- Email: [email protected]
Acute, but not chronic, exercise lowers the body weight set-point in male rats
Physiology&Behavior,Vol.52, pp. 1173-1177, 1992
0031-9384/92 $5.00+ .00 Copyright© 1992PergamonPressLtd.
Printedin the USA.
Acute, But Not Chronic, Exercise Lowers the Body Weight Set-Point in Male Rats M. C A B A N A C 1 A N D J. M O R R I S S E T T E
Ddpartement de Physiologie, Facult~ de M£decine, UniversitO Laval, QuObec G1K 7P4, Canada Received 4 F e b r u a r y 1992 CABANAC, M. AND J. MORRISSETTE.Acute, but not chronic, exercise lowersthe body weightset-point in male rats. PHYSIOL BEHAV 52(6) 1173-1177, 1992.--The influence of muscular training on overall energy balance and body weight is not clear. A group of male rats was trained to feed every day from 1000 to 1200. Then the intersect of regression line of food hoarded during meal time vs. body weight with the X-axis was measured. Finally, the rats were trained to run 1 h every day on a motor-driven treadmill. When the training took place in the morning, just before the hoarding session, the mean intersect was significantly lowered from control (497 + 18 g to 433 _+9 g). When the training took place in the afternoon, after the hoarding session, the mean intersect was not significantlydifferent (504 _+21 g) from control. Food intake during the hoarding sessionswas affected neither by body weight changes nor by muscular exercise. These results suggest that the set-point for body weight regulation is acutely lowered just after muscular exercise, but is not influenced by chronic training. Energy balance
Hoarding behavior
Food intake
BODY weight is the result of the balance between energy intake and energy expenditure. Increased muscular activity encountered at work and endurance sports can elevate energy requirements considerably. As long as food intake does not compensate for the increased energy expenditure, exercise may induce a negative energy balance and cause some body weight reduction. In 1956, J. Mayer et al. (22) published a study showing that moderate muscular work decreased body weight, and food intake. These results have become controversial in recent years. The amount of body weight loss is quite variable from study to study, probably in relation with the protocols that were used. For example, human subjects lost several kilograms over months of training (12,21). Others did not change their body weight (2,17). Rats chronically (4) or acutely (5) exercised were thus protected against the drop of body weight normally occurring when the animals are switched to 2 h/day feeding, while other trained rats lost 100 g compared to their sedentary controls (25). An attempt at studying the influence of exercise on body weight by doing energy balance measurement is not easily achieved because that involves the chronic measurements of energy intake, energy expenditure, and energy storage. The concept of body weight regulation helps overcome the difficulty. If body weight is regulated, or a correlate of body weight is regulated, then the set-point is the value of body weight that the system achieves by controlling both inflow and outflow of energy. The set-point can be different from the actual body weight, at least during transients. There exists a behavioral open-loop method to measure the body weight set-point in rats. When rats are deprived of food they start to hoard food. The more their body weight drops, the
Body weight set-point
more food they hoard. It has been previously shown that the amount of food a rat hoards is proportional to its body weight loss (3,7-10). The intersect of the regression line of hoarded food vs. body weight with the X-axis is therefore the threshold for a proportional regulatory response opposing the weight deficit and may be used to estimate the body weight set-point in that species. In the present study the influence of both acute and chronic muscular exercise, on the intersect of regression line of hoarded food vs. body weight with the X-axis, i.e., the threshold of the hoarding response, was studied in rats. METHOD
Subjects The subjects were six Long-Evans rats from Charles River Inc. of Canada. We chose male rats because hoarding is especially active in males of that strain (6). The rats were trained to feed once a day from 1000 to 1200 every day for 2 weeks before the beginning of the experiment, then throughout the experiment. Light went on at 0600 h and off at 1800 h.
Housing and Hoarding The rats were housed one in a cage in wire-meshed and steelwalled rabbit cages (0.48 X 0.41 X 0.34 m). In each cage the rat had permanent access to a home (0.24 x 0.19 X 0.10 m) made of a plastic water can painted black, in which a door had been cut to permit passage of the animal. The ambient temperature, an important factor of hoarding behavior in the rat (9), was regulated at 20°C.
xRequests for reprints should be addressed to M. Cabanac. Email: [email protected].
