Neurobiology of Aging 26 (2005) 135144

Homeostatic sleep response to naps is similar in normal

elderly and young adults
Ian G. Campbell , Irwin Feinberg
UCD Sleep Laboratory, Department of Psychiatry and Behavioral Sciences, University of California, Davis, CA 95616, USA
Received 9 June 2003; received in revised form 29 January 2004; accepted 27 February 2004

Abstract
Delta homeostatic regulation can be challenged by reducing delta need with daytime naps and measuring delta in post-nap sleep. We
previously demonstrated that, after a late afternoon nap, young adults reduce the amount of delta in post-nap sleep by the amount in the
nap. We compared homeostatic responses of 19 young adults (mean age 22.4 years) and 19 normal elderly subjects (mean age 71.4 years).
Each participated in four separate 2-day sessions that consisted of a baseline night, a nap, and post-nap sleep. Nap times were 0900, 1200,
1500 and 1800 h. The 1800 h nap contained the largest amount of delta and produced the largest reduction in post-nap delta. The young
and elderly groups respectively produced 28 and 24% of baseline delta in the 1800 h nap. Both groups showed equivalent delta regulation,
reducing post-nap delta by 28 and 25%, respectively. In both age groups, the decrease in post-nap delta resulted from a reduced rate of
delta production (power/min) and reduced non-rapid eye movement (NREM) sleep duration. Period-amplitude analysis showed that the
reduction in power/min resulted from decreases in delta wave amplitude and incidence. None of the responses to nap challenges differed
significantly across age groups nor were there gender differences or age by gender interactions. These results show that delta homeostatic
responses to naps in the elderly parallel those of young subjects. REM sleep showed no homeostatic reductions following naps in either
group. We believe that the striking differences in the delta and REM responses point to different biological roles of the two kinds of sleep.
2004 Elsevier Inc. All rights reserved.
Keywords: Aging; Sleep; EEG; Delta; REM; Naps

1. Introduction
Understanding the relationship of sleep to age over the
human life span is fundamentally important to gerontology.
This relation holds clues to the nature of brain maturation
and aging as well as to the function of sleep. The deep sleep
EEG shows the most marked age related changes. Deep sleep
is characterized by high amplitude slow (delta) waves (visually scored stage 4 or computer-measured 0.33 Hz power).
The age changes in delta gain interest because this stage
of sleep reflects the homeostatic balance of sleep and waking [5,15]. Thus, the intensity (power in 0.33 Hz EEG) of
NREM delta increases as the duration of prior waking increases. Delta intensity declines systematically across sleep
as the homeostatic balance is restored. The age related reduction in deep sleep is most rapid during late childhood
and adolescence. However, delta continues to decline slowly
during adulthood. As a result, delta EEG power at age 70
years is about 50% of the level at age 20 years [14,17,20,28].

Corresponding author. Tel.: +1-530-752-7216; fax: +1-530-752-5350.

E-mail address: igcampbell@ucdavis.edu (I.G. Campbell).

0197-4580/$ see front matter 2004 Elsevier Inc. All rights reserved.
doi:10.1016/j.neurobiolaging.2004.02.021

In addition to EEG changes, aging alters the sleep-wake

cycle in ways perceptible to the individual. The most prominent change is an increase in the amount of waking across
adulthood [2]. The number of awakenings increases linearly
across the life span. The duration of awakenings begins to
increase in midlife and accelerates in the fifth to seventh
decade [18]. The resulting fragmentation of sleep in the elderly often produces complaints of insomnia that are difficult
to treat. Current hypnotics act at the GABAbenzodiazepine
complex. They provide short-term relief for most patients,
but increase the risk of falls and produce tolerance that can
progress to dependence. Furthermore, current hypnotics, including the non-benzodiazepine zolpidem, distort the sleep
EEG pattern by decreasing the slow wave EEG that is an
indicator of homeostasis [22]. The functional significance
of these distortions is unknown. One possibility is that they
cause less restorative sleep, a frequent complaint of patients
taking hypnotics.
The sleep fragmentation in the elderly is likely an aging
or degenerative phenomenon. The delta EEG decline across
adulthood is also usually interpreted as an aging or degenerative change. However we have recently hypothesized that
the same processes that cause the maturational decrease in

