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Monell Chemical Senses Center, Philadelphia, PA 19104-3308
4To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • monosodium glutamate • inosine-5'-monophosphate • C57BL/6 and 129 mouse strains • taste • consumption
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). There is substantial evidence that the sensory basis for
this effect is that MSG stimulates the sense of taste (Dove 1948
, Kawamura and Kare 1987
). Indeed, recent
studies have provided convincing evidence that the taste quality
elicited by MSG and related substances such as inositol monophosphate
(IMP), herein labeled "umami," is unique. That is, it is not some
combination of sweet, sour, salty and bitter, the presumed other
primary taste qualities [but see (Halpern 1997
)].
The mechanism(s) underlying detection and recognition of umami
substances and the basis for their powerful ability to enhance
palatability and increase intake remain controversial or unknown.
Physiologic and behavioral studies using animal models and genetic
dissection of umami taste responses can potentially unravel these
mechanisms. MSG and other umami substances are detected and preferred
by several species of animals; most of the work, albeit still a very
small amount, has concentrated on rats and mice (Ninomiya and Funakoshi 1989a
and 1989b
, Yamamoto et al. 1991
and 1988
).
We recently reported differences in MSG acceptance between two inbred
mouse strains, C57BL/6ByJ and 129/J (Beauchamp et al. 1998
). Here, we further characterize ingestive responses to MSG
and IMP in these two strains and provide a preliminary report of
genetic analyses based on C57BL/6ByJ x 129/J hybrids.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Mice of the C57BL6/ByJ (B6) and 129/J (129) strains were obtained from The Jackson Laboratory (Bar Harbor, ME). The mice were housed in individual cages in a temperature-controlled room at 23°C on a 12-h light:dark cycle; mice had free access to deionized water and Teklad Rodent Diet 8604, which contains 0.31% sodium, 0.99% potassium and 1.46% calcium.
For genetic analyses, the B6 and 129 mice were outcrossed to produce
the first filial generation of hybrids (F1); these were
intercrossed to produce the second hybrid generation (F2).
The F1 was generated by reciprocal crosses using both
strains and genders: 1B F1 (
129 x 
B6) and B1
F1 (B6 x 129). Three types of the
F2 hybrids (n = 455) were obtained: 1B
x 1B F2 (1B F1 x 1B
F1; 92 females and 103 males), B1 x B1 F2
(B1 F1 x B1 F1; 106 females and 91
males) and B1 x 1B F2 (B1 F1 x 1B F1; 29 females and 34 males). Pups were weaned at
21–30 d of age and reared in same-sexed groups of 4–6.
Measurement of fluid intake.
Fluid intake was measured using two-bottle preference tests of
individually caged mice. Construction of drinking tubes and other
experimental details have been described previously (Bachmanov et al. 1996
). The drinking tubes were positioned to the right
of the feeder with their tips 15 mm apart, and each extended 25 mm into
the cage. Each tube had a stainless steel tip with a 3.175-mm diameter
hole from which the mice could lick fluids.
Solutions of monosodium salt of L-glutamic acid (MSG), disodium salt of inosine-5'-monophosphate (IMP), sucrose, D-phenylalanine and sodium saccharin (Sigma Chemical, St. Louis, MO) were prepared in deionized water. The mice were presented with one tube containing a solution and the other tube containing deionized water. The positions of the tubes were switched every 24 h to control for side preferences. Daily measurements were made in the middle of the light period by reading fluid volume to the nearest 0.2 mL. Body weights (BW) of individual mice were measured before and after each test series.
Data analyses.
Because fluid intakes can depend on BW (Bachmanov et al. 1998a
and 1998b
), we analyzed fluid intakes expressed per mouse (raw
intakes) and per BW. In experiments presented here, the B6 mice
consumed more MSG and IMP solutions than did the 129 mice, and they
also were heavier than the 129 mice. Therefore, in all cases when
intake per BW was higher in the B6 mice, the strain difference was even
larger for raw intakes. On the contrary, in some cases when raw intakes
were significantly higher in the B6 mice than in the 129 mice, intakes
expressed per BW did not differ significantly. Because intake per BW is
a more conservative index for characterizing strain differences, we
report only intakes per BW and preferences.
In all experiments with free access to MSG solutions, the B6 mice gained more weight than did the 129 mice. Among individual mice, there was a positive correlation between MSG intakes and BW gain. Thus, mice that consumed more MSG gained more weight. Therefore, in tests with MSG, we corrected MSG intakes using body weights measured before access to MSG. Because during access to IMP or sweeteners changes in BW were similar in the two strains, we used average BW before and after the tests to calculate intake of these solutions per BW.
