Differential temperature dependence of taste nerve responses to various taste stimuli in dogs and rats MAKOTO NAKAMURA AND KENZO KURIHARA Faculty of Pharmaceutical Sciences, Hokkaido University, Sapporo 060, Japan
NAKAMURA, MAKOTO, AND KENZO KURIHARA. Differential temperature dependence of taste nerve responses to various taste stimuli in dogs and rats. Am. J. Physiol. 261 (Regulatory Integrative Comp. Physiol. 30): R&402-R1408, 1991.-The temperature dependence of the canine and rat chorda tympani nerve responses to various taste stimuli was examined. The temperature dependence greatly varied with species of stimuli. In the dog, the tonic responses to fructose, sucrose, acetic acid, and guanosine 5’-monophosphate (GMP) and the response induced by the synergism between monosodium glutamate (MSG) and GMP showed peaks at %30°C, whereas those to NaCl, NH&l, and MSG showed peaks between 10 and 20°C. In the rat, the tonic response to NH&l increased with an increase in temperature up to 45”C, whereas the responses to other stimuli examined showed peaks at -30°C. The responses to glycine, sucrose, and quinine showed sharp temperature dependence, and the responses to acids (HCl and acetic acid) and salts (NaCl and KCl) showed relatively flat dependence. The effects of the temperature change on dose-response curves for fructose, NH&l, and GMP were examined using dogs. The temperature change did not practically affect the thresholds for these stimuli and affected the magnitude of the responses to higher concentrations of stimuli. The origins of the temperature dependence were discussed in terms of taste receptor mechanisms. chorda tympani
nerve response; taste receptors;
thresholds
INTENSITIES vary with temperature of stimulus solution. It is especially important in food sciences how taste intensities of various stimuli vary in cold or hot foods. The temperature dependence of taste intensities raises the question of whether enzyme reactions are involved in the taste transduction process (5, 6). Many studies on the temperature dependence have been carried out psychophysically (4, 6, 9, 10, 15, 16, 23, 24). It was suggested that the slope of the psychophysical function for sweet taste is unaltered by temperature (16), suggesting that temperature changes affect threshold concentrations of stimuli and do not affect maximal responses. On the other hand, it was shown that low concentrations of sucrose gain sweetnessas temperature increases (4). This result was supported by current studies (9, 10); for glucose, fructose, and aspartame, the slopes of the psychophysical function were increased by cooling the tongue. Interestingly, the slope for saccharin was unaltered by temperature. The temperature dependence has also been studied electrophysiologically using the rat (1, 5, 8, 27, 30, 31), cat (18, 28, 32), rabbit (28), hamster (8), frog (29), and
TASTE
R1402
0363-6119/91
$1.50 Copyright
human (22). It was pointed out that the taste nerves sensitively respond to cold or warm water (18, 22). To obtain accurate temperature dependence of the taste responses, the responses to temperature changes themselves must be subtracted from the responses to stimulus solutions of different temperature. Using this method, the response-temperature relationships in various animals were examined, and it was demonstrated that the responses to different taste stimuli have a similar temperature dependence; the responses to most stimuli showed peaks at 20-30°C (18, 29, 31, 32). However, detailed analysis of the temperature dependence has not been carried out; e.g., whether the temperature change affects threshold concentrations or the maximal responseshas not been examined. In the present study, we have systematically examined the temperature dependence of the chorda tympani nerve responses to various taste stimuli. We mainly used dogs because no study on temperature dependence of the canine taste system has been carried out. For comparison, we also used rats. The results obtained show that the temperature dependence of the taste responses greatly varies with species of stimuli. The results also show that the temperature changes do not practically affect the thresholds for stimuli and mainly affect the magnitudes of the responses to higher concentrations of stimuli. The results are discussedin terms of taste receptor mechanisms. MATERIALS
AND METHODS
Dissection of chorda tympani nerves. Thirty-five adult mongrel dogs (7-12 kg) were used in the experiments. The dissection of the chorda tympani nerve was carried out essentially as described previously (9). The dog was anesthetized with an injection of pentobarbital sodium (20 mg/kg ip) after ketamine hydrochloride (2 mg/kg) was injected into muscle of the hind leg and maintained at a surgical level of anesthesia with supplemental injection of pentobarbital sodium. The animal was subjected to tracheotomy. The chorda tympani nerve was exposed by removing the musculature of the lower jaw. The nerve exposed was cut proximally near its entrance to the bulla and covered with liquid paraffin and petroleum jelly. The anesthetized animals were placed in a room with temperature kept at 20°C. Forty male albino rats of Wistar stock weighing 189250 g were used in the experiments. The dissection of the chorda tympani nerve was carried out essentially as
0 1991 the American
Physiological
Society
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
TEMPERATURE
DEPENDENCE
described previously (9). The rat was anesthetized with an injection of pentobarbital sodium (70 mg/kg ip) after ketamine hydrochloride (15 mg/kg) was injected into muscle of the hind leg and maintained at a surgical level of anesthesia with supplemental injections of pentobarbital sodium. The anesthetized rat was placed on a heating pad maintained at 40°C. The animal was subjected to tracheotomy, and the chorda tympani nerve was exposed by removing the condyloid and coronoid processes of the mandible and retracting the underlying musculature. The nerve was cut proximally near its entrance to the bulla and covered with liquid paraffin and petroleum jelly. Recording of chorda tympani nerve activities. The neural activities of the whole chorda tympani nerve of the dog and the rat were recorded with an Ag-AgCl hook electrode. The impulses were amplified with an alternating current amplifier, passed through an integrator (time constant 0.3 s), and displayed on a pen recorder. The initial peak height of the integrated response and the height at 20 s after onset of stimulation were taken as the magnitudes of the phasic and tonic responses, respectively. Chemical stimulation. Various chemicals were used to stimulate canine and rat tongues. Fructose and sucrose (sugar stimuli), glycine (amino acid stimulus), acetic acid and HCl (acid stimuli), NaCl, NH&l, and KC1 (salt stimuli), monosodium glutamate (MSG) and guanosine 5 ’ -monophosphate (GMP) (umami stimuli), and quinine (bitter stimulus) were used as chemical stimuli. Concentrations of the chemicals to induce large enough responseswere chosen. Temperature of the solutions was varied between 5 and 40 or 45°C. In these temperature ranges, the temperature of the tongue surface was readily controlled by flowing water and stimulus solution of different temperature on the tongue, and the taste nerve responses were completely reversible. Stimulus solutions were prepared by dissolving chemicals in deionized water. The pH of stimulating solutions was 5.6-6.0. pH changes that accompanied the temperature variation employed were 0.3 units at the most. This did not bring about any significant pH effect on the responses because the pH dependences of the responses around neutral pH were rather small. Stimulus solutions were applied to the tongue at a flow rate of 5 ml/s for 30 s in the dog and 15 ml/min for 1 min in the rat. These solutions were applied through a condenser in which water regulated to constant temperature was circulated. Temperature of stimulus solutions was monitored with a thermistor placed on the tongue surface. About 5 min were interposed between stimulations. The chorda tympani nerve responded to temperature changes themselves; e.g., application of deionized water of 10°C to the rat tongue adapted previously to deionized water of 30°C induced a response (19). To eliminate the responses to temperature changes themselves, the experiments were carried out as follows. First, deionized water of the temperature to be tested was flowed on the tongue for 2 min. During this flowing, the response due to the temperature changes themselves was readily adapted to a spontaneous level. After adaptation, stimulating solution of the same temperature was applied to the tongue.