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I.G. Campbell, I. Feinberg / Neurobiology of Aging 26 (2005) 135144

delta across childhood-adolescence produce the slower delta

decline during adulthood [16,17].
It is generally acknowledged that better treatments
for insomnia are needed. A step toward more rational
pharmacotherapy would be to establish the physiological
causes of insomnia in the elderly. One possibility is that
sleep fragmentation in the elderly results from impaired
homeostatic sleep regulation. An alternative possibility
is that this age change is caused by impaired circadian
regulation.
There have been a relatively large number of studies
comparing the amplitude and period of circadian rhythms in
young and elderly subjects (reviewed in [3]). Fewer studies
have examined homeostatic sleep responses in the elderly.
The experiments thus far have tested the response to the
increased homeostatic need imposed by sleep deprivation.
These studies have shown that the elderly can increase visually scored slow wave sleep following prolonged waking
[4,8,33,37]. The converse challengedecreasing homeostatic need by reducing waking duration with daytime
napshas not previously been investigated in the elderly.
Nap challenges are also clinically interesting because the
elderly often nap and the consequences of such naps for nocturnal sleep have not been thoroughly tested. Monk et al. [29]
have shown that afternoon napping reduces nighttime sleep
efficiency in the elderly, but the effects on slow wave EEG
were not reported. Compared to sleep deprivation, nap challenges may provide a more quantitative test of homeostatic
mechanisms because the average delta response to naps is
more precise. In young adults, the amount of delta expressed
in naps taken late in the day is subtracted from post-nap
sleep; i.e. the 0.33 Hz activity accumulated in these naps,
when added to that in post-nap sleep, closely approximates
the 0.33 Hz activity of a baseline night [25,38]. A similar
quantitative response does not hold for the delta response
to sleep deprivation. In both young and elderly subjects, the
increase in 0.33 Hz EEG following a night of sleep deprivation is far smaller than the amount lost.
This article is the second of a series of papers that compare the responses of young and elderly normal subjects to
naps taken at four different times of day. Our first report
showed that delta increases linearly across daytime naps
and declines linearly across non-REM periods (NREMPs)
on a baseline night [17]. Because absolute delta is greatly
reduced in the elderly, their linear slopes across waking
and sleep are significantly flatter. However, when the data
are normalized to each subjects baseline level, the slopes
of the two age groups are essentially the same. This means
that the normalized homeostatic delta need in young and
elderly subjects increases at about the same rate per hour
of waking and declines at similar rates across NREM
periods.
In this report we compared the ability of young and
normal elderly subjects to conserve delta across nap and
post-nap sleep. We also examined the homeostatic responses
of NREM and REM durations in the two groups.

Table 1
Age and gender characteristics of the subjects in the two age groups
Group

Age (years)
Mean

S.D.

Median

Range

Young (n = 19)
Female (n = 10)
Male (n = 9)

22.4
22.6
22.2

1.4
1.7
1.0

22.0
22.2
22.0

20.225.1
20.225.1
20.824.2

Elderly (n = 19)
Female (n = 11)
Male (n = 8)

71.4
72.3
70.2

4.9
4.8
5.0

70.5
72.0
69.5

65.381.8
66.481.8
65.378.8

2. Methods
2.1. Subjects
Nineteen normal young adult subjects and 19 normal
elderly subjects (Table 1) gave informed consent and received payment for participation in the study. Young adults
were recruited among UC Davis graduate and undergraduate students. Elderly subjects were recruited from the Davis
community with newspaper advertisements and presentations at senior centers. Prospective subjects were initially
screened via a medical history interview. Those with current psychiatric illness, or a history of head injury, epilepsy,
or stroke were excluded. Subjects using medication with
known CNS effects were also rejected. Urinalysis confirmed that subjects were not using prohibited prescription
or non-prescription drugs. Habitual nappers and subjects
with known sleep abnormalities were also excluded. The
final screening was a two night polygraphic recording in
the laboratory. Young subjects who slept less than 5 h or
had less than 15% combined stages 3 and 4 were excluded.
Elderly subjects who slept less than 5 h were excluded. Subjects whose ability to sleep in the laboratory was compromised by frequent nighttime awakenings or arousals were
excluded.
2.2. Study design
Each subject participated in four 2-day recording sessions. Each session consisted of a baseline night, a nap the
following day, and a post-nap night. Nap times were 0900,
1200, 1500, and 1800 h. Each subject completed all four
nap times with the order varied according to the subjects
personal schedules. Their busy schedules made systematic
or random variation of the nap order impractical. Intervals
between recording sessions varied from 4 days to several
weeks. The median interval between two recording sessions
was 11 days for young adults and 9 days for elderly. Subjects
repeated the 2-day session if their total sleep in the scheduled nap was less than the 25 min minimum. Subjects who
failed to meet this criterion in three sessions were dropped
from the study. One elderly subject and two young adults
were eliminated for this reason.

I.G. Campbell, I. Feinberg / Neurobiology of Aging 26 (2005) 135144

Nineteen young adult and 19 elderly subjects passed all

the initial screenings and completed all four naps. All elderly subjects and seven of the young subjects were in
bed from 2300 to 0700 h on baseline and post-nap nights.
Twelve young adults had been recorded with a 23300700 h
time-in-bed schedule before any elderly subjects were studied. We had intended to use the 23300700 h schedule for
all subjects, but the elderly proved unwilling to stay up until 2330 h. Therefore, all elderly, and the remaining seven
young subjects were studied with 23000700 h time-in-bed
schedules. These different time-in-bed schedules did not produce significant differences in NREM or REM durations in
the two subsets of young adults. The seven young adults
who were in bed from 2300 to 0700 h had more wake time.
All subjects maintained the experimental time-in-bed for the
3 days prior to each study. We explained the importance
of maintaining this schedule and of not napping during the
day. Each night subjects were questioned about their compliance. Subjects who reported inadvertent daytime napping
were rescheduled. To further document compliance, subjects
phoned the laboratory upon retiring and upon awakening.
These calls were recorded and stamped with the time and
phone number of origin.

