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Departments of Psychology, Psychiatry, Food Science and Nutrition, Surgery and Medicine, University of Minnesota, Minneapolis 55455; and Minnesota Obesity Center, Research Service Veterans Affairs Medical Center, Minneapolis, Minnesota 55417
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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We tested whether carbohydrate source (corn starch, sucrose, Polycose) influences the choice between a high-fat and high-carbohydrate diet in spontaneously feeding rats and in rats stimulated to eat by neuropeptide Y (NPY) administration or food deprivation. Rats were tested under three diet options: 1) a high-fat diet versus a high-corn starch diet; 2) a high-fat diet versus a high-sucrose diet; and 3) a high-fat diet versus a high-Polycose diet. During daily and stimulated feeding rats ate more of the high-carbohydrate diet than the fat diet when the source of carbohydrate was sucrose or Polycose; however, when corn starch was provided as the carbohydrate source rats ate more of the high-fat diet. Food-deprived rats increased intake of both the high-fat and the high-carbohydrate diets, with the proportion of energy ingested from each of the diets resembling that noted during 3 days of spontaneous feeding. NPY-injected rats ate more of both the high-fat and high-carbohydrate diets during diet options 1 and 3, but not during option 2 when the high-sucrose and high-fat diets were offered concurrently. In that case, rats did not significantly increase their intake of the high-fat diet. Although carbohydrate source and NPY administration each influenced diet selection, altering the source of carbohydrate had a more marked effect.
fat; corn starch; sucrose; Polycose; food deprivation
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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OVER THE LAST DECADE or so, there have been claims that certain neuroregulatory agents can selectively modulate intake of particular classes of macronutrients (i.e., carbohydrate, fat, or protein). For example, it has been argued that opiates or neuropeptide Y (NPY) exert an influence on fat (7, 8) or carbohydrate ingestion (13, 14), respectively. The latter link between NPY and carbohydrate intake has received considerable empirical support. Administration of NPY into the cerebroventricles or the paraventricular nucleus of the hypothalamus of rats allowed to self-select from pure dietary macronutrients resulted in increased carbohydrate consumption relative to fat and protein (13, 16), whereas rats given a choice between high-fat and high-carbohydrate diets increased intake of carbohydrate relative to fat (9). Furthermore, there is a high positive correlation between hypothalamic levels of NPY and carbohydrate intake, whereas NPY levels appear unrelated to both fat and protein ingestion (4). Such evidence has led to the hypothesis that NPY may influence carbohydrate ingestion along a hypothalamic arcuate nucleus-paraventricular (perifornical) circuit that regulates a set of complex peripheral and central mechanisms altering metabolic pathways (1, 5). However, other variables may modulate the hyperphagic effects of NPY, as demonstrated by recent evidence showing that preexisting preferences for fat or carbohydrate impacted macronutrient or dietary choice in NPY-stimulated animals (2, 16).
Although the evidence to date suggests that NPY exerts a preferential role in mediating carbohydrate intake, the generality of this hypothesis is uncertain. Most studies examining the effects of NPY on nutrient/diet selection have relied on a particular mixture of carbohydrates, and findings have been extended to cover the entire class of carbohydrates. However, carbohydrates represent a diverse group of compounds that differ in a number of respects, including length of glucose polymerization, taste, texture, as well as postingestive absorption and metabolism (3, 12, 15). Furthermore, there is evidence that rats display different preferences for high-carbohydrate diets that differ in their source of carbohydrate (17).
