etc., and

I. INTRODUCTION AND BACKGROUND OF SLEEP DISRUPTION

84

8. SLEEP SATISFACTION, SLEEP-WAKE PATTERN, AND AGING

Score ± SEM

(A) 4

KSS (Sleepiness)

5 6 7 8

Age:

≤25

26-45

>45

Age:

≤25

SSS ≤3.5

Score ± SEM

(B)

26-45

>45

Age:

≤25

SSS=3.6-4.0

26-45

>45

SSS>4.0

Wakeability) 6

0

-6

Age:

≤25

26-45

>45

Age:

≤25

SSS ≤3.5

Score ± SEM

(C)

V (Da

26-45

>45

Age:

≤25

SSS=3.6-4.0

26-45

>45

SSS>4.0

Wakeability)

6

0

-6

Age:

≤25

26-45

>45

Age:

≤25

SSS ≤3.5

Score ± SEM

(D)

S(

26-45

>45

Age:

≤25

SSS=3.6-4.0

26-45

>45

SSS>4.0

Sleepability)

6

0

-6

Age:

≤25

26-45

>45

Age:

≤25

SSS ≤3.5

26-45

>45

Age:

≤25

SSS=3.6-4.0

26-45

>45

SSS>4.0

FIGURE 8.2 Self-assessments of wakeability and sleepability in groups with different age and SSS. See notes to Fig. 8.1.

such a sleep was observed after prolonged previous wakefulness and in close proximity to the minimum of rectal temperature rhythm. The second factor was represented by ease of awakening and feeling refreshed after sleep. Its relationship with objective measures of night sleep quality and circadian phase was found to oppose the relationship shown by the first factor.26,27 One can suggest that contribution of the items loading at the second factor to general sleep satisfaction can increase due to age-associated weakening of the sleep drive in combination with advance of phase of the sleepewake cycle and other circadian rhythms. Indeed, the idea that older ages are characterized by reduction of the homeostatic sleep drive was corroborated by numerous experimental findings. Particularly, the experimental research

suggested that the reduction of slow-wave activity and slow-wave sleep is the most obvious age-related modification of the sleep electroencephalographic spectrum.28,29 Since such reduction appears to be already present in middle-aged adults,30 the age-associated dumping of amplitude of slow-wave activity and decrease of percentage of slow-wave sleep signify the earliest phase of the process of sleep aging.4 However, neither reduction of the sleep drive nor advance of the sleepewake cycle can explain why those older healthy people who report good night sleep fully ignore the clearly recognized signs of worsening of their night sleep quality. The answer can be found in the theoretic framework of slightly different from the two-process model

I. INTRODUCTION AND BACKGROUND OF SLEEP DISRUPTION

REFERENCES

conceptualization of sleepewake regulation known as the opponent process model.31,32 Based on lesion studies involving squirrel monkeys, Edgar et al.31 conceptualized the sleepewake regulation as an interaction between the competing drives for sleep and wake (i.e., the sleep- and wake-promoting processes). These two drives oppose each other and interact to regulate the daily cycle of sleep and wakefulness in an optimal manner. For instance, the circadian alerting process can oppose the sleep-promoting process in the species of diurnal primates during the subjective day.31 Similar interaction of opponent processes was proposed by Dijk and Czeisler32 to explain the maintenance of sleep across the whole night in humans. We earlier showed that a weakening of the sleep drive in older participants of nap and sleep deprivation studies was associated with the electroencephalographic changes pointing at possibility of disinhibition of their wake drive.33e35 Such relative strengthening of this drive can bring some advantages to healthy older people living in our postindustrial 24-hour societies. For instance, they may better tolerate sleep deprivation compared to younger people.36,37 Another example is the age-associated changes in maximal sleep capacity revealed in the experimental studies of sleep duration in the absence of social and circadian constraints. When younger adults have an opportunity to extend time in bed for several nights in a row, their sleep tends to lengthen to approximately 9 h, whereas significant shortening of such maximal sleep capacity to approximately 7.5 h was found in older people.38 The present results indicate that sleep satisfaction remained positively linked to the wakeability characteristics of the sleepewake cycle on the whole interval of ages from early to late adulthood. Therefore, the expected age-associated decline of sleepability characteristics of the sleepewake cycle shown by participants with high SSS was compensated by an increase of all their wakeability characteristics. Particularly, scores on anytime and daytime wakeability scales were elevated. Besides, score on morning lateness scale and KSS score at 9:00 after sleepless night were reduced. It seems that ability of adjustment of the perception of good night sleep to the typical for this age sleep-wake pattern persists in middle-aged adults due to the age-associated strengthening of their wake drive relative to their drive for sleep. Unimportance of the perceived signs of deterioration of night sleep quality (i.e., due to the weakening of the drive for sleep) can be explained by the appearance of feeling of full refreshment after night sleep and easiness of awakening in people of this and older ages (i.e., due to the strengthening of the opposing drive for wake). In sum, the feeling of good night sleep is not declining with advancing of age. There exists a significant link between sleep satisfaction and typical for this age features

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of sleepewake pattern. Sleep satisfaction can remain adjusted to the age-typical sleepewake pattern due to certain underlying neurophysiological changes across the life span, such as the change in relative strengths of the opposing drives for sleep and wake.

Acknowledgments The author was supported by a grant from the Russian Foundation for Basic Research (grant number19-013-00424). Conflict of Interest No potential conflict of interest was reported by the author.

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I. INTRODUCTION AND BACKGROUND OF SLEEP DISRUPTION