Vol. 88, Issue 5, 1853-1858, May 2000
Light-dark differences in the effects of ambient temperature
on gaseous metabolism in newborn rats
Erin L.
Seifert and
Jacopo P.
Mortola
Department of Physiology, McGill University, Montreal, Quebec,
Canada H3G 1Y6
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ABSTRACT |
Body
temperature (Tb) of rat pups (7-9 days old) raised
under a 12:12-h light-dark (L-D) regimen (L: 0700-1900, D:
1900-0700) was consistently higher in D than in L by ~1.1°C.
We tested the hypothesis that the L-D differences in Tb
were accompanied by differences in the set point of thermoregulation.
Measurements were performed on rat pups at 7-9 days after birth.
O2 consumption (
O2) and CO2
production (CO2) were
measured with an open-flow method during air breathing, as ambient
temperature (Ta) was decreased from 40 to 15°C at the
constant rate of 0.5°C/min. At Ta 
33°C, O2 was not significantly
different between L and D, whereas CO2 was higher in L,
suggesting a greater ventilation. Over the 33 to 15°C range the
O2 values in D exceeded
those in L by ~30%. Specifically, the difference was contributed by
differences in thermogenesis at Ta = 30 to 20°C. As
Ta was decreased, the critical temperature at which
O2 began to rise
was lower in L. We conclude that the higher Tb of rat pups
in D is accompanied by a higher set point for thermoregulation and a
greater thermogenesis. These results are consistent with the idea that,
in newborns, endogenous changes in the set point of thermoregulation
contribute to the circadian oscillations of Tb.
body temperature; circadian rhythms; neonatal thermoregulation; oxygen consumption
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INTRODUCTION |
A CIRCADIAN RHYTHM IN BODY temperature (Tb)
is present in the adult of numerous species, including rats (18). Rats
are nocturnal animals, and their higher values of Tb and
O2 consumption
(O2) occur during the dark
phase of the circadian cycle. Newborn rats as well show a daily
Tb oscillation (14-17, 20-22). Observations of
Tb oscillations in rat pups separated from the mother and
artificially reared indicated the existence of an endogenous neonatal
Tb rhythm (14, 16, 17).
In adults, the possibility that Tb changes may be related
to daily oscillations in the set point of thermoregulation, defined as
an adjustable reference value of Tb, which the organism
tends to protect by a process of regulation (1), has been often
considered, but the results are mixed (18). Newborn rats are capable of increasing heat production when ambient temperature (Ta)
falls below thermoneutrality, which at this age is
~33-34°C (8, 10, 19, 24), but whether the daily
variations in Tb of rat pups reflect changes in the
thermogenic response is not clear. Spiers (22) reported that
Tb measured after 1 h of exposure to Ta of
35, 32.5, 30, and 25°C was higher in the night and was accompanied by a higher O2 at all
Ta at days 2 and 7. Daily differences in
O2 were observed in rat pups
between 5 and 8 days of age artificially reared at Ta = 33°C (14). On the other hand, other measurements suggested that the
daily changes in Tb would be apparent only in pups
maintained below thermoneutrality (16). Hence, it is not clear whether
the oscillations in Tb and
O2 reflect circadian
differences in the thermogenic response to Ta, in which case they would occur only below thermoneutrality, or differences in
the metabolic condition, in which case they may occur also at and above
thermoneutrality. The activity of the brown adipose tissue (BAT), which
is the primary thermogenic mechanism in neonatal animals, is decreased
during the minimum phase of the Tb cycle, presumably
because of a reduction of its sympathetic activation (16, 17). This
latter information has been interpreted as indicating a depression of
thermogenesis during the phase of low Tb. Whether circadian
changes in Tb may be accompanied by a shift in the set
point of thermoregulation toward a lower Ta cannot be
concluded from the studies available, since the measurements were
performed at one or only a few values of Ta.
In this study we tested the hypothesis that the endogenous
Tb circadian rhythm of rat pups was contributed by changes
in the set point of thermoregulation. To this end, we constructed the whole metabolism-Ta relationship, covering the ranges of
heat dissipation (>33°C), thermoneutrality (~33-34°C),
and heat production (<33°C) (10), during the light (L) and dark
(D) phases of the daily cycle.
