- Email: [email protected]
Effects of acids on neural activity elicited by other taste stimuli in the rat chorda tympani
Brain Research 859 Ž2000. 369–372 www.elsevier.comrlocaterbres
Short communication
Effects of acids on neural activity elicited by other taste stimuli in the rat chorda tympani Norio Sakurai, Fukujyu Kanemura, Ken Watanabe, Yasutake Shimizu, Keiichi Tonosaki
)
Department of Veterinary Physiology, Faculty of Agriculture, Gifu UniÕersity, 1-1 Yanagido, Gifu, Gifu 501-1193, Japan Accepted 14 December 1999
Abstract The purpose of this study is whether the gustatory neural response of taste cell to a binary mixture with threshold concentration of acid becomes synergistic or antagonistic can be estimated from the whole chorda tympani ŽCT. nerve in the rat. The present data demonstrate that acids are synergistic enhancer for sugars, and suppressor for NaCl and QHCl, but no effect to glycine and alanine. These results suggest that the acid was modifying the interaction of the other stimulus with its transduction mechanism. q 2000 Elsevier Science B.V. All rights reserved. Keywords: Acid; Binary mixture; Chorda tympani nerve; Gustatory; HCl
Understanding of the recognition mechanism of mixed taste is quite important, because taste stimuli actually encountered in natural feeding are complex mixture of various taste substances. Physiological and behavioral studies of the sensory effects of the taste stimuli in mixtures have been done in hamsters and rats w3,6–8,12– 14,18,20,22,30x w33,35x. These studies used variety of taste chemicals which clearly elicited good taste responses, and have shown that the responses to the mixtures are stronger or weaker than the superposition; that is, the synergetic or antagonistic effect appears, depending on the combinations of two components and their concentrations. However, there are few neural and behavioral studies that show the threshold concentration of acids affect other taste qualities. Here, we report that the threshold concentrations of acids are synergistic enhancer for sugars, and suppressor for NaCl and QHCl, but no effect to glycine and alanine. We used twenty Wistar rats weighing 250–300 g, which were housed in plastic cages at 228C with a 12:12-h light–dark cycle Žlight on 0700–1900 h.. They were given free access to laboratory chow ŽLABO MR Stock, NihonNosan, Yokohama, Japan. and water.
)
Corresponding author. Tel.: q81-58-293-2938; fax: q81-58-2932938; e-mail: [email protected]
Chorda tympani ŽCT. nerve responses were recorded as previously described w26x. Briefly, each rat was deeply anesthetized by an intraperitoneal injection of sodium pentobarbital Ž50 mgrkg body weight. and the trachea was cannulated and the hypoglossal nerve was transected bilaterally to prevent tongue movements. The CT nerve was then exposed through a mandibular approach and placed upon a pair of silver wire electrodes. The electrical activity of the whole nerve was fed to an AC amplifier and then displayed on an oscilloscope screen. Neural responses, resulting from chemical stimulation on the tongue, were integrated Žtime constant: 1.0 s. and recorded on a chart recorder. The tongue was gently extended with a hook, and test solutions were applied for 20 s at a constant rate of 0.5 mlrs by a gravity flow system. Each stimulus was followed by a deionized distilled water rinse delivered at the same rate for more than 60 s to avoid aftereffects of the preceding stimulation. The steady-state phase of the integrated CT neural response was measured at 10 s after the onset of stimuli, was normalized to the response to 0.1 M NH 4 Cl, which was taken as unity Ž1.0.. The integrity of each preparation was monitored by the periodic application of 0.1 M NH 4 Cl. The taste stimuli employed were as follows: sucrose, glucose, fructose, galactose, maltose, lactose, glycine, alanine, NaCl, QHCl, HCl, acetic acid, citric acid and NH 4 Cl. All chemicals were reagent grade, dissolved in deionized
0006-8993r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 0 6 - 8 9 9 3 Ž 0 0 . 0 2 0 0 2 - 3
370
N. Sakurai et al.r Brain Research 859 (2000) 369–372
Fig. 1. Typical examples of the CT nerve responses to several taste stimuli. Upper row presents the integrated responses to various concentrations of HCl, and middle row presents the responses to individual components, and lower row presents responses to one heterogeneous binary mixture with HCl Ž0.5 mM.. All of the records were obtained from the same CT nerve. Suc: 0.5 M sucrose, Glu: 0.5 M glucose, Fru: 0.5 M fructose, Gal: 0.5 M galactose, Mal: 0.5 M maltose, Lac: 0.5 M maltose, Gly: 0.5 M glycine, Ala: 0.5 M alanine, NaCl: 20 mM sodium chloride, QHCl: 20 mM quinine–HCl.
