- Email: [email protected]
Weight gain in postweaned rats as a function of predictable and unpredictable feeding schedules
Physiology&Behavior,Vol. 40, pp. 287-289. Copyright©PergamonJournals Ltd., 1987.Printed in the U.S.A.
0031-9384/87$3.00 + .00
Weight Gain in Postweaned Rats as a Function of Predictable and Unpredictable Feeding Schedules R O N A L D R. U L M , J O S E P H R. V O L P I C E L L I , 1 ROBERT CERPA AND KEITH MclNTYRE
Department of Psychology, Salisbury State College, Salisbury, MD 21801 and Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104 R e c e i v e d 25 A u g u s t 1986 ULM, R. R., J. R. VOLPICELLI, R. CERPA AND K. MclNTYRE. Weightgain in postweaned rats as a function of predictable and unpredictablefeeding schedules. PHYSIOL BEHAV 40(3) 287-289, 1987.--In two experiments rats given unpredictable feeding schedules gained less weight over a 24 or 30 day training period than rats which consumed an equivalent amount of food on a predictable schedule. These results suggest that irregular feeding schedules disrupt food utilization. Feeding schedules
Unpredictable events
Stress
U N P R E D I C T A B L E aversive events have been associated with a variety of behavioral and physiological indices often associated with "stress" responses in animals and humans. Exposure to equivalent amounts of predictable events, in contrast, does not lead to these deleterious effects. So, for example, unpredictable shocks are associated with higher levels of corticosterone [12,13], more severe stomach ulceration [2, 9, l 1, 13], greater weight loss [12], myocardial dysfunction [5] and disruption of instrumental responding [1, 3, 4, 10]. Other aversive events, such as unpredictable restraint, are associated with alterations in plasma levels of corticosterone, glucose, and free fatty acids [8]. While the investigation of unpredictable aversive events have been systematically studied, investigations of the effects of unpredictable appetitive events have received far less attention. One exception is Welker, Garber and Brooks [14], who found that unpredictable feeding schedules were associated with more weight loss, glandular lesions, and death relative to regular feedings. In this study, we further investigate the effects of unpredictable feeding schedules on weight change. In the Welker, Garber and Brooks [14] experiment, both the timing of food presentations and duration of access to food were varied for the unpredictable group. Thus the effects of predictable and unpredictable food presentations is confounded by the unpredictable duration of access to food. Since the unpredictable group tended to eat less food overall during training periods, it is not surprising that they lost more weight. It is unclear, however, whether weight loss in the unpredictable feeding groups was due to disruption of food utilization
caused by the unpredictable feeding schedule, as suggested by Welker, Garber and Brooks [14], or simply reflected less caloric intake. In our study, all animals are fed the same amount of food and only the timing of food presentations is varied. Thus, any differences in weight can be attributed to the unpredictability of food presentations per se, and not simply to differences in caloric intake. In addition, our deprivation schedule was utilized in growing postweaned animals which continued to gain weight in the course of the experiment. EXPERIMENT 1 METHOD
Subjects The subjects were 24 male Sprague-Dawley rats obtained at 21 days old from Dominion Labs, Dublin, VA. The animals were individually housed, allowed free access to water, and maintained on a 16/8 light/dark cycle (lights on at 7:30 a.m.). This experiment was conducted at Salisbury State College.
Procedure Following a 7 day training baseline period during which animals were given ad lib access to Purina lab chow, the subjects were randomly divided into two groups of 12 subjects. The predictable (P) group was fed 15 grams of lab chow at 3:30 p.m. just following the daily weighing. The unpredict-
1Requests for reprints should be addressed to Joseph R. Volpicelli M.D., Ph.D., Department of Psychology, 3815 Walnut St., Philadelphia, PA 19104.