2.3. EEG recording and analysis

Sleep EEG was recorded on baseline nights, naps and
post-nap nights in the same individual bedroom of a four-bed
sleep laboratory. Subjects reported to the laboratory 11.5 h
prior to bed time for electrode application. Electrode
impedance was less than 5 k
at the time of application.
EEG was recorded from electrodes applied at C3, C4 and
O1 referred to the contralateral mastoid. EOG was recorded
between the left outer canthus and the mid-forehead. Signals were amplified and filtered (0.3 Hz low, 100 Hz high,
notch filter out) on Grass 7P511 amplifiers and digitized at
200 Hz on computer.
PASS PLUS (Delta Software, St. Louis) software performed period amplitude and power spectral analysis on
EEG in all artifact-free 20 s epochs. Power spectral analysis was configured to perform the fast Fourier transform
(FFT) on 5.12 s Welch tapered windows with 2.62 s overlap, producing eight windows per epoch. With these digitization and analysis settings, FFT does not yield the traditional frequency bands. Thus, the delta band was actually
0.293.03 Hz. For convenience we report it here as 0.33 Hz.
The effects of naps on the entire EEG spectrum within
NREM and REM will be presented in a future report.
The EEG power measure produced by FFT combines the
effects of wave amplitude and wave incidence. Period amplitude analysis [24] allows these variables to be measured
separately. Pass Plus performs period amplitude analysis on
halfwaves identified by baseline (zero) crossing or zero first
derivative points. Baseline crossing analysis is more effective for low frequency waves and was used to produce the

137

following measures of delta. Delta integrated amplitude (IA),

in V s, is the area under all halfwaves in 0.33 Hz frequency
band. IA is analogous to spectral power in that it reflects both
wave amplitude and incidence. Delta time in band (TIB), in
s, is the sum of all halfwave periods in the 0.33 Hz band.
TIB is almost entirely determined by wave incidence. Delta
wave amplitude is estimated as average sample amplitude
(ASA) in V. ASA is equal to IA divided by TIB.
2.4. Scoring
The digitized EEG and eye movement leads were displayed on a computer monitor in 20 s epochs. These epochs
were scored visually as NREM, REM and waking according
to modified Rechtschaffen and Kales criteria [32]. A second
individual checked the scored sleep data, and a third person
resolved differences. Epochs with artifact were also marked.
Artifacts included low frequency waves caused by sweating or loose electrodes, high frequency EMG artifacts, and
60 Hz activity. Artifact-containing epochs made up about
4% of the total NREM and REM epochs on baseline nights.
The visually scored data were linked to the computer EEG
analyses for each epoch. Epochs containing artifact were included in the sum of vigilance states but were excluded from
EEG results.
2.5. Evaluation of delta EEG in naps and post-nap sleep
We first investigated delta homeostasis by testing whether
the naps reduced total 0.33 Hz power and integrated amplitude on the post-nap night. To do this we established each
subjects baseline delta production as his/her mean across
the four baseline nights of the four experimental sessions.
We then compared this mean baseline value with delta power
in each of the four post-nap nights using a repeated measures analysis of variance (ANOVA) with age and gender
grouping factors. When the ANOVA was significant at =
0.05 each post-nap night was compared against the baseline
mean with post-hoc t-tests using Bonferroni corrections for
multiple comparisons. We also examined whether the delta
reduction on post-nap nights approximated the amount of
delta in the naps. Similar evaluations were made for NREM
and REM durations.
We examined the age and gender effects on NREM
delta power across the four naps with a repeated measures
ANOVA with age and gender as grouping factors. We decided, a priori, to separately evaluate the delta in the young
and elderly groups even if the initial ANOVAs revealed
no age by nap interaction. Similar ANOVAs evaluated age
and gender effects on trends in NREM duration and REM
duration across the four naps and the trends in delta power,
NREM duration and REM duration across the four post-nap
nights. Data were normalized as percents of each subjects
four night baseline mean values for presentation in figures
and in tables.

