Effect of the shift of the sleep-wake cycle on three robust
endocrine markers of the circadian clock
Bernard
Goichot,
Laurence
Weibel,
Florian
Chapotot,
Claude
Gronfier,
François
Piquard, and
Gabrielle
Brandenberger
Laboratoire des Régulations Physiologiques et des Rythmes
Biologiques chez l'Homme, Institut de Physiologie, 67085 Strasbourg Cedex, France
 |
ABSTRACT |
To determine the effect of a phase shift in sleep on the
circadian clock, thyroid-stimulating hormone (TSH), cortisol, and melatonin, three robust markers of the circadian clock, were analyzed using a 10-min blood sampling procedure. In an initial
experiment eight subjects were studied during two experimental
sessions: once under baseline conditions with normal nighttime sleep
from 2300 to 0700 (baseline) and once after a night of sleep
deprivation followed by daytime sleep from 0700 to 1500 (day 1). In a second experiment,
carried out on seven subjects, the 24-h hormone profiles of the first
day (day 1) were compared with those
of the second day (day 2) of the
sleep shift. During the night of sleep deprivation (day 1) the TSH surge was higher
than during baseline conditions, whereas melatonin and cortisol rhythms
remained unaffected. On day 2 the
amplitude of the nocturnal TSH surge was reduced in comparison to
day 1, whereas the amplitudes of
melatonin and cortisol rhythms were unchanged. There was a clear phase
shift in the three endocrine rhythms. Triiodothyronine levels were
slightly higher in the morning after the first night of sleep
deprivation. These results demonstrate that 2 consecutive days of sleep
shift are sufficient to affect the timing of the commonly accepted
circadian markers, suggesting the existence of a rapid resetting effect on the circadian clock. TSH reacts in a distinctive manner to the
sleep-wake cycle manipulation by modulating the amplitude of the
nocturnal surge. This amplitude modulation is probably an integral part
of the phase-shifting mechanisms controlled by the circadian clock.
thyroid-stimulating hormone; melatonin; cortisol; circadian
rhythms
 |
INTRODUCTION |
UNDER NORMAL CONDITIONS many physiological functions
display circadian rhythms. These rhythms are driven by an endogenous biological clock and synchronized on the 24-h period by environmental clues. Two kinds of stimuli synchronize endogenous rhythms in humans:
the light-dark cycle, which is the most important "zeitgeber" in
humans (13, 24), and various nonphotic stimuli, predominantly social
factors (5, 21). Several factors have been described as
accelerating synchronization. Bright-light exposure (12, 13, 24),
melatonin (4, 14), hypnotic drugs (20), and physical exercise (32, 33)
have a measurable effect on the markers of circadian clock in the 24 h
after the stimulus.
Previous studies involving one abrupt shift in the sleep-wake cycle
have shown that the time necessary for an endocrine rhythm to adapt to
a newly imposed sleep-wake cycle depends on the hormone. Sleep-dependent hormonal rhythms, such as prolactin and growth hormone,
adapt more rapidly than the circadian rhythms of melatonin and
cortisol, so that these latter rhythms are usually considered to be the
best endocrine markers of the circadian clock (10, 28). The
thyroid-stimulating hormone (TSH) rhythm has been described as reacting
in a distinctive manner to an abrupt shift in the sleep period. In the
case of sleep deprivation, the amplitude of the circadian surge
markedly increases and the maximum occurs later in the night than in
the case of normal nocturnal sleep (25), so that it is generally
assumed that sleep exerts an inhibitory effect on the circadian rhythm
of TSH.
To better understand how neuroendocrine rhythms adapt to
chronobiological challenges, we conducted an experiment involving 2 successive days of sleep shifts, with no other confounding influences. We performed a concomitant analysis of the 24-h profiles of melatonin, cortisol, and TSH. This study allows us to characterize for the first
time the effect of 2 consecutive days of a sleep-wake cycle manipulation on the circadian clock.
 |
SUBJECTS AND METHODS |
Subjects.