287
288
ULM, V O L P I C E L L I . CERPA AND McINTYRE
able (UP) group was also weighed at 3:30 daily, but was fed 15 grams once a day during the light part of each cycle but on a random schedule which occurred anytime between the hours of 7:30 a.m. and 11:30 p.m. The feeding intervals varied from 16 to 33 hours with an average intermeal interval of 24 hr. On Day 29 of this training schedule, all rats were weighed and given food at 3:30 p.m. Then on Day 30, test weight was measured at 3:30 p.m. At this point all rats were given free access to food. RESULTS Mean weights at the start of the experiment for the P and UP groups were comparable (76.9 g and 82.7 g, respectively). During the 30 day feeding schedule, however, the P group gained an average of 86.3 g (SD=5.7 g), whereas the UP group gained only 56.0 g (SD= 15.14 g). t-Test comparisons revealed that the P group gained reliably more weight during the 30 day feeding period, t(22)=6.49, p<0.001. The results of Experiment 1 clearly demonstrate that the effects of unpredictable feeding schedules produce less weight gain relative to predictable feeding even when amount of food consumed during the training is held constant. EXPERIMENT 2 The next study attempted to replicate the difference in weight gain in the UP and P schedules of Experiment 1 in another laboratory. METHOD Subjects
Sixteen male Sprague-Dawley rats were obtained from Holtzman, Company, Madison, WI, The animals were received just after weaning at approximately 21 days of age and were housed in a single colony room in a 14/10 hr light/dark cycle (lights on at 8 a.m.). This experiment was conducted at the University of Pennsylvania. During the treatment phase the P group received one feeding every 24 hours predictably at 6 p.m. The UP group was fed randomly during the light part of the cycle with intermeal intervals varying from 15 to 34 hours with a mean of 24 hr. Both groups received equal amounts of food, 14.5 g per feeding, and had free access to water throughout the study. Procedure
All rats were group housed and given free access to food and water for seven days prior to the initiation of the experiment. At age 28 days subjects were divided into two groups of eight animals each and food deprived for 24 hours. During the next 24 days subjects were individually housed and maintained on their respective feeding schedules. All animals were weighed daily between 6:00 and 6:30 p.m. On day 24, both groups were fed at 6 p.m. and were weighed 24 hours later. RESULTS As found in the first experiment, rats fed on an unpredictable schedule gained less weight than rats fed the same amount of food, but on a predictable schedule. On day one of the treatment phase there were no reliable differences in the two groups but by day 24 the UP group gained less weight
than the predictable group. The mean weight gain in the U P group was 77.0 g, (SD=4.39 g) and the mean weight gain in the P group was 87.6 g, (SD=6.36 g); t(14)=3.464, p<0.01. G E N E R A L DISCUSSION These experiments demonstrate in two different laboratories that rats fed in an unpredictable manner gain less weight than regularly fed rats, despite equivalent food consumption. Although possible, it is unlikely that the rats in the unpredictable feeding group differentially spilled more food. This is unlikely since all rats were observed to eat all their daily allotment of food immediately upon feeding. Since animals consumed equivalent amounts of food, the results are consistent with two possibilities: (1) unpredictably fed rats absorbed their food source less efficiently, or (2) they expended more calories. The results support Welker, Garber and Brooks [14] suggestion that unpredictable feeding schedules disrupt food utilization more than predictable schedules, even when total amount of food consumed is held constant. The unpredictably fed rats may have absorbed food less efficiently because of the timing of their meals relative to the light-dark cycle. For example, it has been demonstrated in both rodents [6] and fish [7] that meals which occur later in the light part of the light-dark cycle lead to less weight gain when food consumption is held constant. In Experiment 1. the predictably fed rats received meals at the midpoint of their light-dark cycle, whereas the unpredictably fed rats received meals both early and late in the cycle, thus perhaps biasing the results toward less weight gain in the irregularly ted subjects. This explanation cannot account for the results of Experiment 2, however, since predictably fed rats received their meals late in the cycle thus biasing the results aL,ainxt the predictably fed rats. Since predictable fed rats gain more weight even when food access is limited to the late part of the light-dark cycle, meal timing relative to the lightdark cycle cannot easily account for these results. A second possible explanation is that rats could prepare themselves lbr food presentations by timing physiological processes to coincide with food delivery. Since the predictably fed rats ate at the same time each day immediately after being weighed, conditioned physiological changes (i.e., insulin release) could be entrained to underlying circadian rhythms or be elicited to the external stimulus of being weighed. While this experiment cannot distinguish between these two possibilities, either mechanism could permit food to be more effectively absorbed. Clearly insulin release can be conditioned to external stimuli 115] and insulin release can promote intracellular transport of glucose and anabolic processes. Finally, a third possible explanation is that unpredictably fed rats metabolized calories at a faster rate than predictably fed rats. If unpredictable feedings are more stressful than regular feeding as demonstrated by the higher incidence of ulceration and death found by Welker, Garber and Brooks [14], then the increased stress may elicit more activity or higher metabolic rats. In this way, while differences in food absorption may not occur, the unpredictable feedings may promote faster food utilization. In general, these results replicate and extend an important finding of Welker, Garber and Brooks [14] and suggest that the regularity of feeding schedules may have important metabolic effects.
