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1 Discipline of Anatomy and Physiology, School of Medicine, University of Tasmania, Hobart, Tasmania 7001; and 2 Department of Zoology, La Trobe University, Melbourne, Victoria 3086, Australia
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Genetically obese Zucker (Z) rats
have been reported to display a body core temperature
(Tb) that is consistently below that of their lean
littermates. We asked the question whether the lower Tb was
a result of deficits in thermoregulation or a downward resetting of the
set point for Tb. For a period of 45 consecutive hours,
lean and obese Z rats were free to move within a thermal gradient with
an ambient temperature (Ta) range of 15-35°C, while subjected to a 12:12-h light-dark cycle. Tb was measured
using a miniature radio transmitter implanted within the peritoneal cavity. Oxygen consumption (
O2) was
measured using an open flow technique. Movements and most frequently
occupied position in the gradient (preferred Ta) were
recorded using a series of infrared phototransmitters. Obese Z rats
were compared with lean Z rats matched for either age (A) or body mass
(M). Our results show that obese Z rats have a lower Tb
[37.1 ± 0.1°C (SD) vs. 37.3 ± 0.1°C, P < 0.001] and a lower O2 (25.3 ± 1.9 ml · kg
1 · h1) than
lean controls [33.1 ± 3.7 (A) and 33.9 ± 3.9 (M)
ml · kg1 · h1,
P < 0.001]. Also, the obese Z rats consistently chose
to occupy a cooler Ta [20.9 ± 0.6°C vs. 22.7 ± 0.6°C (A) and 22.5 ± 0.7°C (M), P < 0.001] in the thermal gradient. This suggests a lower set point for
Tb in the obese Z rat, as they refused the option to select
a warmer Ta that might allow them to counteract any thermoregulatory deficiency that could lead to a low Tb.
Although all rats followed a definite circadian rhythm for both
Tb and O2, there was no
discernible circadian pattern for preferred Ta in either
obese or lean rats. Obese Z rats tended to show a far less
definite light-dark activity cycle compared with lean rats.
body temperature; preferred ambient temperature; metabolic rate
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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GENETICALLY OBESE
Zucker (Z) rats have been reported to display a body core temperature
(Tb) that is consistently below that of their lean
littermates (1, 2, 20, 22, 24). A low Tb could
be brought about either by a decreased rate of heat production, an
increased rate of heat loss, or some combination of these two conditions. The reports regarding the relative rates of heat production or oxygen consumption (O2) in obese
compared with lean Z rats are contradictory. Obese Z rats are variously
claimed to show a higher O2 (1,
6), a lower O2 (17,
28), or a similar O2 (2,
22). Moreover, the situation is further complicated by effects
of ambient temperature (Ta; Refs. 6,
17), prior temperature acclimatization (2,
17), or the actual units and exponents used to report the
O2 measurements (2, 22, 28). Less information has been reported on possible differences in the rate of heat loss for obese compared with lean Z rats. Because
obese Z rats have more body fat (28), it follows
intuitively that they possess more body insulation. Against this are
reports that obese Z rats display a higher minimal rate of heat loss
than lean rats (6).
A possibly more important question is whether the lower Tb in obese Z rats is due to deficits in temperature regulation or the result of a controlled resetting of the set point for Tb. It appears that obese Z rats can certainly match their lean littermates in heat production if required to do so (1, 2, 6, 22, 34). It could be, however, that heat loss is much less well-regulated in obese Z rats. After all, it is known that obese Z rats show evidence of diabetes (8, 10, 21), which in turn is associated with deficits in autonomic innervation to peripheral blood vessels and a correspondingly poor control of peripheral blood flow. On the other hand, diabetes limits substrate supply to body cells. It might make sense to lower the basal levels of heat production required to maintain Tb and so to lower the set point around which Tb is controlled.
Regulation of Tb is not solely due to changes in autonomic
function; Tb is also controlled by behavioral means.