OF
TASTE
NERVE
R1403
RESPONSES
Chemicals. The chemicals were obtained as follows: MSG from Nakarai Chemicals, disodium GMP from Yamasa Shoyu, and fructose, sucrose, and glycine from Wako Pure Chemicals. RESULTS
The summated responsesof the canine chorda tympani nerve to 500 mM sucrose and 500 mM fructose at different temperatures are shown in Fig. 1, top. Magnitudes of the responses at onset of stimulation (phasic response) and at 20 s after onset of stimulation (tonic response) are plotted as a function of temperature in Fig. 1, A and B, respectively. Here magnitude of the response to each
500 mM Sucrose vP+%m
*%v
JL
‘vJ+
30 s 500
mM
I
Fructose
i y@+Jv&
5
44&+++4,
10
JAIL
‘h
$Jhi
20
30
4o"c
IV. A 08. u 04.
B
r
u
OI 0
’
’ ’ I ’ I ’ I 10 20 30 40 Temperature (OC)
’
’
50
FIG. 1. Temperature dependence of canine chorda tympani nerve responses to 500 mM sucrose (0) and 500 mM fructose (0). Top: summated responses at different temperatures. Phasic (A) and tonic (B) responses (R) are plotted as a function of temperature. Magnitude of phasic or tonic response to each stimulus at 30°Cis taken as unity. Each point is mean & SE of data obtained from 5 (fructose) or 6 (sucrose) preparations.
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
R1404
TEMPERATURE
DEPENDENCE
OF
TASTE
stimulus at 30°C is taken as unity. Both responses to sucrose and fructose show peaks at -30°C. The response to sucrose more steeply decreases with a decrease in temperature to ~30°C than that to fructose. Figure 2 shows the response to acetic acid (pH 3.0). Both the phasic and tonic responses have peaks at -3OOC. The phasic response to acetic acid decreases less with a decrease in temperature to ~30°C than the responses to the sugars. Figure 3 shows the temperature dependence of the responses to 200 mM NaCl and 50 mM NH&l. The phasic responses to NaCl and NH&l are rather flat with the temperature change, whereas the tonic responses show peaks between 10 and 20°C, and a further increase in temperature leads to a decrease in the responses. Figure 4 shows the concentration-response relationships for fructose, NH&l, and GMP at different temperatures (10, 20, and 30°C). Here only the magnitudes of the tonic responses are plotted. The data for fructose at different temperatures follow a single curve within stand-
NERVE
RESPONSES
1.2 r 08. .
a 04. . Acetic
acid
(PH 3.0)
5
10
20
30
4o”c
12.
B 08.
A
a 04.
a 04. 0 01.‘.‘.‘.‘.’
a
0’ 0
’
50
FIG. 3. Temperature dependence of canine chorda tympani nerve responses to 200 mM NaCl (0) and 50 mM NH&l (0). Top: summated responses at different temperatures. Phasic (A) and tonic (I?) responses are plotted as a function of temperature. Magnitude of phasic or tonic response to each stimulus at 30°C is taken as unity. Each point is mean & SE of data obtained from 6 preparations.
T-.
B
10 20 30 40 Temperature (OC)
’ ’ ’ ’ ’ ’ ’ 10 20 30 40 Temperature (OC)
’
’ 50
FIG. 2. Temperature dependence of canine chorda tympani nerve response to acetic acid (pH 3.0, 50 mM). Top: summated responses at different temperatures. Phasic (A) and tonic (B) responses are plotted as a function of temperature. Magnitude of phasic or tonic response at 30°C is taken as unit. Each point is mean k SE of data obtained from 6 preparations.
ard error when the data at 10 and 20°C are normalized to those at 30°C. This is also true for GMP. These results suggest that threshold concentrations for these stimuli are not practically affected by temperature. The results also suggest that the affinity of the stimuli to the receptor sites is not practically affected by temperature. On the other hand, the data for NH&l do not follow a single curve when the data are normalized, and the threshold is affected by temperature. In common with fructose, GMP, and NH&l, the magnitudes of the responses to higher concentrations of stimuli are greatly decreased at 10°C. In a previous paper (2l), we showed that the canine chorda tympani nerve response to MSG alone is sup-
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
TEMPERATURE
DEPENDENCE
TASTE
NERVE
RESPONSES
4
25.
R1405
T
20. 15. a
OF
/
$
10.
05. 0
-2 .0
10 log [F;uctose]
0 (M)
2.0
B
1.6
a
0.8
12 l
A
04. 0 -3.0
-2.0 -1.0 log [NH&I] (M)
08.
0
u 04.
161 .
a
0
08 '
12.
B 08 l
I
I
-4.0
I
I
I
-3.0
log WPI
I
I
-2.0
uw
4. Temperature dependence of dose-response curves for tonic responses of canine chorda tympani nerve to fructose (A), NH&l (B), and guanosine 5’-monophosphate (GMP; C). Magnitude of response to 1 M fructose at 30°C is taken as unity. Each point is mean & SE of data obtained from n preparations as follows: n = 4 for fructose at 2O”C, NH&l at 30°C, and GMP at each temperature; n = 5 for fructose at 30 and 10°C and NH&l at 20°C; and n = 6 for NH&l at 10°C. A, 30°C; 0, 20°C; 0, 10°C.
cc
04.
FIG.
pressed by amiloride similarly to the response to NaCl (ZO), whereas the response to a mixture of low concentrations of MSG and GMP or that to GMP alone is not suppressed by amiloride. That is, the response to MSG is composed of what may be described as a “salt-dependent” component, and the response induced by the synergism between MSG and GMP or GMP alone is composed of an “umami-dependent” component. Figure 5 shows the temperature dependence of the responses to 300 mM MSG, the mixture of 100 mM MSG and 0.5 mM GMP, and 3 mM GMP. The response to MSG alone shows peaks at -15°C (phasic response) and 10°C (tonic response). On the other hand, the responses to the mixture of MSG and GMP and to GMP alone show peaks at -3O’C. Thus the temperature dependence of the response to MSG is quite different from that of the responses to the mixture and GMP alone. The present results support the conclusion in the previous paper (21) that the response to MSG is composed of a salt-depend-
0
1 0
10 20 30 40 Temperature (OC)
50
FIG. 5. Temperature dependence of canine chorda tympani nerve responses to 300 mM monosodium glutamate (MSG; 0), 3 mM GMP (A), and a mixture of 100 mM MSG and 0.5 mM GMP (0). Top: summated responses at different temperatures. Phasic (A) and tonic (B) responses are plotted as a function of temperature. Magnitude of phasic or tonic response to each stimulus at 30°C is taken as unity. Each point is mean & SE of data obtained from 5 (MSG) or 4 (MSG + GMP and GMP alone) preparations.
