Am J Physiol Regul Integr Comp Physiol 309: R1112–R1121, 2015.
First published September 2, 2015; doi:10.1152/ajpregu.00127.2015.
Morning and evening physical exercise differentially regulate the autonomic
nervous system during nocturnal sleep in humans
Yujiro Yamanaka,1 Satoko Hashimoto,2 Nana N. Takasu,3 Yusuke Tanahashi,4 Shin-ya Nishide,1
Sato Honma,5 and Ken-ichi Honma5
1
Department of Physiology, Hokkaido University Graduate School of Medicine, Sapporo, Japan; 2Research Center for
Cooperative Projects, Hokkaido University Graduate School of Medicine, Sapporo, Japan; 3Laboratory of Oral
Chronobiology, Graduate School of Dentistry, Osaka University, Osaka, Japan; 4Department of Pediatrics, Asahikawa
Medical University, Asahikawa, Japan; and 5Department of Chronomedicine, Hokkaido University Graduate School of
Medicine, Sapporo, Japan
Submitted 26 March 2015; accepted in final form 25 August 2015
Yamanaka Y, Hashimoto S, Takasu NN, Tanahashi Y, Nishide S,
Honma S, Honma K. Morning and evening physical exercise differentially
regulate the autonomic nervous system during nocturnal sleep in humans. Am
J Physiol Regul Integr Comp Physiol 309: R1112–R1121, 2015. First
published September 2, 2015; doi:10.1152/ajpregu.00127.2015.—Effects of
daily physical exercise in the morning or in the evening were exam-
ined on circadian rhythms in plasma melatonin and core body tem-
perature of healthy young males who stayed in an experimental
facility for 7 days under dim light conditions (⬍10 lux). Sleep
polysomnogram (PSG) and heart rate variability (HRV) were also
measured. Subjects performed 2-h intermittent physical exercise with
a bicycle ergometer at ZT3 or at ZT10 for four consecutive days,
where zeitgeber time 0 (ZT0) was the time of wake-up. The rising
phase of plasma melatonin rhythm was delayed by 1.1 h without
exercise. Phase-delay shifts of a similar extent were detected by
morning and evening exercise. But the falling phase shifted only after
evening exercise by 1.0 h. The sleep PSG did not change after
morning exercise, while Stage 1⫹2 sleep significantly decreased by
13.0% without exercise, and RE sleep decreased by 10.5% after
evening exercise. The nocturnal decline of rectal temperature was
attenuated by evening exercise, but not by morning exercise. HRV
during sleep changed differentially. Very low frequency (VLF) waves
increased without exercise. VLF, low frequency (LF), and high
frequency (HF) waves increased after morning exercise, whereas HR
increased after evening exercise. Morning exercise eventually en-
hanced the parasympathetic activity, as indicated by HRV, while
evening exercise activated the sympathetic activity, as indicated by
increase in heart rate in the following nocturnal sleep. These findings
indicated differential effects of morning and evening exercise on the
circadian melatonin rhythm, PSG, and HRV.
physical exercise; melatonin; body temperature; autonomic nervous
system; sleep EEG; heart rate variability
TIMED PHYSICAL EXERCISE WAS reported to facilitate phase shifts
of the human circadian rhythms to a new time schedule,
suggesting a circadian clock resetting capability of physical
exercise (5, 22). However, the mechanism of resetting by
physical exercise is not well understood. Previously, a single
trial of physical exercise phase shifted the human melatonin
rhythm in a phase-dependent manner (7), suggesting that
physical exercise acts as a time cue for the human circadian
pacemaker similar to a bright light pulse. However, an exercise
pulse under dim light conditions failed to shift the circadian
Address for reprint requests and other correspondence: K. Honma, Dept. of
Chronomedicine, Hokkaido Univ. Graduate School of Medicine, N15 W7,
Kita-ku, Sapporo 060-8638, Japan (e-mail: kenhonma@med.hokudai.ac.jp).
R1112 0363-6119/15 Copyright © 2015 the American Physiological Society
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melatonin rhythm (22). On the other hand, daily physical
exercise accelerated the reentrainment of the sleep-wake cycle
but not of the circadian melatonin rhythm to 8-h phase-
advanced sleep-schedule under dim light conditions (39).
These findings indicated differential effects of physical exer-
cise on the circadian pacemaker and sleep-wake cycle in
humans. Interestingly, reentrainment of both sleep-wake cycle
and circadian melatonin rhythm was accelerated by physical
exercise under bright light conditions (38). Physical exercise
was interpreted to reset the circadian melatonin rhythm indi-
rectly through stimulation of the sympathetic activity, which
enhanced the light inputs to the circadian pacemaker.
Effects of physical exercise on the following nocturnal sleep
were controversial in the literature (10, 40). Physical exercise
in the evening was reported to deteriorate sleep structure by
increasing arousal and inadequate sleep hygiene (4, 15). A
more recent study indicated that heart rate increased and
relaxation time decreased in subsequent sleep after evening
exercise, while there was no change in the sleep polysomno-
gram (PSG) (23). On the other hand, physical exercise in the
daytime was reported to have no effect on the following
nocturnal sleep (15) or to increase non-rapid eye movement
(NREM) sleep (32). The discrepancy in the effect of physical
exercise on sleep was ascribed to a number of factors, includ-
ing the strength and the time of physical exercise (40). The
effects of physical exercise could also depend on whether the
subjects are physically trained or not (19). Physical exercise is
well known to change the activity of autonomic nervous
system, which is involved in a variety of physiology, such as
circulation, endocrinology, metabolism, and thermoregulation
and are under the control of circadian pacemaker (36). Thus,
the effect of physical exercise on the nocturnal sleep could well
depend on the time of exercise.
Physical exercise stimulates the autonomic nervous system
to various extents (27). Heart rate variability (HRV) has been
used to evaluate the effect of physical exercise on the auto-
nomic nervous activity. However, the wide variety of results
was reported on the effect of physical exercise on the auto-
nomic nervous system as measured by HRV (29).
In the present study, effects of daily physical exercise in the
morning or in the evening were examined, focusing on the
circadian rhythms in plasma melatonin and rectal temperature
of young male subjects, who stayed in a living facility for 6
nights. The effects were also examined on sleep PSG and
HRV. We found that physical exercise had differential effects
on these parameters depending on the time of day.
http://www.ajpregu.org
 DAILY PHYSICAL EXERCISE AND HUMAN CIRCADIAN RHYTHMS R1113

