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Sham-Feeding response of rats to polycose and sucrose
Neuroscience & Biohehavioral Reviews, Vol. I1, pp. 215-222..c Pergamon Journals Ltd., 1987. Printed in the U.S.A.
0149-7634/87 $3.00 + .00
Sham-Feeding Response of Rats to Polycose and Sucrose JEFFREY
W. N I S S E N B A U M
AND ANTHONY
SCLAFANI
z
D e p a r t m e n t o f Psychology, Brooklyn College and the Graduate School o f the City UniversiO, o f N e w York Brooklyn, N Y 11210 Received
17 M a r c h 1986
NISSENBAUM, J. W. AND A. SCLAFANi. Sham-feeding response oJ" rats to Polycose and sucrose. NEUROSC! BIOBEHAV REV 11(2) 215-222, 1987.--Adult female rats were fitted with gastric fistulas and maintained at 85% of their ad lib body weight. Their real-feeding (fistula closed) and sham-feeding (fistula open) responses to polysaccharide (Polycose) and sucrose solutions were measured during 30 min/day one-bottle tests. The rats consumed similar amounts of a 1% Polycose solution during real- and sham-feeding tests, but their sham-intakes of 4%, 16% and 32~ Polycose solutions greatly exceeded their real-intakes of these solutions. Similar results were obtained with sucrose solutions. The rats sham-fed more Polycose than sucrose at the 1% and 4% concentrations, while their sham-intakes of the 16% and 32% Polycose and sucrose solutions were comparable. In subsequent two-solution sham-feeding tests, the rats preferred I% Polycose to I% sucrose, but preferred sucrose to Polycose at 4%, 16% and 32% concentrations. These preference results indicate that rats find Polycose more palatable than sucrose at low concentrations, but sucrose more palatable at high concentrations. In addition, the findings that the rats preferred 4% sucrose to 4% Polycose in the two-bottle test, but sham-fed more 4% Polycose than 4% sucrose in the one-bottle tests, suggest that sucrose is more "orally-satiating" than is Polycose. These results provide further evidence for qualitative differences in the tastes of sucrose and polysaccharide. They also indicate that the amount of solution sham-fed does not necessarily reflect the palatability of the solution. Polysaccharide taste
Sweet taste
Palatability
Oral satiety
Gastric sham-feeding
gested can be taken as a measure of the animal's hedonic response to the tastant. Using sucrose again as an example, the amount of sucrose solution sham-fed increases monotonically as concentration increases [3, 5, 21]. In a previous study in this series the gastric sham-feeding technique was used to determine the role of orosensory factors in the rat's appetite for polysaccharide solutions (Polycose) [14]. The finding of that study that rats sham-fed substantial amounts of a 32% Polycose solution provided the first e v i d e n c e that rats are attracted to the taste of polysaccharides. S u b s e q u e n t experiments with " r e a l - f e e d i n g " animals further d o c u m e n t e d that polysaccharide solutions are very palatable to rats [9, I l, 15]. In fact, at low concentrations rats were found to prefer Polycose to sucrose solutions, although at higher concentrations the reverse was true [9, 10, 16]. In the present experiment we returned to the shamfeeding technique to further compare the palatability o f p o l y saccharide and sucrose solutions. In our previous studies we observed that rats sham-fed as much of a 32% Polycose solution as of a 32% sucrose solution, but in real-feeding tests they significantly preferred the 32% sucrose solution to the 32% Polycose solution [10, 14, 16]. Taken together these results question the validity of the sham-feeding response as a measure of palatability. Alternatively, some aspect of the
A variety of techniques have been used to measure the hedonic response of animals to taste stimuli. In many o f these techniques the influence of postingestive factors on the hedonic response measure is minimized by limiting the amount of tastant c o n s u m e d during the test session. F o r example, in brief intake tests the amount c o n s u m e d is limited by restricting the animal's temporal access to the tastant, while in operant tests, e.g., bar pressing tests or runway tests, the size of the reinforcements and their schedule of presentation limits consumption. This is of importance because with some tastants postingestive satiety can interfere with the determination of hedonic response. For example, with sucrose solutions the amount c o n s u m e d in l hr or 24 hr/day tests decreases as concentrations increase above 9%, but, as measured by several different methods, the rat's hedonic response to sucrose increases monotonically with concentration [I, 2, 9, 23]. An alternative approach to the study o f taste and palatability that does not require limiting intake involves the use of the " s h a m - f e e d i n g " preparation. In this preparation postingestive factors are minimized by fitting animals with an esophageal or gastric fistula such that the ingested solution drains out the fistula as the animal drinks [5,17]. In this way postingestive satiety is eliminated and the amount in-
1This research was supported by grants from the National Institutes of Health (DK-31135) and the Faculty Research Award Program of the City University of New York. Polycose was generously supplied by Ross Laboratories. 2Requests for reprints should be addressed to Dr. Anthony Sclafani, Department of Psychology, Brooklyn College, Brooklyn, NY 11210.
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sham-feeding test may alter the relative palatability of Polycose and sucrose solutions. For example, the rats were food-deprived in the sham-feeding tests, but food sated in the real-feeding tests. To clarify this issue the present experiment investigated the sham-feeding response of rats to Polycose and sucrose solutions in greater detail.
METHOD
Subjects Eight adult female rats (CD strain, Charles River Lab, Wilmington, MA) weighing 260-330 g were used. The rats were housed in an air conditioned vivarium maintained at 21°C and under a 12:12 hr light-dark cycle.