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I.G. Campbell, I. Feinberg / Neurobiology of Aging 26 (2005) 135144

Normalized data were also used in all statistical analyses not involving direct comparisons with baseline values.
Because baseline values normalized as a percent of baseline are by definition 100% and therefore have no error, raw
data were used for statistical comparisons involving the four
night baseline means.
3. Results
3.1. Nap effects on post-nap night NREM and REM
durations
Table 2 presents polysomnography data for the mean of
the four baseline nights, the 1800 h nap, and the 1800 h
post-nap night. The elderly had less total sleep time, less
NREM, and less REM on baseline nights, naps, and post-nap
nights. On the baseline nights, sleep latency was approximately 17 min in both the young and elderly groups, but the
elderly had more wake time. This was due to both decreased
total sleep time and the longer time in bed requested by the
elderly subjects.
NREM duration in the naps did not increase substantially or significantly (F3,102 = 1.80, P = 0.15) as naps
were taken later in the day (Fig. 1). Nor were there any
age (F1,34 = 1.81, P = 0.19) or gender effects (F1,34 =
0.65, P = 0.43) on NREM duration in the naps. Post-nap
night NREM sleep decreased following naps, and the decrease was greater following later naps (F3,102 = 5.02, P =
0.0027). There were no age (F1,34 = 0.03, P = 0.85) or
gender (F1,34 = 0.76, P = 0.39) effects on the post-nap
night NREM duration. In separate analyses of the young and
elderly groups, post-hoc multiple comparisons showed that
the decrease from baseline in post-nap NREM durations was
statistically significant (at = 0.01) following the 1500 and
1800 h naps. In addition, post-nap NREM durations were
significantly decreased on the post-nap night for the 1200 h

nap in the young adults and for the 0900 h nap in the elderly.
The sum of nap plus post-nap NREM durations significantly
exceeded baseline levels (P < 0.0005 for all nap times in
both young and elderly) even when post-nap NREM duration was significantly reduced (Fig. 2). Although, as shown
below, a post-nap decrease in NREM duration contributed to
delta conservation, NREM duration itself was not conserved.
REM sleep duration in naps decreased (F3,102 = 7.93,
P = 0.0001) as naps were taken later in the day (Fig. 1), and
the elderly had significantly (F1,34 = 7.93, P = 0.0001)
less REM in the naps than young adults. Although there
was no significant (F3,102 = 0.98, P = 0.41) interaction
between age and nap time effects on REM duration in the
naps, separate analyses showed the decreasing trend to be
significant only in the young adults. In young adults stage
REM duration decreased from a mean of 28 4 min in the
0900 h nap to 133 min in the 1800 h nap (significant effect
of nap time, F3,54 = 5.03, P = 0.0038). In the elderly REM
duration decreased from a mean 11 3 min in the 0900 h
nap to 41 min in the 1800 h nap (F3,54 = 2.28, P = 0.10).
REM in naps did not reduce REM duration in post-nap sleep
in either group. In young adults post-nap REM duration was
slightly but not significantly elevated following the afternoon naps, and in the elderly post-nap REM duration was
slightly but not significantly decreased. For young adults
the sum of nap and post-nap REM duration significantly exceeded baseline levels (P < 0.01 for all nap times) by about
25% (Fig. 3). In the elderly who had small amounts of REM
in the naps, nap+post nap REM duration did not differ from
baseline.
3.2. Nap effects on post-nap night delta power
3.2.1. Age and gender effects
As previously reported [17], delta power in the naps increased as naps were taken later in the day, i.e. were pre-

Table 2
Vigilance state data for four night baseline mean, 1800 h nap, and 1800 h post-nap night

Baseline mean
Young adult
Elderly
1800 h nap
Young adult
Elderly
1800 h post-nap
Young adult
Elderly
a
b

Time in beda (min)

Sleep latency (min)

Total sleepb (min)

NREMb (min)

Mean
S.E.
Mean
S.E.

461.05
3.04
480.00
0

16.82
2.16
16.95
2.85

404.03
3.04
367.02
6.75

307.18
2.18
284.83
5.83

96.85
2.16
82.19
2.88

25.68
2.75
56.86
6.34

Mean
S.E.
Mean
S.E.

120
0
120
0

9.78
1.86
15.09
3.87

86.81
5.68
67.70
3.87

73.53
5.30
63.31
3.42

13.28
2.76
4.39
1.26

24.96
4.35
33.77
4.65

Mean
S.E.
Mean
S.E.

461.05
3.04
480.00
0

43.11
8.31
29.84
4.25

375.58
7.72
339.58
11.04

270.63
6.68
257.05
8.92

104.95
3.13
82.53
4.97

48.12
8.25
81.35
10.99

Scheduled time in bed. Actual time in bed may differ slightly.

Does not include movement or stage 1.

