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90:1211-1218, 2001. ;J Appl Physiol
J. Leppäluoto, I. Korhonen and J. Hassi
and norepinephrine in men exposed to cold air
Habituation of thermal sensations, skin temperatures,
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Habituation of thermal sensations, skin temperatures,
and norepinephrine in men exposed to cold air
J. LEPPA
¨
LUOTO,
1
I. KORHONEN,
2
AND J. HASSI
2
1
Department of Physiology, University of Oulu, 90014 Oulu; and
2
Oulu Regional
Institute of Occupational Health, 90220 Oulu, Finland
Received 28 February 2000; accepted in final form 2 October 2000
Leppa¨ luoto, J., I. Korhonen, and J. Hassi. Habituation
of thermal sensations, skin temperatures, and norepineph-
rine in men exposed to cold air. J Appl Physiol 90:
1211–1218, 2001.—We studied habituation processes by ex-
posing six healthy men to cold air (2 h in a 10°C room) daily
for 11 days. During the repeated cold exposures, the general
cold sensations and those of hand and foot became habitu-
ated so that they were already significantly less intense after
the first exposure and remained habituated to the end of the
experiment. The decreases in skin temperatures and in-
creases in systolic blood pressure became habituated after
four to six exposures, but their habituations occurred only at
a few time points during the 120-min cold exposure and
vanished by the end of the exposures. Serum thyroid-stimu-
lating hormone, total thyroxine and triiodothyronine, norepi-
nephrine, epinephrine, cortisol, and total proteins were mea-
sured before and after the 120-min cold exposure on days 0,
5, and 10. The increase in norepinephrine response became
reduced on days 5 and 10 and that of proteins on day 10,
suggesting that the sympathetic nervous system became
habituated and hemoconcentration became attenuated. Thus
repeated cold-air exposures lead to habituations of cold sen-
sation and norepinephrine response and to attenuation of
hemoconcentration, which provide certain benefits to those
humans who have to stay and work in cold environments.
body temperature; cold adaptation; cold sensations; epineph-
rine; hemoconcentration; norepinephrine; thyroid hormones;
thyroid-stimulating hormone
WHOLE BODY COLD-AIR EXPOSURE in laboratory conditions
has been used previously in several studies on human
cold adaptation. It has been observed that the decrease
in deep body temperature was greater after cold-air
exposures than before them (3, 16, 18), but decreases in
mean skin temperature remained unchanged (3). Cold-
induced stimulation of the metabolic rate has also been
found to be attenuated after repeated cold exposures
(3, 11, 16). Only a few studies have reported peripheral
skin temperatures or cold sensations during repeated
cold-air exposures. Nighttime toe and arch tempera-
tures were found to be higher after 14 days of daily
cold-air exposures than before (18), but no differences
were found in face, finger, or forearm temperatures
(16, 18). Subjective sensations of cold diminished after
3 days in the cold room (7), and discomfort caused by
cold-air exposure, as well as shivering, started later or
at 0.5°C lower body temperature after four to seven
cold-air exposures (2). Thus repeated cold-air expo-
sures in laboratory conditions appear to lead to adap-
tive changes such as central hypothermia, decreased
metabolic response, delayed onset of shivering, and
reduced cold sensations. These findings bear some cor-
relation to those seen in cold-exposed Australian ab-
origines or Lapps (for reviews see Refs. 19, 35).
The role of hormones regulating metabolism and
energy production in cold adaptation has been little
studied in humans. After a single cold-air exposure,
serum thyroid hormone, thyroid-stimulating hormone
(TSH), epinephrine, and cortisol levels remain un-
changed (20, 34), but serum norepinephrine levels in-
crease, and serum prolactin and growth hormone levels
decrease (20, 23, 24, 26, 34). When a 30-min cold-air
exposure was repeated 80 times during 2 mo, serum
thyroxine, TSH, and epinephrine levels remained un-
changed, but serum free triiodothyronine decreased,
and the plasma norepinephrine increase was attenu-
ated (11). In other studies, serum total triiodothyro-
nine decreased (32) and serum norepinephrine re-
sponse increased after repeated cold-water immersions
(36). The decrease in serum-free triiodothyronine oc-
curs also under natural winter conditions, e.g., on an
Antarctic base (30) or in northern Finland (21). Al-
though serum triiodothyronine levels decreased during
long-term cold exposures (11, 21, 30, 32), the produc-
tion and tissue availability of triiodothyronine have
been shown to increase (30). High-serum norepineph-
rine and triiodothyronine production in response to
cold exposures is useful, because both hormones are
known to increase metabolic rate.