Procedure The animals were fitted with a stainless steel gastric cannula as previously described [13]. Following recovery from surgery, the rats were maintained at 85% of their ad lib body weight by giving them restricted amounts of Purina chow each day; water remained freely available. The rats were tested 30 min/day in small cages {24 cm long × 10.5 cm wide × 10 cm high) kept in a quiet room adjacent to the vivarium. Pans below the test cages collected the gastric drainage during the sham-feeding tests. The test solution was available through a stainless steel drinking tube attached to a 100 ml graduated cylinder. The cylinder was mounted on a device that automatically positioned the drinking tube in front of the cage at the start of the session and retracted it at the end of the session. The rats licked at the drinking tube through a 2 cm hole in the front wall of the cage. A contact sensitive electronic drinkometer measured licking behavior, and licks/ min were recorded by a microcomputer. For the fistula open (sham-feeding) tests, the screw that occluded the fistula was removed, and the rat's stomach was washed clean with isotonic saline. The rat was then placed in
the test chamber. At the end of the 30 min session, the fistula was closed with the screw and the animal was returned to its home cage. If the amount of gastric drainage collected equaled or exceeded the amount of solution sham-fed this was taken as evidence that the fistula remained patent throughout the test session. (This does not mean, however, that all of the ingested solution passed out the fistula [12].) For the fistula closed tests, the rats were treated in an identical manner except that their fistula was closed prior to the beginning of the test session. The rats" daily food rations were provided approximately one hour after the end of the 30 min feeding sessions. The animals were trained to drink a 1% solution of Polycose (Ross Laboratories, Columbus, OH) in the test cages for one week before formal testing began. They were then tested, in successive 6-day blocks, with Polycose at 1%, 4%, 16% and 32% concentrations. During the first 3 days at each concentration the rats were tested with their fistula closed (real-feeding test), and during the next three days with their fistula open (sham-feeding test). Following the last scheduled 6-day block, the rats were given a two-bottle preference test, with their fistula open, using the 4% and 32% Polycose solutions. This test was conducted over two successive 30min/day sessions, with the left-right position of the solutions counterbalanced over sessions. The reason for this test will become apparent in the Results section. The rats were next tested, in successive 6-day blocks, with sucrose solutions at 1%, 4%, 16% and 32% concejatrations. As in the Polycose tests, the fistulas were closed during the first three days, and open during the last three days at each concentration. The rats were then given two-bottle preference tests, with their fistula open, using 1%, 4%, 16%. and 32% Polycose and sucrose solutions (e.g., 1% Polycose vs. 1% sucrose). The animals were tested twice at each concentration, with the left-right position of the Polycose and sucrose solution being alternated. Lick rates were not measured during the twobottle tests.
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Statistical Analysis For statistical analysis, solution intakes during the last two feeding sessions of each test condition were averaged. In addition, intakes during successive 5-rain periods during the 30-min tests were determined using the lick rate and 30-min intake data. These data were analyzed using a repeated measure analysis of variance procedure.
RESULTS
The mean 30-min intakes of Polycose during the real- and sham-feeding tests are summarized in Fig. 1. At the 1% concentration, the rats sham-fed no more than they "real-fed" but at all higher concentrations their sham-intakes were significantly greater (p<0.01) than their real-intakes. Furthermore, the rats' sham-intakes of the 4%, 16% and 32% Polycose solutions were similar, and exceeded (p<0.01) that of the 1% solution. As illustrated in Fig. 2, there was also a concentration effect on the within session rate of feeding (intake/5 min periods). With the I% Polycose solution the rats did not differ in their real- and sham-feeding rates. The real- and sham-feeding rates significantly (p<0.01) differed,
however, with the 4%, 16% and 32% Polycose solutions. In particular, at these concentrations the intake rates were comparable during the first 5 rain of testing but during the remaining 25 min the real-intake rates declined more rapidly than the sham-feeding rates (/9<0.01, rate by time interaction). As with the total intake measure, there was no reliable difference between the sham-feeding rates at the 4%, 16% and 32% concentrations. These latter findings could be interpreted to mean that the 4%, 16% and 32% Polycose solutions were equally palatable to the rat. This possibility was tested using the high (32%) and low (4%) concentrations in a two-bottle sham-feeding test. In this test the rats sham-fed substantially more 32% Polycose than 4% Polycose (69.5 vs. 0.4 ml/30, p<0.01). A generally similar pattern of results was obtained with the sucrose solutions. The rats did not sham-feed more 1% sucrose solution than they real-fed, but at the higher concentrations their sham-intakes reliably (p<0.01) exceeded their real-intakes (Fig. 1). However, the rats sham-fed less (,o<0.05) of the 4% sucrose than they did of the 16% and 32% sucrose solutions. Their feeding rates also differed as a function of feeding condition and solution concentration (Fig. 3). With the 1% sucrose solution the real- and sham-
218
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feeding rates were comparable, whereas at the higher concentrations their real-feeding rates were less than their sham-feeding rates. That is, the rats displayed a more rapid within-session decline in feeding rate during the real-feeding tests as compared to the sham-feeding tests (p<0.01). Also, their rate of sham-feeding declined faster with the 4% solution than with the 16% and 32% solutions. To facilitate the comparison of the Polycose and sucrose results obtained in the one-bottle tests the results described above are replotted in Figs. 4 and 5. In the real-feeding tests (Fig. 4), the rats consumed comparable amounts of Polycose and sucrose, and their intakes of both solutions increased as concentration increased from 1% to 4%, and then decreased as concentration increased from 4% to 32% (p<0.01). In the sham-feeding tests, however, the intakes of the two carbohydrates differed, i.e., there was a solution by concentration interaction (p<0.01). Further analysis revealed that at the 1% concentration 7 of the 8 rats consumed more Polycose than sucrose, although this difference failed to be statistically significant. At the 4% concentration all of the rats consumed more Polycose than sucrose and this difference was highly significant (/9<0.01). At the 16% and 32% concentra-
tions the rats did not reliably differ in their Polycose and sucrose intakes. The rats also differed in their Polycose and sucrose sham-feeding rates (Fig. 5). That is, the rats sham-fed the 1% and 4% Polycose solutions at faster rates (p<0.01) than the 1% and 4% sucrose solution. In the case of the 4% solutions, the rats initially sham-fed the solutions at comparable rates, but during the 30 rain sessions their sucrose sham-feeding rate declined more than did the Polycose sham-feeding rate (p<0.01). The rats did not reliably differ in their shamfeeding of the 16% solutions, although their rate of shamfeeding declined somewhat faster with the sucrose than with the Polycose solution. With the 32% solutions, on the other hand, the rats sham-fed the sucrose solution at a slightly, but significantly greater rate than the Polycose solution. The results of the two-bottle, sham-feeding preference tests are summarized in Fig. 6. Analysis of these data revealed a solution by concentration interaction (.o<0.01). At the I% concentration the rats sham-fed more (,o<0.05) Polycose than sucrose, while at the three higher concentrations they sham-fed substantially more (p<0.01) sucrose than Polycose. In terms of percent of total solution intake, the
POLYCOSE AND SUCROSE SHAM-FEEDING
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rats preference for the Polycose solution at the 1%, 4%, 16% and 32% concentrations was 67.3%, 20.7%, 12.0% and 9.7%, respectively.
