Modification of diurnal feeding patterns by palatability

Physiology & Behavior, Vol. 15, pp. 673--677. Pergamon Press and Brain Research PubL, 1975. Printed in the U.S.A.

Modification of Diurnal Feeding Patterns by Palatability J A A K PANKSEPP AND KATHLEEN KROST

Department o f Psychology, Bowling Green State University, Bowling Green OH 43403 (Received 18 December 1974) PANKSEPP, J. AND K. KROST. Modification of diurnal feeding patterns by palatability. PHYSIOL. BEHAV. 15(6) 673-677, 1975. - The normal nocturnal feeding patterns of rats could be changed to a daytime pattern simply by providing a palatable diet during daylight hours. This effect was larger in females than males. The shift in feeding patterns was accompanied by corresponding shifts in diurnal body temperature and water intake rhythms. Running wheel activity remained unmodified. Access to a 0.25 percent saccharin solution as the only fluid source during daylight also produced a shift in the diurnal distribution of fluid intake, but left feeding unmodified. Ventromedial hypothalamic (VMH) lesions eliminated the normal diurnal distribution of feeding but did not modify the shift in feeding patterns resulting from presentation of a more palatable diet during daylight hours. However, sex differences in feeding patterns were abolished by VMH lesions. Feeding

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USUALLY rats eat at night. It seems unlikely that this behavior pattern could have evolved merely as a mechanism to deal with metabolic requirements, since equally effective metabolic processing of nutrients should be possible during daytime. More probably it is an innate behavior pattern which has provided a yet unspecified survival advantage for rodents. Possibly, nocturnal feeding has evolved in response to selective pressures related to sources of food. For instance, it may be an optimal way to cope with vigorous competitors which forage in the same ecological niche during daylight. Alternatively, it may reflect an effective solution for predatory pressures, whether as hunter or hunted. In any case, there is presently no clear evidence that the nocturnal pattern of feeding is a necessary consequence of fluctuating diurnal metabolic states of the animal, even though much evidence exists for diurnal fluctuations in metabolic processes which might subserve in such a capacity [8,9]. From an ecological perspective it certainly seems incongruous that considerable research effort is expended in studying finer and finer events in the feeding patterns o f animals in the hope that momentary physiological states which govern energy intake regulation will be clarified [4,7]. If feeding patterns are largely dictated by environmental constraints, only weak relationships may link ongoing feeding behaviors to underlying metabolic requirements which are ultimately subserved. To determine the degree of potential environmental control over diurnal feeding patterns, a simple question was posed: Will a rat modify its diurnal distribution o f food intake when allowed access to its normal laboratory

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maintenance food during the night but a more palatable food during the day when feeding is normally low? If animals drastically alter their patterns of food intake in response to non-systemic manipulations such as palatability, the value of diurnal feeding patterns as anything more than another reliable species typical behavior pattern could realistically be brought into question. To the contrary, if animals do not modify their feeding patterns reliably in response to gustatory manipulations alone, strong arguments could be made for positions that diurnal feeding patterns are direct and powerful manifestations of either static evolutionary or dynamic physiological imperatives. Since it rapidly became apparent that laboratory rats will readily shift to a daytime feeding pattern in response to palatability, a variety of additional experiments were performed to see how other cyclic processes were concurrently affected - body temperature, drinking, and activity. Further, since ventromedial hypothalamic lesions are known to disrupt both the regulation of food intake and to reduce the diurnal patterning of feeding, diet induced changes in the distribution of feeding were also measured in rats with such brain damage. GENERAL METHOD Mature Sprague Dawley albino (Experiment 1 ) a n d Long-Evans hooded rats (Experiments 2 - 5 ) , 1 0 0 - 1 9 0 days of age, were employed. In all experiments animals were housed tingly in wire-mesh cages, with free access to powdered Purina Laboratory Chow, from spillproof feeding jars, and water from 100 ml graduated drinking tubes

This work was supported by NSF Grant GB-40150 and NIH Grant I RO1 AM 17157-01. Preliminary reports of this research have been presented at the Midwestern Psychological Association, May 2, 1974 and at the Fifth International Conference on the Physiology of Food and Fluid Intake, Jerusalen, Israel, October, 1974. We thank Constance Campbell for useful comments on an earlier form of this manuscript. 673

