Enhancement of gustatory nerve fibers to NaCl and formation of ion channels by commercial novobiocin

1994 ◽  
Vol 266 (5) ◽  
pp. C1165-C1172 ◽  
Author(s):  
A. M. Feigin ◽  
Y. Ninomiya ◽  
S. M. Bezrukov ◽  
B. P. Bryant ◽  
P. A. Moore ◽  
...  

Single fibers of the rat chorda tympani nerve were used to study the mechanism of action of the antibiotic novobiocin on salt taste transduction. In the rat, novobiocin selectively enhanced the responses of sodium-specific and amiloride-sensitive chorda tympani nerve fibers (N type) without affecting more broadly responsive cation-sensitive and amiloride-insensitive fibers (E type). In the presence of amiloride, novobiocin was ineffective at enhancing the response of N-type fibers toward sodium chloride. Novobiocin also increased the conductance of bilayers formed from neutral lipids by forming nonrectifying ion channels with low conductance (approximately 7 pS in 110 mM NaCl), long open times (several seconds and longer), and high cation selectivity. Amiloride did not alter either the conductance or kinetics of these novobiocin channels. These observations suggest that even though novobiocin is able to form cation channels in lipid bilayers, and possibly in cell membranes as well, its action on the salt-taste response is through modulation of existing amiloride-sensitive sodium channels.

1992 ◽  
Vol 263 (1) ◽  
pp. R169-R176 ◽  
Author(s):  
A. C. Spector ◽  
H. J. Grill

Gustatory deafferentation of the anterior tongue by bilateral section of the chorda tympani nerve, which removes only 15% of the total taste buds in the rat, severely impaired the rat's ability to discriminate NaCl from KCl. The discrimination deficit was selective. Denervated rats were able to discriminate sucrose from quinine. Despite eliminating four times as many taste buds by bilateral section of the glossopharyngeal nerve, posterior lingual deafferentation had no effect on NaCl vs. KCl discrimination performance. Collectively, these data suggest that afferents in the chorda tympani nerve provide the highest degree of disparity between the peripheral signals representing NaCl and KCl. Electrophysiological findings of others implicate the sodium-specific afferents that appear to exclusively exist in the chorda tympani nerve as the critical elements subserving the NaCl vs. KCl discrimination.


1994 ◽  
Vol 104 (5) ◽  
pp. 885-907 ◽  
Author(s):  
Q Ye ◽  
G L Heck ◽  
J A DeSimone

Taste sensory responses from the chorda tympani nerve of the rat were recorded with the lingual receptive field under current or voltage clamp. Consistent with previous results (Ye, Q., G. L. Heck, and J. A. DeSimone. 1993. Journal of Neurophysiology. 70:167-178), responses to NaCl were highly sensitive to lingual voltage clamp condition. This can be attributed to changes in the electrochemical driving force for Na+ ions through apical membrane transducer channels in taste cells. In contrast, responses to KCl over the concentration range 50-500 mM were insensitive to the voltage clamp condition of the receptive field. These results indicate the absence of K+ conductances comparable to those for Na+ in the apical membranes of taste cells. This was supported by the strong anion dependence of K salt responses. At zero current clamp, the potassium gluconate (KGlu) threshold was > 250 mM, and onset kinetics were slow (12 s to reach half-maximal response). Faster onset kinetics and larger responses to KGlu occurred at negative voltage clamp (-50 mV). This indicates that when K+ ion is transported as a current, and thereby uncoupled from gluconate mobility, its rate of delivery to the K+ taste transducer increases. Analysis of conductances shows that the paracellular pathway in the lingual epithelium is 28 times more permeable to KCl than to KGlu. Responses to KGlu under negative voltage clamp were not affected by agents that are K+ channel blockers in other systems. The results indicate that K salt taste transduction is under paracellular diffusion control, which limits chemoreception efficiency. We conclude that rat K salt taste occurs by means of a subtight junctional transducer for K+ ions with access limited by anion mobility. The data suggest that this transducer is not cation selective which also accounts for the voltage and amiloride insensitive part of the response to NaCl.


1997 ◽  
Vol 22 (3) ◽  
pp. 249-255 ◽  
Author(s):  
Kazumi Osada ◽  
Michio Komai ◽  
Bruce P. Bryant ◽  
Hitoshi Suzuki ◽  
Atsuko Goto ◽  
...  