A Zeitgeber time (h) The experiment was carried out in a living facility. Details of the
facility have been reported elsewhere (13). Briefly, the facility con-
0 4 8 12 16 20 0
sists of four rooms that are isolated from natural day-night alterna-
tions. Each room is equipped with a bed, desk, comfortable chair,
Pre-Exp2 Sleep PSG and HRV
bicycle ergometer, compact disk player, kitchen, and bathroom. The
1 Natural day light main illumination is supplied from the ceiling by fluorescent tubes and
2 controlled by the experimenter. Communication with the subject was
performed by letter through the anteroom or by intercom. There was
Day

3 no indication of time in the room. In addition, the subjects were not

4 allowed to use timing devices such as a watch, television, radio, and
5 Sleep PSG and HRV cellular phone in the facility.
The light intensity in the waking period was less than 10 lux
6
measured on the forehead of standing subject throughout the experi-
7 ment. There were accessory dim lights of less than 10 lux at bedside
and bathroom. The main illumination and accessory lights were turned
B 0 4 8 12 16 20 0

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150
Pre-Exp2 Sleep PSG and HRV Control

Plasma melatonin (%)

1 Natural day light

2 100
3 Exer
Day

4
5 Sleep PSG and HRV 50
6
7

0
C 0 4 8 12 16 20 0
10 12 14 16 18 20 22 0 2 4 6 8 10

150
Pre-Exp2 Sleep PSG and HRV Morning exercise
Plasma melatonin (%)

1 Natural day light

2 100
Exer
Day

3
4
5 Sleep PSG and HRV 50
6
7

Fig. 1. Schematic presentation of experimental protocols. Experimental pro- 0

tocols are illustrated for the subjects without exercise (A), with morning 10 12 14 16 18 20 22 0 2 4 6 8 10
exercise (B), and with evening exercise (C). Zeitgeber 0 (ZT0) denotes the time 150
of wake-up. The shaded areas indicate the waking period with dim light
conditions (⬍10 lux), and the closed areas indicate the sleeping period. Open Evening exercise
Plasma melatonin (%)

columns with “Exer” in B and C indicate the time of 2-h physical exercise with
a bicycle ergometer. Arrows indicate the time of serial blood sampling. “Sleep
PSG” in the boxed areas indicate the night when sleep polysomnography 100
(PSG) and heart rate variability (HRV) were recorded.

50
MATERIALS AND METHODS

Subjects and Facility

A total of 22 healthy male subjects (age, 22.0 ⫾ 1.8 years; means ⫾ 0
SD; body mass index, 20.9 ⫾ 2.2 kg/m2) participated in the present 10 12 14 16 18 20 22 0 2 4 6 8 10
study as paid volunteers. They had neither a job in the early morning Zeitgeber time (h)
or late at night nor did they go abroad 4 wk before the experiment. The
subjects were not athletes specifically trained for competitive sports, Fig. 2. Twenty-four hour profiles of plasma melatonin rhythms. Mean 24-h
profiles of plasma melatonin on days 1 and 2 (Œ, open circles) and days 6 –7
but had a habit of light exercise, such as cycling, swimming, and (●, solid circles) are plotted in the control (top), morning exercise (middle), and
jogging, once or twice a week. The subjects gave written informed evening exercise (bottom) groups. Melatonin levels were standardized as
consent, which allowed them to withdraw from the experiment at any percentages of the maximum melatonin value on days 1 and 2. Values were
time they wanted. This study was approved by the Ethical Committee expressed as the mean and SD; control, n ⫽ 7; morning exercise, n ⫽ 7;
of Hokkaido University Graduate School of Medicine (no. 04-001). evening exercise, n ⫽ 8.