Rodents have been shown consistently to select a particular
Ta (preferred Ta) when given the opportunity to
move along a thermal gradient (11). This preferred
Ta can be altered by a number of factors, including the
light-dark cycle (4, 12), experimentally induced fever (32), and exposure to hypoxia (7, 14). It
also varies with the strain of rat studied (11, 31). The
preferred Ta for Z rats has not been reported. Even the
thermoneutral temperature (Ttn) for Z rats is not
definitely established, being variously quoted as 25°C
(17) and 29°C (see Ref. 22). Even so, it is known that Ttn is no guide to the preferred Ta,
rats normally selecting a Ta somewhat below Ttn
(11). Neither is Ttn necessarily the
temperature to which the rat is best suited from the point of view of
normal health (35). The circadian rhythms for
Tb and activity in Z rats have been reported by Murakami et
al. (24), and circadian changes in hormone levels have
been reported by Martin et al. (21). However, neither of
these studies provides information on O2
or preferred Ta.
The present study was conceived to investigate whether the lower Tb in obese Z rats is due to either 1) a deficit in thermoregulation or 2) a controlled reduction in set point. We argue that if a deficit in thermoregulation were the case, then the obese rats would select a higher Ta than their lean littermates and that the difference in Tb between the two groups would decrease and perhaps vanish. On the other hand, if a controlled reduction in set point were the case, then the obese Z rats would select a lower Ta and the difference in Tb would persist. As controls, we used both age-matched and weight-matched lean Z rats to investigate possible contributions of age and mass to any differences observed.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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All experiments had the approval of the La Trobe University Animal Ethics Committee.
Obese (n = 8, age = 46 ± 3 days, mass = 172.1 ± 28.3 g), lean age-matched (n = 8, age = 45 ± 3 days, mass = 121.0 ± 15.5 g), and lean weight-matched (n = 8, mass = 172.6 ± 11.4 g) Z rats were housed at a Ta of 22°C and a 12:12-h light-dark photoperiod with the onset of the light phase at 0700. Before experimentation, each rat was anesthetized with Fluothane, and a small abdominal incision was made. A calibrated (±0.1°C) single-stage miniature radio transmitter (mass ~1 g, Sirtrack, New Zealand) in which pulse frequency altered with temperature was inserted into the peritoneal cavity to record Tb, and the wound was closed with vicryl sutures. After a minimum recovery time of 48 h, rats were ready to be used for experimental purposes.
A preweighed rat was placed in a chamber (1,500 mm × 100 mm × 100 mm) with the base and walls constructed from 10-mm-thick aluminum and fitted with a plastic floor raised 10 mm above the base. A Plexiglas lid (5-mm thick) fitted with an inlet and outlet port for air was sealed with a film of grease and screwed down to ensure an airtight seal. Air flow through the chamber was 1,200 ml/min.
The chamber was preheated at one end by water at 43°C and cooled at the other end by water at 5°C, thereby establishing a thermal gradient that was approximately linear from 15°C to 35°C. The sides of the chamber were fitted with a series of infrared phototransistors spaced at 35-mm intervals; the photocell closest to the warm end of the gradient that was obscured by the rat recorded the position (i.e., preferred Ta) of the animal within the thermal gradient. An antenna placed alongside the thermal gradient and connected to a scanner (Uniden Scanner, UBC900XLT) obtained the pulse signal from the implanted transmitter, which in turn was transformed to a rate (pulses/min; in-house converter).
Food and water were available ad libitum; the food was distributed along the gradient, and water was provided at three sites, centrally and one at each end of the chamber. A 12:12-h light-dark photoperiod was maintained with the onset of light at 0700. Experiments were started at 1500, and rats remained in the chamber for 45 h.
Air from the outlet port in the chamber lid was subsampled (100 ml/min)
and passed through a drying column (Drierite) and CO2 scrub
(Ascarite) before passing through an oxygen analyzer (S3A-I, Applied
Electrochemistry). The fractional concentration of oxygen
(FO2) was measured continuously. Baseline
values of FO2 were checked every 3 h using
a solenoid that switched between incurrent and excurrent gas. Any drift
in the recorded signal was assumed to be linear. The rate of
O2 was determined from the product of
the air flow through the chamber and the difference between inflowing
and outflowing FO2
(FIO2 and
FEO2, respectively), taking into
account respiratory quotient-related errors (see Ref. 9),
as
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Data collection and analysis.
The outputs from the oxygen analyzer, the photocells, and the rate of
the implanted temperature transmitter were recorded every 5 min using
an analog-to-digital converter (PowerLab/800, AD Instruments, Sydney,
Australia). For O2, Tb, and
Ta (calculated from photocell position), the data were
averaged for each hour. Data were statistically analyzed by
repeated-measures ANOVA, with post hoc Bonferroni modified
t-tests for the comparisons of interest. In all cases,
significance was defined at P < 0.05.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Obese rats displayed a significantly greater mass than lean Z rats
of the same age (Table 1). Over a 24-h
period, the mean values for Tb,
O2, and preferred Ta in
age-matched lean Z rats were identical to those recorded from
weight-matched lean Z rats (Table 1).
