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1 Pennington Biomedical Research Center, Louisiana State University, Baton Rouge, Louisiana 70808-4124; and 2 University of California- Lawrence Berkeley Laboratory, Berkeley, California 94720
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS AND PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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Nutrient preferences and orosensory responses were characterized in two mouse inbred strains. In two-bottle solution tests (tastant vs. vehicle; ascending concentrations), the effects of strain and chow type (12 or 26% fat) on preference thresholds for sucrose and corn oil were compared in AKR/J and SWR/J mice. SWR/J mice displayed lower preference thresholds and ingested more sucrose than AKR/J mice did. SWR/J mice also showed lower preference thresholds and consumed more corn oil than AKR/J mice did; corn oil preference was suppressed 3.5-fold in AKR/J mice compared with SWR/J mice when fed 26% fat chow. Next, licking was recorded during 30-s access to sucrose or corn oil across a range of concentrations. SWR/J mice licked the tastants more than AKR/J mice did. Analysis of modal interlick intervals during lick training revealed that SWR/J mice licked water faster than AKR/J mice when water deprived, suggesting that motor as well as sensory factors may determine lick responses to tastants in brief-access tests. Finally, in two-bottle tests pitting maximally preferred concentrations of sucrose (8 or 16%) against corn oil (20%), SWR/J mice highly preferred sucrose over corn oil at either sucrose concentration. AKR/J mice preferred corn oil over 8% sucrose but reversed their preference when 16% sucrose was offered. These results support a primary role of flavor in the nutrient preferences of SWR/J mice. In AKR/J mice, the low lick activity for sucrose and corn oil and greater suppression of corn oil preference by the high-fat chow suggest that their preferences depend more on postingestive factors than on flavor.
taste; drinking; inbred strains; mouse
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS AND PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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PREVIOUS STUDIES of the mouse inbred strains AKR/J and SWR/J have revealed a strain difference in their self-selected intake of fat and carbohydrate (25-27) and in their susceptibility to dietary obesity (31). Overall, AKR/J mice self-select a higher proportion of energy from fat sources, and SWR/J mice select a higher proportion of carbohydrate across a variety of experimental diet paradigms (25-27). The strain difference in this model is due largely to the robust and reliable fat preference of the AKR/J mice. In contrast, the carbohydrate preference by SWR/J mice is more variable across paradigms, suggesting a greater responsivity by this strain to some orosensory or postingestive factor(s).
Responses to carbohydrate- and fat-containing diets in studies of nutrient self-selection are not simply a function of generic macronutrient composition. Experimental animals respond also to nutrient type and physical form, which contribute to the specific sensory properties of a diet formulation (3) and to its postingestive effects. Therefore, the aim of the present studies was to isolate and investigate two common diet components that may influence patterns of macronutrient diet selection in AKR/J and SWR/J mice. First, preference thresholds for sucrose and corn oil were evaluated separately in naive mice. Because baseline fat intake may affect fat preference in experimental tests (29), mice were maintained on rodent chow containing either 12 or 26% fat. Next, lick responses to sucrose or corn oil were investigated in brief-access tests designed to minimize the influence of postingestive effects. Finally, the preference behavior of AKR/J and SWR/J mice for corn oil vs. sucrose was examined by pitting the maximally preferred concentration of corn oil against two sucrose concentrations identified as maximal or submaximal, on the basis of results from experiment 1.
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METHODS AND PROCEDURES |
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TOP
ABSTRACT
INTRODUCTION
METHODS AND PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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Animals
Five-week-old male AKR/J and SWR/J mice were purchased from The Jackson Laboratory (Bar Harbor, ME) and individually housed and tested in plastic boxes with corncob bedding. Mice were maintained on a 12:12-h light-dark cycle at an ambient temperature of 24-26°C. Mice used in the sucrose and corn oil experiments were fed either no. 5001 (12% fat by energy) or no. 5015 (26% fat) rodent chow (LabDiet, Richmond, IN) ad libitum on arrival in our facility (see macronutrient composition below). All other mice were fed no. 5001 ad libitum.Procedures
Preference experiments. Solutions were presented in 50-ml conical tubes fitted with rubber stoppers and stainless steel spouts of uniform size. Mice were first adapted to drinking from two bottles containing deionized water for 3-4 days. During the experiments, one bottle containing deionized water and the other containing the test solution were mounted on the wire feeder top with a distance of 7.5 cm between the two spout openings. Food was provided ad libitum between the two bottles, and the right-left position of the two bottles was alternated every 24 h to control for side preferences. Preference ratios were determined by pooling the data for each solution over 48 h (right and left bottle position) and were calculated with the equation [test solution consumed (g)]/[test solution + water or vehicle consumed (g)].