AJP-Regul Integr Comp Physiol • doi:10.1152/ajpregu.00127.2015 • www.ajpregu.org

R1114 DAILY PHYSICAL EXERCISE AND HUMAN CIRCADIAN RHYTHMS
off automatically during the sleeping period. The room temperature
and humidity were kept in a narrow range (24 ⫾ 2°C and 60 ⫾ 10%).
Experimental Protocols
The subjects were instructed to keep a regular sleep-wake cycle
schedule with 8 h sleep (0000 to 0800) for 2 wk before the experi-
ment. Sleeping time was recorded by the subjects themselves and
movements by an ambulatory device, Actiwatch (Actiwatch-L, Mini-
mitter, USA). One week before the experiment, the subjects stayed in
the facility from 1700 to 1200 on the next day. They were asked to go
to bed at 0000 and wake up at 0800. To examine the circadian peak
phase of plasma melatonin, a serial blood sampling was performed
every 2 h from 1800 to 1000 under dim light conditions (⬍10 lux)
(Pre-Exp1). To adjust the sleep-wake cycle among the subjects in
reference to the circadian cycle, the times of retiring to bed and
wake-up were fixed in such a way that the retirement time should be
4 h before the melatonin peak, which was determined in Pre-Exp1 and
sleep length should be 8 h. And they were expressed as zeitgeber time
(ZT), where the times of wake-up, retirement to bed, and the mela-
tonin peak were defined as ZT0, ZT16, and ZT20, respectively.
The experimental protocols were illustrated in Fig. 1. One day
before the experiment (Pre-Exp2), the subjects came to the facility at
1700 for the measurement of sleep PSG. In the next morning, after
conducting the symptom-limited exercise test (11), the subjects re-
turned to their home and came back to the facility at 1700 on the same
day (day 1). The subjects participated in one of three experiments
(groups) as follows.
Subjects were instructed to keep the sleep-wake schedule consist-
ing of an 8-h sleep and a 16-h wake (Fig. 1). A phone call was given
to the subjects at 30 min before the scheduled bed time (ZT16) and
wake-up call at the scheduled wake-up time (ZT0). Three meals were
supplied at fixed times at ZT1, ZT7, and ZT13. The time of the meal
was announced by phone. They were allowed to drink water and
caffeine-free tea anytime. They took a shower regularly at ZT12.
During the waking period, the subjects were requested to take a
computer-based performance test and fill out a questionnaire (35)
every 2 h from the time of waking up to 2 h before bedtime. Each test
was finished in about 10 min. In their free time, they were allowed to
read books, listen to music, and watch videos. Smoking, napping, and
physical exercise was prohibited.
From day 3 to day 6 of the experiment, the subjects in the exercise
group performed physical exercise for 2 h with a bicycle ergometer
from ZT3 to ZT5 (morning exercise, n ⫽ 7) or from ZT10 to ZT12
(evening exercise, n ⫽ 8), respectively. Subjects without physical
exercise (control, n ⫽ 7) were instructed to rest during the waking
period.
Measurements and Data Analysis
Plasma melatonin. Serial blood sampling was performed at 1-h
intervals for 24 h through an indwelling catheter with a heparin lock
Table 1. Phases, amplitudes, durations, and AUC of plasma melatonin rhythm
Groups Onset, ZT, h Peak, ZT, h
Control (n ⫽ 7)
Day 1 14.0 ⫾ 1.1 19.7 ⫾ 1.2
Day 6 15.1 ⫾ 1.1* 20.5 ⫾ 1.2*
Morning exercise (n ⫽ 7)
Day 1 14.2 ⫾ 1.0 19.6 ⫾ 1.3
Day 6 15.4 ⫾ 1.4* 20.6 ⫾ 1.1*
Evening exercise (n ⫽ 8)
Day 1 14.7 ⫾ 1.5 19.7 ⫾ 1.2
Day 6 16.0 ⫾ 2.0* 20.8 ⫾ 1.4*
Values are expressed as the means ⫾ SD. AUC, area under the curve; ZT, zeitgeber time. *P ⬍ 0.05 vs. day 1 by one-way repeated-measures ANOVA test
with post hoc t-test.
AJP-Regul Integr Comp Physiol • doi:10.1152/ajpregu.00127.2015 • www.ajpregu.org
placed in the forearm. The blood sampling was done from 1800 in
local time on day 1 to 1800 on day 2 and 1800 on day 6 to 1800 on
day 7 (Fig. 1). Thus, the actual sampling time was slightly different
from subject to subject since subjects’ daily schedule was based on
ZT. Immediately after blood sampling, whole blood was centrifuged
to separate plasma, which was frozen at ⫺40°C until melatonin assay.
Plasma melatonin was determined by a double-antibody radioimmu-
noassay (14). The sensitivity of the assay was 1.56 pg/ml, and the
intra-assay and inter-assay variances were 6.6 and 7.0%, respectively.
The phase of plasma melatonin rhythm was determined by a
geometric method, as described previously (35). Briefly, the original
melatonin rhythm was smoothed by a three-point moving average
method. The difference between the maximum and minimum levels
was defined as the amplitude of rhythm. The onset and offset phases
of nocturnal melatonin rise were defined as the time at which the
horizontal line of 20% amplitude crossed the ascending and descend-
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ing portions, respectively. The peak melatonin phase was defined as
the midpoint between the onset and offset phases. The phase shift of
melatonin rhythm was calculated by comparing the differences in the
phases (onset, peak, offset) on day 1 and on day 6.
Core body temperature. Rectal temperature was continuously mea-
sured by a thermistor probe inserted into the rectum by 15 cm from the
anus, except when the subjects were taking a shower or defecating.
The temperature data were fed into a computer every 30 s and were
averaged at every 10-min interval. The trough phase of temperature
rhythm was determined by a geometric method, as described previ-
ously (9). The amplitude of temperature rhythm was defined as the
difference between the maximum and minimum levels. The trough
phase and amplitude of temperature rhythms were calculated on day
1 and day 6. Time-to-time difference in body temperature was
calculated between nocturnal sleep on day 2 without physical exercise
and on day 5 with physical exercise.
Sleep-wake cycle. The sleep-wake cycle was recorded by three
different methods; bed sensors (weight sensor), bed lamp, and wrist
actograph. The subjects were instructed to use the bed only for sleep,
to turn off the bed lamp when they went to bed, and to turn on the bed
lamp when awakened. Signals from these monitoring tools were
continuously recorded and fed into a computer system.
Sleep polysomnogram. PSG consisting of single-channel (C3-A2)
electroencephalogram, electrooculogram, and electromyogram was
recorded on the Pre-Ex2 day and at night on day 5. The data were
stored in an electronic computer by the data-acquisition program,
SleepSign (KisseiComtec, Nagano, Japan), with a resolution of 128
Hz. The sleep stages were visually scored in every 20-s epoch,
according to the standard criteria (26). The sleep latency was defined
as the time until the appearance of stage 1 sleep, which was followed
by stage 2. NREM sleep contains four stages (stage 1, 2, 3, and 4). The
total sleep time (TST) was defined as the sum of NREM sleep
[S1⫹S2, slow-wave sleep (SWS)] and rapid eye movement (REM)
sleep times. The sleep period time (SPT) was defined as the time from
Offset, ZT, h Amplitude, pg/ml Duration, h AUC, pg/ml
1.2 ⫾ 1.4 93.5 ⫾ 34.1 11.2 ⫾ 0.8 808 ⫾ 297
1.8 ⫾ 1.4 89.7 ⫾ 42.5 10.7 ⫾ 1.0 695 ⫾ 291
1.2 ⫾ 1.9 54.6 ⫾ 20.6 11.1 ⫾ 1.1 414 ⫾ 162
1.3 ⫾ 1.0 57.8 ⫾ 19.9 9.9 ⫾ 1.2 388 ⫾ 132
0.6 ⫾ 1.1 67.6 ⫾ 34.0 9.9 ⫾ 0.9 458 ⫾ 263
1.6 ⫾ 0.9* 59.3 ⫾ 30.7 9.6 ⫾ 1.4 397 ⫾ 220
 DAILY PHYSICAL EXERCISE AND HUMAN CIRCADIAN RHYTHMS R1115