Fifteen healthy male subjects, aged 23-30 yr old, participated in
the experiment. All gave their informed consent, and the local ethics
committee approved the protocol. The subjects participated in the study
after medical examination and screening tests. All had regular
sleep-wake habits, and none was taking medication.
The study was conducted in two parts. In the first experiment eight
young, healthy male subjects were studied during a 24-h period from
1900 to 1900, once with sleep being permitted between 2300 and 0700 (baseline) and another time (1 mo later) with sleep being permitted
between 0700 and 1500 (first day of the shift, day
1). This experiment was preceded by an habituation
night from 2300 to 0700. The experiments were randomized.
In the second experiment seven different subjects were studied from
1900 to 1900 with sleep being permitted from 0700 to 1500. This
experiment was preceded by two different sleep periods: in one case the
subjects slept during the day before the experiment (from 0700 to 1500)
and were then studied from 1900 to 1900, i.e., during the first day of
the shift (day 1); in the other case
they slept during the day before the experiment (from 0700 to 1500) and
the subjects were then studied from 1900 to 1900, i.e., during the
second day of the shift (day
2).
The experiments were carried out in a sound-proof, air-conditioned
sleep room. The subjects remained supine throughout the investigation
and for 4 h before the beginning of the experiment. During awakening,
measured light intensity was maintained below 100 lux, and darkness was
created during the sleep periods. When awake, the subjects were allowed
to read and watch television. During the night of sleep deprivation,
they were kept under continuous surveillance and conversed with a
member of the laboratory staff.
A catheter was inserted into an antecubital vein 3 h before the
beginning of the experiment, and blood was pumped continuously in an
adjoining room and sampled into 10-min aliquots from 1900 to 1900. Blood was immediately centrifuged, and plasma was stored at
25°C until analysis. Blood was sampled at hourly intervals for free (F) thyroid hormone measurements, thyroxine
(T4) and triiodothyronine
(T3)(FT4
and FT3). A
nasogastric tube was used for continuous enteral nutrition, which began
4 h before blood sampling (Sondalis, ISO, Sopharga, Puteaux, France;
50% carbohydrate, 35% fat, 15% protein, 1 kcal/ml and 90 ml/h).
Electrodes for polysomnography were applied 2 h before the beginning of
the sleep recordings.
Hormone assays.
TSH was measured by a commercial immunoradiometric assay kit (Incstar,
Stillwater, MN). The intra-assay coefficient of variation (CV) was 6.0% for concentrations between 0.05 and 0.5 mU/l and 3.0%
for concentrations between 0.5 and 10 mU/l. The interassay CV was 8.4%
for concentrations between 0.05 and 0.5 mU/l and 4.0% for
concentrations between 0.5 and 10.0 mU/l. The detection limit was 0.013 mU/l. No sample fell below this detection limit. Cortisol was measured
by RIA (Ciba Corning Diagnostics) with a detection limit of 0.2 µg/dl. The intra-assay CV was 4.0% above 6 µg/dl and 10.0% for
levels below. The interassay CV was 5.2% for levels above 6 µg/dl
and 11.5% for levels below. FT4
and FT3 were assayed by RIA
(Magic, Ciba Corning Diagnostics). The intra-assay CV was 4.9% for
concentrations between 1.0 and 4.0 pg/ml and 2.6% for concentrations
between 4.0 and 8.0 pg/ml for FT3,
and 6% for concentrations between 1.0 and 2.0 ng/dl for
FT4. The detection limit was 0.16 pg/ml for FT3 and 0.09 ng/dl for
FT4. Plasma melatonin was measured by an RIA kit (ImmunoBiological Laboratories, Hamburg, Germany). The
detection limit was 2.5 pg/ml. The intra-assay CV was 10% below 20 pg/ml, 7% between 20 and 120 pg/ml, and 20% above 120 pg/ml. The
interassay CV was 13% below 20 pg/ml, 10% between 20 and 120 pg/ml, and 26% above 120 pg/ml. All samples from a given subject were
measured in the same assay.
Data analysis.