ent component and the response induced by the synergism between MSG and GMP or by GMP alone is composed of an umami-dependent component. The temperature dependence of the rat chorda tympani nerve responses to stimuli was also examined. Figure 6 shows the dependence of the tonic responses to 500 mM glycine, 500 mM sucrose, acetic acid (pH 3.0), and hydrochloric acid (pH 3.0). The responses to sucrose and glycine show sharp temperature dependence, with a peak at m30°C, whereas those to the acids show rather flat dependence. Figure 7A shows the temperature dependence of the responses to salts such as 100 mM NaCl,
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
R1406
TEMPERATURE
DEPENDENCE
OF
TASTE
NERVE
RESPONSES
summarized in Table 1. Here the magnitude of maximal response is taken as unity. As shown in Table 1, the A temperature dependence of the responses greatly varies 0.8 with species of stimuli. For example, the canine taste nerve responses to fructose, sucrose, acetic acid, and u GMP show peaks at -30°C, whereas the responses to NaCl and NH&l show peaks between 10 and ZOOC.In the rat, the response to NH&l increases with an increase in temperature up to 45°C (see also Fig. 7), whereas the responses to KC1 and NaCl as well as sweet, sour, and 1.2 r bitter stimuli show peaks at -30°C. Thus the temperaB ture dependence is greatly different even among salt stimuli. 08. Chemicals applied to the tongue surface stimulate the u receptor sites or channels and produce the receptor potentials. The receptor potential triggers a release of a 0.4 transmitter, which generates impulses in the taste nerve (17). Hence there are possibilities that the temperature 0: dependences of the taste nerve responses come from the 0 10 20 30 40 50 dependences of structures of channels or receptor sites, Temperature (“C) the second messenger system (3, 11, 25, 26), or the FIG. 6. Temperature dependence of tonic responses of rat chorda process of the transmitter release. In the process of the tympani nerve. A: responses to 500 mM sucrose (0) and 500 mM glycine transmitter release, there was no essential difference (0). B: responses to 1 mM hydrochloric acid (pH 3.0) (0) and 50 mM among different tastants (l7), and hence this process acetic acid (pH 3.0) (0). Magnitude of response to each stimulus at does not seem to contribute to the difference in the 30°C is taken as unity. Each point is mean t SE of data obtained from 4 (sucrose, glycine, and acetic acid) or 5 (hydrochloric acid) preparatemperature dependence among different tastants. tions. Therefore the temperature dependence of the taste nerve responses seemsto come from either the second messen1.2 ger system or the structure of the channels or receptor sites. In the following, the possibility that the second messenger system contributes to the temperature dependence is discussed. There is a possibility that the transduction mechanisms for the canine taste responses to fructose, sucrose, acetic acid, and GMP, with peaks at w30°C, are different from those of responses to NaCl, NH&l, and MSG alone, with peaks between 10 and ZOOC.The responses to the former stimuli may be mediated by a second messenger system, whereas those to the latter stimuli may be mediated by direct activation of cation channels (7, 12) or cation adsorption (5). The synergistic effect between GMP and MSG may be induced by a second messengersystem; a second messenger accumulated by stimulation of the MSG receptor may lead to an increase in the affinity to GMP (21). I 0' ' ' ' ' ( ' ' ' ' ' In general, enzyme activities involved in second mes0 10 20 30 40 50 senger systems are increased with a temperature increase Temperature (“C) up to at least the body temperature of mammals. There FIG. 7. Temperature dependence of tonic responses of rat chorda is no system in which a second messenger level is detympani nerve.A: responses to 100 mM NH&l (A), 100 mM NaCl (0), creased with an increase in temperature to ~30°C as far and 100 mM KC1 (0). B: response to 1 mM quinine. Magnitude of as we know. The sharp decreasesin the magnitude of the maximal response to each stimulus is taken as unity. Each point is taste responses with a temperature increase to ~30°C mean + SE of data obtained from 4 preparations. cannot be simply explained by the second messenger KCl, and NH&l. The responses to NaCl and KC1 have system. Hence we must consider another origin of the a peak at ~30’C, whereas the response to NH&l in- temperature dependence, especially of the decrease of creases with an increase in temperature up to 45OC. The the responses at >3O”C. A change in temperature at response to 1 mM quinine has a peak at -30°C (Fig. 7B). tongue surface leads to a conformational change of the receptor membranes, which will expose the receptor site or channels on the receptor membranes or bury the sites DISCUSSION or the channels into the membranes. The temperature dependence of the dose-response Statistical data on the temperature dependence of the tonic responses to va.rious stimuli in the dog and rat are curves in the dog (Fig. 4) indicates that the temperature I
.
I
.
r
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
TEMPERATURE
DEPENDENCE
OF
TASTE
NERVE
R1407
RESPONSES
Dog Fructose (500 mM) Sucrose (500 mM) Acetic acid (pH 3.0) NaCl(200 mM) NH&l (50 mM) MSG (300 mM) MSG (100 mM) + GMP GMP (3 mM)
(0.5 mM)
5 6 6 6 6 5 4 4
0.490&O. 180 0.350t0.130 0.370~0.070 0.580t0.090 0.710t0.070 0.630t0.130 0.330t0.100 0.140t0.130
4 4 4 4 4 4 4
0.050t0.036 0.07OkO.016 0.290t0.038 0.204t0.034
0.580t0.160
0.900~0.140 0.67OkO.060 0.590t0.060 1.000 0.900t0.090 0.680t0.140 0.830t0.030 0.780,tO.lOO
0.390t0.120
0.400t0.050 0.970t0.070 1.000 1.000 0.430t0.070 0.360t0.060
1.000 1.000 0.940t0.050 0.610t0.090 0.160t0.080 1.000 1.000
0.570t0.040 0.600t0.070 0.650t0.050 0.410t0.110 0.160t0.060 -0.lOOt0.080 0.000t0.090 O.llO,tO.180
1.000 1.000 1.000 1.000 0.810t0.033 1.000 1.000
0.48OkO.035 0.720~0.101 0.910t0.123 0.665kO.010 1.000 0.460t0.112 0.380t0.035
1.000
Rat Sucrose (500 mM) Glycine (500 mM) Acetic acid (pH 3.0) NaCl(lO0 mM) NH&l (100 mM) KC1 (100 mM) Quinine (1 mM)
0.090-1-0.041
0.160&0.010 0.210~0.095
0.070t0.042 0.13OkO.020 0.490t0.032 0.519t0.011 0.24OkO.031 0.280t0.029 0.290t0.048
Values are means t SE of magnitudes of tonic responses to various unity. MSG, monosodium glutamate; GMP, guanosine 5’-monophosphate.
change does not greatly affect the thresholds and affects magnitudes of the responses to higher concentrations of stimuli. This suggests that the temperature change at the tongue surface does not greatly affect the affinity of the stimuli with the receptor sites and affects efficacy or structure of receptor sites or channels. As shown in Table 1, the temperature dependence of the responses to some stimuli is different between dogs and rats. That is, although the temperature dependences of the responses to sugars and acids in the dog are not greatly different from those in the rat, the dependence of the responses to salts in the dogs is greatly different from that in the rat. Canine taste response to NaCl is composed of amiloride-sensitive and -insensitive cornponents with temperature dependences that are different from each other (19). On the other hand, the canine taste response to NaCl is composed only of an amiloridesensitive component (20). Probably, the difference in the temperature dependence of NaCl responses between the dog and the rat comes from the difference in the structure of channels or receptor sites for Na+. Further study will be needed to clarify to what extent the second messenger system and the structural changes of the receptor sites and the channels contribute to the temperature dependence of the taste nerve responses. Address Received
reprint 22 January
requests
to K. Kurihara.