distilled water and presented at room temperature. We used the threshold level concentration of each acid solution, that is, it did not elicit the taste response of the CT nerve by itself. Final concentration of each chemical in the binary mixed taste solution with acid was adjusted to be the respective concentration. All values are presented as means" S.E. Statistical significance was examined by two-way analysis of variance ŽANOVA., with post-hoc testing by means of Duncan’s multiple range test. Comparisons between groups were made by Student’s t-test. To test whether the threshold concentration of acid solution affects on the taste response to sucrose, glucose, fructose, galactose, maltose, lactose, glycine, alanine, NaCl
and QHCl have been studied in rats. Fig. 1 shows the typical example of the taste responses, and all of the records were obtained from the same CT nerve. The low concentration of acid stimulus ŽHCl: 0.5 mM. did not elicit the taste response of the CT nerve by itself, but it enhanced the response to sugars, and suppressed the response to NaCl and QHCl, while it did not affect the response to glycine and alanine. Fig. 2 presents the data for concentration–response relationships of HCl ŽFig. 2a., sucrose ŽFig. 2b., glycine ŽFig. 2c., alanine ŽFig. 2d., NaCl ŽFig. 2e. and QHCl ŽFig. 2f.. The HCl significantly affected the response magnitude measures except glycine and alanine response. Similar results were obtained when the threshold
Fig. 2. Concentration–response relationships for Ža. HCl Ž n s 15., Žb. sucrose Ž n s 6. and sucrose q HCl Ž n s 6., Žc. glycine Ž n s 6. and glycineq HCl Ž n s 6., Žd. alanine Ž n s 6. and alanineq HCl Ž n s 6., Že. NaCl Ž n s 7. and NaCl q HCl Ž n s 7., and Žf. QHClŽ n s 7. and QHClq HCl Ž n s 7.. HCls in b to f are 0.5 mM concentration. Steady-state responses of the integrated CT nerve activity were normalized to means of those to 0.1 M NH 4 Cl, which were taken as unity Ž1.0. and the values were presented as means" S.E. The numbers within vertical axis show the relative response magnitude and the horizontal axis shows concentrations. Asterisks and double asterisks indicate p - 0.05 and p - 0.01, respectively.
N. Sakurai et al.r Brain Research 859 (2000) 369–372
concentration of acetic acid or citric acid was binary, applied with each taste chemicals Ždata not shown.. The threshold concentration of acid stimulus ŽHCl. is a synergistic effect for sugars, and a suppressive effect for NaCl and QHCl, but it has no effect for glycine and alanine. Both glycine and alanine are amino acids and are known as a sweetish substances. It is, however, clear from the present study that, either by sugars or amino acids, an entirely different type of response is elicited. This can be explained that the taste cell has multidifferent receptor cites for sweeteners w3,17,30–34x. These results also suggest that HCl was modifying the interaction of the other stimulus with its transduction mechanism. This mechanism does not necessarily need to be specific for HCl, but may be common for all acids because analogous effects were observed in the case of acetic acid and citric acid. There are wide variety of mechanisms by which acids cause the taste responses w1,2,4–16,18–25,27–29,35x. However, the mechanism by which the acid affects the CT nerve activity is not clear at present. Alternatively, it has been suggested that cytoplasmic acidification of the taste cells can be related to acid detection w9,19,25x. In accordance with this, Bigiani and Roper w4x observed that electrical coupling between taste receptor cells in Necturus were reduced in response to cytoplasmic acidification. This observation is supported by the evidence that a decrease in cytoplasmic pH impairs electrical communication via gap junctions w11,15,16,27,28,35x. Weak acids can penetrate cell membranes and are expected to dissociate intracellularly leading to cytoplasmic acidification w9,10x. It is, therefore, probable that the acid penetration into taste cells leads various kinds of membrane permeability and the taste response profiles.