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METHODS |
Experiments were conducted on Sprague-Dawley rat pups, aged 7, 8, and 9 days (day 0 = day of birth), from five litters after approval
from the Animal Ethics Committee of this institution. Adult pregnant
females were housed in individual cages at 20-25°C, relative
humidity 50-53%, and 12:12-h L-D cycle (lights on
0700-1900). Food and water were available ad libitum. After birth,
pups remained with the dam under these same conditions. All experiments
were conducted in the L phase. Hence, during the experimental days, the
L-D cycle was 15:9 h (lights on 0700-2200). Body weight of the 3 experimental days in the morning and evening averaged 15.1 ± 0.5 and 16.0 ± 0.5 (SE) g, respectively.
The general protocol consisted of measurements of
O2 and CO2
production (CO2) at various
Ta within the time interval 0730-0930 (L phase) and
1930-2130 (D phase). Each experiment lasted 1 h.
Measurements.
O2 and
CO2
(ml · min
1 · kg1
STPD) were measured by an open-flow system (4). The pups,
in sets of two, were placed in a respirometer, which consisted of a
cylindrically shaped transparent plastic 75-ml container (10). The pups
were maintained isolated from each other by a separator to avoid the
effect of Ta on huddling and metabolic rate (11, 19).
Airflow through the respirometer was controlled by a flowmeter set at
325 ml/min. Inflowing and outflowing gases were passed through a drying
column (Drierite, Hammond Drierite, Xenia, OH), then sampled by a
calibrated infrared CO2 analyzer (model CD-3A, Applied
Electrochemistry, Pittsburgh, PA) and a polarographic O2
analyzer (model OM-11, Beckman Instrument, Anaheim, CA). Gas
concentrations were displayed on a computer monitor during on-line
acquisition. O2 and
CO2 were calculated as the
product of the flow rate and the inflow-outflow gas concentration difference, averaged over several minutes.
Ta was monitored by two tungsten-constantan thermocouples
(model DP30, Omega, Stamford, CT) placed at the opposite ends of the
respirometer. The
Ta-O2
relationship was constructed according to a previously used protocol
(10, 13). Pups were placed in the respirometer preheated to 35°C by
adjusting a 13-cm-diameter heating lamp. Because the heating source was
large relative to the size of the respirometer, regional Ta
differences were minimal. During the following 10 min, Ta
was gradually increased to 40°C, at which point measurements
started. Ta was reduced from 40 to 15°C by adjusting
the distance of the heating lamp and by placing cold pads on the outer
surface of the respirometer. The rate of Ta change was
0.5°C/min (Fig. 1) and was identical in
all experiments.
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Fig. 1.
Experimental protocol. Ambient temperature (Ta) was
decreased at a rate of 0.5°C/min. Values are means of 18 runs in
light ( ) and dark ( ). Error bars, SE; when not shown, SE was
within size of symbol.
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Colonic temperature was measured during the L and D phases in all pups
of each litter by a fine tungsten-constantan thermocouple (model DP30,
Omega) and was taken as representative of Tb. These data
were collected immediately after the pup was removed from the cage.
Because before the metabolic measurement the pups were left in the
chamber at 35-40°C for 10 min, on a separate group of 7- and
9-day-old pups (n = 18) we measured the effect of this period
on their Tb in the L and D phases.
Number of animals and statistical analysis.
Values are means ± SE. For graphical purposes, the
Ta-metabolism curves are also presented with the 95%
confidence intervals. From a total of five litters, the
Ta-O2
relationship was obtained in 18 sets of pups in L and 18 sets in D,
equally distributed among postnatal days 7, 8, and 9.
Of these, 13 L and D sets were the same animals studied in the L and D
phases of the same day (9 sets) or in the D and then the L phase of the
next day (4 sets). All the remaining D and L sets consisted of animals
studied only once, in the L or D session. These procedures were
adopted to avoid a possible biasing of the results by subtle
differences related to age or habituation to the experimental
condition. For analytic purposes (see below) the D sets were numbered
consecutively (1D, 2D, 3D, ... ,18D) and matched to the L sets
(1L, 2L, 3L, ... ,18L).
Two analytic approaches were adopted. First, the individual data points
of the average Ta-metabolism curve of the 18 D sets were
compared with the corresponding points of the L average curve by
two-tailed paired Student's t-test. The metabolic values at six selected Ta (15, 20, 25, 30, 35, and 40°C) were
then compared by ANOVA and subsequently by post hoc contrasts with six
Bonferroni limitations.