1991; accepted
in final
stimuli;
0.370~0.095
0.300t0.083 0.87OkO.073 0.874t0.031 0.440t0.025 0.790t0.077 0.570t0.048
n, no. of animals.
Physiol.
Behav.
5* BEIDLER, L. M. 133-139,1954. 6 CALVINO, A. M.
Maximal
value
for each stimulus
is taken
as
28: 905-910, 1982. A theory
of taste
stimulation.
J. Gen. Physiol.
38:
Perception of sweetness: the effects of concentration and temperature. Physiol. Behav. 36: 1021-1028, 1986. 7. DESIMONE, J. A., G. L. HECK, S. MIERSON, AND S. K. DESIMONE. The active ion transport properties of canine lingual epithelia in vitro. J. Gen. Physiol. 83: 633-656, 1984. I. Y. Single fiber gustatory impulses in rat and hamster. 8* FISHMAN, J. CeZZ Comp. Physiol. 49: 319-334, 1957. g GREEN, B. G., AND S. P. FRANKMANN. The effect of cooling the ’ tongue on the perceived intensity of taste. Chem. Senses 12: 609l
619,1987. GREEN, B. G., AND S. P. FRANKMANN. The effect of cooling on the perception of carbohydrate and intensive sweeteners. Physiol. Behav. 43:515-519,1988. 11 HWANG, P. M., A. VERMA, D. S. BREDT, AND S. H. SNYDER. ’ Localization of phosphatidylinositol signaling components in rat taste cells: role in bitter taste transduction. Proc. NatZ. Acad. Sci. USA 87: 7395-7399,199O. KINNAMON, S. C., AND S. D. ROPER. Evidence for a role of voltage12* sensitive apical K+ channels in sour and salt taste transduction. Chem. Senses 13:115-121,1988. 13. KUMAZAWA, T., AND K. KURIHARA. Large enhancement of canine taste responses to sugars by salts. J. Gen. Physiol. 95: 1007-1018,
lo*
1990. KUMAZAWA, T., AND K. KURIHARA. Large synergism between 14*monosodium glutamate and 5’-nucleotides in canine taste nerve responses. Am. J. Physiol. 259 (Regulatory Integrative Comp. PhysioZ. 28): R420-R426, 1990. 15. MCBURNEY, D. H., V. B. COLLINGS, AND L. H. GLANZ. Temperature dependence of human taste responses. Physiol. Behav. 11:
89-94,1973. form
22 July
1991.
REFERENCES 1. ABOTT, P. S. The Effects of Temperature on Taste in the White Rat. Providence, RI: Brown University Press, 1953. 2. ANDERSEN, H. T., M. FUNAKOSHI, AND Y. ZOTTERMAN. Electraphysiological responses to sugars and their depression by salt. In: Olfaction and Taste, edited by Y. Zotterman. New York: Macmillan, 1963, p. 177-192. 3. AVENET, P., F. HOFMANN, AND B. LINDEMANN. Transduction in taste receptor cells requires CAMP-dependent protein kinase. NatureLond. 331:351-354,1988. 4. BARTOSHUK, L. M., K. RENNERT, J. RODIN, AND J. C. STEVENS. Effects of temperature on the perceived sweetness of sucrose.
16. MOSKOWITZ, H. R. Effects of solution temperature on taste intensity in humans. Physiol. Behav. 10: 289-292, 1973. 17. NAGAHAMA, S., AND K. KURIHARA. Norepinephrine as a possible transmitter involved in synaptic transmission in frog taste organs and Ca dependence of its release. J. Gen. Physiol. 85: 431-442,
1985. 18. NAGAKI, to taste
J., S. YAMASHITA, stimuli of varying
AND M. SATO. Natural response temperatures. Jpn. J. Physiol.
of cat
14: 67-
89, 1964. 19. NAKAMURA, M., AND K. KURIHARA. Temperature dependence of amiloride-sensitive and -insensitive components of rat taste nerve response to NaCl. Brain Res. 444: 159-164, 1988. M., AND K. KURIHARA. Non-specific inhibition by 20. NAKAMURA, amiloride of canine chorda tympani nerve responses to various salts: do Na+-specific channels exist in canine taste recentor mem-
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
R1408
TEMPERATURE
DEPENDENCE
branes? Bruin Res. 524: 42-48, 1990. 21. NAKAMURA, M., AND K. KURIHARA. Canine taste nerve responses to monosodium glutamate and disodium guanylate: differentiation between umami and salt components by amiloride. Bruin Res. 541: 21-28,1991. 22. OAKLEY, B. Taste responses of human chorda tympani nerve. Chem. Senses 10: 469-481,1985. 23. PANGBORN, R. M., R. B. CHRISP, AND L. L. BERTOLERO. Gustatory, salivary and oral thermal responses to solutions of sodium chloride at four temperatures. Percept. Psychophys. 8: 69-75, 1970. 24. STONE, H., S. OLIVER, AND J. KLOEHN. Temperature and pH effects on the relative sweetness of suprathreshold mixtures of dextrose and fructose. Percept. Psychophys. 5: 257-260, 1969. 25. STRIEM, B. J., U. PACE, U. ZEHAVI, M. NAIM, AND D. LANCET. IS adenylate cyclase involved in sweet taste transduction? (Abstract). Chem. Senses 11: 669,1986. 26. TONOSAKI, K., AND M. FUNAKOSHI. Cyclic nucleotides may me-
OF
TASTE
NERVE
RESPONSES
diate taste transduction. Nature Land. 331: 354-356, 1988. 27. YAMADA, K. Gustatory and thermal responses in the glossopharyngeal nerve of the rat. Jpn. J. Physiol. 16: 599-611, 1966. 28. YAMADA, K. Gustatory and thermal responses in the glossopharyngeal nerve of the rabbit and cat. Jpn. J. Physiol. 17: 94-110, 1967. 29. YAMASHITA, S. Chemoreceptor response in frog as modified by temperature change. Jpn. J. Physiol. 14: 488-504, 1964. 30. YAMASHITA, S., H. OGAWA, T. KIYOHARA, AND M. SATO. Modification by temperature change of gustatory impulse discharges in chorda tympani fibers of rats. Jpn. J. Physiol. 20: 348-363, 1970. 31. YAMASHITA, S., AND M. SATO. The effects of temperature on gustatory response of rats. J. Cell. Camp. Physiol. 66: 1-18, 1965. 32. YAMASHITA, S., K. YAMADA, AND M. SATO. The effect of temperature on neural taste response of cats. Jpn. J. Physiol. 14: 505-514, 1964.