UNPREDICTABLE
FEEDING SCHEDULES
289
REFERENCES 1. Azrin, N. H. Some effects of two intermittent schedules of immediate and non-immediate punishment. J Psychol 142: 3-21, 1956. 2. Caul, W. F., D. C. Buchanan and R. C. Hays. Effects of unpredictability of shock on incidence of gastric lesions and heart rate in immobilized rats. Physiol Behav 8: 669-672, 1972. 3. Hymovitz, N. Comparisons between variable-interval and fixed-interval schedules of electric shock delivery. J Exp Anal Behav 19:101-111, 1973. 4. lmada, H. and M. Okamura. Some cues rats can use as predictors of danger and safety. Anita Learn Behav 3: 221-225, 1975. 5. Miller, D. G., Z. D. Grossman, R. L. Richardson, B. W. Wistow and F. D. Thomas. Effect of signaled versus unsignaled stress on rat myocardium. Psychosom Med 40: 432-434, 1978. 6. Nelson, W., L. Scheving and F. Halberg. Circadian rhythms in mice fed a single daily meal at different stages of the lighting regimen. J Nutr 105: 171-184, 1975. 7. Noeske-Hallin, T. A., R. E. Spieler, N. C. Parker and M. A. Suttle. Feeding time differentially affects fattening and growth of channel catfish. J Nutr 115: 1228--1232, 1985.
8. Quirce, C. M., M. Odio and J. M. Solano. The effects of predictable and unpredictable schedules of physical restraint upon rats. Life Sci 28: 1897-1902, 1981. 9. Sawrey, W. L. Conditioned responses of fear in relationship to ulceration. J Comp Physiol Psychol 54: 347-348, 1961. 10. Seligman, M. E. P. Chronic fear produced by unpredictable electric shock. J Comp Physiol Psychol 66: 402-411, 1968. 11. Seligman, M. E. P. and B. Meyer. Chronic fear and ulcers in rats as a function of unpredictability of safety. J Comp Physiol Psychol 73: 202-207, 1970. 12. Weiss, J. M. Somatic effects of predictable and unpredictable shock. Psychosom Med 32: 397-408, 1970. 13. Weiss, J. M. Effects of coping behavior in different warning signal conditions on stress pathology in rats. J Comp Physiol Psychol 77: 1-13, 1971. 14. Welker, R. L., J. Garber and F. Brooks. Stress as a function of irregular feeding of food deprived rats. Physiol Behav 18: 639645, 1977. 15. Woods, S. C., R. A. Hutton and W. Makous. Conditioned insulin secretion in the albino rat. Proc Soc Exp Biol Med 133: 964-968, 1970.
0031-9384/87$3.00 + .00
Weight Gain in Postweaned Rats as a Function of Predictable and Unpredictable Feeding Schedules R O N A L D R. U L M , J O S E P H R. V O L P I C E L L I , 1 ROBERT CERPA AND KEITH MclNTYRE
Department of Psychology, Salisbury State College, Salisbury, MD 21801 and Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104 R e c e i v e d 25 A u g u s t 1986 ULM, R. R., J. R. VOLPICELLI, R. CERPA AND K. MclNTYRE. Weightgain in postweaned rats as a function of predictable and unpredictablefeeding schedules. PHYSIOL BEHAV 40(3) 287-289, 1987.--In two experiments rats given unpredictable feeding schedules gained less weight over a 24 or 30 day training period than rats which consumed an equivalent amount of food on a predictable schedule. These results suggest that irregular feeding schedules disrupt food utilization. Feeding schedules
Unpredictable events
Stress
U N P R E D I C T A B L E aversive events have been associated with a variety of behavioral and physiological indices often associated with "stress" responses in animals and humans. Exposure to equivalent amounts of predictable events, in contrast, does not lead to these deleterious effects. So, for example, unpredictable shocks are associated with higher levels of corticosterone [12,13], more severe stomach ulceration [2, 9, l 1, 13], greater weight loss [12], myocardial dysfunction [5] and disruption of instrumental responding [1, 3, 4, 10]. Other aversive events, such as unpredictable restraint, are associated with alterations in plasma levels of corticosterone, glucose, and free fatty acids [8]. While the investigation of unpredictable aversive events have been systematically studied, investigations of the effects of unpredictable appetitive events have received far less attention. One exception is Welker, Garber and Brooks [14], who found that unpredictable feeding schedules were associated with more weight loss, glandular lesions, and death relative to regular feedings. In this study, we further investigate the effects of unpredictable feeding schedules on weight change. In the Welker, Garber and Brooks [14] experiment, both the timing of food presentations and duration of access to food were varied for the unpredictable group. Thus the effects of predictable and unpredictable food presentations is confounded by the unpredictable duration of access to food. Since the unpredictable group tended to eat less food overall during training periods, it is not surprising that they lost more weight. It is unclear, however, whether weight loss in the unpredictable feeding groups was due to disruption of food utilization
caused by the unpredictable feeding schedule, as suggested by Welker, Garber and Brooks [14], or simply reflected less caloric intake. In our study, all animals are fed the same amount of food and only the timing of food presentations is varied. Thus, any differences in weight can be attributed to the unpredictability of food presentations per se, and not simply to differences in caloric intake. In addition, our deprivation schedule was utilized in growing postweaned animals which continued to gain weight in the course of the experiment. EXPERIMENT 1 METHOD
Subjects The subjects were 24 male Sprague-Dawley rats obtained at 21 days old from Dominion Labs, Dublin, VA. The animals were individually housed, allowed free access to water, and maintained on a 16/8 light/dark cycle (lights on at 7:30 a.m.). This experiment was conducted at Salisbury State College.