References w1x L.M. Beidler, Anion influences on taste receptor response, in: T. Hayashi ŽEd.., Olfaction and Taste II, Pergamon, New York, 1967, pp. 509–535. w2x L.M. Beidler, Taste receptor stimulation with salts and acids, in: L.M. Beidler ŽEd.., Handbook of Sensory Physiology IV: Chemical Senses, Part 2: Taste, Springer-Verlag, Berlin, 1971, pp. 200–220. w3x L.M. Beidler, K. Tonosaki, Multiple sweet receptor sites and taste theory, in: D.W. Pfaff ŽEd.., Taste, Olfaction and the Central Nervous System, Rockefeller Univ.Press, 1985, pp. 47–64. w4x A. Bigiani, S.D. Roper, Reduction of electrical coupling between Necturus taste receptor cells, a possible role in acid taste, Neurosci. Lett. 176 Ž1994. 212–216. w5x M.E. Frank, An analysis of hamster afferent taste nerve response functions, J. Gen. Physiol. 61 Ž1973. 588–618. w6x M.E. Frank, Processing of mixtures of stimuli with different tastes by primary mammalian taste neurons, in: D.G. Laing, W.S. Cain, R.L. McBride, B.W. Ache ŽEds.., Perception of Complex Smells and Tastes, Academic Press, Boston,1989, pp. 127–147. w7x M.E. Frank, R.J. Contreras, T.P. Hettinger, Nerve fibers sensitive to ionic taste stimuli in the chorda tympani of the rat, J. Neurophysiol. 50 Ž1983. 941–960.
371
w8x B.F. Formaker, M.E. Frank, Responses of the chorda tympani nerve to binary component taste stimuli: evidence for peripheral gustatory mixture interactions, Brain Res. 727 Ž1996. 79–90. w9x P.G. Ganzevles, J.H. Kroeze, Effects of adaptation and cross-adaptation to common ions on sourness intensity, Physiol. Behav. 4 Ž1987. 641–646. w10x R.J. Gardner, Lipid solubility and the sourness of acids: implications for models of the acid taste receptor, Chem. Senses Flavour 5 Ž1980. 185–194. w11x T.A. Gilbertson, P.A. Avenet, S.C. Kinnamon, S.D. Roper, Proton currents through amiloride-sensitive Na channel in hamster taste cells. Roll in acid transduction, J. Gen. Physiol. 100 Ž1992. 803–824. w12x A.M. Hyman, M.E. Frank, Effects of binary taste stimuli on the neural activity of the hamster chorda tympani, J. Gen. Physiol. 76 Ž1980. 125–142. w13x A.M. Hyman, M.E. Frank, sensitivities of single nerve fibers in the hamster chorda tympani to mixtures of taste stimuli, J. Gen. Physiol. 76 Ž1980. 143–173. w14x Y. Kashimori, M. Naito, N. Sasaki, T. Kambara, Mechanism of nonlinear responses of taste cells to mixed tastes, Am. J. Physiol. 271 Ž1996. c405–c422. w15x S.C. Kinnamon, V.E. Dionne, K.G. Beam, Apical localization of K channels in taste cells provides the basis for sour taste transduction, Proc. Natl. Acad. Sci. U.S.A. 85 Ž1988. 7023–7027. w16x S.C. Kinnamon, S.D. Roper, Membrane properties of isolated mudpuppy taste cells, J. Gen. Physiol. 91 Ž1988. 351–371. w17x T. Kumazawa, K. Kurihara, Large enhancement of canine taste responses to sugars by salts, J. Gen. Physiol. 