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1174
ttoarding measurements took place during the period of time when the animals had access to food. At 1000 h, the front door of the cage was swung open and the rat had access to a tray, 0.35 m from the cage door, containing a large quantity of regular rat chow pellets of unequal size, weighing about 4 g each. For 2 h the rat could feed and carry pellets from the tray to its dark home. At 1200 h the cage door was closed and the food hoarded in the rat's home was removed.
Measuremenl.s The rats were weighed every morning, 7 days a week, prior to the beginning of the other measurements. The amount of food on the tray was weighed before the hoarding session. The food remaining in the tray at the end of the session and the food hoarded by the rat were also weighed. The food eaten by the rat was computed by subtracting remaining and hoarded food from offered food. Repeated control manipulation of rat chow has shown that this procedure entails a negligible error on the missing weight. The number of foraging trips from home to food was counted in rat No. 6 three times per hour for 5 min, at min 5, 25, 45, 65, 85, and 105 of each hoarding session.
Training The rats' muscular exercise was a l-h running on a motordriven treadmill. The training started 59 days after the beginning of the experiment. On the first week of training the speed of the treadmill and the duration of the session were progressively increased up to 50 min at 20 m . min ~and 10 min at 25 m . min ~, which was then maintained daily 7 days a week for 39 days. This procedure was similar to, or slightly higher than, currently used in rats (11).
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increase the rats received additional food just aller the hoardil/g session. l'he amount of tbod thus added was estimated empirically from the influence of supplements on body weight obtained on previous days.
Procedure Alter being trained for 2 weeks to feed once a clay tot 2 h from 1000 to 1200, the control hoarding response was measured for 35 days and the rats' body weight hoarding threshold was calculated. Then the rats were trained to run on the treadmill for 2 weeks, as described above, after which their hoarding response was measured daily and their threshold for hoarding was calculated under two different schedules: A. On even days, the 1-h exercise took place from 0830 to 0930 I1, i.e., just before the hoarding session. This condition will be called acute in the following because this schedule intended to explore the short-term influence of exercise on hoarding threshold. Twelve such sessions took place in fully trained rats. B. On odd days, the l-h exercise took place in the early alternoon, i.e., after the hoarding session. This condition will be called chronic in the following because this schedule intended to explore the hoarding threshold of trained but not tired rats. Fourteen such sessions took place in fully trained rats. RESUt:rs
Hoarding Thresholds Figure 1 shows the amount of food hoarded as a function of body weight in the one rat with the highest slope (rat No. 5). Figures 2 and 3 show the group results, obtained with the mean
Body Weight Threshold[or Hoarding Herberg et al. (13) were the first to relate the rat's hoarding behavior to the extent of displacement of body weight below the set-point. The method used here to assess the value of this threshold was that used previously (3,7-10). For each animal and each condition, the regression line of food hoarded on body weight was computed. The threshold for the hoarding behavior was determined for each animal from the intersect of this regression line with the X-axis. All the individual coefficients of correlation of hoarded amount vs. rat body weight obtained in the control, chronic, and acute conditions were significant below the threshold of 5%, except for rat No. 3 in the acute condition. This rat, therefore, was not included in the calculation of group means in the acute condition.
Body H~ight Manipulations Rats do not hoard food when their body weight is at its setpoint. The method of measuring hoarding threshold therefore implies a drop, then a recovery, of body weight. It took the rats 1 week to get accustomed to the one meal a day procedure. The rats were weighed every morning before the beginning of the hoarding-feeding session. After the 2 weeks necessary to get them used to the new feeding schedule, they had lost enough weight to allow the measurement of their hoarding response. To increase body weigh loss the experimental sessions were occasionally suppressed, so as to skip one day. During the exercise period the rats were having access to food 2 h every day, but they spent too much time hoarding to allow a sufficient food intake for a compensation of their increased energy needs. Therefore, during the training they tended to lose weight. To allow body weight
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FIG. 4, Mean hoarding threshold, obtained from individual intersects
parameters of individual regression lines. The results from the chronic sessions, when the training took place in the afternoon, are given in Fig. 2. It can be seen, both on the individual result and on the group result, that the hoarding by fully trained animals in chronic sessions was not different from the hoarding prior to training. Figure 3 shows the results obtained in acute sessions when the training took place just before the hoarding. It can be seen both on the individual result (Fig. 1) and the group result (Fig. 3) that the hoarding was depressed in acute sessions but the mean slope of the regression line remained unchanged in all three conditions, from -8.21 ___1.06 control to -9.8 + 1.20 acute and - 9 . 4 chronic (one-factor ANOVA, F = 0.761, NS). The hoarding threshold in the chronic condition (504 + 21 g) was not significantly different from control (497 + 18 g), but this threshold in the acute condition (433 + 9 g) was significantly lower than both control and chronic conditions (one-factor ANOVA, F = 9.247, p < 0.01) (Fig. 4).