2006 ◽  
Vol 96 (6) ◽  
pp. 3088-3095 ◽  
Author(s):  
Ryusuke Yoshida ◽  
Noriatsu Shigemura ◽  
Keisuke Sanematsu ◽  
Keiko Yasumatsu ◽  
Satoru Ishizuka ◽  
...  

It is known that a subset of taste cells generate action potentials in response to taste stimuli. However, responsiveness of these cells to particular tastants remains unknown. In the present study, by using a newly developed extracellular recording technique, we recorded action potentials from the basolateral membrane of single receptor cells in response to taste stimuli applied apically to taste buds isolated from mouse fungiform papillae. By this method, we examined taste-cell responses to stimuli representing the four basic taste qualities (NaCl, Na saccharin, HCl, and quinine-HCl). Of 72 cells responding to taste stimuli, 48 (67%) responded to one, 22 (30%) to two, and 2 (3%) to three of four taste stimuli. The entropy value presenting the breadth of responsiveness was 0.158 ± 0.234 (mean ± SD), which was close to that for the nerve fibers (0.183 ± 0.262). In addition, the proportion of taste cells predominantly sensitive to each of the four taste stimuli, and the grouping of taste cells based on hierarchical cluster analysis, were comparable with those of chorda tympani (CT) fibers. The occurrence of each class of taste cells with different taste responsiveness to the four taste stimuli was not significantly different from that of CT fibers except for classes with broad taste responsiveness. These results suggest that information derived from taste cells generating action potentials may provide the major component of taste information that is transmitted to gustatory nerve fibers.


1998 ◽  
Vol 80 (3) ◽  
pp. 1362-1372 ◽  
Author(s):  
John D. Boughter ◽  
David V. Smith

Boughter, John D., Jr. and David V. Smith. Amiloride blocks acid responses in NaCl-best gustatory neurons of the hamster solitary nucleus. J. Neurophysiol. 80: 1362–1372, 1998. Biophysical studies of isolated taste receptor cells show that one mechanism of Na+ salt transduction involves the inward movement of Na+ through amiloride-blockable ion channels on the apical receptor cell membrane, which leads to a direct depolarization. Hamster taste receptor cells with amiloride-blockable Na+ responses also show an amiloride-sensitive H+ current. Thus one mechanism for the transduction of acid taste involves the amiloride-sensitive channel. We investigated the effects of amiloride on responses to acids in neurons of the nucleus of the solitary tract (NST) of the hamster. The responses of 47 NST neurons were recorded extracellularly while the anterior tongue was stimulated with solutions representing the four taste qualities (NaCl, sucrose, HCl, quinine), which were used to characterize each cell on the basis of its best stimulus. The effects of amiloride on responses to 10 mM HCl, 10 mM citric acid, 100 mM NaCl, and 100 mM sucrose were then investigated. Stimuli were presented alone for 30 s (control trials) and also presented for 10 s, followed by a mixture of the stimulus with 10 μM amiloride for 10 s, followed by the stimulus alone again for 10 s (amiloride trials). The effects of amiloride were assessed by comparing the responses of cells with the stimulus + amiloride with that of the stimulus alone. In neurons classified as NaCl-best, amiloride reversibly blocked responses to NaCl, HCl, and citric acid. In HCl-best neurons, amiloride had no effect on responses to any of these stimuli. In sucrose-best neurons, amiloride blocked the response to NaCl but not to sucrose or to either acid. These results support the hypothesis that acids are transduced by at least two different receptor mechanisms in the hamster, amiloride sensitive and amiloride insensitive. At the NST, these inputs are tightly maintained in two separate populations of neurons. Sucrose-best neurons, which show amiloride effects on NaCl but not acids, appear to receive converging inputs from both amiloride-sensitive (N-best) and amiloride-insensitive (H-best) chorda tympani nerve fibers.


1995 ◽  
Vol 268 (5) ◽  
pp. C1295-C1300 ◽  
Author(s):  
J. A. DeSimone ◽  
E. M. Callaham ◽  
G. L. Heck

The chorda tympani nerve response of the rat to HCl was obtained with the lingual receptive field under voltage clamp. Unlike NaCl responses, HCl responses were not affected by inside positive voltage perturbations. However, HCl responses under negative voltage clamp were suppressed in contrast to NaCl responses, which were enhanced. Unlike NaCl responses, HCl responses were amiloride insensitive. HCl rinsing from the tongue produced a large off-response. At zero current clamp the off-response coincided with an anomalous increased positive potential. The paracellular resistance was also higher for HCl relative to the same concentration of NaCl. This is evidence that H+ binds to the normally fixed anionic sites of the paracellular pathway rendering it anion selective. It is postulated that release of bound H+ from surface buffer sites is responsible for the second burst of neural activity upon rising HCl. Acids stimulate primarily through the paracellular pathway, which also furnishes buffering sites that regulate H+ concentration, thereby protecting the sensory apparatus from hyperacidic conditions.