Indices of fluid acceptance were calculated using average daily (24-h) fluid intakes for each mouse for each solution concentration. We determined the following: 1) raw intakes per mouse, 2) intakes per 30 g of BW (approximate weight of an adult mouse), and 3) preference scores [the ratio of the averaged solution intake to averaged total fluid (solution + water) intake, as a percentage].
The data were analyzed using Pearson correlation coefficients, t tests, ANOVA and planned comparisons as appropriate. The significance of preference/avoidance of a solution over water in the two-bottle tests was determined by comparing the solution and water intakes using paired t tests. Dominance in the F2 generation was detected when the F2 value differed significantly from a midparental value (this was achieved by collapsing B6 and 129 values, assigning the coefficient 1 for each of them, and assigning the coefficient -2 to the F2 value in planned comparison tests). All statistical tests used a two-tailed criterion for significance of P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Experiment 1. 0.1–1000 mmol/L MSG solutions were tested in ascending order in 5.5 mo old male B6 (n = 12) and 129 (n = 12) mice. Each MSG concentration was tested with water for 2 d. Before this experiment, the mice had been tested in two-bottle tests with series of concentrations of glycyrrhizic acid, SC-45647 (a guanidineacetic acid sweetener), sucralose and Polycose.
MSG intakes and preferences were significantly affected by MSG
concentration [F(9,198) = 69.9 and 93.3, respectively,
P < 0.0001, two-way ANOVA] and were higher
overall in the B6 strain compared with the 129 strain
[F(1,22) = 25.6 and 64.4, P < 0.0001]. The strain differences depended on MSG concentration [strain
x concentration interaction F(9,198) = 19.0 for
intakes and 2.2 for preferences, P < 0.05]. The two
strains drank similar amounts of 0.1–100 mmol/L MSG, but the B6 mice
drank more 300-1000 mmol/L MSG than did the 129 mice (Fig. 1
, top). Consumption of 300 mmol/L MSG by the B6 mice was remarkably
high, i.e., for some B6 mice, daily consumption of MSG exceeded one
half of their body weight.
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90%) preference over
the range of 1–300 mmol/L MSG concentrations and avoided 1000 mmol/L
MSG (Fig. 1
, lower panel). The 129 mice preferred 1–300
mmol/L MSG, reached peak of preference (95%) at 100 mmol/L
concentration, were indifferent to 600 mmol/L MSG and avoided 1000
mmol/L MSG. The B6 mice exhibited significantly higher MSG preference
scores compared with the 129 mice at 0.3–30 and 300-1000 mmol/L
concentrations. Thus, the B6 mice preferred a wider range of MSG
concentrations and had higher MSG preference scores than did the 129
mice. This experiment demonstrated concentration-specific strain differences in MSG acceptance. At lower MSG concentrations (0.3–30 mmol/L), the B6 mice had higher preference scores than did the 129 mice, but they did not differ significantly in intakes. At higher MSG concentrations (especially 300 and 600 mmol/L), the B6 mice consumed much more MSG than did the 129 mice. To confirm this pattern of strain differences, we conducted several additional experiments testing 1 and 300 mmol/L MSG (Experiments 2, 3 and 4).
Experiment 2. In this experiment, 4.5 mo old male B6 (n = 10) and 129 (n = 10) mice were given two-bottle tests with 1 mmol/L MSG and water for 4 d; for the next 4 d they received 300 mmol/L MSG and water. Before this experiment, the mice had been tested in two-bottle tests with solutions of saccharin, glycine, D-phenylalanine and sucrose.
Consistent with the results of Experiment 1, the two strains had
similar intakes of 1 mmol/L MSG, but the B6 mice had higher preferences
for this solution (Table 1
). When given 300 mmol/L MSG, the B6 mice had higher MSG preferences and
intakes compared with the 129 mice.
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Fluid intakes and preferences were analyzed using three-way ANOVA
to assess the effects of strain, gender and period of test (1–2 d vs.
3–4 d of the 96-h test). There were no significant changes in 1 mmol/L
MSG acceptance during the experiment; therefore all results are
presented as 4-d averages (Table 2
). Consistent with the previous observations, the two strains did not
differ significantly in 1 mmol/L MSG intakes [Table 2
; effect of
strain F(1,35) = 3.5, P > 0.05], and
the B6 mice had higher preferences for 1 mmol/L MSG compared with the
129 mice [Table 2
; effect of strain F(1,35) = 29.2,
P < 0.0001].