A Control
39.0
Day 1 Day 2 Day 3 Day 4 Day 5 Day 6 Day 7
38.5
Rectal temperature (°C)

38.0

37.5

37.0

36.5

36.0

35.5
0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0
Morning exercise
39.0

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38.5
Rectal temperature (°C)

38.0

37.5

37.0

36.5

36.0

35.5
0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0
Evening exercise
39.0

38.5
Rectal temperature (°C)

38.0

37.5

37.0

36.5

36.0

35.5
0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0 6 12 18 0

Zeitgeber time (h)

B 37.4
Control
37.4
Morning exercise
37.4
Evening exercise

*
Rectal temperature (°C)
Rectal temperature (°C)
Rectal temperature (°C)

37.2 37.2 37.2

*
37.0 37.0 37.0
*
36.8 36.8 36.8

36.6 36.6 36.6

*
36.4 36.4 36.4

36.2 Day 1 36.2 Day 1 36.2 Day 1

Day 6 Day 6 Day 6
36.0 36.0 36.0
14 16 18 20 22 0 2 4 6 8 14 16 18 20 22 0 2 4 6 8 14 16 18 20 22 0 2 4 6 8
Zeitgeber time (h) Zeitgeber time (h) Zeitgeber time (h)
Fig. 3. Twenty-four-hour profiles of rectal temperature rhythms. Circadian rhythms of rectal temperature are plotted in the control (top), morning exercise
(middle), and evening exercise (bottom) groups, respectively (A). Solid horizontal bars at the bottom of each column indicate the sleep period. Values are
expressed as the mean and SD. Arrows indicate the time of taking a shower at ZT12. Open column in the middle and bottom panel indicate the time of 2-h
physical exercise in the morning (ZT 3–5) and the evening (ZT 10 –12). Values are expressed as the means and SD; control, n ⫽ 7; morning exercise, n ⫽ 7;
evening exercise, n ⫽ 8. Mean rectal temperatures were plotted in the control, morning, and evening exercise groups on day 1 (gray) and day 6 (black),
respectively (B). Asterisks with horizontal bars indicate the time when significant differences were detected between day 1 and day 6 (*P ⬍ 0.05, one-way
repeated-measures ANOVA test with post hoc t-test).