2012 ◽  
Vol 303 (11) ◽  
pp. R1195-R1205 ◽  
Author(s):  
Kimberly R. Smith ◽  
Yada Treesukosol ◽  
A. Brennan Paedae ◽  
Robert J. Contreras ◽  
Alan C. Spector

In rodents, at least two transduction mechanisms are involved in salt taste: 1) the sodium-selective epithelial sodium channel, blocked by topical amiloride administration, and 2) one or more amiloride-insensitive cation-nonselective pathways. Whereas electrophysiological evidence from the chorda tympani nerve (CT) has implicated the transient receptor potential vanilloid-1 (TRPV1) channel as a major component of amiloride-insensitive salt taste transduction, behavioral results have provided only equivocal support. Using a brief-access taste test, we examined generalization profiles of water-deprived C57BL/6J (WT) and TRPV1 knockout (KO) mice conditioned (via LiCl injection) to avoid 100 μM amiloride-prepared 0.25 M NaCl and tested with 0.25 M NaCl, sodium gluconate, KCl, NH4Cl, 6.625 mM citric acid, 0.15 mM quinine, and 0.5 M sucrose. Both LiCl-injected WT and TRPV1 KO groups learned to avoid NaCl+amiloride relative to controls, but their generalization profiles did not differ; LiCl-injected mice avoided the nonsodium salts and quinine suggesting that a TRPV1-independent pathway contributes to the taste quality of the amiloride-insensitive portion of the NaCl signal. Repeating the experiment but doubling all stimulus concentrations revealed a difference in generalization profiles between genotypes. While both LiCl-injected groups avoided the nonsodium salts and quinine, only WT mice avoided the sodium salts and citric acid. CT responses to these stimuli and a concentration series of NaCl and KCl with and without amiloride did not differ between genotypes. Thus, in our study, TRPV1 did not appear to contribute to sodium salt perception based on gustatory signals, at least in the CT, but may have contributed to the oral somatosensory features of sodium.


1988 ◽  
Vol 91 (6) ◽  
pp. 861-896 ◽  
Author(s):  
M E Frank ◽  
S L Bieber ◽  
D V Smith

Electrophysiological measurements of nerve impulse frequencies were used to explore the organization of taste sensibilities in single fibers of the hamster chorda tympani nerve. Moderately intense taste solutions that are either very similar or easily discriminated were applied to the anterior lingual surface. 40 response profiles or 13 stimulus activation patterns were considered variables and examined with multivariate statistical techniques. Three kinds of response profiles were seen in fibers that varied in their overall sensitivity to taste solutions. One profile (S) showed selectivity for sweeteners, a second (N) showed selectivity for sodium salts, and a third (H) showed sensitivity to salts, acids, and other compounds. Hierarchical cluster analysis indicated that profiles fell into discrete classes. Responses to many pairs of effective stimuli were covariant across profiles within a class, but some acidic stimuli had more idiosyncratic effects. Factor analysis of profiles identified two common factors, accounting for 77% of the variance. A unipolar factor was identified with the N profile, and a bipolar factor was identified with the S profile and its opposite, the H profile. Three stimulus activation patterns were elicited by taste solutions that varied in intensity of effect. Hierarchical cluster analysis indicated that the patterns fell into discrete classes. Factor analysis of patterns identified three common unipolar factors accounting for 82% of the variance. Eight stimuli (MgSO4, NH4Cl, KCl, citric acid, acetic acid, urea, quinine HCl, HCl) selectively activated fibers with H profiles, three stimuli (fructose, Na saccharin, sucrose) selectively activated fibers with S profiles, and two stimuli (NaNO3, NaCl) activated fibers with N profiles more strongly than fibers with H profiles. Stimuli that evoke different patterns taste distinct to hamsters. Stimuli that evoke the same pattern taste more similar. It was concluded that the hundreds of peripheral taste neurons that innervate the anterior tongue play one of three functional roles, providing information about one of three features that are shared by different chemical solutions.


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