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; effect of strain
F(1,35) = 93.2 and 11.8, respectively, P
< 0.01]. However they changed during the 4-d test in a
strain-specific manner [strain x period interaction
F(1,35) = 61.0 for intakes and 14.1 for preferences,
P < 0.001]. Male and female B6 mice drank more 300
mmol/L MSG in the second half of the test compared with the first half,
whereas the MSG intakes decreased in the 129 males and did not change
in the 129 females (Fig. 2
, upper panel). Preferences for 300 mmol/L MSG decreased
significantly in 129 males, and they did not change in the other groups
(Fig. 2
, lower panel). As a result, the strain differences
in 300 mmol/L MSG acceptance were larger during the last 2 d of
the experiment compared with the first 2 d.
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There were no significant differences in 1 mmol/L MSG intakes [4.3
± 0.5 and 3.2 ± 0.4 mL/(30 g BW · d) for the B6 and 129
strains, respectively] or preferences (64 ± 3 and 59 ± 5%, respectively). The strain differences in acceptance of 300 mmol/L
MSG depended on whether this solution was tested before or after 1
mmol/L MSG, i.e., for both intakes and preferences, there was a
significant interaction between strain and group (Table 3
). The B6 mice that received first 1 mmol/L MSG and then 300 mmol/L MSG
had higher indices of 300 mmol/L MSG acceptance than similarly treated
129 mice and than B6 mice that received 300 mmol/L MSG before 1 mmol/L
MSG. Thus, these results are consistent with the results of Experiment
3, indicating that exposure to MSG exaggerates strain differences in
its acceptance. It is also consistent with the following experiment
conducted on the same mice showing a strain difference in 300 mmol/L
MSG acceptance in 4-d tests.
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During the initial 4-d test with 300 mmol/L MSG, the B6 mice drank more MSG than did the 129 mice [6.4 ± 1.3 and 3.0 ± 0.4 mL/(30 g BW · d), respectively, P < 0.05, t test]. Preference scores were 57 ± 8 and 53 ± 5%, respectively, (not significant).
Both B6 and 129 mice tested with saccharin strongly preferred it over water (preference scores were 96 ± 1 and 88 ± 4%, respectively; not significant, t test). Saccharin intakes were higher in the B6 mice than in the 129 mice [10.3 ± 0.5 and 6.1 ± 1.0 mL/(30 g BW · d), respectively, P < 0.01, t test]. Compared with the water-treated 129 mice, the water-treated B6 mice consumed more water [6.1 ± 0.3 and 5.2 ± 0.2 mL/(30 g BW · d), respectively, P < 0.05].
Indices of 300 mmol/L MSG acceptance before and after saccharin or
water tests were compared using three-way ANOVA with strain, group
(saccharin- or water-treated) and period (before and after saccharin or
water tests) as factors. During both MSG tests, saccharin- and
water-exposed B6 mice had higher 300 mmol/L MSG intakes than did
the 129 mice from corresponding groups [Fig. 3
; effect of strain F(1,20) = 6.2, P < 0.05]. All mice slightly but significantly increased MSG intakes in
the second test compared with the first test [Fig. 3
; effect of period
F(1,20) = 6.0, P < 0.05]. However
there were no significant differences between saccharin- and
water-exposed groups (no significant effects of group or
interactions between group and other factors). No significant effects
on 300 mmol/L MSG preferences were detected in this experiment.
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IMP solutions (0.01–100 mmol/L) were tested in ascending order in the same male B6 (n = 12) and 129 (n = 12) mice tested in Experiments 4 and 5. Each IMP concentration was tested with water for 2 d.