To test the importance of carbohydrate type on NPY-stimulated diet selection, corn starch, sucrose, and Polycose were substituted as the main carbohydrate source of high-carbohydrate diets in three regimens wherein a high-carbohydrate diet was offered along with a high-fat diet (i.e., a high-corn starch diet vs. a high-fat diet, a high-sucrose diet vs. a high-fat diet, and a high-Polycose diet vs. a high-fat diet). These nutrient types were chosen as the main carbohydrate sources for the high-carbohydrate diets because they each represent different degrees of carbohydrate complexity, and there is evidence derived from short-term preference tests that rats differ in their liking for these diets (17). Furthermore, because baseline preferences impact NPY-stimulated diet choice, we examined the relationship between baseline diet choice and diet selection after NPY stimulation. As a point of comparison, another means of stimulating eating, food deprivation, was chosen to determine whether it would result in patterns of diet choice similar to that of NPY. Additionally, we examined the relationship between daily and stimulated feeding by comparing diet selection during the first hour of the dark cycle with baseline diet choice.
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Animals
Thirty-two male Sprague-Dawley rats (Harlan Sprague Dawley, Madison, WI), weighing 275-350 g, were maintained on a 12:12-h light-dark cycle in a temperature-controlled room. Animals were individually housed in stainless steel wire cages with ad libitum food and water access, except where noted. Rats were fed a standard laboratory diet (Certified Rodent Chow, Teklad, Indianapolis IN) before exposure to the experimental diets. Animals were presented with a choice between a high-fat diet (77% kcal derived from fat) and one of three isocaloric high-carbohydrate diets that differed only in the source of the carbohydrate (sucrose, Polycose, corn starch) in three regimens (detailed below). Rats were adapted to the diets for 10-14 days. The composition of the diets is shown in Table 1. Placement of food jars was rotated to avoid any placement preference, and intake was corrected for spillage.
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Surgery
Animals under pentobarbitol sodium anesthesia were implanted with stainless steel guide cannulas into the right lateral ventricle. The cannula was placed 1.0 mm posterior and 1.5 mm lateral to bregma at a depth of 3.5 mm below the outer surface of the skull. Correct cannula placement was verified by drinking at least 5 ml of water in 20 min after 100 ng infusion of angiotensin II (Peninsula Laboratories, Belmont, CA). Rats with improperly placed cannulas were not included in the final data analyses. Peptides were dissolved in saline (0.9%) and injected in a 5-µl volume.Procedure
NPY regimen. The effect of carbohydrate type on diet selection was examined by substituting different carbohydrate sources in high-carbohydrate diets presented to NPY-stimulated rats. All subjects (n = 23) were exposed to all combinations of diets (corn starch-based high-carbohydrate diet and high-fat diet, sucrose-based high-carbohydrate diet and high-fat diet, and Polycose-based high-carbohydrate diet and high-fat diet) in two phases: 1) spontaneous baseline feeding and 2) NPY stimulation. Spontaneous baseline feeding is here defined as a consistent pattern of diet choice over 3 days after a 10- to 14-day interval, during which time rats were adapted to each respective diet combination.After this, rats were given NPY. During this phase food was removed from home cages at 1000-1100 and the animals were immediately injected (icv) with NPY (5 µg/5 µl) or 0.9% saline. All subjects received both NPY and saline (within-subjects design). After 15 min, preweighed food jars, one high fat and the other high carbohydrate, were returned to the home cages. Food intake was quantified and corrected for spillage after 1 h. One rat was excluded from all analyses because it ate <0.1 g of food after NPY injection.
Food-deprivation regimen. Under the food deprivation regimen all rats (n = 9) were exposed to all diet combinations, as in the NPY regimen. First spontaneous diet selection was determined, as described above, and then rats were food deprived for 24 h. After this period, preweighed food jars, one containing high-fat and the other high-carbohydrate diet, were returned to home cages. Food intake was quantified and corrected for spillage after 1 h (1000-1100).
Nocturnal feeding regimen. In the early stages of evaluating data from experiments 1 and 2, a close correspondence was seen between 3-day baseline intake patterns and diet selection after NPY stimulation. We questioned whether the similarity between baseline and NPY-stimulated eating was particular to the 1-h stimulated-feeding period or perhaps reflected a pattern of intake present at other times. To answer this question, eating during the first hour of the dark cycle was studied. This period was judged to be ideal in that it is several hours removed from the time of day in which stimulated feeding was studied, and there is evidence that hypothalamic NPY levels exhibit a circadian rhythm, with release occurring during the early part of the dark cycle. Thus at the start of the dark cycle, preweighed food jars were presented to a group of eight rats used in the NPY study. At the end of 1 h, food intake was quantified and corrected for spillage.