Food Intake
of regression lines with X-axis, in control, acute (morning training), and chronic (afternoon training) conditions, p < 0.0h one-factor ANOVA, F = 0.0083.
was able to modify food intake as compared to control food intake (one-factor ANOVA, F = 2.5 l, NS).
Foraging Trips Figure 6 presents the mean results of periodic counting of foraging trips in rat No. 6. On the top the two curves show the pooled results from the sessions prior to training separated into two halves, low and high body weight, respectively. At the bottom the two curves show the pooled results from sessions in acute and in chronic conditions. It can be seen that over a session the frequency of foraging trips tended to decrease logarithmically with time. Acute exercise modified the frequency comparatively, to the chronic condition in the same way as high body weight, comparatively, to low body weight.
Figure 5 shows the group means of individual food intakes measured during the daily 2-h hoarding sessions. Under the experimental conditions neither acute exercise nor chronic training
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FIG. 5. Mean food intake during the hoarding sessions from 1000 to 1200, obtained from mean individual data in control, acute (morning training), and chronic (afternoon training) conditions.
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Thus, the literature does not allow a firm conclusion about the influence of exercise on the body weight set-point, and the direct measurement of the hoarding threshold in the present work is therefore of great interest. The present results show that when the hoarding threshold was measured 19 h after the training session, no lowering of this threshold was obtained. Yet the animals were fully trained. Chronic training was therefore unable to change the set-point of body weight regulation in these male rats, The absence of change of hoarding threshold in trained rats found here confirms the conclusion that long-term animal studies do not show an influence of exercise on energy expenditure and that exercise affects energy balance by increasing expenditure mainly through its intrinsic cost (23).
10
Acute Influence o/Exercise
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FIG. 6. Time course of the frequency of foragingtrips by rat No. 6 over the 2-h duration of hoarding sessionduring the control period (top) and trained period (bottom). All the sessionsof the control period were separated into two halves:at low body weight(lean) and at high body weight (heavy). During the trained period, the morning training is the acute condition and the afternoon training is the chronic condition.
DISCUSSION
Influence qf Exercise on Body Weight Set-Point Exercise training increases the energy expenditure; however "the role played by muscular exercise in energy balance" (and thus in the regulation of body weight) "may be more complex than it appears a priori" (26). For example, the food intake of male rats has been shown to decrease after acute exercise (19) and chronic training (1), and energy expenditure of rats has been shown to increase beyond the elevated rate theoretically expected when exercise is performed ( 14,15). Exercise training protected female rats (11) and mice (30) against the influence of weight cycling; i.e., their body weight and food intake remained only slightly changed. The results in humans were also confusing. The influence of exercise training on both food intake and energy expenditure is reflected on long-term energy balance, i.e., body weight. Human subjects lost several kilograms over months of training (12,21 ), whereas others did not change their body weight (2,18). The measurement of food intake showed no decrease for 16 (21) and 18 (31) weeks of training, but dietary thermogenesis was diminished in athletes (20,29). One may speculate about the evolution of body weight setpoint in the experiments briefly reviewed above. Three situations were observed: 1. when food intake and body weight remained stable the setpoint was likely to have remained unchanged:
When exercise took place before the hoarding session, the hoarding threshold was lowered as compared to control. The influence of exercise on body weight and energy balance was therefore acute, in the hours following exercise, but not chronic, since no hoarding threshold change occurred when the training took place in the afternoon, after the hoarding-feeding session. The foraging pattern of rat No. six was similar when underweight in the acute situation and when at normal body weight in the control situation (Fig. 6). Such an influence of exercise lasted only a few h, since it was absent when the rats were tested before running. A lowering of set-point should be accompanied by a decrease of food intake, and an increase of thermogenesis (16). Since the lowering of the hoarding threshold was merely transient, one should expect these responses to occur only in the h following exercise. The amount of food hoarded was smaller when exercise took place before the hoarding-feeding session. One may hypothesize that the decreased hoarding in sessions immediately following exercise might have been caused by mere fatigue. However, fatigue may be rejected as the cause of reduced hoarding for the following reasons: 1) There is some indication that food intake in a meal immediately following a strenuous exercise is diminished, in rats (24) and in humans (17), but not after a moderate exercise (27,28). In the present experiment food intake was not significantly depressed in the acute sessions (Fig. 5). This is an indication that the exercise was not strenuous for the rats. 2) If fatigue were the cause of the reduced hoarding, its influence should show more in undernourished animals that may be expected to be more easily fatigued. That was not the case: the regression line of the amount hoarded remained parallel to the control regression line in all rats (except rat No. 3, which was excluded from the group results for that reason). When undernourished, say at 300 g body weight, the rats hoarded an average 1250 g of food, i.e., much more than when they were not lean, say at 400 g body weight. Finally, a close examination of diet-induced thermogenesis confirmed that the increase of oxygen consumption was only transient in trained rats, which were otherwise energy savers as compared to their sedentary controls (26). Such a transient increase is consistent with the hypothesis of a transient lowering of the set-point just after the running, which was found in the present work. The different effects obtained on body weight set-
SET-POINT AND EXERCISE
1177
point after acute exercise and chronic training are likely to explain the variable results reported in the literature on body weight and food intake after variable experimental and training protocols.