Procedure Following a 7 day training baseline period during which animals were given ad lib access to Purina lab chow, the subjects were randomly divided into two groups of 12 subjects. The predictable (P) group was fed 15 grams of lab chow at 3:30 p.m. just following the daily weighing. The unpredict-
1Requests for reprints should be addressed to Joseph R. Volpicelli M.D., Ph.D., Department of Psychology, 3815 Walnut St., Philadelphia, PA 19104.
287
288
ULM, V O L P I C E L L I . CERPA AND McINTYRE
able (UP) group was also weighed at 3:30 daily, but was fed 15 grams once a day during the light part of each cycle but on a random schedule which occurred anytime between the hours of 7:30 a.m. and 11:30 p.m. The feeding intervals varied from 16 to 33 hours with an average intermeal interval of 24 hr. On Day 29 of this training schedule, all rats were weighed and given food at 3:30 p.m. Then on Day 30, test weight was measured at 3:30 p.m. At this point all rats were given free access to food. RESULTS Mean weights at the start of the experiment for the P and UP groups were comparable (76.9 g and 82.7 g, respectively). During the 30 day feeding schedule, however, the P group gained an average of 86.3 g (SD=5.7 g), whereas the UP group gained only 56.0 g (SD= 15.14 g). t-Test comparisons revealed that the P group gained reliably more weight during the 30 day feeding period, t(22)=6.49, p<0.001. The results of Experiment 1 clearly demonstrate that the effects of unpredictable feeding schedules produce less weight gain relative to predictable feeding even when amount of food consumed during the training is held constant. EXPERIMENT 2 The next study attempted to replicate the difference in weight gain in the UP and P schedules of Experiment 1 in another laboratory. METHOD Subjects
Sixteen male Sprague-Dawley rats were obtained from Holtzman, Company, Madison, WI, The animals were received just after weaning at approximately 21 days of age and were housed in a single colony room in a 14/10 hr light/dark cycle (lights on at 8 a.m.). This experiment was conducted at the University of Pennsylvania. During the treatment phase the P group received one feeding every 24 hours predictably at 6 p.m. The UP group was fed randomly during the light part of the cycle with intermeal intervals varying from 15 to 34 hours with a mean of 24 hr. Both groups received equal amounts of food, 14.5 g per feeding, and had free access to water throughout the study. Procedure
All rats were group housed and given free access to food and water for seven days prior to the initiation of the experiment. At age 28 days subjects were divided into two groups of eight animals each and food deprived for 24 hours. During the next 24 days subjects were individually housed and maintained on their respective feeding schedules. All animals were weighed daily between 6:00 and 6:30 p.m. On day 24, both groups were fed at 6 p.m. and were weighed 24 hours later. RESULTS As found in the first experiment, rats fed on an unpredictable schedule gained less weight than rats fed the same amount of food, but on a predictable schedule. On day one of the treatment phase there were no reliable differences in the two groups but by day 24 the UP group gained less weight
than the predictable group. The mean weight gain in the U P group was 77.0 g, (SD=4.39 g) and the mean weight gain in the P group was 87.6 g, (SD=6.36 g); t(14)=3.464, p<0.01. G E N E R A L DISCUSSION These experiments demonstrate in two different laboratories that rats fed in an unpredictable manner gain less weight than regularly fed rats, despite equivalent food consumption. Although possible, it is unlikely that the rats in the unpredictable feeding group differentially spilled more food. This is unlikely since all rats were observed to eat all their daily allotment of food immediately upon feeding. Since animals consumed equivalent amounts of food, the results are consistent with two possibilities: (1) unpredictably fed rats absorbed their food source less efficiently, or (2) they expended more calories. The results support Welker, Garber and Brooks [14] suggestion that unpredictable feeding schedules disrupt food utilization more than predictable schedules, even when total amount of food consumed is held constant. The unpredictably fed rats may have absorbed food less efficiently because of the timing of their meals relative to the light-dark cycle. For example, it has been demonstrated in both rodents [6] and fish [7] that meals which occur later in the light part of the light-dark cycle lead to less weight gain when food consumption is held constant. In Experiment 1. the predictably fed rats received meals at the midpoint of their light-dark cycle, whereas the unpredictably fed rats received meals both early and late in the cycle, thus perhaps biasing the results toward less weight gain in the irregularly ted subjects. This explanation cannot account for the results of Experiment 2, however, since predictably fed rats received their meals late in the cycle thus biasing the results aL,ainxt the predictably fed rats. Since predictable fed rats gain more weight even when food access is limited to the late part of the light-dark cycle, meal timing relative to the lightdark cycle cannot easily account for these results. A second possible explanation is that rats could prepare themselves lbr food presentations by timing physiological processes to coincide with food delivery. Since the predictably fed rats ate at the same time each day immediately after being weighed, conditioned physiological changes (i.e., insulin release) could be entrained to underlying circadian rhythms or be elicited to the external stimulus of being weighed. While this experiment cannot distinguish between these two possibilities, either mechanism could permit food to be more effectively absorbed. Clearly insulin release can be conditioned to external stimuli 115] and insulin release can promote intracellular transport of glucose and anabolic processes. Finally, a third possible explanation is that unpredictably fed rats metabolized calories at a faster rate than predictably fed rats. If unpredictable feedings are more stressful than regular feeding as demonstrated by the higher incidence of ulceration and death found by Welker, Garber and Brooks [14], then the increased stress may elicit more activity or higher metabolic rats. In this way, while differences in food absorption may not occur, the unpredictable feedings may promote faster food utilization. In general, these results replicate and extend an important finding of Welker, Garber and Brooks [14] and suggest that the regularity of feeding schedules may have important metabolic effects.
UNPREDICTABLE
FEEDING SCHEDULES
289
REFERENCES 1. Azrin, N. H. Some effects of two intermittent schedules of immediate and non-immediate punishment. J Psychol 142: 3-21, 1956. 2. Caul, W. F., D. C. Buchanan and R. C. Hays. Effects of unpredictability of shock on incidence of gastric lesions and heart rate in immobilized rats. Physiol Behav 8: 669-672, 1972. 3. Hymovitz, N. Comparisons between variable-interval and fixed-interval schedules of electric shock delivery. J Exp Anal Behav 19:101-111, 1973. 4. lmada, H. and M. Okamura. Some cues rats can use as predictors of danger and safety. Anita Learn Behav 3: 221-225, 1975. 5. Miller, D. G., Z. D. Grossman, R. L. Richardson, B. W. Wistow and F. D. Thomas. Effect of signaled versus unsignaled stress on rat myocardium. Psychosom Med 40: 432-434, 1978. 6. Nelson, W., L. Scheving and F. Halberg. Circadian rhythms in mice fed a single daily meal at different stages of the lighting regimen. J Nutr 105: 171-184, 1975. 7. Noeske-Hallin, T. A., R. E. Spieler, N. C. Parker and M. A. Suttle. Feeding time differentially affects fattening and growth of channel catfish. J Nutr 115: 1228--1232, 1985.
8. Quirce, C. M., M. Odio and J. M. Solano. The effects of predictable and unpredictable schedules of physical restraint upon rats. Life Sci 28: 1897-1902, 1981. 9. Sawrey, W. L. Conditioned responses of fear in relationship to ulceration. J Comp Physiol Psychol 54: 347-348, 1961. 10. Seligman, M. E. P. Chronic fear produced by unpredictable electric shock. J Comp Physiol Psychol 66: 402-411, 1968. 11. Seligman, M. E. P. and B. Meyer. Chronic fear and ulcers in rats as a function of unpredictability of safety. J Comp Physiol Psychol 73: 202-207, 1970. 12. Weiss, J. M. Somatic effects of predictable and unpredictable shock. Psychosom Med 32: 397-408, 1970. 13. Weiss, J. M. Effects of coping behavior in different warning signal conditions on stress pathology in rats. J Comp Physiol Psychol 77: 1-13, 1971. 14. Welker, R. L., J. Garber and F. Brooks. Stress as a function of irregular feeding of food deprived rats. Physiol Behav 18: 639645, 1977. 15. Woods, S. C., R. A. Hutton and W. Makous. Conditioned insulin secretion in the albino rat. Proc Soc Exp Biol Med 133: 964-968, 1970.