DISCUSSION
The present results confirm and extend previous observations concerning the relative palatability of Polycose and sucrose solutions. In addition, the results revealed an unexpected finding concerning the "oral satiating" properties of Polycose and sucrose. Consistent with our previous report [14], the rats shamfed approximately 60 ml/30 min of the 32% Polycose solution. Their sham-intakes of the 4% and 16% solutions were just as high, and at these concentrations their sham-intakes greatly exceeded their real-intakes. With the 1% solution, however, the animals did not sham-feed more Polycose than they real-fed. Thus, there appears to be a substantial increase in palatability as Polycose concentration increases from 1 to 4%. This is further indicated by the increase in the real-intake of Polycose that occurred over this concentration range (see also [9]). Although the rats sham-fed comparable amounts of the 4%, 16% and 32% Polycose solutions, the solutions were not equivalent in palatability. That is, the results of the two-bottle preference test revealed a very strong (99%) peference for the 32% Polycose solution over the 4% solution. The failure of the one-bottle sham-feeding tests to reveal this preference difference can be attributed to a "ceiling" effect; with 4% Polycose the rats were consuming 60 ml/30 rain which appears to be at or near the maximum rate of consumption. Examination of the lick rate data also revealed that the rats licked almost continuously throughout the 30-min test sessions with the 4%, 16% and 32% Polycose solutions. The results obtained in the one-bottle sucrose tests were
generally similar to those obtained with Polycose. That is, at the 4%, 16% and 32% concentrations, but not at the 1% concentration, the rats sham-fed more than they real-fed of the surcose solutions. However, in contrast to their response to Polycose, the rats sham-fed significantly less of the 4% sucrose than they did of the 16% and 32% solutions. In this respect, the present results are consistent with the findings of Weingarten [19-21] that rats sham-fed less of a 6% sucrose solution than of a 16% solution. On the other hand, contrary to the present results, Weingarten [19-21] reported that rats did not sham-feed more 6%. sucrose than they real-fed of this solution, and that they sham-fed reliably more of a 30% or 36% sucrose solution than they did of a 16% or 18% solution. The procedures of the present experiment and Weingarten's studies differed in a number of respects which may account for the discrepant fndings. In addition, whereas Weingarten used male rats, the present experiment used female rats, and females are generally more responsive to sweet-tasting solutions than are male rats [18]. In the two-bottle, sham-feeding preference tests the rats strongly preferred the sucrose to Polycose at the 4%, 16% and 32% concentrations, but preferred the Polycose at the 1% concentration. This agrees with findings obtained in preference tests conducted with real-feeding rats [9, 10, 16]. These data indicate that, although in the one-bottle tests the rats sham-fed similar amounts of Polycose and sucrose at the 16% and 32% concentrations, they clearly found the sucrose to be more palatable than the Polycose at these concentrations. The failure of the one-bottle, sham-feeding tests to reveal this difference can be attributed to a ceiling effect. The rats sham-fed over 60 ml/30 min of the 16% and 32% sucrose and Polycose solutions which, as noted above, is at or near their maximum rate of intake. A similar explanation cannot account for the sham-feeding results obtained with the 4% sucrose and Polycose solutions. At this concentration the rats consumed signifi-
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cantly more Polycose than sucrose in the one-bottle tests, but yet reliably preferred the sucrose to the Polycose in the two-bottle tests. Given that several intervening tests occurred between the one- and two-bottle tests with the 4% solutions, the rats were retested with these solutions at the end of the experiment. The results were the same: the rats sham-fed more 4% Polycose than sucrose in the one-bottle tests but preferred the sucrose to Polycose in the two-bottle test. Since the two-bottle results indicate that 4% sucrose was more palatable to rats than 4% Polycose why did they sham-feed more Polycose than sucrose in one-bottle tests'? One possible explanation is that sucrose and Polycose differ in their "'oral satiating" effects. "'Oral satiety" refers to the fact that under certain conditions orosensory cues are sufficient to terminate a bout of ingestion, i.e., a meal. Mook et al. [6], for example, have demonstrated that with saccharin solutions it is oral rather than postingestive stimuli that cause the animal to terminate its saccharin "meal" (see also [14]). These investigators also reported that oral satiety operates to limit the intake of glucose solutions when postingestive satiety is eliminated as in the sham-feeding prepara-
tion. Most other sham-feeding studies, however, have discounted the importance of oral satiety since hungry animals were observed to consume enormous amounts of food when postingestive satiety was eliminated [17,24]. Yet, under some conditions, i.e., minimal deprivation levels or dilute sugar solutions, sham-feeding animals do not eat continuously but terminate their meal after consuming normal or near-normal amounts of food [3, 4, 19]. In the present experiment, for example, the rats did not sham-feed any more of the 1% sucrose or Polycose solutions than they real-fed of these solutions. With respect to the 4% solutions, it may be that sucrose, while more palatable to the rats than Polycose, is also more orally-satiating. Thus, in the two-bottle situation the rats may have preferred the sucrose over Polycose based on palatability, whereas in the one-bottle situation they may have sham-fed more Polycose than sucrose because they satiated to the taste of sucrose faster than to the taste of Polycose. Some support for this interpretation is provided by the feeding rate data. In the one-bottle tests the rats initially sham-fed the 4% sucrose and Polycose at comparable rates,