The cold stimuli used in previous studies dealing
with the adaptation of physiological responses to cold
have varied considerably as to time and intensity, e.g.,
the heat losses have been 6–13 kJ/kg body wt when
cold-air exposures have been used (2, 10, 11, 18), but in
cold-water immersions they have been 21–26 kJ/kg (1,
27, 36), assuming that the skin temperature reaches
the water temperature at the end of the immersion.
The durations of the experimental cold exposures re-
Address for reprint requests and other correspondence: J. Lep-
pa¨luoto, Dept. of Physiology, Univ. of Oulu, P. O. Box 5000, 90014
Oulu, Finland (E-mail: juhani.leppaluoto@oulu.fi).
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
J Appl Physiol
90: 1211–1218, 2001.
8750-7587/01 $5.00 Copyright
©
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ported in the literature have also varied much, from 4
(2) to 80 (11) days.
Physiological processes by which an individual
adapts to his or her environment are habituation, ac-
climatization, or acclimation (35). Habituation involves
the diminution of normal responses or sensations to
repeated stimuli and may thus protect the individual
from possibly harmful effects of cold exposures, for
example. Extensive epidemiological and experimental
studies show that cold-induced increases in blood pres-
sure, norepinephrine secretion, and hemoconcentra-
tion are risk factors that are believed to explain partly
the excess mortality due to cardiovascular diseases in
winter (4, 6, 17, 25). Also, decreases in skin tempera-
tures and unpleasant cold sensations lead to poor
safety and decreased efficiency in cold work (9, 15, 28).
Previous information about the time course of the de-
velopment of these habituation processes during re-
peated cold-air exposures in humans is scanty (see
above). Therefore, we sought answers to the following
questions: Do the thermal sensations, body tempera-
tures, blood pressure, and hormonal responses become
habituated to the repeated cold-air exposures? Can the
different time courses of the habituation processes
explain the underlying mechanisms? Can the habitua-
tion to cold air under laboratory conditions be used to
improve physical performance in the cold? As a stimu-
lus, we used a daily 2-h exposure to cold air for 11 days.
This results in a heat loss of ⬃10 kJ/kg and in maximal
sensations of cold (10) but is still under the tolerance
limit (22) and can occur in natural conditions.
METHODS
Subjects. Six healthy male Caucasian volunteers gave
their informed consent for the study. Mean (⫾ SE) age,
weight, height, and body fat (as measured from the skinfolds)
were 20.5 ⫾ 0.2 yr, 66 ⫾ 3 kg, 174 ⫾ 2 cm, and 17 ⫾ 1%,
respectively. The experiments were carried out between June
and August at the Department of Physiology with outdoor
temperatures between 8 and 22°C. The subjects were famil-
iarized with the experimental procedures (cold chamber, in-
sertion of thermodes, and blood sampling) before the tests.
The experimental protocol was accepted by the Ethics Review
Board of the Medical Faculty, University of Oulu.
Experimental protocol. Our present study consisted of a
daily 2-h cold exposure repeated on 11 successive days. The
subjects were dressed in shorts during the cold exposures.
Physical training, sauna baths, tobacco, and alcohol intake
were not allowed during the study and 2 days before it. The
subjects woke up at 6 AM, had a light breakfast, and arrived
at the Department of Physiology at 8 AM. On the study days,
the following recordings were performed. Eighteen skin ther-
modes and one rectal thermode (Yellow Springs Instruments)
were put in place, and the subjects were taken to a room with
a temperature of 27–28°C (range) for 30 min. Body temper-
atures were recorded continuously by a Hewlett-Packard
data logger 9000/216. In Figs. 1–3, temperatures are shown
at time points 0, 30, 60, and 120 min. A physician recorded
blood pressure by a sphygmomanometer and recorded heart
rate every 15 min. At 25 min in 27–28°C, oxygen consump-
tion was measured by Morgan Oxylog. Afterward a venous
blood sample was taken on study days 1, 5, and 10. At 30 min,
the subjects were taken to a cold chamber (Vo¨tsch) with a
preset temperature of 10°C, air velocity ⬍0.2 m/s, and air
humidity of 2–4 g/m
3
. The actual air temperature was re
-
corded by a dry bulb globe thermometer in the cold chamber.