Statistical analyses. All data are presented as means ± SE. Differences between mean intakes of the high-fat and high-carbohydrate diets were compared using paired t-tests with a Bonferonni correction for multiple comparisons. Comparison of spontaneous baseline intake with that observed after food deprivation or NPY injection were evaluated by a two-factor analysis of variance [carbohydrate source (3 levels: corn starch, sucrose, Polycose) × treatment (repeated measure 2 levels: spontaneous baseline or stimulated)]. The nocturnal data were compared with spontaneous baseline values by the same analysis. Data presented as percent of control intake were transformed (arcsine; used for comparison of proportions) prior to analysis of variance.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Effect of Carbohydrate Source on Daily Diet Selection
We found that the carbohydrate source affected selection between a high-carbohydrate and high-fat diet during a 3-day baseline period (Fig. 1). Specifically, rats ingested more high-carbohydrate diet (g) when the carbohydrate source was either sucrose or Polycose. However, rats ingested more of the high-fat diet (g) when the high-carbohydrate diet contained corn starch. When measured on the basis of kilocalories of food ingested, a similar pattern emerged; however, sucrose intake was not significantly increased compared with fat intake. These rats ingested ~25% of total baseline energy intake from the high-carbohydrate diet when corn starch was the carbohydrate source. With sucrose as the main source of the high-carbohydrate diet, rats consumed ~57% of total energy intake from this diet, and when Polycose served as the main carbohydrate source, ~59% of total energy intake was from the high-carbohydrate diet.
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Role of Carbohydrate Type on NPY-Stimulated Diet Consumption
After establishment of baseline intakes, 22 of these rats were used to evaluate the effects of NPY on diet selection (1 rat was eliminated because it did not eat after NPY injection). As expected, NPY significantly stimulated food intake (Table 2). Intake of the high-fat and high-carbohydrate diets increased significantly (kcal or g) in all groups compared with vehicle-injected rats, except for the high-fat diet in the high-fat and sucrose diet choice group. To study whether the pattern of intake after NPY injection was similar to that observed during the baseline periods, we calculated the percent of total kilocalories or grams ingested as fat or carbohydrate during each period in each rat. Conversion of data to a proportion was necessary because the spontaneous baseline intake was determined over a 3-day period, and the stimulated intake was measured for a 1-h period. There was a main effect of both carbohydrate source [kcal: F(2,63) = 20.52, P = 0.0001; g: F(2,63) = 19.83, P = 0.0001] and treatment (i.e., NPY vs. baseline) [kcal: F(1,63) = 8.95, P = 0.004; g: F(1,63) = 5.86, P = 0.018] on the percent of kilocalories and grams ingested, but no significant interaction was noted [kcal: F(2,63) = 0.47, P = 0.6299; g: F(2,63) = 0.52, P = 0.594]. After injection of NPY, rats consumed a significantly larger proportion of their total energy or grams ingested from the high-starch diet compared with that observed during the 3-day baseline period (Fig. 2). Also, NPY-injected rats consumed a significantly larger proportion of their total energy from the high-sucrose diet compared with that observed during the 3-day baseline period (Fig. 2). However, when rats were presented with the high-fat diet and the high-Polycose diet, NPY did not significantly alter the baseline preference pattern based on energy intake or amount of food eaten (Fig. 2). If preference is defined as eating >60% of kcal from one food, we found that during the baseline period all 22 rats preferred the high-fat diet to the starch diet. After NPY administration 21 of 22 rats preferred the high-fat diet to the starch diet. On a gram intake basis (>60% of g from 1 diet) a similar pattern of preference for the high-fat diet emerges (baseline: 0/22; NPY: 6/22 preferred the high-fat diet). During the baseline period, 14 of 22 rats ingested >60% of kilocalories from the high-sucrose diet, and after NPY 13 of 22 rats preferred the sucrose diet. A similar pattern was seen based on grams of food eaten (baseline: 16 of 22; NPY: 15 of 22). We should note that NPY did increase the percentage of carbohydrate ingested compared with baseline data in the majority of the rats exposed to all three diet choices (cornstarch: 15 of 22; sucrose: 16 of 22; Polycose: 15 of 22).