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but during the course of the 30-min session their feeding rate declined faster in the sucrose tests than in the Polycose tests. A similar trend was o b s e r v e d with the 16% solutions, and perhaps with less deprived animals, which show greater oral satiety, this difference would have been more robust. N o t e that to fully account for the present results it is necessary to postulate that oral satiation to sucrose also satiates the rat to Polycose. Otherwise in the two-bottle sham-feeding situation as the rat orally satiates to the sucrose solution it should sham-feed more and more of the
Polycose solution. Yet, at the 4% concentration the rats consumed relatively little Polycose in the two-bottle test and their total consumption (sucrose plus Polycose) was less than their sham-intake in the one-bottle 4% Polycose test (60.6 vs. 48.6 ml, p<0.01). The m e c h a n i s m responsible for oral satiety is not clearly understood. Mook et a! [7] suggested that oral satiety to saccharin is mediated by gustatory adaptation. W h e t h e r this adaptation is mediated at a peripheral (receptor) or central level remains to be determined, although some data suggest a central origin [22]. We have previously reported that sucrose and Polycose have qualitatively different tastes to rats, and have hypothesized that they activate different gustatory receptors [8]. The present finding that Polycose and sucrose differ in their oral satiety properties is consistent with this hypothesis. If different receptors are in fact involved, then the apparent generalization of sucrose oral satiety to Polycose would indicate that central mechanisms are involved. Clearly more w o r k is needed to resolve this issue and to elucidate the functional significance of oral sateity. Finally, a practical implication of the present findings concerns the use of the sham-feeding response as a measure of palatability. In two respects the one-bottle sham-feeding test was found to provide an inaccurate measure of palatability. First, because of a ceiling effect on the rate of ingestion, the test did not fully reveal the influence of concentration on solution palatability. This limitation was most pronounced in the case of the 4% and 32% Polycose solutions; the rats sham-fed comparable amounts of these solutions in the onebottle tests e v e n though they strongly preferred the 32% solution to the 4% solution, as revealed in the two-bottle preference test. Second, because o f the apparent difference in the oral satiating properties of 4% Polycose and sucrose solutions, the relative palatability of these solutions as indicated by the one-bottle sham-feeding test was just the opposite to that revealed by the two-bottle sham-feeding test. These results indicate that data o b t a i n e d with one-bottle sham-feeding tests must be interpreted with caution, particularly when qualitatively different tastants are used.
REFERENCES
1. Collier, G. and L. Myers. The loci of reinforcement. J Exp Pscyhol 61: 57-66, 1961. 2. Davis, J. D. The effectivensss of some sugars in stimulating licking behavior in the rat. Physiol Behav l h 39-45, 1973. 3. Joyner, K., G. P. Smith, R. Shindledecker and C. Pfaffmann. Stimulation of sham feeding in the rat by sucrose, maltose, glucose and fructose. Soc Neurosc'i Abstr ll: 1223, 1985. 4. Kraly, F. S., W. J. Catty and G. P. Smith. Effect of pregastric food stimuli on meal size and intermeal interval in the rat. Physiol Behav 20: 77%784, 1978. 5. Mook, D. G. Oral and postingestional determinants of the intake of various solutions in rats with esophageal fistulas. J Comp Physiol Psychol 56: 645-659, 1963. 6. Mook, D. G., C. A. Bryner, L. D. Rainey and C. L. Wall. Release of feeding by the'sweet taste in rats: oropharyngeal satiety. Appetite 1: 29%315, 1980. 7. Mook, D. G., B. D. Kushner and L. R. Kushner. Release of feeding by the sweet taste in rats: The specificity of oral satiety. Appetite 2: 267-280, 1981. 8. Nissenbaum, J. W. and A. Sclafani. Qualitative differences in polysaccharide and sugar tastes in the rat: A two-carbohydrate taste model. Neurosci Biobehav Rev ll: 187-196, 1987.
9. Sclafani, A. and A. E. Clyne. Hedonic response of rats to polysaccharide and sugar solutions. Neurosci Biobehav Rev 11: 173-180, 1987. 10. Sclafani, A., H. Hertwig and M. Vigorito. Sex differences in polysaccharide and sugar preferences in rats. Neurosci Biobehav Rev ll: 241-251, 1987. 11. Sclafani, A., H. Hertwig, M. Vigorito, H. Sloan and B. Kerzher. Influence of saccharide length on polysaccharide appetite in the rat. Neurosci Biobehav Rev It: 197-200, 1987. 12. Sclafani, A. and J. W. Nissenbaum. Is gastric sham-feeding really sham-feeding? Am J Physiol 248: R387-R390, 1985. 13. Sclafani, A. and J. W. Nissenbaum. On the role of the mouth and gut in the control of saccharin and sugar intake: A reexamination of the sham-feeding preparation. Brain Res Bull 14: 56%576, 1985. 14. Sclafani, A. and J. W. Nissenbaum. Oral versus postingestive origin of polysaccharide appetite in the rat. Neurosci Biobehav Rev ll: 16%172, 1987. 15. Sclafani, A. and J. W. Nissenbaum. Taste preference thresholds for Polycose, maltose and sucrose in rats. Neurosci Biobehav Rev lt: 181-185, 1987.