REM (min)

Total wakeb (min)

I.G. Campbell, I. Feinberg / Neurobiology of Aging 26 (2005) 135144

139

Fig. 1. NREM delta power, NREM duration, and REM duration in naps (filled circles) and post-nap nights (open circles). Nap data are means of each
subjects data expressed as a percent of that subjects four night baseline mean. Post-nap night data are means of each subjects data expressed as
percent change from that subjects four night baseline mean. In both young and elderly subjects, NREM delta power in naps increased significantly as
naps were taken later in the day and NREM delta power on the post-nap night decreased significantly as naps were taken later in the day. Nap NREM
duration did not change significantly across the four nap times in either group. However, for the young adults post-nap night NREM duration decreased
more following later naps. REM duration decreased significantly across the naps in the young adults, but the decrease was not significant in the elderly.
Post-nap REM duration did not change from baseline in the elderly but increased significantly in the young adults following later naps.

ceded by longer waking durations. Fig. 1 shows that this

increase in delta as naps were taken later in the day was accompanied by decreasing delta in the delta on the post-nap
nights. With delta power standardized as the percent of baseline power for each subject, ANOVA revealed no significant
effects of age (F1,34 = 1.62, P = 0.21), gender (F1,34 =
3.77, P = 0.06) or age by gender interaction (F1,34 = 0.02,
P = 0.88) on delta in the naps. Nor was there any significant interaction between age (F3,102 = 0.40, P = 0.75) or
gender (F3,102 = 0.67, P = 0.57) and the increase in delta
as naps were taken later in the day. There were also no effects of age (F1,34 = 0.23, P = 0.64), gender (F1,34 =
0.00, P = 0.03) or age by gender interaction (F1,34 = 1.24,
P = 0.27) on the amount of delta on the post-nap nights.
There were no significant interactions between age (F3,102 =
0.84, P = 0.48) or gender (F3,102 = 0.50, P = 0.68)
and the amount of the delta decrease across the post-nap
nights.

3.2.2. Young adults

Examined separately in the young adult group, delta
increased significantly (F3,54 = 14.2, P < 0.0001) as
naps were taken later in the day. Expressed as a percent
of the amount of total delta power on the baseline night,
delta power in the naps increased from (mean S.E.)
11.4 1.3% in the 0900 h nap to 27.9 2.7% in the 1800 h
nap. As the amount of delta in the naps increased, total
delta power on the post-nap night decreased significantly
(F3,54 = 16.4, P < 0.0001) (Fig. 1). However, the decrease from baseline in total delta power on the post-nap
night was significant only following the 1500 h (paired
t18 = 4.61, P = 0.0001) and 1800 h (paired t18 = 4.79,
P < 0.0001) naps. For the 1800 h nap delta power on the
post-nap night was 28.4% below the baseline mean, almost equal to the 27.9% (of baseline) delta expressed in
the nap. Therefore, the sum of total NREM delta power
in the nap and the total delta power on the post-nap night

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I.G. Campbell, I. Feinberg / Neurobiology of Aging 26 (2005) 135144

Fig. 2. Comparison of NREM duration on the baseline night with the

sum of nap and post-nap night NREM duration. Data are means of each
subjects data expressed as a percent of that subjects four night baseline
mean. Error on the nap bar is the S.E. of the sum of nap and post-nap night.
NREM duration decreased significantly on the post-nap night following
the 1500 and 1800 h naps in both the young adults and the elderly.
In young adults post-nap night NREM duration was also significantly
decreased following the 1200 h nap. In contrast to delta power (Fig. 4),
the sum of NREM duration in the nap plus the post-nap night exceeded
baseline for all nap times.

closely approximated total delta power on the baseline night

(Fig. 4).
The conservation of delta in the young adult group was
an average result that did not hold for every individual. For
the 1800 h nap, nap+post-nap night delta sums ranged from
74 to 145% of baseline. Furthermore, although delta power
in the 1800 h nap was significantly correlated (r = 0.50,
P = 0.001) with the reduction in post-nap night delta, this
correlation was absent for the 1500 h nap (r = 0.01, P =
0.97). The significant correlation for the 1800 h nap largely
resulted from two outliers (r = 0.26 P = 0.12 with outliers
removed).

Fig. 3. Comparison of REM duration on the baseline night with the sum
of nap and post-nap night REM duration. REM duration was not reduced
on the post-nap night following any of the naps in young adults or elderly
subjects. Post-nap REM duration increased following the 1500 and 1800 h
naps in young adults. In contrast to NREM delta power (Fig. 4), in
young adults the sum of nap and post-nap REM duration greatly exceeded
baseline REM duration. In the elderly who had less REM in the naps,
this sum did not differ significantly from baseline.