95 Ž1990. 1007–1018. w18x B. Lindemann, Taste reception, Physiol. Rev. 76 Ž1996. 718–766. w19x V. Lyall, G.M. Feldman, G.L. Heck, J.A. DeSimone, Effects of extracellular pH, PCO 2 , and HCO 3 on intracellular pH in isolated rat taste buds, Am. J. Physiol. 273 Ž1997. c1008–c1019. w20x R. Matsuo, T. Yamamoto, Effects of inorganic constituents of saliva on taste responses of the rat chorda tympani nerve, Brain Res. 583 Ž1992. 71–80. w21x T. Miyamoto, Y. Okada, T. Sato, Ionic basis of receptor potential of frog taste cells induced by acid stimuli, J. Physiol. ŽLondon. 405 Ž1988. 623–699. w22x G.H. Nowlis, M.E., Frank, Quality coding in gustatory systems of rats and hamsters, in: D.M. Nowlis ŽEd.., Perception of Behavioral Chemicals, ElsevierrNorth-Holland Biomedical Press, Amsterdam, 1981, pp. 59–80. w23x H. Ogawa, M. Sato, S. Yamashita, Gustatory impulse discharges in response to saccharin in rats and hamsters, J. Physiol. ŽLondon. 294 Ž1969. 311–329. w24x R.G. Settle, K. Mechan, G.R. Williams, R.L. Doty, A.C. Sisley, Chemosensory properties of sour tastants, Physiol. Behav. 36 Ž1986. 619–623. w25x H.N.J. Schifferstein, J.E.R. Frijters, Two-stimulus versus onestimulus procedure in the frame work of functional measurement: a comparative investigation using quinine HClrNaCl mixtures, Chem. Senses 17 Ž1992. 127–150. w26x Y. Shimizu, K. Tonosaki, Low environmental temperature modulates gustatory nerve activity and behavioral responses to NaCl in rats, Am. J. Physiol. 277 Ž1999. R368–R373. w27x D.C. Spray, A.L. Harris, M.V. Bennett, Gap junctional conductance is a simple and sensitive function of intracellular pH, Science 211 Ž1981. 712–715. w28x D.C. Spray, M.V. Bennett, Physiology and pharmacology of gap junctional, Physiol. Rev. 47 Ž1985. 281–303. w29x R.E. Stewart, J.A. DeSimone, D.L. Hill, New perspective in a gustatory physiology: transduction, development, and plasticity, Am. J. Physiol. 272 Ž1997. c1–c26. w30x H. Tateda, Sugar receptor and a-amino acid in the rat, in: T. Hayashi ŽEd.., Olfaction and Taste II, Pergamon, Oxford, 1967, pp. 383–397. w31x K. Tonosaki, M. Funakoshi, Intracellular taste cell responses of mouse, Comp. Biochem. Physiol., A 78 Ž1984. 651–656.
372
N. Sakurai et al.r Brain Research 859 (2000) 369–372
w32x K. Tonosaki, Cross-adapted sugar response in the mouse taste cell, Comp. Biochem. Physiol., A 92 Ž1989. 181–183. w33x K. Tonosaki, L.M. Beidler, Sugar best single chorda tympani fiber responses to various sugar stimuli, Comp. Biochem. Physiol., A 94 Ž1989. 603–605.
w34x K. Tonosaki, H. Uebayashi, Adaptation effect of sucrose on the salt taste response, Comp. Biochem. Physiol., A 102 Ž1992. 249–252. w35x S. Ugawa, Y. Minami, W. Guo, Y. Saishin, K. Takatsuji, T. Yamamoto, M. Tohyama, S. Shimada, Receptor that leaves a sour taste in the mouth, Nature 395 Ž1998. 555–556.