The mean of the measurements was 9.78 ⫾ 0.30°C at the
beginning of the cold exposure and 10.08 ⫾ 0.15°C at 120
min. The difference was 0.31 ⫾ 0.20°C and did not differ
significantly among the experimental days. The subjects sat
on netted chairs in the cold chamber for 120 min, and oxygen
consumption, blood pressure, and subjective cold sensations
were recorded every 10–30 min, starting from the time point
of 5 min before the cold-air exposure (⫺5 min). They were
asked about shivering and their cold sensations in the fol-
lowing locations, general, hand, feet, and face, according to
the following validated scale: 1 ⫽ cold, 2 ⫽ cool, 3 ⫽ slightly
cool, 4 ⫽ neutral, 5 ⫽ slightly warm, 6 ⫽ warm, and 7 ⫽ hot
(33). Tissue conductance, heat debt, and mean skin temper-
ature were calculated from the equations given (1). Another
blood sample was taken at 120 min immediately after the
subjects left the cold chamber.
Assays. Blood samples were centrifuged, and 20 lof1M
Na
2
S
2
O
2
per milliliter were added for the HPLC measure
-
ment of epinephrine and norepinephrine with interassay
coefficient of variation ⬍5% (5). Serum total triiodothyro-
nine, thyroxine, and cortisol were measured by using radio-
immunoassay kits from Farmos (Turku, Finland), and TSH
was measured by using a kit from Corning. Serum free fatty
acids (FFAs) were measured by autoanalyzer (Technicon),
and total proteins were measured by a biuret method. The
analyses were performed according to the instructions pro-
vided by the manufacturers mentioned above. Each analyte
was assayed in one assay with an interassay coefficient of
variation ⬍8%.
Statistical analysis. The arithmetic mean ⫾ SE was calcu-
lated for all data. The effects of cold exposures on the vari-
ables temperature, sensation, and hormone measures were
analyzed separately through a two-way analysis of variance
for repeated measures (BMD P2V) as day of exposure (days
0–10) and time of exposure in minutes as factors 1 and 2,
respectively. Comparisons of each exposure time against the
respective day 0 value for exposure days 1–10 were carried
out with the method using contrast of trials (deltas). A
statistically significant reduction in this test was regarded as
an indication of the presence of habituation.
RESULTS
Rectal and skin temperatures, cold sensations, meta-
bolic rates, and blood pressures. Table 1 shows the
results of the repeated-measures analysis of variance
performed on body temperature (10 locations) and
thermal sensations (4 locations) during the 11-day ex-
periment. Significant differences in time factor 1 (day)
were detected in mean skin, forearm, and chest tem-
peratures and in all of the thermal sensations, suggest-
ing that these variables have became habituated as
demonstrated below. As the cold exposure resulted in
great decreases in skin temperatures and subjective
thermal sensations (units) on every experimental day,
the differences in the variables for time factor 2
(minute) were always highly significant. There was a
significant interaction of forearm and thigh tempera-
tures, indicating that the decreases in the tempera-
tures were delayed on days 5–8.
The mean preexposure rectal temperature on day 0
was 37.1 ⫾ 0.11 (SE) °C and decreased on average by
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0.5°C during the 120-min cold exposure (Fig. 1). The
decrease was significant between time points 0 and 120
min on day 0 (significance not shown). During the next
10 daily exposures to cold air, the decreases in the
rectal temperatures were similar, and hence no habit-
uation process in deep body temperature was observed.