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
NAKAMURA, MAKOTO, AND KENZO KURIHARA. Differential temperature dependence of taste nerve responses to various taste stimuli in dogs and rats. Am. J. Physiol. 261 (Regulatory Integrative Comp. Physiol. 30): R&402-R1408, 1991.-The temperature dependence of the canine and rat chorda tympani nerve responses to various taste stimuli was examined. The temperature dependence greatly varied with species of stimuli. In the dog, the tonic responses to fructose, sucrose, acetic acid, and guanosine 5’-monophosphate (GMP) and the response induced by the synergism between monosodium glutamate (MSG) and GMP showed peaks at %30°C, whereas those to NaCl, NH&l, and MSG showed peaks between 10 and 20°C. In the rat, the tonic response to NH&l increased with an increase in temperature up to 45”C, whereas the responses to other stimuli examined showed peaks at -30°C. The responses to glycine, sucrose, and quinine showed sharp temperature dependence, and the responses to acids (HCl and acetic acid) and salts (NaCl and KCl) showed relatively flat dependence. The effects of the temperature change on dose-response curves for fructose, NH&l, and GMP were examined using dogs. The temperature change did not practically affect the thresholds for these stimuli and affected the magnitude of the responses to higher concentrations of stimuli. The origins of the temperature dependence were discussed in terms of taste receptor mechanisms. chorda tympani
nerve response; taste receptors;
thresholds
INTENSITIES vary with temperature of stimulus solution. It is especially important in food sciences how taste intensities of various stimuli vary in cold or hot foods. The temperature dependence of taste intensities raises the question of whether enzyme reactions are involved in the taste transduction process (5, 6). Many studies on the temperature dependence have been carried out psychophysically (4, 6, 9, 10, 15, 16, 23, 24). It was suggested that the slope of the psychophysical function for sweet taste is unaltered by temperature (16), suggesting that temperature changes affect threshold concentrations of stimuli and do not affect maximal responses. On the other hand, it was shown that low concentrations of sucrose gain sweetnessas temperature increases (4). This result was supported by current studies (9, 10); for glucose, fructose, and aspartame, the slopes of the psychophysical function were increased by cooling the tongue. Interestingly, the slope for saccharin was unaltered by temperature. The temperature dependence has also been studied electrophysiologically using the rat (1, 5, 8, 27, 30, 31), cat (18, 28, 32), rabbit (28), hamster (8), frog (29), and
TASTE
R1402
0363-6119/91
$1.50 Copyright
human (22). It was pointed out that the taste nerves sensitively respond to cold or warm water (18, 22). To obtain accurate temperature dependence of the taste responses, the responses to temperature changes themselves must be subtracted from the responses to stimulus solutions of different temperature. Using this method, the response-temperature relationships in various animals were examined, and it was demonstrated that the responses to different taste stimuli have a similar temperature dependence; the responses to most stimuli showed peaks at 20-30°C (18, 29, 31, 32). However, detailed analysis of the temperature dependence has not been carried out; e.g., whether the temperature change affects threshold concentrations or the maximal responseshas not been examined. In the present study, we have systematically examined the temperature dependence of the chorda tympani nerve responses to various taste stimuli. We mainly used dogs because no study on temperature dependence of the canine taste system has been carried out. For comparison, we also used rats. The results obtained show that the temperature dependence of the taste responses greatly varies with species of stimuli. The results also show that the temperature changes do not practically affect the thresholds for stimuli and mainly affect the magnitudes of the responses to higher concentrations of stimuli. The results are discussedin terms of taste receptor mechanisms. MATERIALS
AND METHODS
Dissection of chorda tympani nerves. Thirty-five adult mongrel dogs (7-12 kg) were used in the experiments. The dissection of the chorda tympani nerve was carried out essentially as described previously (9). The dog was anesthetized with an injection of pentobarbital sodium (20 mg/kg ip) after ketamine hydrochloride (2 mg/kg) was injected into muscle of the hind leg and maintained at a surgical level of anesthesia with supplemental injection of pentobarbital sodium. The animal was subjected to tracheotomy. The chorda tympani nerve was exposed by removing the musculature of the lower jaw. The nerve exposed was cut proximally near its entrance to the bulla and covered with liquid paraffin and petroleum jelly. The anesthetized animals were placed in a room with temperature kept at 20°C. Forty male albino rats of Wistar stock weighing 189250 g were used in the experiments. The dissection of the chorda tympani nerve was carried out essentially as
0 1991 the American
Physiological
Society
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
TEMPERATURE
DEPENDENCE
described previously (9). The rat was anesthetized with an injection of pentobarbital sodium (70 mg/kg ip) after ketamine hydrochloride (15 mg/kg) was injected into muscle of the hind leg and maintained at a surgical level of anesthesia with supplemental injections of pentobarbital sodium. The anesthetized rat was placed on a heating pad maintained at 40°C. The animal was subjected to tracheotomy, and the chorda tympani nerve was exposed by removing the condyloid and coronoid processes of the mandible and retracting the underlying musculature. The nerve was cut proximally near its entrance to the bulla and covered with liquid paraffin and petroleum jelly. Recording of chorda tympani nerve activities. The neural activities of the whole chorda tympani nerve of the dog and the rat were recorded with an Ag-AgCl hook electrode. The impulses were amplified with an alternating current amplifier, passed through an integrator (time constant 0.3 s), and displayed on a pen recorder. The initial peak height of the integrated response and the height at 20 s after onset of stimulation were taken as the magnitudes of the phasic and tonic responses, respectively. Chemical stimulation. Various chemicals were used to stimulate canine and rat tongues. Fructose and sucrose (sugar stimuli), glycine (amino acid stimulus), acetic acid and HCl (acid stimuli), NaCl, NH&l, and KC1 (salt stimuli), monosodium glutamate (MSG) and guanosine 5 ’ -monophosphate (GMP) (umami stimuli), and quinine (bitter stimulus) were used as chemical stimuli. Concentrations of the chemicals to induce large enough responseswere chosen. Temperature of the solutions was varied between 5 and 40 or 45°C. In these temperature ranges, the temperature of the tongue surface was readily controlled by flowing water and stimulus solution of different temperature on the tongue, and the taste nerve responses were completely reversible. Stimulus solutions were prepared by dissolving chemicals in deionized water. The pH of stimulating solutions was 5.6-6.0. pH changes that accompanied the temperature variation employed were 0.3 units at the most. This did not bring about any significant pH effect on the responses because the pH dependences of the responses around neutral pH were rather small. Stimulus solutions were applied to the tongue at a flow rate of 5 ml/s for 30 s in the dog and 15 ml/min for 1 min in the rat. These solutions were applied through a condenser in which water regulated to constant temperature was circulated. Temperature of stimulus solutions was monitored with a thermistor placed on the tongue surface. About 5 min were interposed between stimulations. The chorda tympani nerve responded to temperature changes themselves; e.g., application of deionized water of 10°C to the rat tongue adapted previously to deionized water of 30°C induced a response (19). To eliminate the responses to temperature changes themselves, the experiments were carried out as follows. First, deionized water of the temperature to be tested was flowed on the tongue for 2 min. During this flowing, the response due to the temperature changes themselves was readily adapted to a spontaneous level. After adaptation, stimulating solution of the same temperature was applied to the tongue.