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except as indicated. Illumination was on a 24 hr lighting cycle with lights on at 9 a.m. and off at 9 p.m. Food intakes (0.1 g) and water intakes (1.0 ml), were measured twice daily at transitions of the lighting periods each morning and evening. In all 5 experiments of this report, baseline measures were obtained, the treatment (high-fat, palatable diet) was introduced for the stated period of time, followed by a posttreatment return to baseline. All statistical comparisons were done using one-tailed tests since it was expected that the high-fat diet would tend to shift feeding into the day part of the illumination cycle. The high-fat diet consisted of 9 parts (by weight) Purina Laboratory Chow, 3 parts Crisco vegetable shortening, 1 part confectioners sugar, and 1 part Hershey's chocolate syrup. The estimated macronutrient content of the Purina chow by weight was 23 percent protein, 5 percent fat, and 60 percent carbohydrate (3.61 KCal/gm), and that of our high-fat diet, 15 percent protein, 23 percent fat, and 53 percent carbohydrate (4.73 KCal/gm).

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After three days of baseline measurements for 12 male rats, half the animals were given access to just the palatable high-fat diet during the day while continuing to receive maintenance chow at night. The remaining animals continued to receive normal lab chow throughout. After 4 days of this dietary access, ordinary lab chow data was collected for 3 additional days. Results

Although presentation of the palatable diet during the daytime increased total daily caloric intake by about 20 percent, the distribution of feeding was more drastically modified (Fig. 1). Whereas these animals consumed more than 60 percent of their food during the night when only powdered laboratory chow was available, they consumed more than 80 percent of their food during daytime when access to the tastier diet was permitted (t = 4.1, d f = 5, p<0.005). During the posttreatment period, the distribution of feeding did not immediately return to pretreatment levels. Also, the control animals showed a marked dimunition of their circadian rhythm. These effects are probably due to the use of a relatively old group of males (approx. 1 8 0 - 1 9 0 days) - animals which are known to exhibit relatively poor diurnal cycling of feeding behavior.

FIG. 1. Day/Night food intake ratios before, during, and after 4 experimental days when the palatable high fat diet was available during daytime. Results

During access to the high-fat diet during daytime, there was both an increase in daily food intake and a shift to predominantly daytime feeding. Daily caloric intake of female rats increased from a baseline level of 50.5 (-+ 3.6) C to 88.4 (-+ 18.1) C/day (t = 27.9, d f = 4, p<0.001), and food intake of males increased from 82.0 (+ 10.2) C to 120.4 (+ 13.8) C/day (t = 10.4, d f = 4, p<0.001). Diurnal distribution of feeding is summarized in Fig. 2, and it is clear that female rats exhibited a larger shift in diurnal intakes than male rats (t = 1.78, d f = 13, p<0.05). During baseline days, when all animals were consuming approximately 80 percent of their food at night, the rectal temperature was higher at the start of the dark cycle than at the start of the light cycle. During the dietary manipulation, when feeding shifted to daylight hours, diurnal body temperature differences were reliably attenuated in both males (t = 4.78, d f = 5, p<0.005) and females (t = 7.07, d f = 7, p<0.001). The return of maintenance chow was followed by accentuation of the diurnal patterns of body temperature (Fig. 3). EXPERIMENT

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This experiment tested whether males and females react differently to a palatability change in daytime food. Body temperatures were also monitored to determine if changes in feeding would be accompanied by shifts in diurnal body temperature rhythm. Six males and 8 females were allowed free access to ordinary chow for 6 days, followed by 6 days access to the palatable diet during daytime, and then an additional 6 day posttreatment period. Rectal temperatures were recorded twice daily (9 a.m. and 9 p.m.) to 0.1°C throughout the experiment with a thermocouple (Baily Inst. Co., Model BAT-4). Temperatures were recorded after the thermistor reading had been stable for 30 sec.

In the following experiment we determined whether palatability induced changes in the distribution of feeding would also modify other rhythmic behaviors such as drinking and activity. Six female rats were singly housed in running wheel activity cages (Wahman LC-34) throughout the experiment. Food intakes, water intakes, and activity wheel revolutions were monitored at 12 hr intervals. After the baseline period, the palatable diet was presented during daytime for 5 days to 3 animals and for 3 days to the other three. Results

Figure 4 presents the data for the 3 animals which received the dietary treatment for five days. The data of the