The mean skin temperature decreased during the 120
min from 33.1 ⫾ 0.16 to 23.4 ⫾ 0.19°C on day 0 (Fig. 1),
with the decrease from the preexposure levels being
significant already after 10 min (significance not
shown). When the cold-air exposure was repeated, the
mean skin temperature at time points 0, 30, 60, and
120 min became significantly warmer, i.e., ⬃0.8°C on
day 5 compared with day 0. Forearm skin temperature
at time points 60 and 120 min became similarly
warmer, i.e., 1.5–2.0°C on days 5–8 compared with day
0. The reduced responses of mean skin and forearm
temperature to daily cold exposures stand for the ha-
bituation processes that, in these cases, were very
transient. The skin temperature of the chest (Fig. 1)
decreased rapidly on every day, and no significant
changes, i.e., habituation, between day 0 and the other
days were seen.
Thermal sensations were estimated according to a
subjective scale in which 4 ⫽ neutral, 3 ⫽ slightly cool,
2 ⫽ cool, and 1 ⫽ cold. On day 0, the hand thermal
sensations decreased significantly from 4.20 ⫾ 0.21 to
1.38 ⫾ 0.24 (units) during the 120-min cold exposure.
The decrease was significantly reduced at 115 min on
days 1 and 4–10;at35minondays 2–4 and 8–9; and
at 65 min on days 5 and 7–9 (Fig. 2). Thermal sensa-
tion of the foot fell on day 0 to a minimum (1), and the
decrease was significantly reduced at 35 min on days 1,
2, 4, and 8–10; and at 65 min on days 3–5 and 7–10
(Fig. 2). Thermal sensation of the face decreased less
on day 0 than that of hand or foot, from 4.18 ⫾ 0.19 to
2.79 ⫾ 0.29 (P ⬍ 0.01). The decrease was significantly
reduced at 35 min on days 2 and 4–10; and at 65 min
on days 5 and 8–10. The thermal habituation of the
face appeared to be almost complete at the end of the
11-day experiment (Fig. 2). The general thermal sen-
sation was 4.17 ⫾ 0.17 on day 0 before the cold-air
exposure and reached the minimum in all of the sub-
jects in 115 min of the exposure (Fig. 2). During the
next days, the general thermal sensations became sig-
nificantly less intensive at 35 min on days 1–3, 5–6,
and 8;at65minondays 3–5, 7, and 9–10; and at 115
min on days 4–10. Thus there was a clearly perceptible
habituation in the thermal sensations beginning al-
ready after the first cold-air exposure and lasting in
most cases to the end of the 11-day experiment.
The subjects were asked about shivering every 5 min
during the cold exposure. Subjective shivering started
at 15 min on day 0, and the time it started did not
change during the experiments (data not shown).
Metabolic rate increased significantly at the 30–120
min time points from the preexposure levels (Fig. 3).
During the 11-day experiment, the increases in meta-
bolic rate were similar, and no habituation was seen.
Decreases in heat debt were also similar during the
experiments.
Systolic blood pressure readings were 122 ⫾ 3
mmHgat0minonday 0 and increased significantly
after 5 min in response to cold exposure, reaching the
maximum of 137 ⫾ 4 mmHg at 60 min (Fig. 3). The
increase was significantly reduced only at 60 min on
days 4 and 6, indicating that systolic blood pressure
also became very transiently habituated. On day 0, the
diastolic blood pressure (Fig. 3) increased significantly
at the end of the cold exposure, and no habituation was
seen during the 11-day experiment.
We had heart rate recordings available only on
days 0, 1, 5, and 10 at time points 0, 30, 60, and 120
min. On day 0, the heart rate was 78 ⫾ 6 beats/min
before the cold-air exposure and decreased to 64 ⫾ 4
beats/min at 120 min (P ⬍ 0.01), and these decreases
in heart rates were similar during days 1, 5, and 10
(data not shown).
Serum hormones, proteins, and other constituents.