In experiment 1, 12 naive mice from each strain, divided into two chow diet groups (no. 5001 vs. no. 5015), were used for characterizing separately the preference thresholds for sucrose and corn oil. Preferences were assessed in consecutive 48-h, two-bottle tests (tastant vs. vehicle) starting at 0.1% (0.003 M) for sucrose and 0.005% for corn oil; the solution concentration was increased every 48 h. The starting concentration for sucrose was based on earlier rat studies (24). The no. 5001 chow diet (metabolizable energy, 3.30 kcal/g) was composed of 28.1% protein, 12.1% fat, and 59.8% carbohydrate (% of energy); the no. 5015 chow diet (3.7 kcal/g) was composed of 18.3% protein, 25.8% fat, and 55.9% carbohydrate (LabDiet). Chow intake was not measured. Within strain and chow type, groups of mice used for corn oil and sucrose experiments were balanced for initial body weight.Lickometer apparatus. In experiment 2, licking activity during brief-access stimuli presentations was determined using a MS-160 Davis Rig behavioral data-acquisition and analysis system (DiLog Instruments, Tallahassee, FL). This system is designed to record the latency to lick and all interlick intervals (ILIs) with a resolution of 1 ms. The system consists of a test cage with clear plastic sides and back and a stainless steel front with an opening for access to the sipper tube, a movable bottle carriage, and a sipper tube access shutter. The bottle carriage and tube access shutter are moved by computer-controlled stepper motors, allowing smooth acceleration as well as a warning move of the shutter before closure. Tongue contact with the sipper tube is detected via a radio-frequency contact circuit, and licks are stored in a data file. The sipper tube is connected to the circuit through a capacitor to prevent direct current. To minimize possible olfactory cues, the system has been modified to include an air pump, which provides a continuous air flow across the end of the sipper tube.
Lickometer training. A period of training is necessary for the mice to learn to approach the lick spout and drink during test sessions. For this purpose, mice are water deprived ~23 h/day in their home cage and receive water in the test cage only. During the initial 3-4 days of training, the animals are placed in the test cage with the access shutter open and allowed to drink for 10 min from the sipper tube. If animals do not drink sufficiently during the training session, they are given supplemental water in their home cage 2-4 h after the training session. Once the mice have learned how to find water in the apparatus, they receive 3 additional days of training to acclimate to the shutter action. The number of presentations is increased and the length of time the shutter is open is decreased daily until the time is equal to the length of the test presentation.
Lickometer test procedure. For the lick tests conducted in experiment 2, concentrations of sucrose or corn oil were tested in an ascending order of presentation. During each test session, each stimulus concentration series was presented only once, i.e., a single trial per session. The presentation length was 30 s, and the interpresentation interval was 30 s.