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R1116 DAILY PHYSICAL EXERCISE AND HUMAN CIRCADIAN RHYTHMS
the sleep onset to sleep end, including the time of wake after sleep
onset. The sleep efficiency was defined as the percentage of TST to
SPT (37). EEG record was missed in two subjects (a subject in the
morning and a subject in the evening exercise group) because of
technical error.
HRV during sleep. HRV (variability of R-R intervals) during the
sleep period was determined on the Pre-Ex2 and day 5. Heart rate was
recorded by a portable heart rate monitor with a resolution of 1 ms
(active tracer 300, GMS, Tokyo, Japan). HRV was analyzed with
commercially available software (CHIRAM, Suwa-Trust, Tokyo, Ja-
pan), which is based on the maximum entropy, and the nonlinear least
squares methods (31). Artifacts caused by premature contractions or
by body movements were automatically detected and replaced by
estimated values through a linear interpolation method (30). Heart rate
(HR), the power density of the high-frequency wave (HF: 0.15– 0.40
Hz), the very-low frequency wave (VLF; below 0.03 Hz), the low-
frequency wave (LF: 0.04 – 0.15 Hz), and the ratio of LF and HF
(LF/HF) were calculated every 5 min. Sleep-stage dependency of
HRVs was examined according to Ako et al. (1). Sleep stages were
determined in 5-min bins. Since SleepSign evaluates sleep stages
every 20 s, a sleep stage was defined as the stage that appeared more
than 70% in a bin (70% rule). A pair of 5-min HRVs and the 5-min
sleep stage was pooled from all subjects.
Questionnaires for exhaustion and sleepiness. Subjective sleepi-
ness and tiredness were evaluated with the Questionnaire for Subjec-
tive Symptoms in 2002 (QSS2002) (35), which was conducted every
day at 2-h intervals during the waking period.
Physical exercise. To evaluate the exercise capacity in individual
subjects, the symptom-limited exercise test (11) with bicycle ergom-
eter was done from 1000 to 1200 on the next day of the Pre-Ex2. The
mean maximum heart rate (HRmax) was 190 ⫾ 8 beats/min (n ⫽ 22;
mean ⫾ SD). Subjects were randomly assigned to the control and
exercise experiments. Subjects in the two exercise groups performed
an interval exercise for 2 h with a bicycle ergometer from day 3 to day
6 (Fig. 1, B and C). The 2-h exercise session consisted of 10 min of
warming-up, 45 min of exercise, 10 min of rest on a chair, 45 min of
exercise, and 10 min of cooling-down. During the exercise session,
HR was monitored by a heart rate monitor (Polar S610i; POLAR,
Kempele, Finland) every 1 min, and the subjects were instructed to
keep their HR at 65–75% HRmax during exercise.
Statistical Analysis
Temporal changes in the circadian phases, amplitudes, and sleep
parameters along with the experiment were evaluated by a one-way
repeated-measures ANOVA test with post hoc t-test for dependent
measures or two-way factorial ANOVA test with post hoc t-test for
independent measures. The normality and iso-variance of measures
were evaluated before testing. The significance level was set at P ⬍
0.05.
Table 2. Sleep parameters
Control (n ⫽ 7)
PreEx2 Day 5
Sleep latency, min 16 ⫾ 19 24 ⫾ 29
Stage 1 ⫹ 2, min 264 ⫾ 45 229 ⫾ 44* 270 ⫾ 26
SWS, min 105 ⫾ 39 107 ⫾ 26
REM sleep, min 82 ⫾ 29 100 ⫾ 30 125 ⫾ 24
WASO, min 11 ⫾ 10 14 ⫾ 12
TST, min 453 ⫾ 23 442 ⫾ 27 458 ⫾ 18
Sleep efficiency, % 97.7 ⫾ 2.2 97.0 ⫾ 2.6 98.8 ⫾ 0.9
Data are expressed as the means ⫾ SD. SWS, slow-wave sleep; REM, rapid eye movement; WASO, wake after sleep onset; TST, total sleep time. *P ⬍ 0.05
vs. PreEx2 by one-way repeated-measures ANOVA.
AJP-Regul Integr Comp Physiol • doi:10.1152/ajpregu.00127.2015 • www.ajpregu.org
RESULTS
Plasma Melatonin Rhythms
Figure 2 illustrates the circadian rhythms in plasma melato-
nin on day 1 (open circle) and day 6 (closed circle). The
melatonin levels in individuals were standardized by transfor-
mation of the value to percentage of the maximum level on day
1. The mean phase, amplitude, and duration of nocturnal rise
and area under the curve (AUC) of melatonin rhythm were
summarized in Table 1. In all groups, the onset and peak
phases of melatonin rise on day 6 were significantly delayed
relative to those on day 1 (control, onset, ⫺1.1 ⫾ 0.7 h, peak,
⫺0.8 ⫾ 0.4 h, means ⫾ SD, P ⬍ 0.05; morning exercise,
onset, ⫺1.2 ⫾ 1.0 h, peak, ⫺1.0 ⫾ 0.3 h, P ⬍ 0.05; and
evening exercise, onset, ⫺1.3 ⫾ 0.9 h, peak, ⫺1.0 ⫾ 0.5 h, P
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⬍0.05, one-way repeated-measures ANOVA with post hoc
t-test). In contrast, the offset phase was significantly delayed in
the evening groups (⫺1.0 ⫾ 0.8 h, P ⬍0.05) but not in the
control and morning group (Table 1). There was no significant
difference in the amplitude, duration, or AUC of melatonin
rhythm between day 1 and day 6.
Rectal Temperature Rhythms
Figure 3 illustrates the mean rectal temperature of each
group throughout the experiment (Fig. 3A) and the comparison
of the rectal temperature during nocturnal sleep between the 1st
(day without exercise) and 6th night (day with exercise). The
trough phase was not significantly changed in any group. The
nocturnal temperature decline was significantly attenuated in
the evening exercise group (P ⬍0.05, one-way repeated-mea-
sures ANOVA with post hoc t-test), but not in the control or in
the morning exercise group (Fig. 3B). The change in rectal
temperature during 8-h sleep was also evaluated from the
difference in the AUC where rectal temperatures in 10-min
bins were individually summed and averaged for each group.
The AUC in the evening exercise group was significantly
increased by 9.2 ⫾ 10.7°C/8 h when compared with that on the
1st night (P ⬍0.05, one-way repeated-measures ANOVA),
while those in the control and the morning exercise group were
not changed.
Sleep Parameters
Table 2 demonstrates the mean sleep parameters of each
group on the Pre-Ex2 and on day 5. The amount of Stage 1⫹2
sleep in the control group significantly decreased by 13.0 ⫾
Morning Exercise (n ⫽ 6) Evening Exercise (n ⫽ 8)
PreEx2 Day 5 PreEx2 Day 5
16 ⫾ 17 27 ⫾ 24 15 ⫾ 8 20 ⫾ 6
253 ⫾ 18 251 ⫾ 36 235 ⫾ 40
62 ⫾ 27 61 ⫾ 24 93 ⫾ 28 103 ⫾ 34
129 ⫾ 27 110 ⫾ 10 98 ⫾ 14*
6⫾4 8⫾8 7⫾4 21 ⫾ 34
445 ⫾ 23 458 ⫾ 10 439 ⫾ 33
98.2 ⫾ 1.7 98.6 ⫾ 0.9 95.5 ⫾ 7.4
 DAILY PHYSICAL EXERCISE AND HUMAN CIRCADIAN RHYTHMS R1117