Serum hormones were measured before the cold expo-
sure and after the 120-min cold exposure on study days
0, 5, and 10 (Table 2). No significant changes in the
levels of serum total triiodothyronine, thyroxine, TSH,
cortisol, and epinephrine in response to the 120-min
cold exposure were observed. On the other hand, serum
norepinephrine increased significantly from 473 ⫾ 73
to 1,329 ⫾ 154 pg/ml on day 0, but the increase was
significantly reduced on days 5 and 10. Serum FFAs
increased significantly in response to cold-air exposure
on days 0 (P ⬍ 0.01), 5, and 10 (P ⬍ 0.05 for both days),
and the increase on day 10 was significantly smaller
than that on day 0. Serum total proteins tended to
increase in response to cold-air exposure on days 0 and
5, but on day 10 there was no increase (P ⬍ 0.05). Thus
Table 1. Differences of time factors in various body
temperatures and thermal sensations
Variable
Time Factor
Day
Time Factor
Minute Interactions
df F df F df F
Body temperatures
Rectal 10,50 0.6 4,20 22‡ 40/200 0.7
Mean skin 10,50 3.5‡ 4,20 1,036§ 40/200 1.3
Forearm 10,50 2.8† 4,20 96§ 40/200 1.6*
Thigh 10,50 0.4 4,20 601§ 40/200 2.0†
Chest 10,50 2.1* 4,20 377§ 40/200 0.6
Abdomen 10,50 0.9 4,20 125§ 40/200 0.4
Calf 10,50 2.0 4,20 177§ 40/200 0.7
Cheek 10,50 1.5 4,20 870§ 40/200 1.0
Instep 10,50 1.8 4,20 742§ 40/200 1.0
Forefinger 10,50 1.4 4,20 917§ 40/200 1.0
Thermal sensations
Hand 10,50 6.3§ 4,20 58§ 40/200 1.3
Foot 10,50 3.7‡ 4,20 194§ 40/200 1.0
Face 10,50 3.2† 4,20 13‡ 40/200 1.1
General 10,50 4.5§ 4,20 125§ 40/200 1.4
Data were analyzed by repeated-measures two-way analysis of
variance. Time factor day, differences between days 0 and 10 at each
exposure time point; time factor minute, differences between expo-
sure lengths from 0 (or ⫺5) to 120 (or 115) min; df, degrees of
freedom. Significant difference: *P ⬍ 0.05, †P ⬍ 0.01, ‡P ⬍ 0.001,
and §P ⬍ 0.0001.
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serum norepinephrine, FFA, and total proteins became
habituated to repeated cold-air stimuli: norepineph-
rine and FFA on days 5 and 10 and serum proteins on
day 10.
DISCUSSION
To understand better the interplay between physio-
logical mechanisms in cold adaptation, we exposed six
lightly clad male subjects to cold air for 120 min daily
for 11 successive days and recorded the responses in
body temperatures, thermal sensations, blood pres-
sure, and metabolic rate every day and those of cat-
echolamines, thyroid hormones, TSH, and serum pro-
teins on days 0, 5, and 10. The responses to the first
cold exposure were in line with several previous stud-
ies in which healthy subjects had been exposed to cold
air (12, 20, 29).
When the cold-air exposures were repeated daily,
thermal sensations became habituated first. Hand,
foot, and general thermal sensations already became
warmer after the first exposure at some time points (35
and 115 min) and that of the face after the second
exposure. This early habituation in thermal sensations
lasted throughout the 11-day cold exposure period and
was almost complete with regard to face thermal sen-
sations. In another experimental setting in which air
temperature was decreased by 0.35 or 0.5°C/min for
40–60 min, it was observed that thermal sensations
moved from very cold to cold or thermal discomfort was
alleviated after the third daily exposure (2). Our expo-
sure time was longer (120 min), and hence it is possible
that we already observed significant changes after the
first exposure. Increased skin temperatures after long-
term or repeated cold exposures evidently reflect
greater heat transfer from core to shell, because the
cutaneous vasoconstrictor response to cold had become
less pronounced because of habituation.
We observed great changes in the forearm skin tem-
perature, which was 1.5–2.0°C warmer at the time
points 60 and 120 min on days 5–8 than on day 0. Mean
skin temperature sporadically increased on day 5 at
time points 30–120 min. In earlier studies, long-term
cold-air exposures resulted in increased skin tempera-
tures in toe, arch, and calf, but no changes were seen in
chest, hand, forearm, or finger (16, 18). Different ex-
perimental settings explain the differences in the re-
sults.
Adaptive changes in cold sensations and skin tem-
peratures have been regarded as forms of habituation
that belong to the nondeclarative type of memory (14).