ACKNOWLEDGEMENT This work was supported by Conseil de la Recherche en Sciences Naturelles et en Grnie (N. S. E. R. C.), Canada.
REFERENCES 1. Arnold, J.; Richard, D. Exercise during intermittent cold exposure prevents acclimation to cold in rats. J. Physiol. (Lond.) 390:45-54; 1987. 2. Bjorntorp, P.; Dejounge, K.; Krotkiewski, M.; Sullivan, L.; Sjostrom, L.; Sternberg, J. Physical training in human obesity IlL Effects of long-term physical training on body composition. Metabolism 22: 1467-1475; 1973. 3. Cabanac, M.; Swiergiel, A. H. Rats eating and hoarding as a function of body weight and cost of foraging. Am. J. Physiol. 257:R952R957; 1989. 4. Curl, R.; Hell, N. S.; Timo-Iara, C. Meal feeding and physical effort. 1 Metabolic changes induced by exercise training. Physiol. Behav. 47:869-873; 1990. 5. Curl, R.; Hell, N. S.; Timo-Iara, C. Meal feeding and physical effort. 2 Metabolic changes induced by an acute exercise. Physiol. Behav. 47:875-879; 1990. 6. De Bruin, J. P. C. Sex differences in food hoarding behaviour of Long Evans rats. Behav. Proc. 17:191-198; 1988. 7. Fantino, M.; Brinnel, H. Body weight set-point changes during the ovarian cycle: Experimental study of rats during hoarding behavior. Physiol. Behav. 36:991-996; 1986. 8. Fantino, M.; Cabanac, M. Body weight regulation with a proportional hoarding response in the rat. Physiol. Behav. 24:939-942; 1980. 9. Fantino, M.; Cabanac, M. Effect of a cold ambient temperature on the rat's food hoarding behavior. Physiol. Behav. 32:183-190; 1984. 10. Fantino, M.; Faion, F.; Rolland, Y. Effect of dexfenfluramine on body weight set-point: Study in the rat with hoarding behaviour. Appetite 7(Suppl.):115-126; 1986. 11. Gerardo-Gettens, T.; Miller, G. D.; Horwitz, B. A.; McDonald, R. B.; Brownell, K. D.; Greenwood, M. R. C.; Rodin, J.; Stern, J. S. Exercise decreases fat selection in female rats during weight cycling. Am. J. Physiol. 260:R518-R524; 1991. 12. Hadjiolova, I.; Mintcheva, L.; Dunev, S.; Daleva, M.; Handjiev, S.; Balabanski, L. Physical working capacity in obese women after an exercise programme for body weight reduction. Int. J. Obes. 6:405410; 1982. 13. Herberg, L. J.; Pye, J. G.; Blundell, J. E. Sex differences in the hypothalamic regulation of food hoarding: Hormones versus calories. Anim. Behav. 20:186-191; 1972. 14. Hill, J. O.; Davis, J. R.; Tagliaferro, A. R. Effects of diet and exercise training on thermogenesis in adult female rats. Physiol. Behav. 31: 133-135; 1983. 15. Hirata, K.; Nagasaka, T. Enhancement of calorigenic response to cold and to norepinephrine in physically trained rats. Jpn. J. Physiol. 31:657-665; 1981. 16. Keesey, R. E. The relation between energy expenditure and the body weight set-point: Its significance to obesity. In: Burrows, G. D.; Beu-
17. 18.