Short communication
Effects of acids on neural activity elicited by other taste stimuli in the rat chorda tympani Norio Sakurai, Fukujyu Kanemura, Ken Watanabe, Yasutake Shimizu, Keiichi Tonosaki
)
Department of Veterinary Physiology, Faculty of Agriculture, Gifu UniÕersity, 1-1 Yanagido, Gifu, Gifu 501-1193, Japan Accepted 14 December 1999
Abstract The purpose of this study is whether the gustatory neural response of taste cell to a binary mixture with threshold concentration of acid becomes synergistic or antagonistic can be estimated from the whole chorda tympani ŽCT. nerve in the rat. The present data demonstrate that acids are synergistic enhancer for sugars, and suppressor for NaCl and QHCl, but no effect to glycine and alanine. These results suggest that the acid was modifying the interaction of the other stimulus with its transduction mechanism. q 2000 Elsevier Science B.V. All rights reserved. Keywords: Acid; Binary mixture; Chorda tympani nerve; Gustatory; HCl
Understanding of the recognition mechanism of mixed taste is quite important, because taste stimuli actually encountered in natural feeding are complex mixture of various taste substances. Physiological and behavioral studies of the sensory effects of the taste stimuli in mixtures have been done in hamsters and rats w3,6–8,12– 14,18,20,22,30x w33,35x. These studies used variety of taste chemicals which clearly elicited good taste responses, and have shown that the responses to the mixtures are stronger or weaker than the superposition; that is, the synergetic or antagonistic effect appears, depending on the combinations of two components and their concentrations. However, there are few neural and behavioral studies that show the threshold concentration of acids affect other taste qualities. Here, we report that the threshold concentrations of acids are synergistic enhancer for sugars, and suppressor for NaCl and QHCl, but no effect to glycine and alanine. We used twenty Wistar rats weighing 250–300 g, which were housed in plastic cages at 228C with a 12:12-h light–dark cycle Žlight on 0700–1900 h.. They were given free access to laboratory chow ŽLABO MR Stock, NihonNosan, Yokohama, Japan. and water.
)
Corresponding author. Tel.: q81-58-293-2938; fax: q81-58-2932938; e-mail: [email protected]
Chorda tympani ŽCT. nerve responses were recorded as previously described w26x. Briefly, each rat was deeply anesthetized by an intraperitoneal injection of sodium pentobarbital Ž50 mgrkg body weight. and the trachea was cannulated and the hypoglossal nerve was transected bilaterally to prevent tongue movements. The CT nerve was then exposed through a mandibular approach and placed upon a pair of silver wire electrodes. The electrical activity of the whole nerve was fed to an AC amplifier and then displayed on an oscilloscope screen. Neural responses, resulting from chemical stimulation on the tongue, were integrated Žtime constant: 1.0 s. and recorded on a chart recorder. The tongue was gently extended with a hook, and test solutions were applied for 20 s at a constant rate of 0.5 mlrs by a gravity flow system. Each stimulus was followed by a deionized distilled water rinse delivered at the same rate for more than 60 s to avoid aftereffects of the preceding stimulation. The steady-state phase of the integrated CT neural response was measured at 10 s after the onset of stimuli, was normalized to the response to 0.1 M NH 4 Cl, which was taken as unity Ž1.0.. The integrity of each preparation was monitored by the periodic application of 0.1 M NH 4 Cl. The taste stimuli employed were as follows: sucrose, glucose, fructose, galactose, maltose, lactose, glycine, alanine, NaCl, QHCl, HCl, acetic acid, citric acid and NH 4 Cl. All chemicals were reagent grade, dissolved in deionized
0006-8993r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 0 6 - 8 9 9 3 Ž 0 0 . 0 2 0 0 2 - 3
370
N. Sakurai et al.r Brain Research 859 (2000) 369–372
Fig. 1. Typical examples of the CT nerve responses to several taste stimuli. Upper row presents the integrated responses to various concentrations of HCl, and middle row presents the responses to individual components, and lower row presents responses to one heterogeneous binary mixture with HCl Ž0.5 mM.. All of the records were obtained from the same CT nerve. Suc: 0.5 M sucrose, Glu: 0.5 M glucose, Fru: 0.5 M fructose, Gal: 0.5 M galactose, Mal: 0.5 M maltose, Lac: 0.5 M maltose, Gly: 0.5 M glycine, Ala: 0.5 M alanine, NaCl: 20 mM sodium chloride, QHCl: 20 mM quinine–HCl.