222 16. Sclafani, A. and S. Xenakis. Sucrose and polysaccharide induced obesity in the rat. Physiol Behav 32: 169-174, 1984. 17. Smith, G. P. and J. Gibbs. Postprandial satiety. In: Progress in Psychobiology and Physiological Psychology, Vol 8. edited by J. M. Sprague and A. N. Epstein. New York: Academic Press, 1979, pp. 179-242. 18. Wade, G. N. Sex hormones, regulatory behaviors, and body weight. In: Advances in the Slttdy of Behavior, edited by J. S. Rosenblatt, R. A. Hinde. E. Shaw and C. G. Beer. New York: Academic Press, 1976, pp. 201-279. 19. Weingarten, H. P. Diet palatability modulates sham feeding in VMH-lesion and normal rats: Implications for finickiness and evaluation of sham-feeding data..1 Comp Physiol Psychol 96: 223-233, 1982.
NISSENBAUM AND SCLAFANI
20. Weingarten, H. P. and S. D. Watson. Effects of atropine methyl nitrate on sham feeding in the rat. Pllarmacol Biocllem Behav 17: 863-867, 1982. 21. Weingarten, H. P. and S. D. Watson. Sham feeding as a procedure for assessing the influence of diet palatability on food intake. Physiol Behelv 28: 401-407, 1982. 22. Wilcove, W. G. Ingestion affected by the oral environment: The role of gustatory adaptation on taste reactivity in the rat. Physiol Behav 11: 297-312, 1973. 23. Young, P. T. and J. T. Greene. Quantity of food ingested as a measure of relative acceptability. J Comp Physiol Psychol 46: 288--294, 1953. 24. Young, R. C., J. Gibbs, J. Antin, J. Holt and G. P. Smith. Absence of satiety during sham feeding in the rat. J Comp Physiol Psychol 87: 795-800, 1974.
0149-7634/87 $3.00 + .00
Sham-Feeding Response of Rats to Polycose and Sucrose JEFFREY
W. N I S S E N B A U M
AND ANTHONY
SCLAFANI
z
D e p a r t m e n t o f Psychology, Brooklyn College and the Graduate School o f the City UniversiO, o f N e w York Brooklyn, N Y 11210 Received
17 M a r c h 1986
NISSENBAUM, J. W. AND A. SCLAFANi. Sham-feeding response oJ" rats to Polycose and sucrose. NEUROSC! BIOBEHAV REV 11(2) 215-222, 1987.--Adult female rats were fitted with gastric fistulas and maintained at 85% of their ad lib body weight. Their real-feeding (fistula closed) and sham-feeding (fistula open) responses to polysaccharide (Polycose) and sucrose solutions were measured during 30 min/day one-bottle tests. The rats consumed similar amounts of a 1% Polycose solution during real- and sham-feeding tests, but their sham-intakes of 4%, 16% and 32~ Polycose solutions greatly exceeded their real-intakes of these solutions. Similar results were obtained with sucrose solutions. The rats sham-fed more Polycose than sucrose at the 1% and 4% concentrations, while their sham-intakes of the 16% and 32% Polycose and sucrose solutions were comparable. In subsequent two-solution sham-feeding tests, the rats preferred I% Polycose to I% sucrose, but preferred sucrose to Polycose at 4%, 16% and 32% concentrations. These preference results indicate that rats find Polycose more palatable than sucrose at low concentrations, but sucrose more palatable at high concentrations. In addition, the findings that the rats preferred 4% sucrose to 4% Polycose in the two-bottle test, but sham-fed more 4% Polycose than 4% sucrose in the one-bottle tests, suggest that sucrose is more "orally-satiating" than is Polycose. These results provide further evidence for qualitative differences in the tastes of sucrose and polysaccharide. They also indicate that the amount of solution sham-fed does not necessarily reflect the palatability of the solution. Polysaccharide taste
Sweet taste
Palatability
Oral satiety
Gastric sham-feeding
gested can be taken as a measure of the animal's hedonic response to the tastant. Using sucrose again as an example, the amount of sucrose solution sham-fed increases monotonically as concentration increases [3, 5, 21]. In a previous study in this series the gastric sham-feeding technique was used to determine the role of orosensory factors in the rat's appetite for polysaccharide solutions (Polycose) [14]. The finding of that study that rats sham-fed substantial amounts of a 32% Polycose solution provided the first e v i d e n c e that rats are attracted to the taste of polysaccharides. S u b s e q u e n t experiments with " r e a l - f e e d i n g " animals further d o c u m e n t e d that polysaccharide solutions are very palatable to rats [9, I l, 15]. In fact, at low concentrations rats were found to prefer Polycose to sucrose solutions, although at higher concentrations the reverse was true [9, 10, 16]. In the present experiment we returned to the shamfeeding technique to further compare the palatability o f p o l y saccharide and sucrose solutions. In our previous studies we observed that rats sham-fed as much of a 32% Polycose solution as of a 32% sucrose solution, but in real-feeding tests they significantly preferred the 32% sucrose solution to the 32% Polycose solution [10, 14, 16]. Taken together these results question the validity of the sham-feeding response as a measure of palatability. Alternatively, some aspect of the
A variety of techniques have been used to measure the hedonic response of animals to taste stimuli. In many o f these techniques the influence of postingestive factors on the hedonic response measure is minimized by limiting the amount of tastant c o n s u m e d during the test session. F o r example, in brief intake tests the amount c o n s u m e d is limited by restricting the animal's temporal access to the tastant, while in operant tests, e.g., bar pressing tests or runway tests, the size of the reinforcements and their schedule of presentation limits consumption. This is of importance because with some tastants postingestive satiety can interfere with the determination of hedonic response. For example, with sucrose solutions the amount c o n s u m e d in l hr or 24 hr/day tests decreases as concentrations increase above 9%, but, as measured by several different methods, the rat's hedonic response to sucrose increases monotonically with concentration [I, 2, 9, 23]. An alternative approach to the study o f taste and palatability that does not require limiting intake involves the use of the " s h a m - f e e d i n g " preparation. In this preparation postingestive factors are minimized by fitting animals with an esophageal or gastric fistula such that the ingested solution drains out the fistula as the animal drinks [5,17]. In this way postingestive satiety is eliminated and the amount in-
1This research was supported by grants from the National Institutes of Health (DK-31135) and the Faculty Research Award Program of the City University of New York. Polycose was generously supplied by Ross Laboratories. 2Requests for reprints should be addressed to Dr. Anthony Sclafani, Department of Psychology, Brooklyn College, Brooklyn, NY 11210.