For the sucrose lick tests, mice were exposed to the tastant in the lickometer on the day preceding the test day. The sucrose concentrations and the presentation length on the preexposure day were the same as those conducted on the test day (2, 4, 8, 16, and 32%). For the corn oil lick tests, mice were naive to corn oil at the beginning of the experiment. The ascending series of concentrations (0.005, 0.01, 0.025, 0.05, 0.1, 0.25, 0.5, 1, 5, 10, 20, and 30%) was repeated once, i.e., the value for each mouse represents the mean of two trials conducted on 2 sequential test days. On the experimental test days for both sucrose and corn oil, motivation to approach the spout was induced by mild water deprivation, i.e., 9 h during the light period. In experiment 3, determinations of flavor preference were made in a choice between corn oil and sucrose. Two sucrose concentrations were tested: those identified in experiment 1 as maximally or submaximally preferred concentrations for AKR/J and SWR/J mice when maintained on the 12% fat chow type. The 20% concentration of corn oil was selected because it elicited the maximum preference in both mouse strains. Naive SWR/J (n = 16) and AKR/J (n = 15) mice were divided into two groups by sucrose concentration (8 or 16%) and given two 48-h, two-bottle preference tests (20% corn oil vs. sucrose). Thus all mice were tested with only one concentration of sucrose and were given ad libitum access to no. 5001 rodent chow (12% fat by energy).Solutions. Sucrose (ICN, Costa Mesa, CA) was dissolved in deionized water (as %wt/wt solution). The corn oil emulsions (Mazola, Best Foods, Englewood Cliffs, NJ) were prepared as oil in deionized water mixtures (%wt/wt) and stabilized with sodium stearoyl lactylate (Emplex, Patco, Kansas City, MO) at a concentration of 0.2% emulsifier per 10% corn oil. The oil emulsions were prepared with a bench top laboratory homogenizer (PRO Scientific, Monroe, CT) at high speed (15,000 rpm × 10 min) and then cooled to room temperature before use. Corn oil emulsions were prepared fresh daily, and sucrose solutions were prepared fresh every 48 h. When solutions were replaced, the bottles and stoppers were rinsed thoroughly with hot water and drained before adding the new solutions.
Measurement of the phase separation of corn oil from deionized
water.
The experiments reported in this study employed long-term preference
tests. The oil emulsions appeared to remain stable over the 24-h time
periods, i.e., they retained a milky white appearance without evidence
of an obvious oil phase. However, the large intake volumes recorded
suggested an unrealistic fat intake based on total daily calorie
intakes reported previously for these mouse strains (26).
To assess the actual degree of separation that occurred, the following
method was used (28). A 50-ml conical tube was fitted with
a rubber stopper containing a hole into which a stopcock was inserted
in place of the usual stainless steel sipper tube. Immediately after
homogenizing, the tube was filled with the corn oil-water emulsion,
inverted at the same angle as the feeder top on the mouse cage, and
mounted on a ring stand. At intervals, the stopcock was opened, and a
1-ml aliquot was withdrawn, weighed, and dried in an oven for 48 h. Two conical tubes were set up so that duplicate samples could be
obtained for each concentration tested (1, 5, 10, 20, 30, and 50%). In this manner, the percent corn oil remaining in the emulsion was quantified over time as shown in Fig. 1.
A replicate test of the 50% corn oil emulsion was performed, again
with duplicate samples, to verify the increased stability found with
this concentration (see below).
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Data analysis. The data for experiments 1 and 3 were analyzed both as absolute intake and preference ratios using a three-factor (strain × chow type × concentration) and two-factor (strain × concentration) repeated-measures ANOVA, respectively. Preference threshold was defined as the lowest concentration for which the mean consumption of tastant was reliably higher than the mean consumption of water or vehicle (24). In experiment 2, the effects on total licks of concentration and strain with concentration as a repeated factor were examined. A repeated-measures design was used to analyze the effects of strain and time on lick rate over successive seconds; an autoregressive type 1 structure was used in the covariance matrix. In general, when a main effect was observed, individual comparisons were evaluated using Tukey's protected t-test.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS AND PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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Experiment 1A: Sucrose Preference Threshold (2-Bottle Test)
Overall, SWR/J mice consumed more sucrose solution than AKR/J mice did [F(1,434) = 60.63, P < 0.0001], and absolute intake in grams was not affected by chow type [strain × chow type: F(1,434) = 0.45, P = nonsignificant (NS)] (Fig. 2). However, SWR/J mice displayed a lower preference threshold for sucrose than AKR/J mice [strain × concentration: F(22,434) = 76.84, P < 0.0001] that was weakly influenced by chow type [strain × chow type × concentration: F(22,434) = 2.98, P < 0.0001] (Fig. 2). Specifically, SWR/J mice preferred sucrose over water beginning at 0.7% (12% fat chow) and 0.5% (26% fat chow), whereas the lowest concentration at which AKR/J mice preferred sucrose solution over water was 4%, independent of chow type.Sucrose data are presented also as preference ratios within chow type,
allowing direct comparisons between strains across solution
concentrations (Fig. 3). There was a
significant interaction of strain-by-concentration on sucrose
preference in both chow types [12% fat chow:
F(22,214) = 8.79, P < 0.0001; 26% fat
chow: F(22,220) = 4.67, P < 0.0001].