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The mean Tb of the obese Z rats was significantly lower
(P < 0.001) for both lean age and weight groups (Table
1). Likewise, the mean O2 of the obese Z
rats was significantly lower (P < 0.001) than that of
their lean counterparts. These differences persisted
throughout the light-dark cycle (Fig. 1),
with the zenith occurring during the dark phase and the nadir during
the light phase for both Tb and
O2 in both lean and obese rats. Such a circadian pattern has been previously reported for the rat (3, 23). In both lean (age and weight combined) and obese Z rats, Tb oscillated during the 24-h period with an amplitude of
~0.7°C. On the other hand, the light-dark oscillation in
O2 was greater for lean Z rats than in
the obese rats (6.7 and 2.8 ml · min1 · kg1,
respectively).
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The obese Z rats consistently chose to occupy a significantly
(P < 0.001) cooler preferred Ta in the
thermal gradient than that of their lean counterparts (Table 1). In
neither obese nor lean Z rats was there an obvious circadian rhythm
(Fig. 1). In addition, Fig. 2 suggests
that obese Z rats took longer to choose their final preferred
Ta. All rats tended to occupy the cooler end of the
thermocline when first placed within it, but lean rats had settled on
their final mean position 6-12 h from the commencement of the
experiment. Obese rats, on the other hand, took 18-24 h to achieve
their preferred Ta.
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Obese rats tended to show a far less definite light-dark activity cycle
compared with lean rats (Fig. 3). Lean
rats displayed little movement during the light phase and a great deal
of movement during the dark phase, which is to be expected for a
nocturnal animal and is in line with the circadian rhythm found for
Tb and O2. Obese rats, on
the other hand, displayed considerable activity during both the light
and dark phases and during activity tended not to move as far (note the
number of times the rats moved 10 or more positions).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Body temperature difference between obese and lean Z rats. Both lean and obese Z rats display a Tb oscillation of ~0.7°C, which is greater than that previously reported in Z rats (24) and slightly lower than that reported in Sprague-Dawley rats (23). The mean Tb of the obese Z rats (37.1°C) was significantly lower than that of the lean rats (37.3°C). This finding confirms previous studies in which a difference in Tb was reported (1, 10, 20, 22, 24). Variations in Tb between obese and lean rats appear to be independent of age, gender, or prior acclimatization temperature (see Ref. 22 for discussion). Our mean values for Tb are very similar to those reported by Murakami et al. (24). The difference in Tb of 0.2°C, however, is much smaller than that reported from other studies (1, 10, 22), in which the difference was on the order of 1.0-1.2°C. The common features of the present study and that of Murakami et al. (24) include that in both studies 1) Tb was measured using an implanted miniature radio transmitter, 2) the measurements were recorded continuously over an extended period, and 3) the animals were able to exhibit normal behavior. In the studies of Armitage et al. (1) and Godbole et al. (10), Tb was obtained daily as a single value by using a rectal probe. Maskrey et al. (22) also used a rectal probe, but this was kept in place throughout the experiment. However, because this last study included measurements of pulmonary ventilation, the animals were required to remain closely confined so that their body movements were limited.
The relevance of these differences in protocol lies in the fact that rats commonly increase Tb when stressed, whether the stress is due to handling (5), a novel environment (33), or immobilization (25). The important factor in all of this is that lean Z rats show these stress-induced increases in Tb, whereas obese Z rats generally do not (29). The reason for this is that the increase in Tb is mainly brought about by an increased sympathetic outflow to brown adipose tissue (19). Obese Z rats appear to activate this pathway less readily (26, 27, 30, 37). Therefore, eliminating stressors such as handling, novelty, and close confinement reduces brown fat thermogenesis in lean Z rats, allowing the measured Tb to fall. Nevertheless, a significant difference in Tb between the lean and obese Z rats is still apparent. It is the cause of this difference that forms the main subject of the remainder of this report.Metabolic rate difference between obese and lean Z rats. Metabolic rate measured in obese Z rats was significantly lower than that measured from lean rats. This appears to be a general finding when lean and obese rats are compared simply on a body weight basis (2, 17, 28). However, when metabolic rate is recalculated to take into account body surface area (2) or effective body mass (28), then the difference between obese and lean age-matched values disappears, although the difference between obese and weight-matched animals remains. This reflects more the problem of standardization, and the finding in the present study of no difference between the two lean cohorts when standardized per unit body mass supports the argument that metabolic rate is low in obese Z rats when compared with lean rats.