3.2.3. Normal elderly

In the elderly, both the pattern of delta accumulation in
the naps and the effects of the naps on post-nap delta resembled those in young adults. Again delta power tended to
increase as naps were taken later in the day. In the 0900 h
nap, total delta power was 9.2 0.8% of baseline; in the
1800 h nap total delta power was 23.8 2.6% of baseline.
As in the young adults, post-nap delta power was significantly reduced following the 1500 and 1800 h naps. In the
elderly but not the young subjects, delta power following
the 0900 h nap was significantly below baseline (Fig. 1).
As in the young adults, the reduction in delta power following the 1800 h nap (25.3% of baseline) was close to the
delta power (23.8%) in that nap. For the elderly, the sum
of nap and post-nap delta roughly equaled baseline values

I.G. Campbell, I. Feinberg / Neurobiology of Aging 26 (2005) 135144

141

for the three naps in which delta was significantly reduced

(Fig. 4).
3.3. Composition of delta EEG compensation following
the 1800 h nap

Fig. 4. Comparison of total NREM delta power on the baseline nights

with the sum of nap and post-nap night total NREM delta power. In
young adults, following the 1500 and 1800 h naps, post-nap night delta
is reduced (significantly) by the amount of delta expressed in the naps so
that the sum of the nap and post-nap delta equals the amount of delta on
the baseline. For the 0900 and 1200 h naps this sum exceeds the baseline
delta. In the elderly post-nap night delta is significantly reduced following
all naps. The sum of nap and post-nap delta for the 1500 and 1800 h
naps and also for the 0900 h nap is similar to the baseline night delta.
This sum exceeds baseline delta for the 1200 h nap.

Data are presented here, and summarized in Table 2, only

for the 1800 h nap which had the largest effects on post-nap
sleep. Total delta power in post-nap sleep could have been
reduced by a lower rate of delta production (decreased delta
power/min), a decreased NREM duration, or a combination
of both. In young adults, NREM total delta power in the
post-nap night following the 1800 h nap was 28% below the
baseline level. This decrease was produced by a 19% reduction in power/min and a 12% reduction in NREM duration. The same pattern was observed for the 25% reduction in total delta power in the elderly following the 1800 h
nap. Delta power/min was decreased by 17% below baseline, and NREM duration by 9%.
A change in delta power/min can be produced by a change
in delta wave amplitude and/or a change in delta wave incidence. Period amplitude analysis but not FFT can separate
the effects on amplitude and incidence. Integrated amplitude
is the period amplitude measure homologous to power. On
the post-nap night following the 1800 h nap, NREM delta
integrated amplitude decreased by 23% in the young adults.
This change resulted from a 13% reduction in integrated
amplitude/min and the 12% reduction in NREM duration.
The reduction in wave amplitude (10%) was significantly
greater (paired t18 = 3.14, P = 0.006) than the reduction
in incidence (4% reduction in TIB). In the elderly, the same
analysis for the delta reduction after the 1800 h nap showed
a somewhat different pattern. The 7% reduction in average
sample amplitude did not differ significantly from the 5%
reduction in TIB (paired t18 = 0.80, P = 0.44). However,
across group comparisons of the young and elderly showed
no significant difference between the young and elderly for
the effect of the 1800 h nap on any delta EEG measure (t-test
results in Table 3).

Table 3
Composition of NREM Delta decrease in recovery night following 1800 h nap
Variable

Young adult
Decrease (%)

Total delta power

NREM duration
Delta power/min
Total integrated amplitude
Integrated amplitude/min
Time in delta band/min
Average sample amplitude

28.4
12.0
19.3
22.7
12.7
3.7
9.6

4.5
1.8
4.1
3.3
2.8
1.5
1.9

Elderly
Paired t vs. baseline
t18
t18
t18
t18
t18
t18
t18

= 4.79,
= 6.71,
= 3.91,
= 6.48,
= 4.41,
= 2.36,
= 4.74,

P
P
P
P
P
P
P

< 0.0001
< 0.0001
= 0.0005
< 0.0001
= 0.0002
= 0.015
< 0.0001

Elderly vs. young adult

Decrease (%)
25.3
9.3
16.6
20.3
11.1
4.8
6.6

3.5
3.2
3.0
3.1
2.1
1.6
1.5

paired t vs. baseline

t-test

t18 =6.19, P < 0.0001

t18 = 2.92, P = 0.0046
t18 = 5.31, P < 0.0001
t18 = 5.40, P < 0.0001
t18 = 5.74, P < 0.0001
t18 = 3.08, P < 0.0032
t18 = 4.05, P < 0.0001

t36 = 0.54, P = 0.59

t36 = 0.72, P = 0.47
t36 = 0.52, P = 0.60
t36 = 0.53, P = 0.60
t36 = 0.44, P = 0.66
t36 = 0.51, P = 0.62
t36 =1.24, P = 0.22

Mean (S.E.) of data standardized as percent decrease from each subjects four night baseline mean. Nearly all delta measures were significantly
decreased in both young and elderly subjects and the effects did not significantly differ between the two age groups.