distilled water and presented at room temperature. We used the threshold level concentration of each acid solution, that is, it did not elicit the taste response of the CT nerve by itself. Final concentration of each chemical in the binary mixed taste solution with acid was adjusted to be the respective concentration. All values are presented as means" S.E. Statistical significance was examined by two-way analysis of variance ŽANOVA., with post-hoc testing by means of Duncan’s multiple range test. Comparisons between groups were made by Student’s t-test. To test whether the threshold concentration of acid solution affects on the taste response to sucrose, glucose, fructose, galactose, maltose, lactose, glycine, alanine, NaCl
and QHCl have been studied in rats. Fig. 1 shows the typical example of the taste responses, and all of the records were obtained from the same CT nerve. The low concentration of acid stimulus ŽHCl: 0.5 mM. did not elicit the taste response of the CT nerve by itself, but it enhanced the response to sugars, and suppressed the response to NaCl and QHCl, while it did not affect the response to glycine and alanine. Fig. 2 presents the data for concentration–response relationships of HCl ŽFig. 2a., sucrose ŽFig. 2b., glycine ŽFig. 2c., alanine ŽFig. 2d., NaCl ŽFig. 2e. and QHCl ŽFig. 2f.. The HCl significantly affected the response magnitude measures except glycine and alanine response. Similar results were obtained when the threshold
Fig. 2. Concentration–response relationships for Ža. HCl Ž n s 15., Žb. sucrose Ž n s 6. and sucrose q HCl Ž n s 6., Žc. glycine Ž n s 6. and glycineq HCl Ž n s 6., Žd. alanine Ž n s 6. and alanineq HCl Ž n s 6., Že. NaCl Ž n s 7. and NaCl q HCl Ž n s 7., and Žf. QHClŽ n s 7. and QHClq HCl Ž n s 7.. HCls in b to f are 0.5 mM concentration. Steady-state responses of the integrated CT nerve activity were normalized to means of those to 0.1 M NH 4 Cl, which were taken as unity Ž1.0. and the values were presented as means" S.E. The numbers within vertical axis show the relative response magnitude and the horizontal axis shows concentrations. Asterisks and double asterisks indicate p - 0.05 and p - 0.01, respectively.
N. Sakurai et al.r Brain Research 859 (2000) 369–372
concentration of acetic acid or citric acid was binary, applied with each taste chemicals Ždata not shown.. The threshold concentration of acid stimulus ŽHCl. is a synergistic effect for sugars, and a suppressive effect for NaCl and QHCl, but it has no effect for glycine and alanine. Both glycine and alanine are amino acids and are known as a sweetish substances. It is, however, clear from the present study that, either by sugars or amino acids, an entirely different type of response is elicited. This can be explained that the taste cell has multidifferent receptor cites for sweeteners w3,17,30–34x. These results also suggest that HCl was modifying the interaction of the other stimulus with its transduction mechanism. This mechanism does not necessarily need to be specific for HCl, but may be common for all acids because analogous effects were observed in the case of acetic acid and citric acid. There are wide variety of mechanisms by which acids cause the taste responses w1,2,4–16,18–25,27–29,35x. However, the mechanism by which the acid affects the CT nerve activity is not clear at present. Alternatively, it has been suggested that cytoplasmic acidification of the taste cells can be related to acid detection w9,19,25x. In accordance with this, Bigiani and Roper w4x observed that electrical coupling between taste receptor cells in Necturus were reduced in response to cytoplasmic acidification. This observation is supported by the evidence that a decrease in cytoplasmic pH impairs electrical communication via gap junctions w11,15,16,27,28,35x. Weak acids can penetrate cell membranes and are expected to dissociate intracellularly leading to cytoplasmic acidification w9,10x. It is, therefore, probable that the acid penetration into taste cells leads various kinds of membrane permeability and the taste response profiles.