Armitage et al. (1) reported that metabolic rate was higher in obese than in lean Z rats. No absolute body weight data were provided in their study. However, taking into account the statement that the obese rats weighed an extra 230 g, and judging by studies carried out on Z rats of a similar age (22, 28), we anticipate that the obese animals must have been of a body mass at least 35% greater than their lean counterparts. This weight difference would certainly be enough to eliminate the claimed difference in metabolic rates. By contrast, Demes et al. (6) report that, in their hands, obese rats definitely do show a higher metabolic rate than lean rats, whatever the units used to express this measurement. Is it possible that the inconsistencies in the reports comparing metabolic rate in lean and obese Z rats are not entirely due to the units and exponents used to express the data? A clue to an answer to this question lies with the study of Kaplan (17), who reported that the higher metabolic rate seen in lean Z rats compared with obese rats when exposed acutely to a Ta of 25 or 30°C disappeared when rats were acclimatized for 48 h to a Ta of 30°C. Indeed, all studies claiming that metabolic rate in obese Z rats either matched or exceeded that of the lean rats were carried out at a Ta of 28-30°C (1, 6, 22). On the other hand, those studies that report a higher metabolic rate in lean Z rats were carried out at the lower Ta of 25°C (2, 28). In the present study, the Ta was not fixed; instead, the animals were able to select their preferred Ta within a thermal gradient. The mean Ta selected by both lean and obese rats was below 23°C (see below). We suggest that a Ta significantly above 25°C might produce a heat stress to obese Z rats and a consequent increase in metabolic rate. When Z rats are free to behave normally in a thermal environment of their choosing, obese rats settle on a rate of metabolism below that of lean rats of the same age or same body weight.Preferred Ta difference between obese and lean Z rats. During the second day in the temperature gradient, the obese Z rats elected to spend the majority of their time at a Ta significantly below that chosen by lean rats. We believe that this constitutes evidence that the lower Tb in obese Z rats is due to a lower set point compared with their lean counterparts. This argument has been used to demonstrate the association between preferred Ta and set point Tb during fever (e.g., Ref. 32) and has been used by Shido et al. (31) to explain the difference in preferred Ta in two different strains of rat.
An alternative explanation for a lower preferred Ta among the obese Z rats might have been that both rats have a similar rate of metabolism at thermoneutrality but that at a lower Ta the lean rats require a higher rate of thermogenesis because of their greater surface area-to-volume ratio; hence they attempt to offset this by choosing a slightly warmer Ta. The counterargument to this suggestion is that lean rats of the same size as the obese rats (weight-matched controls) also select a warmer Ta. This reinforces the point already made that, because both lean cohorts are similar in all parameters measured, differences between lean and obese Z rats cannot be due to the effects of size. The results of the present study may be compared with a study conducted on rats rendered hypothyroid after treatment with propylthiouracil (36). The treated rats showed deficits in thermogenesis evident as reduced metabolic rate and reduced Tb. Unlike the Z rats in the present study, however, they selected a Ta higher than the untreated controls. Despite this, Tb was still maintained below control levels. This study suggests that even when a thermoregulatory deficit clearly exists, changes in set point may still be relevant. The absolute values for the mean preferred Ta reported here for the Z rat of 22.5-22.7°C (lean) and 21°C (obese) lie below the values reported for other rat strains. Gordon (11) reported that for Sprague-Dawley, Fischer-344, and Long-Evans rats subjected to brief exposure periods, the preferred Ta lay approximately between 20 and 25°C. However, in a later study conducted over a longer exposure period, preferred Ta in the Long-Evans rat was reported to be as much as 9°C higher than that measured short term (13). Shido et al. (31) compared FOK, WKAH, and Donryu rats and reported mean daily preferred Ta values between approximately 22 and 27°C. On the other hand, comparisons between different strains across separate studies may not be entirely valid. For instance, different thermoclines may provide differing microclimates due to the heat-radiating and -conducting properties of various materials used in their construction. The preferred Ta is below the Ttn of the Z rat, variously quoted to be 25°C (17) or 29°C (see Ref. 22). This is in agreement with the report of Gordon (11), who found that in all the rat strains he tested, the preferred Ta was significantly below the lower critical temperature. Gordon in fact observed that his rats very rarely selected a Ta of 30°C or above, even though this is whereO2 was lowest.