Compared with AKR/J, SWR/J mice had significantly higher preference
ratios beginning at 0.7% (12% fat chow) and 0.6% sucrose (26% fat
chow) (Fig. 3) and continuing up to 8% sucrose. At higher
concentrations, sucrose preference began to decline after 4% in SWR/J
but continued to increase in AKR/J mice, up to the highest
concentration tested.
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Experiment 1B: Corn Oil Preference Threshold (2-Bottle Test)
SWR/J mice displayed a lower preference threshold for corn oil than AKR/J mice did [strain × concentration: F(12,234) = 27.01, P < 0.0001], and there was an interaction of strain and chow type on preference threshold [strain × chow type × concentration: F(12,234) = 4.87, P < 0.0001] (Fig. 4). The lowest concentrations at which SWR/J mice preferred corn oil over water were 1% (12% fat chow) and 5% (26% fat chow), whereas the preference threshold for AKR/J mice was 5% (12% fat chow) and 10% (26% fat chow). Thus the higher-fat chow was associated with a higher preference threshold for corn oil in both mouse strains compared with the lower-fat chow type. In addition, SWR/J mice consumed more of the corn oil emulsion than AKR/J mice did [F(1,234) = 34.70, P < 0.0001]. The absolute intake of corn oil emulsion was altered by chow type in both strains [F(1,234) = 38.09, P < 0.0001], i.e., it was lower with a maintenance diet of 26% compared with 12% fat chow, but there was no interaction of strain-by-chow type [F(1,234) = 1.11, P = 0.29] (Fig. 4).
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Corn oil data are also presented as preference ratios within chow type,
allowing direct comparisons between strains across solution
concentrations (Fig. 5). There was a
significant effect of strain-by-concentration on corn oil preference
for both chow types [12% fat chow: F(12,120) = 5.90, P < 0.0001; 26% fat chow: F(12,114) = 8.48, P < 0.0001]. In the groups that were fed 12% fat chow, a reliable strain difference in preference score was seen
only at 50% (P < 0.05). In mice receiving 26% fat
chow, strain comparisons revealed higher preference scores in AKR/J
mice at the lower concentrations of corn oil and a higher preference by SWR/J mice at higher concentrations of 10-20%. However, with 50% corn oil, the AKR/J strain's preference scores in both chow types were
twofold higher than SWR/J (P < 0.0001), which dropped
precipitously at this concentration (Fig. 5).
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Experiment 2: Acute Lick Responses to Sucrose or Corn Oil (1-Bottle Tests)
In Fig. 6, the mean number of total licks per 30 s as a function of mouse strain and sucrose concentration is plotted. Overall, SWR/J mice licked more of the sucrose solution than AKR/J did [F(1,60) = 21.49, P < 0.0001]. As the concentration increased, the SWR/J mice increased their solution intake more than AKR/J [strain × concentration: F(4,60) = 3.15, P < 0.05] (Fig. 6). The mean number of total licks per 30 s as a function of mouse strain and corn oil concentration is shown in Fig. 7. The series was repeated once, i.e., each concentration represents the mean of two trials. SWR/J mice licked more of the corn oil emulsions than AKR/J mice did [F(1,121) = 15.07, P < 0.001], and there was a strain × concentration interaction [F(11,121) = 3.30, P < 0.001] (Fig. 7).