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It is now a common observation that damage to ventromedial hypothalamic areas which produces hyperphagia also tends to reduce the difference between amounts of food consumed during the day and night [1,3]. Accordingly it was of interest to determine whether this manipulation would modify the degree to which palatability factors affected the diurnal distribution of feeding. Also, since ventromedial hypothalamic lesions tend to reduce the quantitative feeding differences between male and female rats [6,13], we also determined whether the sex difference observed with the palatability manipulation (Experiment 2) would be reduced. Procedu re

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other 3 animals was essentially identical. Statistics for all animals during the first 3 days of treatment indicated that both the distribution of feeding (t = 4.05, d f = 5, p<0.01) and drinking (t = 2.78, d.f = 5, p<0.05) were changed by the treatment while the distribution of running in the activity wheel remained unmodified. EXPERIMENT 4 Clearly, the diurnal distribution of water intake appears to be strongly coupled to the diurnal distribution of feeding. In the following experiment, we determined whether this is a symmetrical relationship. A 0.25 percent saccharin solution was presented to 7 male rats during the daytime. As indicated in Fig. 5, this manipulation effectively modified the diurnal distribution of fluid consumption (t = 1.98, d f = 6, p
Bilateral electrolytic lesions of the ventromedial hypothalamus were administered to five female and five male rats as described elsewhere [11]. Lesioning current was 1 - 2 mA for 2 0 - 3 0 sec through a stainless steel pin with 0.75 mm tip exposure. Prior to lesioning, all animals (5 males, 5 females) were tested for dietary reversal of feeding patterns for 6 days. Twelve days after administration of lesions, all animals were again tested for 6 days with the palatable high fat diet presented during daytime. Results The results for this experiment are summarized in Fig. 6. Prior to being lesioned, females again exhibited a larger shift in diurnal distribution of feeding than males. Bilateral damage to the ventromedial hypothalamus eliminated the normal nocturnal feeding pattern in both males and females. The effect of presenting palatable food during the daytime was still intact, except that the sex difference was abolished. A sex difference was observed in the magnitude of hyperphagia produced by these lesions. For females the average dally food intakes for the 6 day prelesion period was 12.9 g and increased to 29.6 g following lesioning (Days 1 9 - 2 6 ) and to 44.0 g during presentation of the palatable daytime diet. The coresponding values for males were 23.9, 29.8, and 40.2 g. It should be noted that the increase in day/night feeding ratios for the lesioned animals was due almost exclusively to an increase in daytime

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PANKSEPP AND KROST intakes, with only a small (11 percent) decrease in nighttime feeding. Prior to the lesions, the nighttime reduction in feeding was 36 percent during the high-fat diet. Also, upon restoration of the laboratory chow after the high-fat diet, lesioned animals exhibited a marked hysteresis in their intake pattern - continuing to consume most of their food during the day. Although a tendency for such an effect was observed in the animals of Experiment 1, it was never observed in subsequent experiments including the prelesion data of the animals in this experiment.

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Rats will reverse their normal nocturnal feeding pattern if access to a tastier food is premitted during periods when feeding is normally low. Thus, if given the option, a rat will distribute its feeding almost exclusively by taste, lending credence to the proposition that taste should be viewed as a primary construct in the control of feeding. It remains to be determined how small a dietary change can yield the effect, but the power of the phenomenon in these experiments suggests that a relatively minor change may

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PALATABILITY AND FEEDING PATTERN

677

suffice. Alternatively, however, it could be argued that the shift of feeding into daylight hours reflected the operation of some subtle type of metabolic homeostasis such as an attempt to dilute the somewhat high protein content (23 percent) of the Purina chow to a more desirable level by consumption of the relatively protein dilute (15 percent) high-fat diet. But this is unlikely not only from the rapidity of the dietary reversal of diurnal feeding patterns, but also from the fact that during the high-fat diet daily protein intake actually increased by 28 percent in females and 14 percent in males (data from Experiment 2). The existence of palatability induced reversals in periods of daily hyperphagia raises questions concerning the productiveness of detailed analyses of feeding patterns in attempting to unravel the underlying metabolic causes of feeding. Although it is clear that the metabolic effects of food are normally expressed systematically in ongoing feeding behavior at one level of analysis [ 12], there is no assurance that this control will be patently manifest at the level of individual meals and intermeal intervals. As argued by Collier and colleagues [4] the detailed patterning of feeding may be largely a behavioral strategy which copes nicely with available food sources. Environmental variables may ultimately provide more potent constraints over feeding patterns than physiological factors. Conversely, physiological factors may guide the total amount of food ingested during a day more than environmental ones. The present results would also pose problems for theories which would attempt to explain feeding patterns purely in terms of rigid evolutionary principles. If nocturnal feeding is a vigorous innate behavior pattern of rats, then it should tend to remain relatively unmodified by exteroceptire sensory manipulations. Not only does the ability of simple dietary manipulations to reverse feeding patterns raise difficulties for the vigor if not the existence of certain types of feeding controls, but the technique also provides a simple method