Each individual TSH, melatonin, and cortisol profile was submitted to a
detailed analysis, including evaluation of circadian parameters. The
wave shape of each profile was quantified by a smooth curve using a
robust locally weighted regression procedure proposed by Cleveland
(11). For each hormone the best circadian markers were used to assess
any changes in the rhythm (31).
For each of the three rhythms, the acrophase and nadir were defined as
the time of occurrence of maximum and minimum, respectively, in the
best-fit curve. The duration of the surge is the lag between the onset
and the offset, and the mean amplitude was defined as the difference
between the value at acrophase and the value at nadir.
The onset of the circadian rise of TSH was defined as the time when the
value of the best-fit curve reached the value of the daytime nadir plus
25% of the difference between the value at the acrophase and the value
at the nadir (31). The offset of the circadian rise of TSH was defined
as the time when the value of the best-fit curve reached the value of
the daytime maximum minus 25% of the difference between the value at
the acrophase and the value of the nadir.
For melatonin the onset of the rise was defined as the time when the
value of the best-fit curve exceeded the mean of the 10 lowest
consecutive melatonin values of the 24-h profile plus 2 SD in at least
10 consecutive samples. The offset of the rise was defined as the time
when the value of the best-fit curve reached the mean of the 10 lowest
consecutive melatonin values of the 24-h profile plus 2 SD in at least
10 consecutive samples (23).
For cortisol the quiescent period was defined as starting when
concentrations <50% of the 24-h mean were observed for at least six
consecutive samples and ending when concentrations >50% of the 24-h
mean were observed in six consecutive samples (15).
The fluctuations of thyroid hormone concentrations were studied using
ANOVA for repeated measures, with time and condition (nocturnal or
diurnal sleep) as dependent factors. Mean comparisons between the two
conditions were conducted using a Wilcoxon signed-rank test with a
threshold of significance at 0.05. All analyses were conducted using
BMDP software (BMDP Statistical Software, Los Angeles, CA). All values
are expressed as means ± SE.
 |
RESULTS |
First experiment: baseline vs. 1st day of shift.
Mean 24-h TSH, cortisol, and melatonin profiles during
baseline conditions and during the first sleep shift
(day 1) are shown in Fig.
1. As expected, TSH reached higher levels
during the first night of sleep deprivation compared with baseline, so
that the amplitude of the TSH rhythm differed between the two
conditions (1.01 ± 0.12 vs. 2.12 ± 0.20 mU/l,
P < 0.01). On day
1 the timing of the circadian markers of the TSH rhythm
remained unaffected by the sleep shift. Cortisol and melatonin rhythms
remained unchanged. There were in particular no differences displayed
by the two rhythms in temporal characteristics for the two conditions
(Table 1). In particular, the amplitudes of
both cortisol (18.4 ± 0.9 vs. 18.4 ± 1.4 µg/dl) and melatonin
(87.0 ± 19.4 vs. 84.4 ± 22.7 pg/ml) rhythms were similar in the
two conditions.

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Fig. 1.
Mean 24-h rhythms of thyroid-stimulating hormone (TSH), melatonin, and
cortisol in 8 subjects during baseline and during 1st day of sleep
shift.
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|
Second experiment: 1st vs. 2nd day of shift.
Mean TSH, melatonin, and cortisol profiles during the 1st and 2nd days
of the sleep shift are shown in Fig. 2. The
temporal markers of the TSH rhythm were shifted during
day 2 compared with day 1 (Table
2). The onset of the surge was delayed by 2 h 53 min ± 40 min, but the duration of the surge did not differ
between the two conditions (12 h 17 min ± 36 min vs. 13 h 20 min ± 73 min, not significant). The amplitude of the TSH surge was
markedly decreased during day 2 (1.47 ± 0.19 vs. 0.84 ± 0.11 mU/l, P < 0.05). The onset of the melatonin surge was shifted on
day 2 compared with
day 1 (2148 ± 16 min vs.