19. 20. 21.
22. 23. 24. 25. 26. 27. 28. 29. 30.
31.
mont, P. J. V.; and Casper, R. C., eds. Handbook of eating disorders, part 2. New York: Elsevier; 1988. Kissileff, H. R.; Pi-Sunyer, F. X.; Segal, K.; Meltzer, S.; Foelsch, P. A. Acute effects of exercise on food intake in obese and nonobese women. Am. J. Clin. Nutr. 52:240-245; 1990. Krotkiewski, M.; Mandroukas, K.; Sjostrom, L.; Sullivan, L.; Wetterqvist, H.; Bjorntorp, P. Effects of long-term physical training on body fat, metabolism, and blood pressure in obesity. Metabolism 28:650-658; 1979. Larue-Achagiotis, C.; Louis-Sylvestre, J. Effects of acute exercise on food intake and plasma free fatty acid levels. Physiol. Behav. 39: 413-415; 1987. Leblanc, J.; Mercier, P.; Samson, P. Diet-induced thermogenesis with relation to training state in female subjects. Can. J. Physiol. Pharmacol. 62:334-337; 1984. Leon, A. S.; Conrad, J.; Hunninghake, D. B.; Serfass, R. Effect of vigorous walking program on body composition and carbohydrate and lipid metabolism of obese young men. Am. J. Clin. Nutr. 32: 1776-1787; 1979. Mayer, J.; Roy, P.; Mitra, K. P. Relation between caloric intake, body weight, and physical works in an industrial male population in West Bengal. Am. J. Clin. Nutr. 4:169-171; 1956. Richard, D.; Arnold, J. Influence of exercise training in the regulation of energy balance. J. Obes. Weight Regul. 6:212-224; 1987. Richard, D.; Arnold, J.; Leblanc, J. Energy balance in exercise-trained rats acclimated at two environmental temperatures. J. Appl. Physiol. 60:1054-1059; 1986. Richard, D.; Lachance, P.; Deshaies, Y. Effects of exercise-rest cycles on energy balance in rats. Am. J. Physiol. 256:R886-R891; 1989. Richard, D.; Rivest, S. The role of exercise in thermogenesis and energy balance. Can. J. Physiol. Pharmacol. 67:402-409; 1989. Staten, M. A. The effect of exercise on food intake in men and women. Am. J. Clin. Nutr. 53:27-31; 1991. Thompson, D. A.; Wolfe, L. A.; Eikelboom, R. Acute effects of exercise intensity on appetite in young men. Med. Sci. Sports Exerc. 20:222-227; 1988. Tremblay, A.; Cotr, J.; Leblanc, J. Diminished dietary thermogenesis in exercise-trained human subjects. Eur. J. Appl. Physiol. 52:1-4; 1983. Wainwright, P. E.; Simpson, J. R.; Camaron, R.; Hoffman-Goetz, L.; Winfield, D.; McCutcheon, D.; MacDonald, M. Effects of treadmill exercise on weight cycling in female mice. Physiol. Behav. 49: 639-642; 1991. Wirth, A.; Diehm, C.; Hanel, W.; Welte, J.; Vogel, I. Training-induced changes in serum lipids, fat tolerance, and adipose tissue metabolism in patients with hyperglycerld~emia. Atherosclerosis 54: 265-271; 1985.
0031-9384/92 $5.00+ .00 Copyright© 1992PergamonPressLtd.
Printedin the USA.