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The availability of data collected during lickometer training
permitted an examination of lick rate in mice motivated by water deprivation. Figure 8A
represents the ILI histogram for SWR/J and AKR/J mice on the last day
of lick training. The reciprocal of the mode of the ILI distribution
represents the rate of licking. Although the pattern of these unimodal
ILI distributions is essentially the same, the SWR/J distribution
consists of ILIs in the range 80-130 ms and the AKR/J distribution
consists of ILIs in the range 100-150 ms. When only the peak or
modal ILI for each mouse is considered, the SWR/J mice showed a mean
ILI of 109 ± 4 ms compared with 129 ± 4 ms for AKR/J mice
(t = 
3.5, P < 0.001) (see Fig. 8A, inset). Thus the ILI data correspond
to a higher overall lick rate in SWR/J (Fig. 8B) under
conditions of 23-h water deprivation as shown by a significant main
effect of strain [F(1,12) = 27.90, P < 0.001]. The decline in the lick rate over time was similar in both
strains [F(29,348) = 2.03, P < 0.01]
as indicated by the absence of a strain-by-time interaction
[F(29,348) = 0.93, P = NS].
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It was not possible by post hoc analysis to address fully the question
of whether strain differences in the motor control system of licking
contributed to the response to palatable stimuli, i.e., mice were not
water deprived in the sucrose and corn oil experiments. However, data
derived from the brief-access sucrose test (Fig. 6) were analyzed for
ILI in the same manner as above. Figure
9A illustrates the ILI
histogram for SWR/J and AKR/J mice during access to 16% sucrose, the
concentration representing the greatest amount of licking in both
strains. When only the peak ILI for each mouse was considered (see Fig.
9A, inset), the SWR/J mice showed a mean ILI of
110 ± 0 ms compared with 116 ± 4 ms for AKR/J mice
(t = 1.79, P = 0.13), indicating that
within-burst lick rates were not different between strains when licking
16% sucrose. However, longer pauses between bursts of licking in AKR/J mice during the 30-s presentation resulted in a lower overall lick rate
in AKR/J relative to SWR/J mice [F(1,11) = 29.71, P < 0.001] (Fig. 9B). The decline in lick
rates over time was not different [F(29,319) = 1.44, P = 0.07], and there was no strain-by-time interaction
[F(29,319) = 0.93, P = NS].
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Experiment 3: Corn Oil vs. Sucrose Preference (2-Bottle Test)
With respect to solution intake (g) during the 4-day preference experiment, SWR/J mice ingested more of the sucrose solution than AKR/J mice did, and the intakes of both strains varied as a function of concentration [strain × sucrose concentration: F(1,78) = 45.76, P < 0.0001] (Fig. 10). Specifically, SWR/J mice highly preferred sucrose on all test days but consumed less sucrose solution relative to 20% corn oil when the sucrose concentration was increased from 8 to 16%. Their daily solute intake of sucrose increased slightly with the higher sucrose concentration, i.e., from approximately 2.0 to 2.4 g/day. AKR/J mice, however, preferred 20% corn oil relative to 8% sucrose but for only 2 of the 4 test days. Inexplicably, AKR/J mice showed no preference on day 1, and their corn oil preference on day 4 was unreliable (P = 0.06). When offered 16% sucrose, AKR/J mice drank significantly more sucrose solution than corn oil.
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The data from experiment 3 also were expressed as the
average of two, 48-h preference ratios. A significant interaction of strain-by-sucrose concentration [F(1,26) = 26.73, P < 0.0001] again was observed (Fig.
11). SWR/J mice highly preferred both concentrations of sucrose over corn oil; AKR/J mice, however, highly
preferred the corn oil emulsion over 8% sucrose but then completely
reversed their preference when the sucrose concentration was increased
to 16%.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS AND PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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Previous studies of strain differences in the phenotype of macronutrient diet selection revealed a robust preference for dietary fat in AKR/J mice and a preference for carbohydrate diets in SWR/J mice that were variable depending on the experimental diet formulation (24-27). These collective results focused attention on the orosensory and postingestive attributes of dietary components that may interact with genetic strain characteristics and influence self-selected macronutrient intakes. Thus the present studies describe preference thresholds and lick behavior in response to corn oil and sucrose in these mouse inbred strains.