Fig. 1. Rectal temperatures (top left), mean skin temperatures (top right), forearm skin temperatures (bottom left),
and chest skin temperature (bottom right) as functions of the duration of the exposures (0–120 min) and the
number of repeats (0–10 days). Means ⫾ SE (only for 0- and 120-min values) are given. *P ⬍ 0.05 from the
respective day 0 value.
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After the first cold stimulus, the successive ones evi-
dently lead to synaptic depression in neural connec-
tions between hippocampal and cortical areas, which
could be reflected in reduced cold sensations and skin
temperatures in a manner that we observed in this
study. It has been shown that different responses, e.g.,
cold-induced pain and an increase in blood pressure,
became habituated at different rates (8). In the present
study, we also observed that cold sensations became
habituated first and lasted the longest. The unpleasant
nature of the cold sensation and its relation to limbic
functions may explain its strong habituation.
We encountered in the present study an unexpected
time course of cold habituation. The significantly in-
creased responses to cold air in mean skin tempera-
tures vanished after day 5 and those in the forearm
after day 8. It should be noted that the significant
changes in thermal sensations lasted to the end of the
exposure period. Why the habituation in skin temper-
atures, but not in cold sensations, vanished after days
5–8 is not known, but it may be related to the low
intensity of the cold-air stimulus used. This is a useful
piece of information for when experiments utilizing
long-term cold-air exposures are planned.
We did not find any significant changes in the re-
sponses of the rectal temperature among the exposure
days. This is in agreement with a previous study in
which subjects were exposed to 30-min cold exposure
80 times and no significant changes in rectal temper-
ature were seen (11). On the other hand, significant
decreases in the responses of rectal temperature to cold
have been observed, but the exposure times have been
longer: 7.5 h (16) or 24 h (18) vs.2hinourstudy. In the
present study, the metabolic rate increased by ⬃40%
after the cold-air exposure on the first day (day 0), and
the increase was similar throughout the whole exper-
iment. In some previous studies, repeated cold-air ex-
posures have led to decreased metabolic responses af-
ter acclimation (3, 11, 16), but the durations of cold
acclimation in those studies were longer.
Adrenal medullary and thyroid hormones and brown
adipose tissue are crucial in maintaining body temper-
ature in experimental animals, but their role in hu-
mans is less well known. A single, whole body cold-air
exposure leads to increased plasma norepinephrine
levels, but epinephrine levels remain unchanged (11,
20, 29, 34), suggesting an activation of the sympathetic
nervous system. We observed in this study that, when
the cold exposure was repeated, the significantly in-
creased norepinephrine response on day 0 disappeared
on days 5 and 10. In earlier studies, habituation of
norepinephrine secretion has been found to occur after
Fig. 2. Hand thermal sensations (top left), foot thermal sensations (top right), face thermal sensations (bottom left),
and general thermal sensations (bottom right) as functions of the duration of the exposures (⫺5–115 min) and the
number of repeats (0–10 days). Means ⫾ SE (only for ⫺5- and 115-min values) are given. *P ⬍ 0.05 from the
respective day 0 value.
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an 8-day stay in a cold room with a temperature of
15.6°C (23) or after 80 cold-air exposures (11). In a
study in which cold-water immersions were used, the
serum norepinephrine response to the cold-air test did
not become habituated but rather increased signifi-
cantly after the acclimation (36). The heat loss in the
latter study was 26 kJ/kg and only 10 kJ/kg in our
present study, explaining the difference in the norepi-
nephrine responses. We emphasize that the observed
habituation of the norepinephrine secretion could also
explain the thermoregulatory changes. The decreases
in circulating norepinephrine levels, as well as in the
activity of sympathetic innervation to vasoconstrictor
arteries, lead to vasodilatation or inhibition of vasocon-
striction. This evidently leads to changes in the periph-
ery, such as increased skin temperature, as seen in this
study. The serum FFA response was also attenuated,
so that the response became less significant. This find-
ing supports the well-known association between nor-
epinephrine and serum fatty acids.
The increase in the number of blood cells and in the
concentration of serum proteins after the cold exposure
is well documented (4, 17). The increase is due to
hemoconcentration caused by cold-induced peripheral
vasoconstriction that leads to extravasation of plasma
water (4, 17). We observed hemoconcentration on days
0 and 5 from the increases in serum proteins, but not
on day 10. It is possible that the serum proteins no
longer become concentrated in response to repeated
cold-air stimuli, because vasoconstrictions had become
reduced. Whether other mechanisms are involved is
not known at the moment.