for analyzing the intercouplings of various rhythmic behaviors and physiological processes. It is clear from the present data that diurnal fluctuation of food intake may be a major cause of the diurnal body temperature rhythm. When feeding shifts, temperature also shifts. Similarly, drinking appears to be strongly coupled to feeding while activity does not. Although without electroencephalographic monitoring no definitive conclusion can be reached, the absence of changes in locomotory rhythms probably indicates that basic sleep-waking activity was not modified by reversal of the feeding pattern. Although the drinking rhythm tends to remain coupled to ongoing feeding, the converse did not occur. Change in drinking rhythms produced by permitting access to a sweet saccharin solution during the day led to no redistribution of feeding. Although this does suggest that drinking m a y b e more strongly coupled to feeding than feeding is to drinking, the difficulties which attend such cross-modality scalings prevent any definitive conclusions. I n summary, these experiments explored the limits of voluntary nocturnal feeding behavior in rodents. The demonstration of palatability induced reversal of feeding rhythms contributes to the growing list of environmental manipulations which are capable of changing the normal diurnal distribution of behavior in rats. Previous studies have indicated that under proper illumination intensities, activity of rats will entrain to a 48 hr day [5] and that feeding, drinking, and activity will entrain even to a 2 hr day [2]. The present study demonstrates that the distribution of behavior can be completely reversed within a normal 24 hr day, indicating that cyclic internal processes of rats do not invariable mandate a nocturnal feeding pattern when acceptable food is freely available throughout the day. Furthermore, the technique employed herein may prove to be a powerful tool for separating fundamental physiological and behavioral rhythms from those which are secondary consequences of feeding behavior.

REFERENCES 1. Balagura, S. and L. D. Devenport. Feeding patterns of normal and ventr0medial hypothalamic lesioned male and female rats. Z comp. physiol. Psychol. 71: 357-364, 1970. 2. Borb61y, A. A. and J. P. Huston. Effects of two-hour light-dark cycles on feeding, drinking, and motor activity of the rat. Physiol. Behav. 13: 795-802, 1974. 3. Brooks, C., R. A. Lockwood and M. L. Wiggins.A study of the effect of hypothalamic lesions on the eating habits of the albino rat. Am. J. Physiol. 147: 735-742, 1946. 4. Collier, G., E. Hirsch and P. H. Hamlin. The ecological determinants of reinforcement in the rat. Physiol. Behav. 9: 705-716, 1972. 5. Goff, M. L. R. and F. W. Fingers. Activity rhythms and a diurnal light-dark control. Science 154: 1346-1348, 1966. 6. Gold, R. M. Hypothalamic hyperphagia: males get just as fat as females. J. comp. physiol. Psychol. 71: 347-356, 1970. 7. Hirsch, E. Some determinants of intake and patterns of feeding in the guinea pig. Physiol. Behav. 11: 687-704, 1973.

8. LeMagnen, J. and M. Devos. Metabolic correlates of the meal onset in the free food intake of rats. Physiol. Behav. 5: 805-814, 1970. 9. LeMagnen, J., M. Devos, J.-P. Gaudilliere, J. Louis-Sylvestre, and S. Tallon. Tolr og lipostatic mechanism in regulation by feeding of energy balance in rats. J. comp. physiol. Psychol. 84: 1-23, 1973. 10. Panksepp, J. A re-examination of the role of the ventromedial hypothalamus in feeding behavior. Physiol. Behav. 7: 385-394, 1971. 11. Panksepp, J. Reanalysis of feeding patterns in the rat. J. comp. physiol. Psychol. 82: 78-94, 1973. 12. Panksepp, J. and M. Ritter. Mathematical analysis of energy regulatory patterns of normal and diabetic rats. J. comp. physiol. Psychol., 1975. 13. Valenstein, E. D., V. C. Cox, and J. W. Kakolewski. Sex differences in hyperphagia and body weight following hypothalamic damage. Ann. N.Y. Acad. ScL 157: 1030-1048, 1969.