Flavor responsiveness is inferred from the solution preferences of experimental animals in two-bottle tests (10). In the present study, preference threshold was defined as the minimum concentration at which the mice prefer to ingest tastant over the vehicle solution. With respect to both sucrose and corn oil, SWR/J mice displayed lower preference thresholds and higher solution intakes than AKR/J mice in 48-h preference tests. In addition, the preference threshold concentration and absolute intake of corn oil emulsion were significantly altered in both strains by the percent fat content of the maintenance chow. To assess the role of orosensory input, dissociated from postingestive events, brief-access tests of each tastant were performed (33). In these tests, SWR/J mice licked more of the sucrose and corn oil, with increasing solution concentrations, than AKR/J mice. Analyses of modal ILIs during lick training revealed a strain difference in maximal lick rate, indicating that motor as well as sensory factors may determine lick responses to tastants in brief-access tests. To our knowledge, this is the first report of 1) a mouse strain difference in deprivation-induced lick rates and 2) mouse lick responses to nutritive stimuli in brief-access tests. In the third experiment, the two-choice preference testing procedure was again used; this time 20% corn oil was paired with either 8 or 16% sucrose. While the SWR/J mice clearly preferred sucrose over corn oil at both sucrose concentrations, the AKR/J strain's preference for corn oil vs. sucrose was reversed when the higher of two sucrose concentrations was presented.
The results of experiment 1 demonstrated lower preference thresholds and a higher consumption of sucrose in SWR/J compared with AKR/J mice. The avidity of SWR mice and the indifference of AKR mice for sweet-tasting substances have been documented previously in group-housed mice (15). However, with the exception of concentration-response results for saccharin (15), published behavioral data available regarding preference thresholds for tastants in mouse inbred strains have not been found. In other mouse strains not including SWR/J and AKR/J, threshold has been measured by electrophysiological methods as the lowest sucrose concentration that evoked chorda tympani response (2, 9, 20). On the basis of the results of behavioral, electrophysiological, and genetic mapping studies, it has been shown that sucrose intake is strongly influenced by two genetic loci on chromosome 4 with independent effects on sensitivity (i.e., response threshold) and response magnitude (2). These loci appear to modify sucrose intake by altering peripheral nerve responses to sucrose (2). Actions of genes in these regions are likely contributing to the strain differences observed in the present studies of AKR/J and SWR/J mice.
SWR/J mice possess the genetically mediated ability to taste various
bitter substances (11); e.g., they have an acute ability to detect sucrose octaacetate, an acetylated sugar (12, 16; Smith, unpublished data), and also show avoidance of quinine (4; Smith, unpublished observation) and 6-n-propylthiouracil (PROP)
(Smith, unpublished observation). Thus the taste abilities of the SWR/J strain are characterized by bitter detection/avoidance as well as their
greater responsivity to sucrose and corn oil. Analogous studies of
genetically mediated sensitivity to bitter taste across human subjects
have employed PROP. Humans classified as PROP supertasters give the
highest intensity ratings to a variety of orosensory stimuli such as
sucrose, sweeteners, fats, and oral irritants; however, they show less
liking, i.e., assign lower hedonic ratings, for both high-sweet and
high-fat foods (8, 14, 21, 30). An explanation for the
relationship between bitter taste acuity and sensitivity to other taste
stimuli has not been elucidated. One area of investigation has
demonstrated differences in tongue anatomy between bitter tasters and
nontasters in both mice and humans that parallel their genetic taste
abilities (18, 19). Another line of evidence suggests that
gustducin, a G protein expressed in taste receptor cells, may mediate
both bitter and sweet signal transduction. Specifically,
-gustducin-deficient mice show reduced behavioral and
electrophysiological responses to sucrose, denatonium, and quinine but
not to sour and salty stimuli (32). Studies aimed at
identifying the genes responsible for a variety of taste traits are
currently in progress. For example, a family of genes encoding human
receptors for bitter taste has been discovered, and some of these genes
map to an interval that is homologous with a cluster of bitter taste
loci on chromosome 6 in the mouse (1, 17). Whether any of
these taste loci are linked with food preferences remains to be shown.