Thyroid hormones are also necessary in the adapta-
tion to cold. We measured serum levels of total triiodo-
thyronine, thyroxine, and TSH at the beginning of our
cold exposures and during days 5 and 10. There were
no changes in total thyroid hormone and TSH levels in
response to cold in our present study, in agreement
with a recent study in which 80 cold-air exposures were
executed (11). Thus there is no firm evidence that a
cold-air stimulus would trigger a neuroendocrine reflex
by stimulating the release of TSH in humans, either in
acute or subacute experiments. Instead, another mech-
anism appears to exist by which cold exposures would
lead to altered thyroid hormone levels. As discussed
above, the concentrations of total thyroid hormones
remained stable during repeated cold-air exposures,
but free triiodothyronine decreased (11, 31). It was
recently shown that an intense cold acclimation, i.e.,
immersion of lower limbs in icy water for up to 1 h
twice a day for 1 mo, decreased serum total triiodothy-
ronine in the cold-air test performed after the acclima-
Fig. 3. Metabolic rate (top left), heat debt (top right), systolic blood pressure (bottom left), and diastolic blood
pressure (bottom left) as functions of the duration of the exposures (0–120 min) and the number of the repeats
(0–10 days). Means ⫾ SE (only for 0- and 120-min values) are given. *P ⬍ 0.05 from the respective day 0 value.
1216 HUMAN HABITUATION TO COLD AIR
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tion (32). Thus cold-air exposures in laboratory condi-
tions have to be long (31) or intense (32) enough to lead
to decreased levels of thyroid hormones.
According to our previous study, serum cortisol does
not respond to a single cold exposure (20). In our
present study, serum cortisol levels did not change
either during the repeated cold exposures. Increases in
serum cortisol levels usually mean the presence of
stress factors in the experimental setup. Although our
cold exposures were experienced as very cold, they did
not activate glucocorticoid secretion.
It is generally accepted that a single, short-time
exposure to cold air results in increased systolic and
diastolic blood pressure and, by a reflex mechanism, in
a decreased heart rate (12, 20, 29). Similar findings
were made in the present study. The systolic blood
pressure increased significantly during the first 5 min
in the cold, whereas the diastolic blood pressure rose at
the end of the 120-min cold exposure. Some earlier
studies have demonstrated a gradual decrease in blood
pressure and heart rate responses to repeated experi-
mental cold stimuli (7, 11). We observed a significant
reduction in the systolic blood pressure on days 4 and
6 only at time point 60 min but no significant changes
in the diastolic blood pressure at any time point. We
had heart rate recordings available from days 0, 1, 5,
and 10 and observed that they were similarly de-
creased on days 0, 1, 5, and 10. The general picture of
the systolic blood pressure responses to repeated cold-
air exposures follows those seen in other parameters,
i.e., habituation within 4–6 days and loss of habitua-
tion after that. It can be stated that cardiovascular
responses to repeated cold exposures are advantageous
because the decreases in systolic blood pressure (days 4
and 6) and heart rate (days 0, 1, 5, and 10) indicate a
reduced oxygen demand of the heart.
We demonstrated here that the thermal sensations
became habituated after the first or second cold-air
exposure, but the other responses became variably
habituated as late as after four daily exposures, and
hemoconcentration was not affected until the end of
the 11-day experiment. Thus the moderate cold-air
exposure we used in this study was not a sufficient
stimulus to achieve a general habituation to cold. The
unpleasant sensations of cold are mediated by limbic
structures that may explain their immediate and per-
sistent habituation. The development of habituation in
skin temperatures (forearm and mean skin), systolic
blood pressure, and norepinephrine responses after
four to five daily exposures relates to a common pro-
cess, probably to the reduction in the activity of the
sympathetic nervous system.
Habituations of cold sensation, norepinephrine re-
sponse, hemoconcentration, and, in lesser amounts,
skin temperature and systolic blood pressure provide
certain benefits to those humans who have to stay and
work in cold environments.
We thank the Scientific Committee of National Defence for the
support rendered to this project.
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