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Role of Carbohydrate Type on Food Deprivation-Induced Diet Intake
The second group of rats was used to study the effects of food deprivation on diet choice. Food deprivation increased food intake compared with nondeprived controls during the lights-on period (Table 2). Intake of the high-fat and high-carbohydrate diets increased significantly (kcal or g) in all groups compared with nondeprived rats. There was a main effect of carbohydrate source [kcal: F(2,24) = 3.47, P = 0.048; g: F(2,63) = 5.03, P = 0.015], but not of treatment (i.e., baseline vs. food deprivation) [kcal: F(1,24) = 0.81, P = 0.38; g: F(1,24) = 0.71, P = 0.41], on the percent of kilocalories and grams ingested. There was no significant interaction noted in these analyses [kcal: F(2,24) = 0.09, P = 0.916; g: F(2,24) = 0.053, P = 0.948]. After food deprivation, rats consumed a similar proportion of their total energy or grams ingested from the high-starch diet compared with that observed during the 3-day baseline period (Fig. 2). The same pattern of choice was noted with the high-sucrose and high-Polycose diets.Role of Carbohydrate Type on Nocturnal Diet Consumption
We found that the pattern of intake during the first hour of the dark cycle agreed with that observed during spontaneous feeding (Fig. 3). There was a main effect of carbohydrate source [kcal: F(2,21) = 13.19, P = 0.0002; g: F(2,21) = 13.33, P = 0.0002], but not treatment (i.e., baseline vs. nocturnal) [kcal: F(1,21) = 1.08, P = 0.31; g: F(1,21) = 0.43, P = 0.52], on the percent of kilocalories and grams ingested during the 1-h nocturnal period. There was no significant interaction noted in these analyses [kcal: F(2,21) = 1.41, P = 0.267; g: F(2,21) = 1.08, P = 0.357]. In the corn starch group, ~24% of energy intake was derived from carbohydrate during daily feeding and ~22% during the 1-h nocturnal period (P > 0.05). In the sucrose group, ~59% of energy intake was derived from carbohydrate during spontaneous feeding and 68% during the 1-h nocturnal period (P > 0.05). Likewise, the rats selected ~72% of their energy intake from carbohydrate in the case of Polycose and 68% during the nocturnal period (P > 0.05).
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Three main findings emerge from the present results. 1) Daily diet selection in free-feeding rats can be modulated through the substitution of carbohydrate sources in high-carbohydrate diets given to rats allowed to choose between a high-carbohydrate and high-fat diet. 2) Diet selection, whether stimulated by NPY, food deprivation, or the onset of the dark cycle, is significantly related to daily diet selection. 3) NPY increases the amount of corn starch or sucrose consumed, relative to baseline consumption, when these carbohydrates are offered concomitantly with a high-fat diet. Although NPY administration increased the percent of food ingested from the corn starch or sucrose diets, it did not convert the majority of rats into carbohydrate preferrers (eating >60% of kcal or g from carbohydrate). On the other hand, the majority of rats did increase their intake of carbohydrate after NPY administration.