A Control Morning exercise Evening exercise

Heart rate (beat/min)

Heart rate (beat/min)

Heart rate (beat/min)

80 80 80
Pre-Exp2 Pre-Exp2 Pre-Exp2
70 Day 5 70 Day 5 70 Day 5

60 60 60

50 50 50

40 40 40
16 18 20 22 0 16 18 20 22 0 16 18 20 22 0
15000 15000 15000

VLF (msec2 )
VLF (msec2 )
VLF (msec2 )

10000 10000 10000

5000

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5000 5000

0 0 0
16 18 20 22 0 16 18 20 22 0 16 18 20 22 0
3000 3000 3000

LF (msec2 )
LF (msec2 )
LF (msec2 )

2000 2000 2000

1000 1000 1000

0 0 0
16 18 20 22 0 16 18 20 22 0 16 18 20 22 0
3000 3000 3000

HF (msec2 )
HF (msec2 )
HF (msec2 )

2000 2000 2000

1000 1000 1000

0 0 0
16 18 20 22 0 16 18 20 22 0 16 18 20 22 0
6 6 6
LF/HF

4 4 4
LF/HF
LF/HF

2 2 2

0 0 0
16 18 20 22 0 16 18 20 22 0 16 18 20 22 0
Zeitgeber time (h) Zeitgeber time (h) Zeitgeber time (h)

B 15 6000 1000 1000 1.5

* *
4000 1.0
10
* **
500 500
ΔHR (beat/min)

ΔVLF (msec2 )

ΔHF (msec2 )

0.5
ΔLF (msec2 )

5 2000
*
ΔLF/HF

0 0 0 0 0.0

-5 -2000 -0.5
-500 -500
-10 -4000 -1.0

-15 -6000 -1000 -1000 -1.5

CTL ME EE CTL ME EE CTL ME EE CTL ME EE CTL ME EE
Fig. 4. Heart rate variability during the sleep period. Mean powers of HRVs [very low frequency (VLF), low frequency (LF), high frequency (HF), and LF/HF]
during the sleep period are plotted in the control (n ⫽ 7), the morning exercise (n ⫽ 7), and the evening exercise (n ⫽ 8) groups on the Pre-Ex2 (gray) and day
5 (black) (A). Differences of HRVs between Pre-Ex2 and day 5 were plotted in the control (CTL; white, n ⫽ 7), the morning exercise (ME; gray, n ⫽ 7) and
the evening exercise (EE; black, n ⫽ 8) groups (B). Asterisks indicate a significant difference (*P ⬍ 0.05, **P ⬍ 0.01, one-sample t-test).

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R1118 DAILY PHYSICAL EXERCISE AND HUMAN CIRCADIAN RHYTHMS

A W

Sleep stages
R
1
2
3
4

B
M

80

HR (beat/min)
80

HR (beat/min)
70 70
*** *** *** ††
60 60

50 50

40
40 W S1+2 SWS REM
Fig. 5. Relationship between polysomnogram 30000
(PSG) and HRVs during the sleep period at VLF (msec 2) 12000 *‡

VLF (msec 2)
‡
Pre-Ex. Representative PSG, heart rate (HR), 20000
8000
and HRVs during the sleep period are illus-

Downloaded from http://ajpregu.physiology.org/ by 10.220.33.5 on May 14, 2017

trated in a subject at Pre-Ex2 (A). Gray areas 10000 4000 *
indicate the episodes of REM sleep. Mean
powers of HRVs were demonstrated in wake 0 0
(W) and each sleep stage (B). Values are 4000 W S1+2 SWS REM
3000
expressed as the mean and SD (n ⫽ 21).

LF (msec 2)
LF (msec 2)

3000 *‡ *‡
Asterisks indicate a significant difference be- 2000
tween the two stages: ***P ⬍ 0.001, **P ⬍ 2000
***
0.01, *P ⬍ 0.05 vs. wake. ††Significant dif- 1000
1000
ference vs. stage 1⫹2, P ⬍0.01. ‡Significant
difference vs. SWS, one-way repeated-mea- 0 0
W S1+2 SWS REM
sures ANOVA test with post hoc t-test P ⬍ 1000
3000
HF (msec 2)

HF (msec 2)
0.001). 800
2000
** ** **
600
400
1000
200
0 0
W S1+2 SWS REM
10
6
8
LF/HF

LF/HF
6 4 ** †† ‡
*‡
4
2 ***
2
0 0
W S1+2 SWS REM
16 17 18 19 20 21 22 23 0
Zeitgeber time (h) Sleep stages