The second approach compared the Ta-metabolism curves over
the range of activation of thermogenesis (Ta = 33-15°C) and the range of thermoneutrality and heat
dissipation (Ta = 33-40°C) (10, 13). The curve of
each set was plotted with fixed axis scales and magnification, and its
area, representing the total O2 used or CO2
produced over that Ta range, was measured with a graphics
tablet connected to a minicomputer. Repeated analysis of the same curve
yielded values that differed by <2%. This approach circumvented the
complexity of analyzing irregularly shaped curves. Areas were then
statistically compared by two-tailed unpaired (whole D group vs. whole
L group) or paired (each D set vs. corresponding L set) Student's
t-test.
Finally, to derive the lower critical Ta (i.e., the
Ta below which
O2 increases in response to
cold), linear regression was performed for each set over the
Ta range 22-29°C, which corresponded to the
approximately linear range of thermogenesis in L and D (see
RESULTS). Linear fitting over this range was statistically significant for 16 and 13 sets in L and D, respectively. The slope of
the lines provided the thermogenic sensitivity (change in
O2 per unitary decrease in
Ta), and the intercept at the minimal O2 gave the lower critical
Ta.
Over the 3 days of the experiments, a significant difference in
Tb between any given session and the immediately preceding one was evaluated by ANOVA followed by post hoc contrasts with five
Bonferroni limitations. Comparisons between two groups of data (e.g.,
whole set L vs. D Tb values, lower critical Ta,
thermogenic sensitivity) were done by two-tailed Student's
t-test, unpaired or paired as required. In all cases, significant
differences were defined at P < 0.05.
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RESULTS |
Tb values.
At all days, the values of Tb in D exceeded those in L
(Fig. 2A). By averaging the 3 experimental days, the L and D values were 34.4 ± 0.09 and 35.5 ± 0.05°C, respectively (Fig. 2B).
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Fig. 2.
A: body temperature (Tb) in light () and dark
() in rat pups at days 7, 8, and 9. Values are
means; error bars show SE. Height of box surrounding symbol indicates
95% confidence intervals. Number of animals is shown in
parentheses.* P < 0.001 from immediately preceding value.
Solid horizontal bars, 12:12-h light-dark regimen during gestation and
first 6 postnatal days; gray horizontal bars, extended light period
during days 7-9, when dark measurements were made.
B: Tb in light and dark for all rat pups on 3 experimental days. Values are means ± SE. ** P < 0.001.
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The 10 min at 35-40°C before the onset of the metabolic
measurements greatly reduced, but did not abolish, this difference; hence, at the onset of the measurements, Tb in L and D
averaged 37.3 ± 0.1 and 37.7 ± 0.1°C, respectively (P < 0.001).
Gaseous metabolism.
Graphical representation of the group-average
Ta-O2 and
Ta-CO2
relationships indicated that the D curve was displaced upward compared
with the L curve in the thermogenic region (Fig. 3). The significance of this displacement
was confirmed, first, by statistical comparison at the corresponding
Ta values for the whole range. Then, post hoc analysis
after ANOVA for the six selected values of Ta (see
METHODS) indicated a significant difference at 25 and
20°C for O2 and at
25°C for CO2. Hence, the
differences between the D and L curves were within the thermogenic
region, i.e., in the Ta range between the lower critical
Ta and those Ta values (15-18°C) where
the Q10 effect predominates.
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Fig. 3.
O2 consumption
(O2, A) and
CO2 production
(CO2, B) as functions
of Ta in rat pups in light () and dark (). Error
bars, SE. Solid and dotted lines demarcate 95% confidence intervals.
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Because of these differences, the D-to-L ratios of the values of
gaseous metabolism (Fig. 4) were
consistently above unity between 20 and 30°C. Over this
Ta range,
O2 and
CO2 in D averaged 32 ± 4 and 27 ± 4%, respectively, more than in L.
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Fig. 4.
Ratio of dark to light O2
(A) and CO2
(B) in rat pups. Error bars, SE. Continuous lines demarcate
95% confidence intervals. A ratio of 1 (dashed line) indicates no
difference between light and dark values.