IMP intakes and preferences were significantly affected by IMP
concentration [F (8,176) = 44.2 and 35.5,
respectively, P < 0.0001, two-way ANOVA] and were
overall higher in the B6 strain compared with the 129 strain
[F(1,22) = 9.5 for intakes and 6.6 for preferences,
P < 0.05]. The strain differences depended on IMP
concentration [strain x concentration interaction F(8,176)
= 2.2 for intakes and 3.9 for preferences, P < 0.05]. Compared with the 129 mice, the B6 mice had higher IMP intakes
at 0.03–0.1 and 1–30 mmol/L concentrations (Fig. 4
, upper panel). The B6 mice preferred all IMP solutions
tested in this experiment (consumed significantly more IMP solution
than water, P < 0.05, paired t tests) and
exhibited high (80%) preference for 3–100 mmol/L IMP (Fig. 4
,
lower panel). The 129 mice preferred IMP solutions with
concentrations 
0.3 mmol/L (the significant preference for 0.01 mmol/L
IMP by this strain is probably due to chance) and exhibited high
(80%) preference for 30 and 100 mmol/L IMP. The B6 mice had
significantly higher IMP preference scores compared with the 129 mice
at 0.03–0.1 and 1–10 mmol/L concentrations. Thus, the B6 mice
preferred a wider range of IMP concentrations and had higher IMP
preference scores than did the 129 mice.
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The B6 and 129 mice (data from Experiment 3) were tested simultaneously with the same solutions as the F2 mice (n = 455). The F2 animals were 4–7 mo old when the tests began. Each taste solution was tested with water for 4 d. The solutions were tested in the following sequence: D-phenylalanine, saccharin, sucrose, 1 mmol/L MSG and 300 mmol/L MSG. One or 2 d with only water available separated tests of each solution. Because there were no (or only small) differences between F2 cross types, all F2 mice were combined in one group.
Mode of inheritance.
In male and female B6, 129 and F2 mice, we
analyzed daily taste solution intakes and preferences averaged for all
4 d of the test and for the last 2 d of the test (when the
strain differences were more pronounced, see Fig. 2
, Experiment 3). The
results were similar for both genders, for all indices of acceptance
(raw intakes, intakes per BW and preferences), and for 4-d and the last
2-d averages. We therefore present here only 4-d average intakes per BW
and preferences for males (Fig. 5
).
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Analysis of correlations.
The F2 mice varied substantially in body weight.
Fluid intakes, both raw and expressed per unit of BW, covaried with
body weight, which resulted in positive correlations among intakes of
all fluids tested. Correlations among preferences for solutions of MSG
and sweeteners for all F2 mice (males and females
together) are shown in Table 4
. Correlations calculated for each gender separately (not shown) were
very close to each other and the correlations in the combined
F2 group. Preferences for sucrose, saccharin and
D-phenylalanine correlated strongly with each other.
However, no significant correlations were found between preferences for
the two MSG solutions and between MSG and sweetener preferences.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MSG and IMP taste similarly to humans. It has also been suggested that
IMP itself is tasteless, but it enhances the taste of glutamate and
thus can make the subthreshold concentrations of glutamic acid
contained in saliva have a taste (Yamaguchi 1991
and 1998
). In any case, our data are consistent with a common
mechanism underlying taste responses to MSG and IMP in both humans and
mice.
We have also confirmed in several experiments a difference between responses to low (e.g., 1 mmol/L) and high (especially 300 mmol/L) MSG concentrations. The B6 mice had higher 1 mmol/L MSG preferences than did the 129 mice, but the two strains did not differ significantly in 1 mmol/L MSG intakes expressed per BW. In contrast, 300 mmol/L MSG intakes were much higher in the B6 than in the 129 mice. Preferences for 1 and 300 mmol/L MSG did not correlate in the F2 hybrid mice, suggesting that acceptance of these solutions depends on different mechanisms determined by different genes. It is possible that low and high MSG concentrations have different taste qualities or flavors. However, the difference between these two solutions may also depend on the postingestive effects of 300 mmol/L MSG, as discussed below.
The amount of 300 mmol/L MSG ingested by the B6 mice is remarkable and
rivals the amounts of very highly preferred sweet substances ingested
by this same strain (see Fig. 5
). What motivates this high consumption
is unknown. There may be several mechanisms, one of which may be
responsible for this high MSG intake, or they may work in concert. The
300 mmol/L MSG solution elicits strong responses in mouse MSG-best
and NaCl-best fibers of the glossopharyngeal and chorda tympani
nerves (Ninomiya et al. 2000
) and thus must have an
easily detectable taste. Therefore, high 300 mmol/L MSG consumption by
the B6 mice relative to the 129 mice may be due to the difference in
taste perception of MSG between these mouse strains. However, it is
evident that postingestive mechanisms also play a role. First, the B6
mice given access to MSG gained more weight than did the 129 mice. This
could be due to accumulation of water (300 mmol/L MSG is an osmotically
hypertonic solution and contains a substantial amount of sodium) or to
changes in metabolism (Jungas et al. 1992
), but in any
case, the difference in body weight gain suggests that the physiologic
consequences of MSG consumption for the B6 and 129 mice are different.