The Ta selected by Z rats did not vary between the light
and dark cycles. This finding contrasts with other studies (4, 12) where a circadian rhythm of preferred Ta was
evident, although this rhythm often took as long as 4 days to become
established (12), whereas our study extended for a 2-day
period only.
The fact that when first placed in the thermal gradient all rats showed
a distinct preference for the cooler end has been observed previously
(12). It is of interest in this regard to note the
differences in time taken for the Z rats to settle on their preferred
Ta. Whereas lean rats took 6-12 h to achieve this, it
took obese rats as long as 18-24 h. The reason for this is not
obvious. It may be that, in addition to having a lower set point for
Tb, obese rats may also display a less precise feedback mechanism for matching peripheral temperature sensory inputs with the
preferred Ta.
Activity differences between obese and lean Z rats. The activity index used for the present study shows that although overall activity levels appear similar between obese and lean Z rats, the pattern of activity over the light-dark cycle is quite different. Whereas the lean rats display a great deal of activity during the dark phase and considerably less in the light, the obese rats show fewer large dark-phase excursions and many more light-phase movements.
A close relationship between the light-dark activity cycle and the Tb cycle is well established (e.g., Ref. 12). However, the degree to which activity determines Tb is not yet fully understood (15, 16). Yet, in the Z rat, where we have shown a significantly lower Tb andO2 in obese compared with lean animals,
this question is particularly pertinent.
Keesey et al. (18) report that the level of activity, as
well as the circadian activity pattern, is similar for lean and obese Z
rats. Murakami et al. (24), on the other hand, report that
obese Z rats show much less overall activity and also a depressed amplitude of circadian rhythm for activity. The present study agrees
with different aspects of each of these studies. We find that overall
activity is similar in the two genotypes but that the circadian rhythm
of activity is much less apparent in obese rats. This last fact is
especially evident in that obese rats appear much more active during
the light phase than do lean rats. This may reflect a higher incidence
of feeding behavior during the light phase. In this regard, Bertin et
al. (2) report that food ingestion during the daytime is
twice as great in obese rats compared with lean rats.
Conclusions. The main conclusion of the present study is that the genetically obese Z rat maintains a lower set point for Tb. This it is able to achieve by maintaining a lower level of metabolic heat production and, if available, selecting a lower Ta. Evidence also suggests that obese Z rats may display a less precise feedback mechanism for matching peripheral temperature sensory inputs with their preferred Ta. The present study is unable to determine whether heat loss is also changed in the obese Z rat compared with lean littermates.
Perspectives
Since the introduction of the term "set point" to describe a controlled end point for Tb into the literature on temperature regulation, much of our thinking has been driven by this concept. Another engineering analogy that has proven useful is "load error," the degree to which actual Tb deviates from set point. In behavioral thermoregulation, preferred Ta may be considered an adjunct to set point in that it describes the external thermal conditions to which an animal aspires. It is interesting to note the longer time interval taken by the obese Z rat to reach its preferred Ta goal. Does this delay denote a poorer ability to detect a load error or a lesser urgency to correct it (i.e., a greater tolerance)? It may prove profitable to pursue this question, not just in the Z rat but in other models of thermoregulatory behavior. The present study also raises once again the unresolved question as to whether the obese Z rat is best regarded as a collection of endocrine, metabolic, and regulatory defects or rather as a unique assemblage of well-integrated, although unusual, physiological adaptations.| |
ACKNOWLEDGEMENTS |
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We acknowledge the contribution of L. Masini in the maintenance of the animals and in assistance with the experiments.
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FOOTNOTES |
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The work was supported in part by a grant to P. B. Frappell.
Address for reprint requests and other correspondence: P. B. Frappell, Dept. of Zoology, La Trobe Univ., Melbourne, Victoria 3086, Australia (E-mail: P.Frappell{at}zoo.latrobe.edu.au).
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.
Received 21 March 2001; accepted in final form 20 July 2001.
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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