10.2% (P ⬍0.05, one-way repeated-measures ANOVA) and of
REM sleep in the evening group by 10.5 ⫾ 9.7% (P ⬍0.05) on
day 5 compared with those on the Pre-Ex2, respectively. In the
morning group, there was no significant change in the sleep
parameters examined.
HRV During Sleep
The HR during 45-min physical exercise was 145 ⫾ 4
beats/min (74 ⫾ 3% of HRmax, means ⫾ SD) on average in
the morning and 143 ⫾ 6 beats/min (76 ⫾ 5% of HRmax)
in the evening of the 4-day exercise session There was no
significant difference between them. The intensity of phys-
ical exercise in the present study was regarded as a hard
level, according to the classification of physical acti-
vity intensity by American College of Sport Medicine
(ACSM) (25).
Figure 4 illustrates the time course of mean HRV in each
group plotted in 5-min bins on the Pre-Ex2 (blue) and day 5
(red) (Fig. 4A) and the differences of HRV between the two
nights (Fig. 4B). HR increased significantly in the evening
group (P ⬍ 0.05, one sample t-test), and VLF increased
significantly in the control and morning group (P ⬍ 0.05). On
the other hand, LF and HF increased significantly in the
morning group (P ⬍ 0.01).
Figure 5 illustrates a representative HRV (HR, VLF, LF
HF, and LF/HF) during nocturnal sleep on the Pre-Ex2 (Fig.
5A) and HRV at each sleep stage. HR was significantly low
in S1⫹S2, SWS, and REMS compared with that in wake
(P ⬍ 0.001, one-way repeated-measures ANOVA test with
post hoc t-test; Fig. 5B). VLF and LF were significantly
lower in SWS (P ⬍ 0.05, P ⬍ 0.001). HF was significantly
high during sleep (P ⬍ 0.01). LF/HF was significantly high
in wake compared with those in sleep (P ⬍ 0.001). During
sleep, LF/HF was significantly lower in SWS (P ⬍ 0.001).
In this analysis, some fractions (16 –34%) of sleep stages
were not used for estimating correlations with HRV, be-
cause of the 70% rule. The validity of the estimation was
guaranteed by using in the analysis only the bins occupied
with a particular sleep stage by 100% and found essentially
the same results.
Figure 6 illustrates sleep-stage-dependent changes in
HRV. In the control, VLF significantly increased in S1⫹S2
(P ⬍ 0.05, one sample t-test), and LF/HF in REM sleep
(P ⬍ 0.01). In the morning group, VLF, LF, and HF

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 DAILY PHYSICAL EXERCISE AND HUMAN CIRCADIAN RHYTHMS R1119
15
Wake Stage1+2 SWS REM
exercise, which showed a dark-pulse type phase-response
10 curve with a phase-advance portion during the evening and a
ΔHR (beat/min)

phase-delay portion during the midnight to the morning (6, 7).

5
However, we failed to confirm these results (22), and in the
0 present study, the circadian melatonin rhythm phase delayed in
-5 a similar amount regardless of physical exercise. The discrep-
-10
ancy between the present and previous studies could be due to
the design of experiments (four trials on successive days vs.
-15
CTL ME EE CTL ME EE CTL ME EE CTL ME EE single trial), and/or to the light intensity (⬍10 lux vs. 42 lux)
during exercise. With respect to the intensity and duration of
10000
Wake Stage1+2 SWS REM exercise, there were slight differences between the two studies:
* 40 min at 75% V̇O2 max is equivalent to 85% HRmax (34) in the
ΔVLF (msec 2)

5000
* previous study, whereas 90 min at 75% HRmax is equivalent to
* 60% V̇O2 max in the present study. According to the classifica-
0
tion of physical activity intensity by ACSM (25), however, the

Downloaded from http://ajpregu.physiology.org/ by 10.220.33.5 on May 14, 2017

-5000
intensities of exercise in both studies are classified similarly as
a hard level of exercise (70 – 89% HRmax). Therefore, the
-10000
discrepancy between the two studies is unlikely due to the
CTL ME EE CTL ME EE CTL ME EE CTL ME EE intensity of physical exercise.
2000
Wake Stage1+2 SWS REM
Physical exercise in the evening produced slight but signif-
icant phase-delay shifts in the offset of nocturnal melatonin rise
** (Table 1), indicating some difference due to the time of
ΔLF (msec 2)

1000
physical exercise. It was reported that the onset and offset of
0 melatonin rise responded differentially to phase shifting stimuli
such as bright light (12, 35). The time of day effect of physical
-1000 exercise could affect the offset phase. The discrepancy be-
tween the previous studies and present one could be due to the
-2000
CTL ME EE CTL ME EE CTL ME EE CTL ME EE existence of a strict sleep-wake schedule in the present study.
2000
Strict sleep-wake schedule is reported to reset the circadian
Wake Stage1+2 SWS REM rhythms in totally blind subjects (17) and in sighted subjects
who stayed in constant dark conditions (2). The circadian
**
ΔHF (msec 2)

1000
* system entrained by a strict sleep-wake schedule could be
0
resistant to perturbing stimuli. A lack of significant phase-
shifts in the circadian temperature rhythm may support the
-1000 above interpretation.
Rectal temperature during nocturnal sleep was increased by
-2000 evening exercise. A similar result was reported previously (33).
CTL ME EE CTL ME EE CTL ME EE CTL ME EE
Nocturnal decline of core body temperature is mainly due to an
4
Wake Stage1+2 SWS REM
increase of heat loss from the skin of extremities (3). Peripheral
vasodilatation contributes to nocturnal heat loss, in which the
2 autonomic nervous system is involved (18). Physical exercise
**
ΔLF/HF