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The above results were further confirmed by separate analysis of the
Ta-O2 areas. Over
the 15-33°C range the D values were significantly increased,
whether by unpaired (i.e., the whole group) or paired analysis (i.e.,
each D set matched to the corresponding L set), whereas no differences
were present over the 33-40°C range. The analysis for the
Ta-CO2 areas gave
similar results over the 15-33°C range, i.e., higher values in
D. On the other hand, over the 33-40°C range, the D values of
CO2 were slightly, yet significantly, lower than in L; hence, at high Ta, the
CO2-to-O2 ratio was higher in L (0.86 ± 0.03) than in D (0.78 ± 0.03, P < 0.001).
The change in O2 per unitary
change in Ta over the 22-29°C range in
Ta did not differ between L and D (4.0 ± 0.4 and 4.2 ± 0.5 ml · kg1 · min1 · °C1,
respectively). The lower critical Ta, on the other hand,
was significantly different between L and D: 29.2 ± 1.0 and 32.9 ± 1.5°C, respectively (Fig. 5).
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Fig. 5.
Semischematic representation of "lower critical Ta"
(LCT) in light ( ) and dark (). Light () and dark ( )
Ta-O2 values are
shown over 22-29°C range. Values are slightly different from
those of Fig. 3A, because only those sets that had a
significant linear fitting have been included, i.e., 16L and 13D (see
text). Extrapolation of linear regression to minimal
O2 (which averaged 30 ml · kg1 · min1,
thin horizontal line) gave LCT. Values are means ± SE.
* Significant difference between LCT values.
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DISCUSSION |
Tb.
Many studies have reported daily differences in Tb of
neonatal rat pups (14-17, 20-22). The findings of daily
Tb cycles during artificial rearing without the dam and of
low Tb values during the L phase of the cycle irrespective
of clock time indicated the endogenous origin of the circadian rhythm
(14-17) without necessarily denying the importance of maternal
influences on the neonatal Tb pattern (14, 15). In the 7- to 9-day-old pups of the present study, Tb was lower in L
than in D, on average by 1.1°C. The daily averages showed a
tendency for this difference to be less marked at day 9 than at
day 7. This is in keeping with observations that the
Tb oscillations gradually decrease their amplitude in rat pups until ~3 wk, to resume it again at a later age (6, 15, 22), an
intriguing phenomenon for which there is no clear explanation (18).
Ta-metabolism relationship.
The most obvious differences between the L-D
Ta-O2 curves
(Fig. 3A) were the lower
O2 values over the 30 to
20°C range and the lower peak (or summit)
O2 in L. Indeed, the various analytic approaches indicated differences in the thermogenic region and
no differences around thermoneutrality or at higher Ta. A low Tb decreases the speed of enzymatic reactions
(Q10 effect) and possibly reduces thermogenesis. However,
the 10-min warming phase before the onset of the measurements greatly
reduced the L-D Tb difference, and any remaining difference
was probably eliminated during the additional time required to lower
Ta toward thermoneutrality (~15 min). Hence, it seems
very unlikely that the L-D differences in thermogenic capacity were
contributed by L-D differences in Tb. Furthermore, the
thermogenic response to cold (slope of the Ta-O2
relationship) did not differ between L and D. On the contrary, several
considerations suggest that the lower thermogenesis in L may have
resulted from a difference in the set point of thermoregulation.
First, the slope of the
Ta-O2 curve over
the 22-29°C range was not different between L and D. Hence,
the rate of the response to cooling did not vary between L and D. Rather, the difference was the lower critical Ta, i.e., the
Ta at which the pup was beginning to respond. This
difference was a strong indication that in L the thermoneutrality range
was shifted toward lower Ta. At Ta >35°C,
O2 was the same in L and D,
whereas CO2 was greater in L. The
CO2-to-O2
ratio, or respiratory gas exchange ratio, is an accurate reflection of
the respiratory quotient only in conditions of steady state, which
undoubtedly did not occur in our experiments, which were designed for a
continuous change in stimulus at a constant rate. In dynamic
conditions, the
CO2-to-O2 ratio is very sensitive to the ventilatory level, increasing with the
level of ventilation, as during hypoxia (10), since the elimination of
CO2 by far exceeds the extra work of breathing due to the
hyperpnea. Hence, a greater ventilation is the simplest explanation for
the higher
CO2-to-O2
ratio in L. Because hyperventilation is a common response to heat
stress as a mechanism for heat dissipation (2), the higher respiratory
exchange ratio in L should indicate that the rat pups perceived the
warm Ta as a more intensive heat stress than in D. Thus
also this result agrees with a lower set point of thermoregulation in L.