The results of experiment 1 also revealed that baseline dietary fat consumption is an environmental factor that can significantly influence chemosensory phenotypes. Both preference threshold and preference magnitude for corn oil were affected by chow type, and this effect was greater in the AKR/J mice (Fig. 3). Specifically, the lower-fat chow enhanced the preference for corn oil emulsions compared with the higher-fat chow. AKR/J mice first preferred corn oil to vehicle solution at 5% when fed the 12% fat chow, and this threshold was increased to 10% with the 26% fat chow. Similarly, in SWR/J mice, a preference for corn oil was first exhibited at 1% compared with 5% when fed the 12 or 26% chow, respectively. These observations are striking in view of the small difference in fat content between the two chow diets and suggest that peripheral neural taste responses can be modulated by nutrients contained in the diet.
The lower corn oil intake in mice fed the 26% fat chow, compared with 12% fat chow, contrasts with previous reports that rats fed a high-fat maintenance diet voluntarily drank more corn oil compared with rats fed a high-carbohydrate diet (22, 29). Results from metabolic studies indicate that a greater acceptance of fat in experiments with rats may be attributed to physiological adaptations resulting from 2-wk exposure to a 63% high-fat (by energy) diet, i.e., an increased capacity to absorb and oxidize fat (23). Alternatively, preexisting metabolic differences may underlie the 3.5-fold suppression of preference for 20% corn oil observed in the AKR/J mice compared with SWR/J mice when fed the 26% fat chow. A differential intake of the maintenance diets cannot be ruled out as a possible explanation for the greater corn oil intakes of mice fed the lower, 12% fat chow because chow intake was not measured.
In two-bottle preference tests performed over 24-48 h, postingestive effects cannot be dissociated from orosensory factors, including the central nervous system integration of both peripheral sensory and metabolic events. If postingestive effects are considered minimal or nonexistent in brief-contact, 3-min tests (6), then 30-s tests should be an even purer assessment of the response to orosensory stimulation. Therefore, experiment 2 examined the 30-s lick response of mice to the flavors of sucrose and corn oil across a range of concentrations using a computer-controlled lickometer. It has been shown that initial rates of licking in brief-access tests are concentration dependent and thus may reflect changes in palatability (5), which has been described as the hedonic response to flavor. If palatability is a contributing factor to the preferences observed in experiment 1, then a significant difference in lick activity between the two strains would be expected. Thus the results from experiment 2 provide evidence of strain differences in flavor responsiveness to these macronutrient solutions, although they do not rule out a role of postingestive effects on sucrose and corn oil consumption during longer periods of access. Electrophysiological studies of neural responses would provide further evidence that this strain difference is mediated by taste.
The observed strain effect on flavor responsiveness to sucrose or corn oil during brief-access tests could be a function of differences in chemosensory responses, in motor control of rhythmic tongue movements, or both. As seen in Figs. 8 and 9, the within-burst rate of licking characteristic of SWR/J mice when motivated by water deprivation was preserved in their response to 16% sucrose, as shown by mean peak ILIs of 109 ± 4 and 110 ± 0 ms, respectively. These peak ILIs correspond to an intraburst lick rate of 9.0 licks/s. AKR/J mice, however, showed mean peak ILIs of 129 ± 4 ms when water deprived and 116 ± 4 ms while licking sucrose, corresponding to intraburst rates of 7.5 and 8.6 licks/s, respectively. Without data describing the ILI for sucrose solution under deprivation conditions, the possible contribution of motor differences (7) cannot be determined. However, based on the modal ILI of 129 ms measured in the AKR/J mice under a highly motivating condition (water deprivation), these mice are capable of producing substantially more licks than 60 in a 30-s period (Fig. 6). It is therefore unlikely that motor factors were responsible for the decreased lick rate for sucrose displayed by AKR/J mice in the brief-access test. Rather, hedonic factors may have influenced their response. Finally, this report of mouse inbred strain differences further supports the existence of within-species variability in lick rates of mice (13).