Second, the strain differences in 300 mmol/L MSG acceptance increased
when mice were exposed to this solution for a longer time (Experiments
3 and 4). In particular, the B6 mice tended to increase, and the 129
mice tended to decrease their MSG acceptance during a 4-d test (Fig. 2)
. This suggests that the postingestive effects of MSG may be
positively reinforcing to the B6 mice and aversive to the 129 mice. It
is unclear what kind of postingestive effects modify MSG acceptance,
but it is possible that the postingestive effects of MSG may interact
with its taste. For example, if osmotically hypertonic 300 mmol/L MSG
is palatable to the B6 animals, drinking this solution would make the
mice thirsty and would further stimulate consumption of this solution,
creating a vicious circle. Regardless of the underlying mechanism,
these studies demonstrate the importance of controlling for previous
experience in long-term taste acceptance tests. In this regard,
another possible carry-over effect, prior testing with sweet
compounds, did not appear to influence the results (Experiment 5).
Our data indicate that responsiveness to sweet or salty taste, which
have both been suggested as being involved in MSG and/or IMP
perception, cannot explain the strain differences in acceptance of the
umami-tasting compounds. There are several lines of evidence that
the strain differences in MSG acceptance do not depend on sweet taste.
First, previous exposure to saccharin did not affect acceptance of
subsequently tested MSG (Experiment 5). Second, the modes of
inheritance were different for MSG (recessive B6 alleles) and
sweeteners (additive or partial dominance of B6 alleles). Third, among
the F2 hybrid mice, preferences for several
sweeteners correlated positively with each other, but not with
preferences for MSG (Table 4)
. Thus, high acceptance of MSG and
sweeteners fortuitously coincides in the B6 mice (and must have been
fixed during inbreeding), and these traits are determined by different
and genetically unlinked genes. The independence of MSG and sweetener
acceptance also provides additional evidence that for mice, the taste
quality of MSG is not "sweet," as has been suggested from some
previous rodent studies (Kawamura and Kare 1987
,
Yamamoto et al. 1991
).
The strain differences in MSG and IMP acceptance were opposite to those
for NaCl, i.e., the B6 mice avoided and the 129 mice preferred NaCl
(Bachmanov et al. 1996
and 1998b
, Beauchamp and Fisher 1993
, Gannon and Contreras 1993
,
Lush 1991
). Thus, the strain differences in MSG and IMP
acceptance depend on factors other than the salty taste of
Na+ in MSG and IMP. The most parsimonious
hypothesis concerning taste quality for MSG and IMP in the mouse is
that it is unique. This is consistent with the results of studies using
a number of other species including humans (Ninomiya and Funakoshi 1989a
and 1989b
, Yamaguchi 1998
).
Obtaining F2 hybrids between mouse strains with
high and low MSG acceptance and characterizing their MSG consumption is
an important step in identifying genes that determine the strain
differences. We have demonstrated that high MSG acceptance by the B6
strain is inherited as a recessive trait (correspondingly, low MSG
acceptance by the 129 strain is inherited as a dominant trait), and
that this variation in MSG acceptance depends on different genes than
does the variation in sweetener acceptance. Using the
F2 mice, we are currently conducting a genome
screen to identify chromosomal regions containing genes that determine
the strain difference in MSG acceptance. On the basis of chromosomal
locations, it should then be possible to identify the genes themselves
(Collins 1992
). Thus, we expect that this study will
eventually result in understanding the molecular genetic basis of umami
taste responsiveness.
To summarize, we have described mouse strain differences in acceptance of the umami-tasting compounds, MSG and IMP, and characterized inheritance of this trait. To our knowledge, this is the first evidence for a specific genetic effect on the response to MSG, and thus should provide a useful tool to investigate the genetic basis for orosensory control of MSG sensitivity and preference.
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FOOTNOTES |
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2 Presented in part at the XII International
Symposium on Olfaction and Taste, San Diego, CA[Beauchamp et al.
1998].
3 Supported by National Institutes of Health grant
DC 00882.
5 Abbreviations used: 129, 129/J mouse strain; B6,
C57BL/6ByJ mouse strain; BW, body weight; IMP, disodium salt of
inosine-5'-monophosphate; MSG, monosodium salt of
L-glutamic acid.
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