2345 ± 32 min, P < 0.05). The
cortisol rhythm was also affected by the sleep shift. The beginning of the quiescent period of cortisol secretion was delayed on
day 2 compared with
day 1 (2052 ± 23 min vs. 2222 ± 35 min, P < 0.05), as well as
the acrophase of the rhythm (0812 ± 54 min vs. 1421 ± 67 min,
P < 0.05). However, no differences
in the amplitude of the melatonin and the cortisol rhythms were
observed in the two conditions.

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Fig. 2.
Mean 24-h rhythms of TSH, melatonin, and cortisol in 7 subjects during
1st and 2nd days of sleep shift.
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|
During this second experiment, thyroid hormones were measured hourly
(Fig. 3) to determine whether the
variations of TSH rhythm amplitude could be the consequence of
variations in the negative feedback of thyroid hormones on TSH
secretion. There was no significant variation of
FT4 during the 24 h. ANOVA for
repeated measures of FT3 showed a
highly significant effect of time (P < 0.0001), with no effect of condition
(P = 0.27) and with an
interaction between time and condition at the limit of significance
(P < 0.05). This indicated that the
fluctuations of FT3 during the 24 h depended on the condition. Visual analysis of the
FT3 profiles indicated higher
levels following the first night of sleep deprivation between 0900 and
1500.

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Fig. 3.
Mean 24-h rhythms of free thyroid hormones in 7 subjects during 1st and
2nd days of sleep shift. FT3, triiodothyronine;
FT4, thyroxine.
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|
 |
DISCUSSION |
The major finding of this study is that 2 days of abrupt sleep shift
suffice to partially shift the 24-h rhythms of TSH, melatonin, and
cortisol, three robust markers of the circadian pacemaker. To our
knowledge this is the first report that argues in favor of the
hypothesis that 2 days of sleep shift have a direct resetting effect on
the circadian clock. Compared with melatonin and cortisol rhythms, the
distinctive feature of TSH is the way in which the TSH rhythm reacts to
manipulation of the sleep-wake cycle. In addition to a shift of its
temporal markers, i.e., the onset of the nocturnal surge and the
acrophase of the rhythm, adaptation of the TSH rhythm also relies on an
amplitude modulation with a return to baseline level of the nocturnal
surge during the second day of the shift. It seems unlikely that the
slight increase in FT3 observed in
the morning after the first night of sleep deprivation should exert an
enhanced negative feedback on TSH secretion the following night.
It is known that the endocrine rhythms are more or less rapidly
displaced after shifts in the sleep-wake cycle. Previous studies on jet
lag and other studies in which a single shift in the sleep period was
used have reported that sleep-dependent hormone rhythms, i.e.,
prolactin and growth hormone, adapt more rapidly than the endocrine
rhythms under circadian influence, i.e., melatonin and cortisol. In the
present study, we demonstrate that an abrupt sleep shift, in itself,
without any other confounding influences, i.e., light, posture, and
meals, can, after 2 days, directly act on the circadian clock. This
effect is independent of the relationships between sleep and hormone
secretion, because TSH is closely related to sleep as a whole and to
sleep structure (17, 18), whereas cortisol is less so and melatonin not
at all.
The regulation of the amplitude of the TSH surge in both healthy and
diseased individuals is not completely understood but seems to be of
critical importance for thyroid economy (8, 9, 19). It has been
previously reported that the time of sleep determines the maximum of
the surge and modulates its amplitude. In the case of sleep
deprivation, the TSH maximum is delayed and reaches higher levels. When
sleep deprivation lasts several days, the circadian TSH rhythm persists
but its amplitude progressively decreases (3, 25, 26). These results
have been interpreted as reflecting a decrease in vigilance and a
tendency to sleepiness resulting from prolonged sleep deprivation (3).