215
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sham-feeding test may alter the relative palatability of Polycose and sucrose solutions. For example, the rats were food-deprived in the sham-feeding tests, but food sated in the real-feeding tests. To clarify this issue the present experiment investigated the sham-feeding response of rats to Polycose and sucrose solutions in greater detail.
METHOD
Subjects Eight adult female rats (CD strain, Charles River Lab, Wilmington, MA) weighing 260-330 g were used. The rats were housed in an air conditioned vivarium maintained at 21°C and under a 12:12 hr light-dark cycle.
Procedure The animals were fitted with a stainless steel gastric cannula as previously described [13]. Following recovery from surgery, the rats were maintained at 85% of their ad lib body weight by giving them restricted amounts of Purina chow each day; water remained freely available. The rats were tested 30 min/day in small cages {24 cm long × 10.5 cm wide × 10 cm high) kept in a quiet room adjacent to the vivarium. Pans below the test cages collected the gastric drainage during the sham-feeding tests. The test solution was available through a stainless steel drinking tube attached to a 100 ml graduated cylinder. The cylinder was mounted on a device that automatically positioned the drinking tube in front of the cage at the start of the session and retracted it at the end of the session. The rats licked at the drinking tube through a 2 cm hole in the front wall of the cage. A contact sensitive electronic drinkometer measured licking behavior, and licks/ min were recorded by a microcomputer. For the fistula open (sham-feeding) tests, the screw that occluded the fistula was removed, and the rat's stomach was washed clean with isotonic saline. The rat was then placed in
the test chamber. At the end of the 30 min session, the fistula was closed with the screw and the animal was returned to its home cage. If the amount of gastric drainage collected equaled or exceeded the amount of solution sham-fed this was taken as evidence that the fistula remained patent throughout the test session. (This does not mean, however, that all of the ingested solution passed out the fistula [12].) For the fistula closed tests, the rats were treated in an identical manner except that their fistula was closed prior to the beginning of the test session. The rats" daily food rations were provided approximately one hour after the end of the 30 min feeding sessions. The animals were trained to drink a 1% solution of Polycose (Ross Laboratories, Columbus, OH) in the test cages for one week before formal testing began. They were then tested, in successive 6-day blocks, with Polycose at 1%, 4%, 16% and 32% concentrations. During the first 3 days at each concentration the rats were tested with their fistula closed (real-feeding test), and during the next three days with their fistula open (sham-feeding test). Following the last scheduled 6-day block, the rats were given a two-bottle preference test, with their fistula open, using the 4% and 32% Polycose solutions. This test was conducted over two successive 30min/day sessions, with the left-right position of the solutions counterbalanced over sessions. The reason for this test will become apparent in the Results section. The rats were next tested, in successive 6-day blocks, with sucrose solutions at 1%, 4%, 16% and 32% concejatrations. As in the Polycose tests, the fistulas were closed during the first three days, and open during the last three days at each concentration. The rats were then given two-bottle preference tests, with their fistula open, using 1%, 4%, 16%. and 32% Polycose and sucrose solutions (e.g., 1% Polycose vs. 1% sucrose). The animals were tested twice at each concentration, with the left-right position of the Polycose and sucrose solution being alternated. Lick rates were not measured during the twobottle tests.
POLYCOSE AND SUCROSE S H A M - F E E D I N G
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Statistical Analysis For statistical analysis, solution intakes during the last two feeding sessions of each test condition were averaged. In addition, intakes during successive 5-rain periods during the 30-min tests were determined using the lick rate and 30-min intake data. These data were analyzed using a repeated measure analysis of variance procedure.