References w1x L.M. Beidler, Anion influences on taste receptor response, in: T. Hayashi ŽEd.., Olfaction and Taste II, Pergamon, New York, 1967, pp. 509–535. w2x L.M. Beidler, Taste receptor stimulation with salts and acids, in: L.M. Beidler ŽEd.., Handbook of Sensory Physiology IV: Chemical Senses, Part 2: Taste, Springer-Verlag, Berlin, 1971, pp. 200–220. w3x L.M. Beidler, K. Tonosaki, Multiple sweet receptor sites and taste theory, in: D.W. Pfaff ŽEd.., Taste, Olfaction and the Central Nervous System, Rockefeller Univ.Press, 1985, pp. 47–64. w4x A. Bigiani, S.D. Roper, Reduction of electrical coupling between Necturus taste receptor cells, a possible role in acid taste, Neurosci. Lett. 176 Ž1994. 212–216. w5x M.E. Frank, An analysis of hamster afferent taste nerve response functions, J. Gen. Physiol. 61 Ž1973. 588–618. w6x M.E. Frank, Processing of mixtures of stimuli with different tastes by primary mammalian taste neurons, in: D.G. Laing, W.S. Cain, R.L. McBride, B.W. Ache ŽEds.., Perception of Complex Smells and Tastes, Academic Press, Boston,1989, pp. 127–147. w7x M.E. Frank, R.J. Contreras, T.P. Hettinger, Nerve fibers sensitive to ionic taste stimuli in the chorda tympani of the rat, J. Neurophysiol. 50 Ž1983. 941–960.
371
w8x B.F. Formaker, M.E. Frank, Responses of the chorda tympani nerve to binary component taste stimuli: evidence for peripheral gustatory mixture interactions, Brain Res. 727 Ž1996. 79–90. w9x P.G. Ganzevles, J.H. Kroeze, Effects of adaptation and cross-adaptation to common ions on sourness intensity, Physiol. Behav. 4 Ž1987. 641–646. w10x R.J. Gardner, Lipid solubility and the sourness of acids: implications for models of the acid taste receptor, Chem. Senses Flavour 5 Ž1980. 185–194. w11x T.A. Gilbertson, P.A. Avenet, S.C. Kinnamon, S.D. Roper, Proton currents through amiloride-sensitive Na channel in hamster taste cells. Roll in acid transduction, J. Gen. Physiol. 100 Ž1992. 803–824. w12x A.M. Hyman, M.E. Frank, Effects of binary taste stimuli on the neural activity of the hamster chorda tympani, J. Gen. Physiol. 76 Ž1980. 125–142. w13x A.M. Hyman, M.E. Frank, sensitivities of single nerve fibers in the hamster chorda tympani to mixtures of taste stimuli, J. Gen. Physiol. 76 Ž1980. 143–173. w14x Y. Kashimori, M. Naito, N. Sasaki, T. Kambara, Mechanism of nonlinear responses of taste cells to mixed tastes, Am. J. Physiol. 271 Ž1996. c405–c422. w15x S.C. Kinnamon, V.E. Dionne, K.G. Beam, Apical localization of K channels in taste cells provides the basis for sour taste transduction, Proc. Natl. Acad. Sci. U.S.A. 85 Ž1988. 7023–7027. w16x S.C. Kinnamon, S.D. Roper, Membrane properties of isolated mudpuppy taste cells, J. Gen. Physiol. 91 Ž1988. 351–371. w17x T. Kumazawa, K. Kurihara, Large enhancement of canine taste responses to sugars by salts, J. Gen. Physiol. 