The contention that there is a correspondence between patterns of diet selection in baseline conditions and stimulated intake is supported by our finding that selection in the first hour of the light-dark cycle (lights off) also correlated with baseline diet preferences. The similarity between both stimulated and nocturnal 1-h diet selection with daily intake is important in that there is some question as to the validity of comparing daily diet selection and short-term (1 h) diet choice after acute drug stimulation (a standard method in macronutrient/diet studies). To establish such a link, it may be necessary to stimulate and measure short-term intake at different time periods (for example, during the day and during the dark cycle) and then determine whether or not they match daily intake patterns. The present results demonstrate a close association between short-term intake measured at two different times of the day, as well as a similarity between diet selection patterns during these times and spontaneous diet choice.
Most hypotheses concerning the mechanisms underlying the orexigenic effects of NPY have emphasized the biochemical and metabolic factors related to energy homeostasis (1, 4, 5) and nutrient balance (5). Although the present results seem to suggest that carbohydrate intake may be favored after NPY administration, they do not show that NPY primarily induces carbohydrate intake. NPY increased the proportion of energy ingested from the high-starch diet by 11% and from the high-sucrose diet by 10% compared with spontaneous intake. On the other hand, altering the source of carbohydrate from starch to sucrose or Polycose increased the proportion of energy ingested from the high-carbohydrate diet by 34 and 37%, respectively. Thus, despite the increased consumption of corn starch and sucrose after NPY stimulation relative to daily feeding, the baseline diet preferences of the animals are strong predictors of diet preference.
The present study did not directly compare selection between high-carbohydrate diets. However, the finding that both Polycose and sucrose were eaten in greater amounts than corn starch relative to the high-fat diet corresponds to recent data determining preferences for high-carbohydrate diets identical to those used in the current study (17). Diets with sucrose as the main source of carbohydrate were preferred to diets that contained either Polycose or corn starch as the main carbohydrate source, and diets containing Polycose were preferred to corn starch, as measured by two-jar preference tests. However, the latter study investigated preferences nocturnally, and preferences for such diets have not been examined over a 24-h period nor after NPY. The current findings emphasizing the importance of daily preference are not unique and are supported by recent results demonstrating a relationship between daily and NPY-stimulated diet selection (16). Taken together these results suggest that factors independent of NPY-induced alterations in energy and/or nutrient balance are important in influencing diet selection patterns after stimulation with this agent. In addition, the importance of metabolic/nutrient factors underlying NPY-induced hyperphagia must be tempered by evidence that NPY stimulates intake of noncaloric palatable solutions (hypotonic saline, saccharin) in satiated animals (while having little effect on water intake) (6). This suggests that NPY administration may play some role in inducing intake of sweet and salty fluids and indicates the influence of palatability independent of caloric value in NPY-induced feeding.
We also found a relationship between spontaneous and food deprivation-induced diet selection. During spontaneous feeding, more energy was derived from the high-fat diet when corn starch was offered as the high-carbohydrate diet. After food deprivation, the high-fat diet was still chosen in greater amounts, as has been previously noted (10, 11). Food deprivation did not significantly alter the preference for the high-sucrose or high-Polycose diets relative to the preference for the high-fat diet observed during baseline conditions.
The present findings emphasize that NPY-induced diet selection is affected by the source of carbohydrate in a high-carbohydrate diet. Furthermore, depending on the source of carbohydrate, rats can select differently among fat and carbohydrate diets during spontaneous feeding, and there is a relationship between stimulated and spontaneous diet selection. Although treatment with NPY can have a stimulatory effect on carbohydrate consumption, there is a strong similarity between daily and NPY-stimulated diet selection. Thus carbohydrate type, daily diet preference, and orexigenic treatment can each influence patterns of diet selection.
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ACKNOWLEDGEMENTS |
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This work was supported by the Department of Veterans Affairs, by National Institute of Drug Abuse Grants DA-03999 and TA-DA-07097, and by the National Institutes of Diabetes and Digestive and Kidney Disease Grants DK-42698 and P30-DK-50456.
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FOOTNOTES |
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Address for reprint requests: A. S. Levine, Research Service (151), VA Medical Center, One Veterans Drive, Minneapolis, MN 55417.
Received 6 June 1997; accepted in final form 5 September 1997.
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REFERENCES |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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