OF
TASTE
NERVE
R1403
RESPONSES
Chemicals. The chemicals were obtained as follows: MSG from Nakarai Chemicals, disodium GMP from Yamasa Shoyu, and fructose, sucrose, and glycine from Wako Pure Chemicals. RESULTS
The summated responsesof the canine chorda tympani nerve to 500 mM sucrose and 500 mM fructose at different temperatures are shown in Fig. 1, top. Magnitudes of the responses at onset of stimulation (phasic response) and at 20 s after onset of stimulation (tonic response) are plotted as a function of temperature in Fig. 1, A and B, respectively. Here magnitude of the response to each
500 mM Sucrose vP+%m
*%v
JL
‘vJ+
30 s 500
mM
I
Fructose
i y@+Jv&
5
44&+++4,
10
JAIL
‘h
$Jhi
20
30
4o"c
IV. A 08. u 04.
B
r
u
OI 0
’
’ ’ I ’ I ’ I 10 20 30 40 Temperature (OC)
’
’
50
FIG. 1. Temperature dependence of canine chorda tympani nerve responses to 500 mM sucrose (0) and 500 mM fructose (0). Top: summated responses at different temperatures. Phasic (A) and tonic (B) responses (R) are plotted as a function of temperature. Magnitude of phasic or tonic response to each stimulus at 30°Cis taken as unity. Each point is mean & SE of data obtained from 5 (fructose) or 6 (sucrose) preparations.
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
R1404
TEMPERATURE
DEPENDENCE
OF
TASTE
stimulus at 30°C is taken as unity. Both responses to sucrose and fructose show peaks at -30°C. The response to sucrose more steeply decreases with a decrease in temperature to ~30°C than that to fructose. Figure 2 shows the response to acetic acid (pH 3.0). Both the phasic and tonic responses have peaks at -3OOC. The phasic response to acetic acid decreases less with a decrease in temperature to ~30°C than the responses to the sugars. Figure 3 shows the temperature dependence of the responses to 200 mM NaCl and 50 mM NH&l. The phasic responses to NaCl and NH&l are rather flat with the temperature change, whereas the tonic responses show peaks between 10 and 20°C, and a further increase in temperature leads to a decrease in the responses. Figure 4 shows the concentration-response relationships for fructose, NH&l, and GMP at different temperatures (10, 20, and 30°C). Here only the magnitudes of the tonic responses are plotted. The data for fructose at different temperatures follow a single curve within stand-
NERVE
RESPONSES
1.2 r 08. .
a 04. . Acetic
acid
(PH 3.0)
5
10
20
30
4o”c
12.
B 08.
A
a 04.
a 04. 0 01.‘.‘.‘.‘.’
a
0’ 0
’
50
FIG. 3. Temperature dependence of canine chorda tympani nerve responses to 200 mM NaCl (0) and 50 mM NH&l (0). Top: summated responses at different temperatures. Phasic (A) and tonic (I?) responses are plotted as a function of temperature. Magnitude of phasic or tonic response to each stimulus at 30°C is taken as unity. Each point is mean & SE of data obtained from 6 preparations.
T-.
B
10 20 30 40 Temperature (OC)
’ ’ ’ ’ ’ ’ ’ 10 20 30 40 Temperature (OC)
’
’ 50
FIG. 2. Temperature dependence of canine chorda tympani nerve response to acetic acid (pH 3.0, 50 mM). Top: summated responses at different temperatures. Phasic (A) and tonic (B) responses are plotted as a function of temperature. Magnitude of phasic or tonic response at 30°C is taken as unit. Each point is mean k SE of data obtained from 6 preparations.
ard error when the data at 10 and 20°C are normalized to those at 30°C. This is also true for GMP. These results suggest that threshold concentrations for these stimuli are not practically affected by temperature. The results also suggest that the affinity of the stimuli to the receptor sites is not practically affected by temperature. On the other hand, the data for NH&l do not follow a single curve when the data are normalized, and the threshold is affected by temperature. In common with fructose, GMP, and NH&l, the magnitudes of the responses to higher concentrations of stimuli are greatly decreased at 10°C. In a previous paper (2l), we showed that the canine chorda tympani nerve response to MSG alone is sup-
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
TEMPERATURE
DEPENDENCE
TASTE
NERVE
RESPONSES
4
25.
R1405
T
20. 15. a
OF
/
$
10.
05. 0
-2 .0
10 log [F;uctose]
0 (M)
2.0
B
1.6
a
0.8
12 l
A
04. 0 -3.0
-2.0 -1.0 log [NH&I] (M)
08.
0
u 04.
161 .
a
0
08 '
12.
B 08 l
I
I
-4.0
I
I
I
-3.0
log WPI
I
I
-2.0
uw
4. Temperature dependence of dose-response curves for tonic responses of canine chorda tympani nerve to fructose (A), NH&l (B), and guanosine 5’-monophosphate (GMP; C). Magnitude of response to 1 M fructose at 30°C is taken as unity. Each point is mean & SE of data obtained from n preparations as follows: n = 4 for fructose at 2O”C, NH&l at 30°C, and GMP at each temperature; n = 5 for fructose at 30 and 10°C and NH&l at 20°C; and n = 6 for NH&l at 10°C. A, 30°C; 0, 20°C; 0, 10°C.
cc
04.
FIG.
pressed by amiloride similarly to the response to NaCl (ZO), whereas the response to a mixture of low concentrations of MSG and GMP or that to GMP alone is not suppressed by amiloride. That is, the response to MSG is composed of what may be described as a “salt-dependent” component, and the response induced by the synergism between MSG and GMP or GMP alone is composed of an “umami-dependent” component. Figure 5 shows the temperature dependence of the responses to 300 mM MSG, the mixture of 100 mM MSG and 0.5 mM GMP, and 3 mM GMP. The response to MSG alone shows peaks at -15°C (phasic response) and 10°C (tonic response). On the other hand, the responses to the mixture of MSG and GMP and to GMP alone show peaks at -3O’C. Thus the temperature dependence of the response to MSG is quite different from that of the responses to the mixture and GMP alone. The present results support the conclusion in the previous paper (21) that the response to MSG is composed of a salt-depend-
0
1 0
10 20 30 40 Temperature (OC)
50
FIG. 5. Temperature dependence of canine chorda tympani nerve responses to 300 mM monosodium glutamate (MSG; 0), 3 mM GMP (A), and a mixture of 100 mM MSG and 0.5 mM GMP (0). Top: summated responses at different temperatures. Phasic (A) and tonic (B) responses are plotted as a function of temperature. Magnitude of phasic or tonic response to each stimulus at 30°C is taken as unity. Each point is mean & SE of data obtained from 5 (MSG) or 4 (MSG + GMP and GMP alone) preparations.