In experiment 3, preference behavior was examined with two-bottle tests pitting sucrose against corn oil at maximally preferred concentrations. Specifically, in long-term tests, the greatest preference for corn oil in both mouse strains was observed at the 20% concentration, whereas for sucrose, the 16% concentration elicited the strongest preference in both strains. In addition, the 16% sucrose solution corresponded to the concentration at which AKR/J mice showed the greatest licking activity during 30-s tests. When presented with a choice between the two tastants, AKR/J mice displayed a higher preference ratio for corn oil relative to 8% sucrose but reversed their preference when 16% sucrose was offered (Fig. 11). This response was consistent with results of both the brief-access and 48-h preference tests, indicating a higher preference threshold for sucrose solutions in AKR/J compared with SWR/J mice. In contrast, SWR/J mice strongly preferred sucrose over corn oil at either concentration of sucrose, suggesting that their ultimate preference in composite diet paradigms may depend primarily on their response to its sweet flavor.
In summary, the results of these studies demonstrate that SWR/J mice have lower preference thresholds and greater flavor preferences for solutions of sucrose and corn oil compared with AKR/J mice. The flavor preferences of both strains to sucrose or corn oil were modified by the maintenance diet. In particular, the higher fat-containing chow resulted in higher preference thresholds and lowered corn oil intake in both mouse strains. The greater responsiveness by SWR/J mice to the flavors of sucrose and corn oil was independent of postingestive effects as shown in the 30-s lick tests. More revealing were the flavor preferences observed when the mice were given a choice between sucrose and corn oil. The SWR/J mice preferred sucrose over corn oil when the sucrose concentration was either 8 or 16%. However, if only a corn oil emulsion was presented, as in experiments 1 and 2, the SWR/J mice avidly consumed it. By contrast, the AKR/J mice strongly preferred corn oil over 8% sucrose, but at 16% sucrose clearly preferred the sucrose solution over corn oil.
Strain differences in dietary fat vs. carbohydrate intake identified in earlier studies were largely attributed to the robust and reliable fat preference of AKR/J mice (25-27). Considerably more variation in macronutrient diet preferences was observed in SWR/J mice across selection paradigms. In the present studies, the observations of lower preference thresholds, higher consumption, and increased lick activity of SWR/J mice for sucrose and corn oil compared with AKR/J mice indicate that a significant component of the macronutrient diet selection phenotype in this animal model may be driven by taste-based factors. Thus within certain inbred strains such as SWR/J, the preference (or relative intake) for fat vs. carbohydrate, particularly sweet-tasting carbohydrate sources, may be driven by chemosensory attributes of the nutrients. By comparison, the relative indifference of AKR/J mice for sucrose both in brief-access and long-term preference tests, as well as for corn oil in brief-access testing, argues against a primary role of flavor in determining the preferential fat selection characteristic of this strain. This, combined with the evidence for a suppression of corn oil intake in AKR/J mice when fed a high-fat chow, suggests that the predisposition of AKR/J mice to select high-fat diets is more dependent on postingestive factors.
Perspectives
The divergence in proportional fat intake characterized previously in this pair of mouse inbred strains provides a model for investigating the genetic basis for macronutrient diet preferences. The present observations of differences in flavor responses to nutrient stimuli by SWR/J and AKR/J mice provide key information for developing valid phenotypic measures of dietary fat and carbohydrate preferences. This is the first report of the use of the brief-access paradigm in mice for the purpose of dissociating orosensory influences on intake from postingestive factors in the mechanisms of feeding and drinking.| |
ACKNOWLEDGEMENTS |
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We thank P. K. Andrews and B. Belton for assistance with data collection, and Dr. H.-R. Berthoud for helpful comments throughout.
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FOOTNOTES |
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This research was supported by National Institute of Diabetes and Digestive and Kidney Diseases Grants DK-53113 (B. K. Smith Richards) and DK-45895 (D. B. West) and by Knoll Pharmaceutical (B. K. Smith Richards).
Address for reprint requests and other correspondence: B. K. Smith Richards, Pennington Biomedical Research Center, 6400 Perkins Rd., Baton Rouge, LA 70808-4124 (E-mail: richarbk{at}pbrc.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 18 October 2000; accepted in final form 30 April 2001.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS AND PROCEDURES
RESULTS
DISCUSSION
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P < 0.05, 
P < 0.005, * P < 0.0001, sucrose vs. water. Values represent means ± SE.
, AKR/J;
, SWR/J.