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4. Discussion
These data shed light on the homeostatic regulation of
sleep in young and elderly normal subjects as evaluated by
the ability to conserve delta EEG across a nap and a post-nap
night. The data also demonstrate that the mechanism of delta
conservation is similar in both groups. Both young and elderly subjects maintain the homeostatic quota by reducing
both the rate of delta production and the duration of NREM
sleep. In both groups NREM duration was partially conserved, apparently at the service of delta conservation. REM
duration was not conserved.
In this study, we tested the homeostatic effects of naps at
four different times of day. Trends of effects across the four
nap times are discussed briefly, but we focus the discussion
on the 1800 h nap, which had the largest amount of delta
and the greatest effect on nighttime sleep.
4.1. Regulation of delta EEG homeostasis
These experiments were based on the proposition that
sleep homeostasis is demonstrated if the amount of delta
EEG expressed in a nap when summed with the amount
in the post-nap night, equals the amount of delta EEG in
baseline night sleep. Such homeostatic regulation requires
that the brain register the amount of delta in the nap, retain
that information until night-time, and then reduce night-time
delta in post-nap sleep by that amount. It seemed plausible
that the elderly brain might lose the ability to accurately recall the amount of delta in the nap. Our data show this is not
the case. Delta homeostasis evaluated by this test is remarkably similar in the young and elderly. In young adults NREM
delta power in the 1800 h nap was 28% of the baseline night
amount, and post-nap delta power was reduced by 28%. In
the elderly group the 1800 h nap contained 24% of baseline
amount of NREM delta power and post-nap delta power was
reduced by 25%. The difference between the young and elderly subjects did not approach significance, suggesting that
the elderly conserve delta as well as the young adults. Although we think it unlikely, it is possible that the 3% difference between groups in decreased delta represents a slight
impairment in homeostatic regulation in the elderly.
Data from the other naps also point to roughly equal
homeostatic regulation in the young and the elderly. Conservation of delta was similar in the two groups following
the 1500 h nap and both groups had smaller delta reductions
following the morning naps. Delta EEG in sleep is strongly
related to the duration of prior waking. If delta regulation
is similar in the two groups, the rate of growth of delta as
naps are taken later in the day should be similar. With delta
power normalized as a percent of baseline night power, both
groups showed a significant increase in delta across the naps
and ANOVA showed no significant interaction between age
and the trend across naps or the trend across post-nap nights.
We also found no effect of gender on any of our tests of
delta regulation. Women have been reported to have higher

levels of delta EEG [7]. However, with delta power normalized, we found no gender difference and no interaction
between age and gender.
The delta conservation observed in the two later naps was
an average result that was not observed in each individual
subject. In fact, correlation coefficients computed between
the amount of delta in the nap and the reduction of delta in
post-nap sleep were negligible even though the group means
showed almost perfect delta conservation. The inability to
predict individual behavior from strong and highly robust
group averages is typical for sleep EEG data. For example,
the decreasing monotonic trend in delta across NREM periods is massively significant with F values often exceeding
100 [24]. Nevertheless, these trends cannot predict the sleep
EEG dynamics of individual subjects who can have more
delta EEG activity in the second or even third NREM period
than in the first (cf. [23]).
The delta conservation found in the young adults confirms
two previous investigations of this question with computer
measurement [25,38]. The present results are also qualitatively consistent with data of Karacan et al. [27]. They measured delta visually as stage four EEG and found that it was
reduced following afternoon naps. They correctly hypothesized that delta represented a consummatory process.
The demonstration here that the elderly maintain a homeostatic response to naps is consistent with visually scored data
showing a homeostatic response to sleep deprivation. The
elderly increase visually scored stages 34 following sleep
deprivation to a degree similar to young adults [9,33,37].
However, recent studies with computer analysis raise the
possibility that young adults have a stronger delta EEG response. Gaudreau et al. [26] found that 25 h of sleep deprivation ending at the habitual waking time produced a
larger relative (expressed a percent of baseline) delta EEG
response in young adults than in middle aged (4060 years)
adults. The circadian change imposed by this protocol prevents direct interpretation of the sleep homeostatic response.
The elderly may have a higher arousal level at the habitual wake time that would diminish their delta response to
sleep loss. Murck et al. [31] performed a 40 h sleep deprivation experiment with onset of recovery sleep at the normal bedtime. They found a smaller delta response in the
elderly. This was primarily an endocrine study and subjects slept with an indwelling catheter. The catheter may
have differentially reduced sleep depth in the elderly group.
A sleep deprivation experiment using computer analysis of
the EEG without circadian or other confounds is sorely
needed.
4.2. Mechanisms of delta conservation in post-nap sleep
In both age groups, a combination of reduced delta EEG
intensity and reduced NREM duration acted to maintain
delta conservation. Thus, delta power/min and integrated
amplitude/min, were significantly reduced on the post-nap
nights. This reduction was caused by decreases in both

I.G. Campbell, I. Feinberg / Neurobiology of Aging 26 (2005) 135144

143

the incidence and amplitude of delta waves. It is thought

that the amplitude of delta waves recorded from the scalp
is produced by synchronous membrane changes in large
populations of cortical neurons. Reduced amplitude following the late naps could be produced by either a reduction in the size of the neuronal pool oscillating in synchrony and/or by smaller membrane changes per neuron.
Comparison of the age groups found no significant difference between the young and elderly for any delta measure. However, the significantly greater effect on amplitude than on incidence in the young but not elderly suggests that there may be some difference in the mechanism
that conserves delta. Moreover, we have not yet completed
the analysis of nap effects on delta in each NREM period of the post-nap night. These will be presented in a future publication. Such analyses may reveal differences between how the young and elderly achieve all night delta
conservation.