95 Ž1990. 1007–1018. w18x B. Lindemann, Taste reception, Physiol. Rev. 76 Ž1996. 718–766. w19x V. Lyall, G.M. Feldman, G.L. Heck, J.A. DeSimone, Effects of extracellular pH, PCO 2 , and HCO 3 on intracellular pH in isolated rat taste buds, Am. J. Physiol. 273 Ž1997. c1008–c1019. w20x R. Matsuo, T. Yamamoto, Effects of inorganic constituents of saliva on taste responses of the rat chorda tympani nerve, Brain Res. 583 Ž1992. 71–80. w21x T. Miyamoto, Y. Okada, T. Sato, Ionic basis of receptor potential of frog taste cells induced by acid stimuli, J. Physiol. ŽLondon. 405 Ž1988. 623–699. w22x G.H. Nowlis, M.E., Frank, Quality coding in gustatory systems of rats and hamsters, in: D.M. Nowlis ŽEd.., Perception of Behavioral Chemicals, ElsevierrNorth-Holland Biomedical Press, Amsterdam, 1981, pp. 59–80. w23x H. Ogawa, M. Sato, S. Yamashita, Gustatory impulse discharges in response to saccharin in rats and hamsters, J. Physiol. ŽLondon. 294 Ž1969. 311–329. w24x R.G. Settle, K. Mechan, G.R. Williams, R.L. Doty, A.C. Sisley, Chemosensory properties of sour tastants, Physiol. Behav. 36 Ž1986. 619–623. w25x H.N.J. Schifferstein, J.E.R. Frijters, Two-stimulus versus onestimulus procedure in the frame work of functional measurement: a comparative investigation using quinine HClrNaCl mixtures, Chem. Senses 17 Ž1992. 127–150. w26x Y. Shimizu, K. Tonosaki, Low environmental temperature modulates gustatory nerve activity and behavioral responses to NaCl in rats, Am. J. Physiol. 277 Ž1999. R368–R373. w27x D.C. Spray, A.L. Harris, M.V. Bennett, Gap junctional conductance is a simple and sensitive function of intracellular pH, Science 211 Ž1981. 712–715. w28x D.C. Spray, M.V. Bennett, Physiology and pharmacology of gap junctional, Physiol. Rev. 47 Ž1985. 281–303. w29x R.E. Stewart, J.A. DeSimone, D.L. Hill, New perspective in a gustatory physiology: transduction, development, and plasticity, Am. J. Physiol. 272 Ž1997. c1–c26. w30x H. Tateda, Sugar receptor and a-amino acid in the rat, in: T. Hayashi ŽEd.., Olfaction and Taste II, Pergamon, Oxford, 1967, pp. 383–397. w31x K. Tonosaki, M. Funakoshi, Intracellular taste cell responses of mouse, Comp. Biochem. Physiol., A 78 Ž1984. 651–656.
372
N. Sakurai et al.r Brain Research 859 (2000) 369–372
w32x K. Tonosaki, Cross-adapted sugar response in the mouse taste cell, Comp. Biochem. Physiol., A 92 Ž1989. 181–183. w33x K. Tonosaki, L.M. Beidler, Sugar best single chorda tympani fiber responses to various sugar stimuli, Comp. Biochem. Physiol., A 94 Ž1989. 603–605.
w34x K. Tonosaki, H. Uebayashi, Adaptation effect of sucrose on the salt taste response, Comp. Biochem. Physiol., A 102 Ž1992. 249–252. w35x S. Ugawa, Y. Minami, W. Guo, Y. Saishin, K. Takatsuji, T. Yamamoto, M. Tohyama, S. Shimada, Receptor that leaves a sour taste in the mouth, Nature 395 Ž1998. 555–556.