RESULTS
The mean 30-min intakes of Polycose during the real- and sham-feeding tests are summarized in Fig. 1. At the 1% concentration, the rats sham-fed no more than they "real-fed" but at all higher concentrations their sham-intakes were significantly greater (p<0.01) than their real-intakes. Furthermore, the rats' sham-intakes of the 4%, 16% and 32% Polycose solutions were similar, and exceeded (p<0.01) that of the 1% solution. As illustrated in Fig. 2, there was also a concentration effect on the within session rate of feeding (intake/5 min periods). With the I% Polycose solution the rats did not differ in their real- and sham-feeding rates. The real- and sham-feeding rates significantly (p<0.01) differed,
however, with the 4%, 16% and 32% Polycose solutions. In particular, at these concentrations the intake rates were comparable during the first 5 rain of testing but during the remaining 25 min the real-intake rates declined more rapidly than the sham-feeding rates (/9<0.01, rate by time interaction). As with the total intake measure, there was no reliable difference between the sham-feeding rates at the 4%, 16% and 32% concentrations. These latter findings could be interpreted to mean that the 4%, 16% and 32% Polycose solutions were equally palatable to the rat. This possibility was tested using the high (32%) and low (4%) concentrations in a two-bottle sham-feeding test. In this test the rats sham-fed substantially more 32% Polycose than 4% Polycose (69.5 vs. 0.4 ml/30, p<0.01). A generally similar pattern of results was obtained with the sucrose solutions. The rats did not sham-feed more 1% sucrose solution than they real-fed, but at the higher concentrations their sham-intakes reliably (p<0.01) exceeded their real-intakes (Fig. 1). However, the rats sham-fed less (,o<0.05) of the 4% sucrose than they did of the 16% and 32% sucrose solutions. Their feeding rates also differed as a function of feeding condition and solution concentration (Fig. 3). With the 1% sucrose solution the real- and sham-
218
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feeding rates were comparable, whereas at the higher concentrations their real-feeding rates were less than their sham-feeding rates. That is, the rats displayed a more rapid within-session decline in feeding rate during the real-feeding tests as compared to the sham-feeding tests (p<0.01). Also, their rate of sham-feeding declined faster with the 4% solution than with the 16% and 32% solutions. To facilitate the comparison of the Polycose and sucrose results obtained in the one-bottle tests the results described above are replotted in Figs. 4 and 5. In the real-feeding tests (Fig. 4), the rats consumed comparable amounts of Polycose and sucrose, and their intakes of both solutions increased as concentration increased from 1% to 4%, and then decreased as concentration increased from 4% to 32% (p<0.01). In the sham-feeding tests, however, the intakes of the two carbohydrates differed, i.e., there was a solution by concentration interaction (p<0.01). Further analysis revealed that at the 1% concentration 7 of the 8 rats consumed more Polycose than sucrose, although this difference failed to be statistically significant. At the 4% concentration all of the rats consumed more Polycose than sucrose and this difference was highly significant (/9<0.01). At the 16% and 32% concentra-
tions the rats did not reliably differ in their Polycose and sucrose intakes. The rats also differed in their Polycose and sucrose sham-feeding rates (Fig. 5). That is, the rats sham-fed the 1% and 4% Polycose solutions at faster rates (p<0.01) than the 1% and 4% sucrose solution. In the case of the 4% solutions, the rats initially sham-fed the solutions at comparable rates, but during the 30 rain sessions their sucrose sham-feeding rate declined more than did the Polycose sham-feeding rate (p<0.01). The rats did not reliably differ in their shamfeeding of the 16% solutions, although their rate of shamfeeding declined somewhat faster with the sucrose than with the Polycose solution. With the 32% solutions, on the other hand, the rats sham-fed the sucrose solution at a slightly, but significantly greater rate than the Polycose solution. The results of the two-bottle, sham-feeding preference tests are summarized in Fig. 6. Analysis of these data revealed a solution by concentration interaction (.o<0.01). At the I% concentration the rats sham-fed more (,o<0.05) Polycose than sucrose, while at the three higher concentrations they sham-fed substantially more (p<0.01) sucrose than Polycose. In terms of percent of total solution intake, the
POLYCOSE AND SUCROSE SHAM-FEEDING
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rats preference for the Polycose solution at the 1%, 4%, 16% and 32% concentrations was 67.3%, 20.7%, 12.0% and 9.7%, respectively.
DISCUSSION
The present results confirm and extend previous observations concerning the relative palatability of Polycose and sucrose solutions. In addition, the results revealed an unexpected finding concerning the "oral satiating" properties of Polycose and sucrose. Consistent with our previous report [14], the rats shamfed approximately 60 ml/30 min of the 32% Polycose solution. Their sham-intakes of the 4% and 16% solutions were just as high, and at these concentrations their sham-intakes greatly exceeded their real-intakes. With the 1% solution, however, the animals did not sham-feed more Polycose than they real-fed. Thus, there appears to be a substantial increase in palatability as Polycose concentration increases from 1 to 4%. This is further indicated by the increase in the real-intake of Polycose that occurred over this concentration range (see also [9]). Although the rats sham-fed comparable amounts of the 4%, 16% and 32% Polycose solutions, the solutions were not equivalent in palatability. That is, the results of the two-bottle preference test revealed a very strong (99%) peference for the 32% Polycose solution over the 4% solution. The failure of the one-bottle sham-feeding tests to reveal this preference difference can be attributed to a "ceiling" effect; with 4% Polycose the rats were consuming 60 ml/30 rain which appears to be at or near the maximum rate of consumption. Examination of the lick rate data also revealed that the rats licked almost continuously throughout the 30-min test sessions with the 4%, 16% and 32% Polycose solutions. The results obtained in the one-bottle sucrose tests were