However, the decrease in amplitude of the TSH surge has also been
observed by Parker et al. (25) despite the absence of sleep
deprivation. It could also be suggested that the metabolic and
thermoregulatory modifications induced by a shift in the sleep period
could explain the changes in the amplitude of the TSH surge, but no
experimental evidence has been provided as yet. Also, some authors
hypothesized that the decreased nocturnal surge after a sleep shift or
a period of sleep deprivation is the consequence of enhanced negative
feedback by thyroid hormones, which increased after sleep deprivation
(30). In our opinion, it is unlikely that the small increase in
FT3 observed by us in the morning
could inhibit TSH levels the following night. In several pathological
situations, such as central or peripheral hypothyroidism (2),
chirurgical stress (7), poorly controlled diabetes (6), or the sick
euthyroid syndrome (1, 16, 27), the amplitude of the TSH rhythm has
also been shown to be decreased. The mechanisms of this decreased surge
amplitude seem to involve abnormal regulation by the
hypothalamo-pituitary axis, as well as abnormal peripheral
T4 to
T3 conversion (16). Because
T3 is decreased in these
situations, negative feedback by thyroid hormones cannot be implicated
in the decrease of the TSH surge.
It seems unlikely that the TSH surge enhanced during sleep deprivation
should act on the temporal characteristics of the melatonin and
cortisol rhythms the following day. There is currently no evidence for
an effect of thyroid hormones on the circadian clock. A direct effect
of TSH on the clock should have been observed in patients having
increased TSH levels, but this, to our knowledge, has not been
reported. However, one cannot exclude the possibility that the effect
of the shift on TSH amplitude, as well as the effect observed on the
temporal characteristics of the three endocrine rhythms, may be related
to a direct effect of the abrupt sleep shift on the circadian
pacemaker. Manipulation of the circadian system using bright light
exposure has been reported in some cases to modify the amplitude of
biological rhythms. In particular, Jewett et al. (22) reported that
bright-light exposure provokes a clear shift of the cortisol rhythm
together with a reduction of the rhythm amplitude. More recently,
Hirschfeld et al. (20) demonstrated that an 8-h advance in the sleep
period resulted in an increased amplitude of the TSH rhythm. This
enhanced amplitude was followed by a slight ascending trend in total
T3 concentrations but without
evidence of a subsequent negative feedback on TSH secretion. Treatment
with bright light or zolpidem limited this increase of TSH with no
effect on T3 levels. Comparing
these results to our own, it appears that the effect on the amplitude
of the TSH rhythm depends on the direction of the shift. On the other hand, Van Cauter et al. (29), using bright light applied at different
moments of the day during a constant routine procedure, showed an
effect of the light exposure on the temporal parameters of the TSH
rhythm but without evidence of any effect on the surge amplitude. The
inconsistencies between these studies clearly show that the exact
significance of the amplitude modulation of the TSH surge is not yet
clearly understood. The physiological meaning of this adaptation
remains unclear because the effects on thyroid hormone levels are weak.
A role of the modification of the amplitude of the TSH rhythm after
advanced or delayed shifts in the subjective signs of jet lag syndrome
has been suggested (20). It remains to be determined whether
stimulation of TSH to avoid the decrease of the surge following phase
delay would also have a symptomatic effect. This could offer new
perspectives in the exploration and the treatment of the decreased TSH
surge observed in nonthyroidal illnesses.
In conclusion, the present results suggest that the sleep-wake cycle
can be considered as a zeitgeber for the circadian clock, as indicated
by the shift of the three endocrine rhythms. TSH reacts in distinctive
manner to this shift with a modulation of the amplitude of its rhythm,
which depends on the direction of the shift. This modulation seems to
be an integral part of the phase-shifting mechanisms controlled by the
circadian clock.
 |
ACKNOWLEDGEMENTS |
We thank Michèle Simeoni and Béatrice Reinhardt for RIA
analysis and experimental assistance, Jean Ehrhart and Daniel Joly for
sleep recording, and Drs. Eve Lonsdorfer and Anne Charloux for medical
assistance.
 |
FOOTNOTES |
The experiments were performed at the Laboratoire de Physiologie et de
Psychologie Environnementales, Centre National de la Recherche
Scientifique, Strasbourg, France (directed by Alain Muzet).
Address for reprint requests: B. Goichot, Laboratoire des
Régulations Physiologique et des Rythmes Biologiques chez
l'Homme, Institut de Physiologie, 4 rue Kirschleger, 67085 Strasbourg,
Cedex, France.
Received 1 December 1997; accepted in final form 16 April 1998.
 |
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