Acute, But Not Chronic, Exercise Lowers the Body Weight Set-Point in Male Rats M. C A B A N A C 1 A N D J. M O R R I S S E T T E
Ddpartement de Physiologie, Facult~ de M£decine, UniversitO Laval, QuObec G1K 7P4, Canada Received 4 F e b r u a r y 1992 CABANAC, M. AND J. MORRISSETTE.Acute, but not chronic, exercise lowersthe body weightset-point in male rats. PHYSIOL BEHAV 52(6) 1173-1177, 1992.--The influence of muscular training on overall energy balance and body weight is not clear. A group of male rats was trained to feed every day from 1000 to 1200. Then the intersect of regression line of food hoarded during meal time vs. body weight with the X-axis was measured. Finally, the rats were trained to run 1 h every day on a motor-driven treadmill. When the training took place in the morning, just before the hoarding session, the mean intersect was significantly lowered from control (497 + 18 g to 433 _+9 g). When the training took place in the afternoon, after the hoarding session, the mean intersect was not significantlydifferent (504 _+21 g) from control. Food intake during the hoarding sessionswas affected neither by body weight changes nor by muscular exercise. These results suggest that the set-point for body weight regulation is acutely lowered just after muscular exercise, but is not influenced by chronic training. Energy balance
Hoarding behavior
Food intake
BODY weight is the result of the balance between energy intake and energy expenditure. Increased muscular activity encountered at work and endurance sports can elevate energy requirements considerably. As long as food intake does not compensate for the increased energy expenditure, exercise may induce a negative energy balance and cause some body weight reduction. In 1956, J. Mayer et al. (22) published a study showing that moderate muscular work decreased body weight, and food intake. These results have become controversial in recent years. The amount of body weight loss is quite variable from study to study, probably in relation with the protocols that were used. For example, human subjects lost several kilograms over months of training (12,21). Others did not change their body weight (2,17). Rats chronically (4) or acutely (5) exercised were thus protected against the drop of body weight normally occurring when the animals are switched to 2 h/day feeding, while other trained rats lost 100 g compared to their sedentary controls (25). An attempt at studying the influence of exercise on body weight by doing energy balance measurement is not easily achieved because that involves the chronic measurements of energy intake, energy expenditure, and energy storage. The concept of body weight regulation helps overcome the difficulty. If body weight is regulated, or a correlate of body weight is regulated, then the set-point is the value of body weight that the system achieves by controlling both inflow and outflow of energy. The set-point can be different from the actual body weight, at least during transients. There exists a behavioral open-loop method to measure the body weight set-point in rats. When rats are deprived of food they start to hoard food. The more their body weight drops, the
Body weight set-point
more food they hoard. It has been previously shown that the amount of food a rat hoards is proportional to its body weight loss (3,7-10). The intersect of the regression line of hoarded food vs. body weight with the X-axis is therefore the threshold for a proportional regulatory response opposing the weight deficit and may be used to estimate the body weight set-point in that species. In the present study the influence of both acute and chronic muscular exercise, on the intersect of regression line of hoarded food vs. body weight with the X-axis, i.e., the threshold of the hoarding response, was studied in rats. METHOD
Subjects The subjects were six Long-Evans rats from Charles River Inc. of Canada. We chose male rats because hoarding is especially active in males of that strain (6). The rats were trained to feed once a day from 1000 to 1200 every day for 2 weeks before the beginning of the experiment, then throughout the experiment. Light went on at 0600 h and off at 1800 h.
Housing and Hoarding The rats were housed one in a cage in wire-meshed and steelwalled rabbit cages (0.48 X 0.41 X 0.34 m). In each cage the rat had permanent access to a home (0.24 x 0.19 X 0.10 m) made of a plastic water can painted black, in which a door had been cut to permit passage of the animal. The ambient temperature, an important factor of hoarding behavior in the rat (9), was regulated at 20°C.
xRequests for reprints should be addressed to M. Cabanac. Email: [email protected].
1173
1174
ttoarding measurements took place during the period of time when the animals had access to food. At 1000 h, the front door of the cage was swung open and the rat had access to a tray, 0.35 m from the cage door, containing a large quantity of regular rat chow pellets of unequal size, weighing about 4 g each. For 2 h the rat could feed and carry pellets from the tray to its dark home. At 1200 h the cage door was closed and the food hoarded in the rat's home was removed.
Measuremenl.s The rats were weighed every morning, 7 days a week, prior to the beginning of the other measurements. The amount of food on the tray was weighed before the hoarding session. The food remaining in the tray at the end of the session and the food hoarded by the rat were also weighed. The food eaten by the rat was computed by subtracting remaining and hoarded food from offered food. Repeated control manipulation of rat chow has shown that this procedure entails a negligible error on the missing weight. The number of foraging trips from home to food was counted in rat No. 6 three times per hour for 5 min, at min 5, 25, 45, 65, 85, and 105 of each hoarding session.