generally similar to those obtained with Polycose. That is, at the 4%, 16% and 32% concentrations, but not at the 1% concentration, the rats sham-fed more than they real-fed of the surcose solutions. However, in contrast to their response to Polycose, the rats sham-fed significantly less of the 4% sucrose than they did of the 16% and 32% solutions. In this respect, the present results are consistent with the findings of Weingarten [19-21] that rats sham-fed less of a 6% sucrose solution than of a 16% solution. On the other hand, contrary to the present results, Weingarten [19-21] reported that rats did not sham-feed more 6%. sucrose than they real-fed of this solution, and that they sham-fed reliably more of a 30% or 36% sucrose solution than they did of a 16% or 18% solution. The procedures of the present experiment and Weingarten's studies differed in a number of respects which may account for the discrepant fndings. In addition, whereas Weingarten used male rats, the present experiment used female rats, and females are generally more responsive to sweet-tasting solutions than are male rats [18]. In the two-bottle, sham-feeding preference tests the rats strongly preferred the sucrose to Polycose at the 4%, 16% and 32% concentrations, but preferred the Polycose at the 1% concentration. This agrees with findings obtained in preference tests conducted with real-feeding rats [9, 10, 16]. These data indicate that, although in the one-bottle tests the rats sham-fed similar amounts of Polycose and sucrose at the 16% and 32% concentrations, they clearly found the sucrose to be more palatable than the Polycose at these concentrations. The failure of the one-bottle, sham-feeding tests to reveal this difference can be attributed to a ceiling effect. The rats sham-fed over 60 ml/30 min of the 16% and 32% sucrose and Polycose solutions which, as noted above, is at or near their maximum rate of intake. A similar explanation cannot account for the sham-feeding results obtained with the 4% sucrose and Polycose solutions. At this concentration the rats consumed signifi-
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cantly more Polycose than sucrose in the one-bottle tests, but yet reliably preferred the sucrose to the Polycose in the two-bottle tests. Given that several intervening tests occurred between the one- and two-bottle tests with the 4% solutions, the rats were retested with these solutions at the end of the experiment. The results were the same: the rats sham-fed more 4% Polycose than sucrose in the one-bottle tests but preferred the sucrose to Polycose in the two-bottle test. Since the two-bottle results indicate that 4% sucrose was more palatable to rats than 4% Polycose why did they sham-feed more Polycose than sucrose in one-bottle tests'? One possible explanation is that sucrose and Polycose differ in their "'oral satiating" effects. "'Oral satiety" refers to the fact that under certain conditions orosensory cues are sufficient to terminate a bout of ingestion, i.e., a meal. Mook et al. [6], for example, have demonstrated that with saccharin solutions it is oral rather than postingestive stimuli that cause the animal to terminate its saccharin "meal" (see also [14]). These investigators also reported that oral satiety operates to limit the intake of glucose solutions when postingestive satiety is eliminated as in the sham-feeding prepara-
tion. Most other sham-feeding studies, however, have discounted the importance of oral satiety since hungry animals were observed to consume enormous amounts of food when postingestive satiety was eliminated [17,24]. Yet, under some conditions, i.e., minimal deprivation levels or dilute sugar solutions, sham-feeding animals do not eat continuously but terminate their meal after consuming normal or near-normal amounts of food [3, 4, 19]. In the present experiment, for example, the rats did not sham-feed any more of the 1% sucrose or Polycose solutions than they real-fed of these solutions. With respect to the 4% solutions, it may be that sucrose, while more palatable to the rats than Polycose, is also more orally-satiating. Thus, in the two-bottle situation the rats may have preferred the sucrose over Polycose based on palatability, whereas in the one-bottle situation they may have sham-fed more Polycose than sucrose because they satiated to the taste of sucrose faster than to the taste of Polycose. Some support for this interpretation is provided by the feeding rate data. In the one-bottle tests the rats initially sham-fed the 4% sucrose and Polycose at comparable rates,
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C0NCrNTRATmN (Z) FIG. 6. Mean (---SE) 30-min intake of Polycose and sucrose during two-bottle sham-feeding preference test. Asterisks indicate significant differences between Polycose and sucrose intakes (.o<0.05 or p<0.01).
but during the course of the 30-min session their feeding rate declined faster in the sucrose tests than in the Polycose tests. A similar trend was o b s e r v e d with the 16% solutions, and perhaps with less deprived animals, which show greater oral satiety, this difference would have been more robust. N o t e that to fully account for the present results it is necessary to postulate that oral satiation to sucrose also satiates the rat to Polycose. Otherwise in the two-bottle sham-feeding situation as the rat orally satiates to the sucrose solution it should sham-feed more and more of the
Polycose solution. Yet, at the 4% concentration the rats consumed relatively little Polycose in the two-bottle test and their total consumption (sucrose plus Polycose) was less than their sham-intake in the one-bottle 4% Polycose test (60.6 vs. 48.6 ml, p<0.01). The m e c h a n i s m responsible for oral satiety is not clearly understood. Mook et a! [7] suggested that oral satiety to saccharin is mediated by gustatory adaptation. W h e t h e r this adaptation is mediated at a peripheral (receptor) or central level remains to be determined, although some data suggest a central origin [22]. We have previously reported that sucrose and Polycose have qualitatively different tastes to rats, and have hypothesized that they activate different gustatory receptors [8]. The present finding that Polycose and sucrose differ in their oral satiety properties is consistent with this hypothesis. If different receptors are in fact involved, then the apparent generalization of sucrose oral satiety to Polycose would indicate that central mechanisms are involved. Clearly more w o r k is needed to resolve this issue and to elucidate the functional significance of oral sateity. Finally, a practical implication of the present findings concerns the use of the sham-feeding response as a measure of palatability. In two respects the one-bottle sham-feeding test was found to provide an inaccurate measure of palatability. First, because of a ceiling effect on the rate of ingestion, the test did not fully reveal the influence of concentration on solution palatability. This limitation was most pronounced in the case of the 4% and 32% Polycose solutions; the rats sham-fed comparable amounts of these solutions in the onebottle tests e v e n though they strongly preferred the 32% solution to the 4% solution, as revealed in the two-bottle preference test. Second, because o f the apparent difference in the oral satiating properties of 4% Polycose and sucrose solutions, the relative palatability of these solutions as indicated by the one-bottle sham-feeding test was just the opposite to that revealed by the two-bottle sham-feeding test. These results indicate that data o b t a i n e d with one-bottle sham-feeding tests must be interpreted with caution, particularly when qualitatively different tastants are used.
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