ent component and the response induced by the synergism between MSG and GMP or by GMP alone is composed of an umami-dependent component. The temperature dependence of the rat chorda tympani nerve responses to stimuli was also examined. Figure 6 shows the dependence of the tonic responses to 500 mM glycine, 500 mM sucrose, acetic acid (pH 3.0), and hydrochloric acid (pH 3.0). The responses to sucrose and glycine show sharp temperature dependence, with a peak at m30°C, whereas those to the acids show rather flat dependence. Figure 7A shows the temperature dependence of the responses to salts such as 100 mM NaCl,
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
R1406
TEMPERATURE
DEPENDENCE
OF
TASTE
NERVE
RESPONSES
summarized in Table 1. Here the magnitude of maximal response is taken as unity. As shown in Table 1, the A temperature dependence of the responses greatly varies 0.8 with species of stimuli. For example, the canine taste nerve responses to fructose, sucrose, acetic acid, and u GMP show peaks at -30°C, whereas the responses to NaCl and NH&l show peaks between 10 and ZOOC.In the rat, the response to NH&l increases with an increase in temperature up to 45°C (see also Fig. 7), whereas the responses to KC1 and NaCl as well as sweet, sour, and 1.2 r bitter stimuli show peaks at -30°C. Thus the temperaB ture dependence is greatly different even among salt stimuli. 08. Chemicals applied to the tongue surface stimulate the u receptor sites or channels and produce the receptor potentials. The receptor potential triggers a release of a 0.4 transmitter, which generates impulses in the taste nerve (17). Hence there are possibilities that the temperature 0: dependences of the taste nerve responses come from the 0 10 20 30 40 50 dependences of structures of channels or receptor sites, Temperature (“C) the second messenger system (3, 11, 25, 26), or the FIG. 6. Temperature dependence of tonic responses of rat chorda process of the transmitter release. In the process of the tympani nerve. A: responses to 500 mM sucrose (0) and 500 mM glycine transmitter release, there was no essential difference (0). B: responses to 1 mM hydrochloric acid (pH 3.0) (0) and 50 mM among different tastants (l7), and hence this process acetic acid (pH 3.0) (0). Magnitude of response to each stimulus at does not seem to contribute to the difference in the 30°C is taken as unity. Each point is mean t SE of data obtained from 4 (sucrose, glycine, and acetic acid) or 5 (hydrochloric acid) preparatemperature dependence among different tastants. tions. Therefore the temperature dependence of the taste nerve responses seemsto come from either the second messen1.2 ger system or the structure of the channels or receptor sites. In the following, the possibility that the second messenger system contributes to the temperature dependence is discussed. There is a possibility that the transduction mechanisms for the canine taste responses to fructose, sucrose, acetic acid, and GMP, with peaks at w30°C, are different from those of responses to NaCl, NH&l, and MSG alone, with peaks between 10 and ZOOC.The responses to the former stimuli may be mediated by a second messenger system, whereas those to the latter stimuli may be mediated by direct activation of cation channels (7, 12) or cation adsorption (5). The synergistic effect between GMP and MSG may be induced by a second messengersystem; a second messenger accumulated by stimulation of the MSG receptor may lead to an increase in the affinity to GMP (21). I 0' ' ' ' ' ( ' ' ' ' ' In general, enzyme activities involved in second mes0 10 20 30 40 50 senger systems are increased with a temperature increase Temperature (“C) up to at least the body temperature of mammals. There FIG. 7. Temperature dependence of tonic responses of rat chorda is no system in which a second messenger level is detympani nerve.A: responses to 100 mM NH&l (A), 100 mM NaCl (0), creased with an increase in temperature to ~30°C as far and 100 mM KC1 (0). B: response to 1 mM quinine. Magnitude of as we know. The sharp decreasesin the magnitude of the maximal response to each stimulus is taken as unity. Each point is taste responses with a temperature increase to ~30°C mean + SE of data obtained from 4 preparations. cannot be simply explained by the second messenger KCl, and NH&l. The responses to NaCl and KC1 have system. Hence we must consider another origin of the a peak at ~30’C, whereas the response to NH&l in- temperature dependence, especially of the decrease of creases with an increase in temperature up to 45OC. The the responses at >3O”C. A change in temperature at response to 1 mM quinine has a peak at -30°C (Fig. 7B). tongue surface leads to a conformational change of the receptor membranes, which will expose the receptor site or channels on the receptor membranes or bury the sites DISCUSSION or the channels into the membranes. The temperature dependence of the dose-response Statistical data on the temperature dependence of the tonic responses to va.rious stimuli in the dog and rat are curves in the dog (Fig. 4) indicates that the temperature I
.
I
.
r
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
TEMPERATURE
DEPENDENCE
OF
TASTE
NERVE
R1407
RESPONSES
Dog Fructose (500 mM) Sucrose (500 mM) Acetic acid (pH 3.0) NaCl(200 mM) NH&l (50 mM) MSG (300 mM) MSG (100 mM) + GMP GMP (3 mM)
(0.5 mM)
5 6 6 6 6 5 4 4
0.490&O. 180 0.350t0.130 0.370~0.070 0.580t0.090 0.710t0.070 0.630t0.130 0.330t0.100 0.140t0.130
4 4 4 4 4 4 4
0.050t0.036 0.07OkO.016 0.290t0.038 0.204t0.034
0.580t0.160
0.900~0.140 0.67OkO.060 0.590t0.060 1.000 0.900t0.090 0.680t0.140 0.830t0.030 0.780,tO.lOO
0.390t0.120
0.400t0.050 0.970t0.070 1.000 1.000 0.430t0.070 0.360t0.060
1.000 1.000 0.940t0.050 0.610t0.090 0.160t0.080 1.000 1.000
0.570t0.040 0.600t0.070 0.650t0.050 0.410t0.110 0.160t0.060 -0.lOOt0.080 0.000t0.090 O.llO,tO.180
1.000 1.000 1.000 1.000 0.810t0.033 1.000 1.000
0.48OkO.035 0.720~0.101 0.910t0.123 0.665kO.010 1.000 0.460t0.112 0.380t0.035
1.000
Rat Sucrose (500 mM) Glycine (500 mM) Acetic acid (pH 3.0) NaCl(lO0 mM) NH&l (100 mM) KC1 (100 mM) Quinine (1 mM)
0.090-1-0.041
0.160&0.010 0.210~0.095
0.070t0.042 0.13OkO.020 0.490t0.032 0.519t0.011 0.24OkO.031 0.280t0.029 0.290t0.048
Values are means t SE of magnitudes of tonic responses to various unity. MSG, monosodium glutamate; GMP, guanosine 5’-monophosphate.
change does not greatly affect the thresholds and affects magnitudes of the responses to higher concentrations of stimuli. This suggests that the temperature change at the tongue surface does not greatly affect the affinity of the stimuli with the receptor sites and affects efficacy or structure of receptor sites or channels. As shown in Table 1, the temperature dependence of the responses to some stimuli is different between dogs and rats. That is, although the temperature dependences of the responses to sugars and acids in the dog are not greatly different from those in the rat, the dependence of the responses to salts in the dogs is greatly different from that in the rat. Canine taste response to NaCl is composed of amiloride-sensitive and -insensitive cornponents with temperature dependences that are different from each other (19). On the other hand, the canine taste response to NaCl is composed only of an amiloridesensitive component (20). Probably, the difference in the temperature dependence of NaCl responses between the dog and the rat comes from the difference in the structure of channels or receptor sites for Na+. Further study will be needed to clarify to what extent the second messenger system and the structural changes of the receptor sites and the channels contribute to the temperature dependence of the taste nerve responses. Address Received
reprint 22 January
requests
to K. Kurihara.