4.4. Partial NREM homeostasis across naps and post-nap

sleep

4.3. Homeostatic regulation, homeostatic drive,

circadian regulation, and sleep disturbances

4.5. Absence of REM homeostasis across naps and

post-nap sleep

If homeostatic regulation is essentially intact in the elderly, could impaired homeostatic drive explain their sleep
disturbances? The level of NREM delta has been interpreted
as an indicator of homeostatic drive or pressure. Therefore,
the amount of sleep fragmentation in the elderly should be
negatively correlated with their delta levels. There is no evidence at present that supports this possibility. Correlation
coefficients previously computed in our laboratory between
reduced visually scored delta and the amount of waking in
normal elderly were statistically insignificant [21]. Moreover, the amount of waking increases steadily across the
fifth to seventh decades although delta levels are apparently
at a plateau. Further work on this question with computer
measures of delta would be useful.
If homeostatic drive and regulation are normal in the
elderly, deficient circadian regulation may cause their impaired sleep. Circadian regulation in the elderly has been
extensively investigated, but the results are inconsistent (reviewed in [3]). Some studies [11,34,36] but not others [30]
report that the amplitude of circadian rhythms is decreased
in the elderly. Studies on the length of the endogenous
circadian period and the presence of phase shifts in the elderly have also yielded inconsistent results (cf. [10,11,30]).
In a clinically relevant study, Campbell and Murphy found
that the body temperature minimum occurred earlier in
normal elderly than in young adults. However, there were
no differences in temperature rhythm between elderly subjects with insomnia and normal elderly [6]. Campbell and
Murphys data argue against the possibility that changes
in circadian rhythm alone explain sleep disturbances in
the elderly. Dijk et al. [13] have proposed that an interaction between weakened homeostatic drive and weakened
circadian regulation produces sleep disturbances in the
elderly.

The total absence of stage REM homeostasis across naps

and post-nap sleep found here contrasts strongly with the
behavior of delta EEG. This result is consistent with findings
of previous nap studies [25,38] and also with investigations
of extended sleep. When sleep is extended in young adults by
increasing time in bed, REM duration increases by 50100%
[19,35]. This increase does not reduce the amount of REM
on the following night or delay REM onset [19,35].
An important clue to the function of REM sleep is that
its rate of occurrence increases with prior sleep but is inversely proportional to prior wake duration; in an important
early study, Aserinsky showed that the same pattern holds
for eye movement density [1]. In the present study REM duration decreased as naps were taken later in the day in both
age groups. This decrease may be related to the circadian
modulation of REM sleep that causes REM to be greatest at
the end of the sleep period and to decrease across the day
[12]. However, it is opposite to the trend one would expect
if REM were homeostatically related to prior waking.
Although the quantity of REM sleep is not conserved its
periodic occurrence in mammalian sleep indicates that it
must serve some essential biological function. The data of
the present experiment are consistent with our hypothesis
that this function is intrinsic to sleep processes and does
not directly involve homeostatic recovery from waking brain
activity [16,17,23].

NREM duration showed some signs of homeostatic regulation but did not meet all our criteria. In both the young
adults and elderly, NREM duration was significantly reduced
following the afternoon naps. However, in contrast to delta
EEG, the sum of NREM duration in the naps and post-nap
sleep exceeded rather than equaled baseline levels. An interesting and unexpected observation was that in both groups
NREM duration did not increase significantly across naps,
i.e. with increasing prior wake duration. This differs strikingly from the robust increase in delta. Thus, although its
reduction on the post-nap nights served as part of the mechanism by which delta EEG is conserved, NREM duration
itself is not homeostatically regulated. The elderly response
did not differ from that of young adults in any tests of NREM
homeostasis.

5. Conclusion
Nap studies can be a powerful probe for investigating the
effects of aging on sleep-wake relations and offer an important complement to sleep deprivation experiments. Together, nap and deprivation studies could lead to new mod-

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I.G. Campbell, I. Feinberg / Neurobiology of Aging 26 (2005) 135144

els of sleep and aging that provide clues to their biological mechanisms. We found here that normal elderly subjects
show homeostatic responses to naps similar to those of normal young adults. It would be interesting to extend this nap
protocol to young and elderly subjects with insomnia. Such
studies could shed light on the possibility that disruption of
homeostatic regulation causes age-related insomnia.

Acknowledgments
This work was supported by NIH grant MH56112. Tara
Montgomery, Mike Kuoppamaki, and Shaun Spaulding provided excellent technical assistance in the data collection
and analysis. We also wish to thank the subjects who participated in this study.
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