Training The rats' muscular exercise was a l-h running on a motordriven treadmill. The training started 59 days after the beginning of the experiment. On the first week of training the speed of the treadmill and the duration of the session were progressively increased up to 50 min at 20 m . min ~and 10 min at 25 m . min ~, which was then maintained daily 7 days a week for 39 days. This procedure was similar to, or slightly higher than, currently used in rats (11).
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increase the rats received additional food just aller the hoardil/g session. l'he amount of tbod thus added was estimated empirically from the influence of supplements on body weight obtained on previous days.
Procedure Alter being trained for 2 weeks to feed once a clay tot 2 h from 1000 to 1200, the control hoarding response was measured for 35 days and the rats' body weight hoarding threshold was calculated. Then the rats were trained to run on the treadmill for 2 weeks, as described above, after which their hoarding response was measured daily and their threshold for hoarding was calculated under two different schedules: A. On even days, the 1-h exercise took place from 0830 to 0930 I1, i.e., just before the hoarding session. This condition will be called acute in the following because this schedule intended to explore the short-term influence of exercise on hoarding threshold. Twelve such sessions took place in fully trained rats. B. On odd days, the l-h exercise took place in the early alternoon, i.e., after the hoarding session. This condition will be called chronic in the following because this schedule intended to explore the hoarding threshold of trained but not tired rats. Fourteen such sessions took place in fully trained rats. RESUt:rs
Hoarding Thresholds Figure 1 shows the amount of food hoarded as a function of body weight in the one rat with the highest slope (rat No. 5). Figures 2 and 3 show the group results, obtained with the mean
Body Weight Threshold[or Hoarding Herberg et al. (13) were the first to relate the rat's hoarding behavior to the extent of displacement of body weight below the set-point. The method used here to assess the value of this threshold was that used previously (3,7-10). For each animal and each condition, the regression line of food hoarded on body weight was computed. The threshold for the hoarding behavior was determined for each animal from the intersect of this regression line with the X-axis. All the individual coefficients of correlation of hoarded amount vs. rat body weight obtained in the control, chronic, and acute conditions were significant below the threshold of 5%, except for rat No. 3 in the acute condition. This rat, therefore, was not included in the calculation of group means in the acute condition.
Body H~ight Manipulations Rats do not hoard food when their body weight is at its setpoint. The method of measuring hoarding threshold therefore implies a drop, then a recovery, of body weight. It took the rats 1 week to get accustomed to the one meal a day procedure. The rats were weighed every morning before the beginning of the hoarding-feeding session. After the 2 weeks necessary to get them used to the new feeding schedule, they had lost enough weight to allow the measurement of their hoarding response. To increase body weigh loss the experimental sessions were occasionally suppressed, so as to skip one day. During the exercise period the rats were having access to food 2 h every day, but they spent too much time hoarding to allow a sufficient food intake for a compensation of their increased energy needs. Therefore, during the training they tended to lose weight. To allow body weight
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parameters of individual regression lines. The results from the chronic sessions, when the training took place in the afternoon, are given in Fig. 2. It can be seen, both on the individual result and on the group result, that the hoarding by fully trained animals in chronic sessions was not different from the hoarding prior to training. Figure 3 shows the results obtained in acute sessions when the training took place just before the hoarding. It can be seen both on the individual result (Fig. 1) and the group result (Fig. 3) that the hoarding was depressed in acute sessions but the mean slope of the regression line remained unchanged in all three conditions, from -8.21 ___1.06 control to -9.8 + 1.20 acute and - 9 . 4 chronic (one-factor ANOVA, F = 0.761, NS). The hoarding threshold in the chronic condition (504 + 21 g) was not significantly different from control (497 + 18 g), but this threshold in the acute condition (433 + 9 g) was significantly lower than both control and chronic conditions (one-factor ANOVA, F = 9.247, p < 0.01) (Fig. 4).
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Foraging Trips Figure 6 presents the mean results of periodic counting of foraging trips in rat No. 6. On the top the two curves show the pooled results from the sessions prior to training separated into two halves, low and high body weight, respectively. At the bottom the two curves show the pooled results from sessions in acute and in chronic conditions. It can be seen that over a session the frequency of foraging trips tended to decrease logarithmically with time. Acute exercise modified the frequency comparatively, to the chronic condition in the same way as high body weight, comparatively, to low body weight.