We did not measure Tb during the experiments, to avoid
undue disturbance to the pups, but measurements on previous occasions (8, 10) indicated that Tb falls rapidly as soon as
Ta is below the thermoneutral range. In other words, in
pups of this size the thermogenic response is too small to appreciably
modify the effects of Ta on Tb. For example,
hyperoxia increased the thermogenic response to cold of newborn rats,
raising O2 from 40 to 60 ml · kg1 · min1,
but without preventing the major fall of Tb in the cold
(3). In fact, it was estimated that, for newborn rats to maintain their Tb at the same value of thermoneutrality when
Ta = 25°C, O2 would have to increase nearly sixfold (10). Hence, the metabolic differences between L and D are too small to make any appreciable difference in the fall of Tb in the cold. As
Ta decreased below ~20°C , the decline in
O2 indicated that the
Q10 effect prevailed over the thermogenic response. This
effect could have limited summit
O2 more in L than in D. In
fact, in L, because the thermoregulatory set point was shifted toward a
lower Ta, whereas the thermogenic response to cold was the
same as in D, the Q10 effect must have curtailed the rise
in O2 at lower values than in
D and before O2 could reach
its summit value. In conclusion, it seems that the finding of a
decreased thermogenic capacity in L could be entirely explained by a
lowering of the set point for thermoregulation.
The interpretation that we are proposing for the present results, a
decrease in the set point of thermoregulation in L, is compatible with
available information. Redlin et al. (17) in rat pups at Ta = 28°C observed that the GDP binding of the BAT was greater and the
drops in Tb and
O2 with propranolol injection were larger in the D than in the L phase. Although these results could
be interpreted as indicating a higher thermogenesis in D, they are also
consistent with the possibility that thermogenesis did not change
throughout the day but that the set point did. In another experiment,
administration of norepinephrine increased O2 to similar values
throughout the day (16), indicating that the thermogenic ability of BAT
did not differ between L and D.
Whether the circadian oscillation of Tb in the adult is a
reflection of changes in the set point has been the object of many studies, but the results are still mixed (1, 18). Several studies in
mammals, including humans, have indicated that autonomic responses and
behavioral preferences change between the L and D phases in a way that
would favor the corresponding changes in Tb. However, other
experiments on rats in a thermocline have indicated that the animal
behaviorally opposes the changes in Tb (reviewed in Ref.
18). We are not aware of studies comparing behavioral thermocontrol in
rat pups between the L and D phases. If behavioral studies confirmed
that the oscillations in Tb were favored, and not opposed,
by the newborn, they would support the present findings. A shift in the
set point has already been shown during hypoxia in rat pups (11). In
fact, hypoxia depresses all forms of thermogenesis, shivering,
nonshivering, and behavioral, and is thought to act at the level of the
thermoregulatory centers of the hypothalamus (12). On the other hand,
specific daily changes in heat dissipation or heat production
mechanisms not accompanied by changes in set point and, therefore,
opposed by behavioral means could have their basis in circadian changes
of neurohumoral factors, of which a few have been demonstrated in the
neonatal period (5, 23).
In conclusion, the results support the hypothesis that, in the newborn,
circadian changes in Tb can be attributed to changes in the
set point of thermoregulation. Changes in thermocontrol can have
implications on a number of regulatory mechanisms. Because the
metabolic level is a major determinant of the ventilatory chemosensitivity (9), it seems likely that the neonatal ventilatory responses to hypoxia and hypercapnia are decreased during the L phase.
In newborn rats, reflexes inhibiting breathing, such as the pulmonary
Hering-Breuer reflex, increase their effectiveness with an increase in
Tb (7). The interaction of these factors during the
circadian changes in Tb and how it would be affected by
hypoxia have never been considered, although it would be important for
our understanding of abnormalities in breathing pattern, including neonatal apneas.
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ACKNOWLEDGEMENTS |
We thank Lina Naso for technical assistance.
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FOOTNOTES |
This study was supported by the Medical Research Council of Canada.
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. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: J. P. Mortola,
Dept. of Physiology, McGill University, McIntyre Basic Sciences Bldg.,
Rm. 1121, 3655 Drummond St., Montreal, PQ, Canada H3G 1Y6 (E-mail:
jacopo{at}med.mcgill.ca).
Received 16 June 1999; accepted in final form 10 December 1999.
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J APPL PHYSIOL 88(5):1853-1858
8570-7587/00 $5.00
Copyright © 2000 the American Physiological Society
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