in the late evening prevents the nocturnal decline of core body

0 temperature, probably through the sympathetic nerve activa-
-2
-4
CTL ME EE CTL ME EE CTL ME EE CTL ME EE
Fig. 6. Changes in HRVs in different sleep stages. Mean differences in HRVs
between Pre-Ex2 and day 5 are illustrated in different sleep stages of the
control (CTL, white; n ⫽ 7), the morning exercise (ME, gray; n ⫽ 6), and the
evening exercise (EE, black; n ⫽ 8) groups. Values are expressed as the mean
and SD. Asterisks indicate a significant difference (*P ⬍ 0.05; **P ⬍ 0.01,
one-sample t-test).
significantly increased in S1⫹S2 sleep (P ⬍ 0.01) and HF
also in SWS (P ⬍ 0.01). In the evening group, the increase
in HR was not sleep stage-dependent.
DISCUSSION
Previous studies demonstrated phase-dependent phase shift
of plasma melatonin rhythm by a single trial of physical
tion. On the other hand, the nocturnal decline of rectal tem-
perature was not changed or even accelerated by the morning
exercise, although statistical evidence is lacking. The above
interpretation is supported by the changes of nocturnal HRVs
by physical exercise (Fig. 4). HR during nocturnal sleep was
significantly increased by the evening exercise, while it was
not changed by the morning exercise. Since HR is stimulated
by the sympathetic nerve activation, the evening exercise may
continuously stimulate the sympathetic nervous system several
hours after physical exercise. On the other hand, morning
exercise significantly increased VLF, LF, and HF during the
nocturnal sleep. HF is widely accepted as a marker of cardiac
parasympathetic activity (8), while the significance of VLF,
LF, and LF/HF is a matter of discussion in relation with the
autonomic nervous functions (8). HRV is dependent to some
extent on sleep stage (Fig. 5). However, the increases of VLF,
LF, and HF by the morning exercise were independent of the
sleep stages (Fig. 6). Since physical exercise in the morning did

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R1120 DAILY PHYSICAL EXERCISE AND HUMAN CIRCADIAN RHYTHMS
not alter the sleep quality, the changes in HRV during sleep
was not secondary to the changes in sleep stages. It is unlikely
that the morning exercise activated the parasympathetic nerve
activity per se. The activity of autonomic nervous system was
possibly altered in a long run after physical exercise in the
morning.
It is well known that bright lights in mammals, including
humans, stimulate the sympathetic activity for several hours,
even after the cessation of stimulation (24, 28). Differential
effects of bright light exposure on melatonin secretion were
reported in humans. Nocturnal bright lights suppressed the
circadian rise of melatonin level (20), while daytime bright
lights enhanced the nocturnal melatonin level (21, 35). Similar
differential effects were reported for thermal stimulation on
nocturnal decline of rectal temperature. Thermal stimulation in
the morning accelerated the nocturnal decline of core body
temperature, while the stimulation in the late evening sup-
pressed the nocturnal decline (16). These findings indicate that
sympathetic stimulation could produce an opposite effect in a
long-run depending on the time of stimulation. The present
results lead us to the hypothesis that although physical exercise
stimulates, in general, the sympathetic nervous system, the
activity of autonomic nervous system changed afterward de-
pending on the time lapse. The sympathetic activity is kept at
the high level for a few hours after stimulation (24, 28), while
the parasympathetic activity becomes predominant by the fol-
lowing nocturnal sleep. Changes in the number of receptors
after physical exercise could be involved in this alternation.
The hypothesis waits to be tested.
In conclusion, daily physical exercise of moderate strength
produced differential effects on circadian melatonin rhythm,
rectal temperature during nocturnal sleep, sleep stages, and
HRV, depending on the time of exercise. The morning exercise
increased LF and HF during nocturnal sleep, while the evening
exercise shifted the offset phase of nocturnal melatonin rise,
suppressed nocturnal decline of rectal temperature, and in-
creased HR during sleep. The morning exercise may eventually
enhance the parasympathetic activity at the following nocturnal
sleep, while the evening exercise keeps the increased sympa-
thetic activity during the following sleep.
Perspectives and Significance
The present findings suggest that morning and evening
exercises differentially affect nocturnal body temperature and
cardiac activity during sleep. These findings could answer the
question at which time of day physical exercise should be done
for better sleep. The morning exercise would improve the
quality of nocturnal sleep by increasing the parasympathetic
nerve activity, whereas high-intensity exercise in the evening
should be avoided. We do not know yet the mechanism of the
time-dependent effect of physical exercise. The specific char-
acteristics of the autonomic nervous system could be respon-
sible.
ACKNOWLEDGMENTS
We appreciate the generous supply of melatonin antibody from Prof. K.
Kawashima, Kyoritsu Pharmaceutical College.
GRANTS
The present study was supported financially in part by grants from the
Japanese Ministry of Education, Culture, Sports, Science and Technology (no.
17590197 and 23390047).
AJP-Regul Integr Comp Physiol • doi:10.1152/ajpregu.00127.2015 • www.ajpregu.org
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the authors.
AUTHOR CONTRIBUTIONS
Author contributions: Y.Y. and K.-i.H. conception and design of research;
Y.Y., S. Hashimoto, N.N.T., Y.T., S.-y.N., and K.-i.H. performed experiments;
Y.Y., S. Hashimoto, N.N.T., S. Honma, and K.-i.H. analyzed data; Y.Y., S.
Hashimoto, S. Honma, and K.-i.H. interpreted results of experiments; Y.Y., S.
Honma, and K.-i.H. prepared figures; Y.Y., S. Honma, and K.-i.H. drafted
manuscript; Y.Y., S. Honma, and K.-i.H. edited and revised manuscript; Y.Y.,
S. Hashimoto, N.N.T., Y.T., S.-y.N., S. Honma, and K.-i.H. approved final
version of manuscript.
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