1991; accepted
in final
stimuli;
0.370~0.095
0.300t0.083 0.87OkO.073 0.874t0.031 0.440t0.025 0.790t0.077 0.570t0.048
n, no. of animals.
Physiol.
Behav.
5* BEIDLER, L. M. 133-139,1954. 6 CALVINO, A. M.
Maximal
value
for each stimulus
is taken
as
28: 905-910, 1982. A theory
of taste
stimulation.
J. Gen. Physiol.
38:
Perception of sweetness: the effects of concentration and temperature. Physiol. Behav. 36: 1021-1028, 1986. 7. DESIMONE, J. A., G. L. HECK, S. MIERSON, AND S. K. DESIMONE. The active ion transport properties of canine lingual epithelia in vitro. J. Gen. Physiol. 83: 633-656, 1984. I. Y. Single fiber gustatory impulses in rat and hamster. 8* FISHMAN, J. CeZZ Comp. Physiol. 49: 319-334, 1957. g GREEN, B. G., AND S. P. FRANKMANN. The effect of cooling the ’ tongue on the perceived intensity of taste. Chem. Senses 12: 609l
619,1987. GREEN, B. G., AND S. P. FRANKMANN. The effect of cooling on the perception of carbohydrate and intensive sweeteners. Physiol. Behav. 43:515-519,1988. 11 HWANG, P. M., A. VERMA, D. S. BREDT, AND S. H. SNYDER. ’ Localization of phosphatidylinositol signaling components in rat taste cells: role in bitter taste transduction. Proc. NatZ. Acad. Sci. USA 87: 7395-7399,199O. KINNAMON, S. C., AND S. D. ROPER. Evidence for a role of voltage12* sensitive apical K+ channels in sour and salt taste transduction. Chem. Senses 13:115-121,1988. 13. KUMAZAWA, T., AND K. KURIHARA. Large enhancement of canine taste responses to sugars by salts. J. Gen. Physiol. 95: 1007-1018,
lo*
1990. KUMAZAWA, T., AND K. KURIHARA. Large synergism between 14*monosodium glutamate and 5’-nucleotides in canine taste nerve responses. Am. J. Physiol. 259 (Regulatory Integrative Comp. PhysioZ. 28): R420-R426, 1990. 15. MCBURNEY, D. H., V. B. COLLINGS, AND L. H. GLANZ. Temperature dependence of human taste responses. Physiol. Behav. 11:
89-94,1973. form
22 July
1991.
REFERENCES 1. ABOTT, P. S. The Effects of Temperature on Taste in the White Rat. Providence, RI: Brown University Press, 1953. 2. ANDERSEN, H. T., M. FUNAKOSHI, AND Y. ZOTTERMAN. Electraphysiological responses to sugars and their depression by salt. In: Olfaction and Taste, edited by Y. Zotterman. New York: Macmillan, 1963, p. 177-192. 3. AVENET, P., F. HOFMANN, AND B. LINDEMANN. Transduction in taste receptor cells requires CAMP-dependent protein kinase. NatureLond. 331:351-354,1988. 4. BARTOSHUK, L. M., K. RENNERT, J. RODIN, AND J. C. STEVENS. Effects of temperature on the perceived sweetness of sucrose.
16. MOSKOWITZ, H. R. Effects of solution temperature on taste intensity in humans. Physiol. Behav. 10: 289-292, 1973. 17. NAGAHAMA, S., AND K. KURIHARA. Norepinephrine as a possible transmitter involved in synaptic transmission in frog taste organs and Ca dependence of its release. J. Gen. Physiol. 85: 431-442,
1985. 18. NAGAKI, to taste
J., S. YAMASHITA, stimuli of varying
AND M. SATO. Natural response temperatures. Jpn. J. Physiol.
of cat
14: 67-
89, 1964. 19. NAKAMURA, M., AND K. KURIHARA. Temperature dependence of amiloride-sensitive and -insensitive components of rat taste nerve response to NaCl. Brain Res. 444: 159-164, 1988. M., AND K. KURIHARA. Non-specific inhibition by 20. NAKAMURA, amiloride of canine chorda tympani nerve responses to various salts: do Na+-specific channels exist in canine taste recentor mem-
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
R1408
TEMPERATURE
DEPENDENCE
branes? Bruin Res. 524: 42-48, 1990. 21. NAKAMURA, M., AND K. KURIHARA. Canine taste nerve responses to monosodium glutamate and disodium guanylate: differentiation between umami and salt components by amiloride. Bruin Res. 541: 21-28,1991. 22. OAKLEY, B. Taste responses of human chorda tympani nerve. Chem. Senses 10: 469-481,1985. 23. PANGBORN, R. M., R. B. CHRISP, AND L. L. BERTOLERO. Gustatory, salivary and oral thermal responses to solutions of sodium chloride at four temperatures. Percept. Psychophys. 8: 69-75, 1970. 24. STONE, H., S. OLIVER, AND J. KLOEHN. Temperature and pH effects on the relative sweetness of suprathreshold mixtures of dextrose and fructose. Percept. Psychophys. 5: 257-260, 1969. 25. STRIEM, B. J., U. PACE, U. ZEHAVI, M. NAIM, AND D. LANCET. IS adenylate cyclase involved in sweet taste transduction? (Abstract). Chem. Senses 11: 669,1986. 26. TONOSAKI, K., AND M. FUNAKOSHI. Cyclic nucleotides may me-
OF
TASTE
NERVE
RESPONSES
diate taste transduction. Nature Land. 331: 354-356, 1988. 27. YAMADA, K. Gustatory and thermal responses in the glossopharyngeal nerve of the rat. Jpn. J. Physiol. 16: 599-611, 1966. 28. YAMADA, K. Gustatory and thermal responses in the glossopharyngeal nerve of the rabbit and cat. Jpn. J. Physiol. 17: 94-110, 1967. 29. YAMASHITA, S. Chemoreceptor response in frog as modified by temperature change. Jpn. J. Physiol. 14: 488-504, 1964. 30. YAMASHITA, S., H. OGAWA, T. KIYOHARA, AND M. SATO. Modification by temperature change of gustatory impulse discharges in chorda tympani fibers of rats. Jpn. J. Physiol. 20: 348-363, 1970. 31. YAMASHITA, S., AND M. SATO. The effects of temperature on gustatory response of rats. J. Cell. Camp. Physiol. 66: 1-18, 1965. 32. YAMASHITA, S., K. YAMADA, AND M. SATO. The effect of temperature on neural taste response of cats. Jpn. J. Physiol. 14: 505-514, 1964.
Downloaded from www.physiology.org/journal/ajpregu at Macquarie Univ (137.111.162.020) on February 12, 2019.