Figure 5 shows the group means of individual food intakes measured during the daily 2-h hoarding sessions. Under the experimental conditions neither acute exercise nor chronic training
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Thus, the literature does not allow a firm conclusion about the influence of exercise on the body weight set-point, and the direct measurement of the hoarding threshold in the present work is therefore of great interest. The present results show that when the hoarding threshold was measured 19 h after the training session, no lowering of this threshold was obtained. Yet the animals were fully trained. Chronic training was therefore unable to change the set-point of body weight regulation in these male rats, The absence of change of hoarding threshold in trained rats found here confirms the conclusion that long-term animal studies do not show an influence of exercise on energy expenditure and that exercise affects energy balance by increasing expenditure mainly through its intrinsic cost (23).
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Acute Influence o/Exercise
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FIG. 6. Time course of the frequency of foragingtrips by rat No. 6 over the 2-h duration of hoarding sessionduring the control period (top) and trained period (bottom). All the sessionsof the control period were separated into two halves:at low body weight(lean) and at high body weight (heavy). During the trained period, the morning training is the acute condition and the afternoon training is the chronic condition.
DISCUSSION
Influence qf Exercise on Body Weight Set-Point Exercise training increases the energy expenditure; however "the role played by muscular exercise in energy balance" (and thus in the regulation of body weight) "may be more complex than it appears a priori" (26). For example, the food intake of male rats has been shown to decrease after acute exercise (19) and chronic training (1), and energy expenditure of rats has been shown to increase beyond the elevated rate theoretically expected when exercise is performed ( 14,15). Exercise training protected female rats (11) and mice (30) against the influence of weight cycling; i.e., their body weight and food intake remained only slightly changed. The results in humans were also confusing. The influence of exercise training on both food intake and energy expenditure is reflected on long-term energy balance, i.e., body weight. Human subjects lost several kilograms over months of training (12,21 ), whereas others did not change their body weight (2,18). The measurement of food intake showed no decrease for 16 (21) and 18 (31) weeks of training, but dietary thermogenesis was diminished in athletes (20,29). One may speculate about the evolution of body weight setpoint in the experiments briefly reviewed above. Three situations were observed: 1. when food intake and body weight remained stable the setpoint was likely to have remained unchanged:
When exercise took place before the hoarding session, the hoarding threshold was lowered as compared to control. The influence of exercise on body weight and energy balance was therefore acute, in the hours following exercise, but not chronic, since no hoarding threshold change occurred when the training took place in the afternoon, after the hoarding-feeding session. The foraging pattern of rat No. six was similar when underweight in the acute situation and when at normal body weight in the control situation (Fig. 6). Such an influence of exercise lasted only a few h, since it was absent when the rats were tested before running. A lowering of set-point should be accompanied by a decrease of food intake, and an increase of thermogenesis (16). Since the lowering of the hoarding threshold was merely transient, one should expect these responses to occur only in the h following exercise. The amount of food hoarded was smaller when exercise took place before the hoarding-feeding session. One may hypothesize that the decreased hoarding in sessions immediately following exercise might have been caused by mere fatigue. However, fatigue may be rejected as the cause of reduced hoarding for the following reasons: 1) There is some indication that food intake in a meal immediately following a strenuous exercise is diminished, in rats (24) and in humans (17), but not after a moderate exercise (27,28). In the present experiment food intake was not significantly depressed in the acute sessions (Fig. 5). This is an indication that the exercise was not strenuous for the rats. 2) If fatigue were the cause of the reduced hoarding, its influence should show more in undernourished animals that may be expected to be more easily fatigued. That was not the case: the regression line of the amount hoarded remained parallel to the control regression line in all rats (except rat No. 3, which was excluded from the group results for that reason). When undernourished, say at 300 g body weight, the rats hoarded an average 1250 g of food, i.e., much more than when they were not lean, say at 400 g body weight. Finally, a close examination of diet-induced thermogenesis confirmed that the increase of oxygen consumption was only transient in trained rats, which were otherwise energy savers as compared to their sedentary controls (26). Such a transient increase is consistent with the hypothesis of a transient lowering of the set-point just after the running, which was found in the present work. The different effects obtained on body weight set-
SET-POINT AND EXERCISE
1177
point after acute exercise and chronic training are likely to explain the variable results reported in the literature on body weight and food intake after variable experimental and training protocols.
ACKNOWLEDGEMENT This work was supported by Conseil de la Recherche en Sciences Naturelles et en Grnie (N. S. E. R. C.), Canada.
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