Taste Responsiveness of Fungiform Taste Cells With Action Potentials

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.

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Membrane currents in taste cells of the rat fungiform papilla. Evidence for two types of Ca currents and inhibition of K currents by saccharin.

The Journal of General Physiology ◽

10.1085/jgp.96.5.1061 ◽

1990 ◽

Vol 96 (5) ◽

pp. 1061-1084 ◽

Cited By ~ 120

Author(s):

P Béhé ◽

J A DeSimone ◽

P Avenet ◽

B Lindemann

Keyword(s):

Action Potentials ◽

Basolateral Membrane ◽

Cell Voltage ◽

Taste Buds ◽

Peak Amplitude ◽

Fungiform Papilla ◽

Whole Cell ◽

Inward Current ◽

Taste Cells ◽

K Currents

Taste buds were isolated from the fungiform papilla of the rat tongue and the receptor cells (TRCs) were patch clamped. Seals were obtained on the basolateral membrane of 281 TRCs, protruding from the intact taste buds or isolated by micro-dissection. In whole-cell configuration 72% of the cells had a TTX blockable transient Na inward current (mean peak amplitude 0.74 nA). All cells had outward K currents. Their activation was slower than for the Na current and a slow inactivation was also noticeable. The K currents were blocked by tetraethylammonium, Ba, and 4-aminopyridine, and were absent when the pipette contained Cs instead of K. With 100 mM Ba or 100 mM Ca in the bath, two types of inward current were observed. An L-type Ca current (ICaL) activated at -20 mV had a mean peak amplitude of 440 pA and inactivated very slowly. At 3 mM Ca the activation threshold of ICaL was near -40 mV. A transient T-type current (ICaT) activated at -50 mV had an average peak amplitude of 53 pA and inactivated with a time constant of 36 ms at -30 mV. ICaL was blocked more efficiently by Cd and D600 than ICaT. ICaT was blocked by 0.2 mM Ni and half blocked by 200 microM amiloride. In whole-cell voltage clamp, Na-saccharin caused (in 34% of 55 cells tested) a decrease in outward K currents by 21%, which may be expected to depolarize the TRCs. Also, Na-saccharin caused some taste cells to fire action potentials (on-cell, 7 out of 24 cells; whole-cell, 2 out of 38 cells responding to saccharin) of amplitudes sufficient to activate ICaL. Thus the action potentials will cause Ca inflow, which may trigger release of transmitter.

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New Insights into the Signal Transmission from Taste Cells to Gustatory Nerve Fibers

International Review of Cell and Molecular Biology - International Review Of Cell and Molecular Biology ◽

10.1016/s1937-6448(10)79004-3 ◽

2010 ◽

pp. 101-134 ◽

Cited By ~ 22

Author(s):

Ryusuke Yoshida ◽

Yuzo Ninomiya

Keyword(s):

Signal Transmission ◽

Nerve Fibers ◽

Gustatory Nerve ◽

Taste Cells

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

AJP Cell Physiology ◽

10.1152/ajpcell.1994.266.5.c1165 ◽

1994 ◽

Vol 266 (5) ◽

pp. C1165-C1172 ◽

Cited By ~ 9

Author(s):

A. M. Feigin ◽

Y. Ninomiya ◽

S. M. Bezrukov ◽

B. P. Bryant ◽

P. A. Moore ◽

...

Keyword(s):

Ion Channels ◽

Lipid Bilayers ◽

Neutral Lipids ◽

Nerve Fibers ◽

Chorda Tympani ◽

Chorda Tympani Nerve ◽

Salt Taste ◽

Cation Selectivity ◽

Taste Response ◽

Gustatory Nerve

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.

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The organization of taste sensibilities in hamster chorda tympani nerve fibers.

The Journal of General Physiology ◽

10.1085/jgp.91.6.861 ◽

1988 ◽

Vol 91 (6) ◽

pp. 861-896 ◽

Cited By ~ 113

Author(s):

M E Frank ◽

S L Bieber ◽

D V Smith

Keyword(s):

Cluster Analysis ◽

Factor Analysis ◽

Hierarchical Cluster Analysis ◽

Nerve Impulse ◽

Hierarchical Cluster ◽

Nerve Fibers ◽

Chorda Tympani ◽

Chorda Tympani Nerve ◽

Activation Patterns ◽

Response Profiles

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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Coding channels for taste perception: information transmission from taste cells to gustatory nerve fibers

Archives of Histology and Cytology ◽

10.1679/aohc.69.233 ◽

2006 ◽

Vol 69 (4) ◽

pp. 233-242 ◽

Cited By ~ 26

Author(s):

Ryusuke Yoshida ◽

Keiko Yasumatsu ◽

Noriatsu Shigemura ◽

Yuzo Ninomiya

Keyword(s):

Information Transmission ◽

Nerve Fibers ◽

Taste Perception ◽

Gustatory Nerve ◽

Taste Cells

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Anion modulation of taste responses in sodium-sensitive neurons of the hamster chorda tympani nerve.

The Journal of General Physiology ◽

10.1085/jgp.101.3.453 ◽

1993 ◽

Vol 101 (3) ◽

pp. 453-465 ◽

Cited By ~ 38

Author(s):

B G Rehnberg ◽

B I MacKinnon ◽

T P Hettinger ◽

M E Frank

Keyword(s):

Nerve Fibers ◽

Na Channel ◽

Acetate Anion ◽

Chorda Tympani ◽

Chorda Tympani Nerve ◽

Wide Range ◽

Nacl Concentration ◽

Stimulus Concentration ◽

Taste Cells ◽

Epithelial Membranes

Beidler's work in the 1950s showed that anions can strongly influence gustatory responses to sodium salts. We have demonstrated "anion inhibition" in the hamster by showing that the chorda tympani nerve responds more strongly to NaCl than to Na acetate over a wide range of concentrations. Iontophoretic presentation of Cl- and acetate to the anterior tongue elicited no response in the chorda tympani, suggesting that these anions are not directly stimulatory. Drugs (0.01, 1.0, and 100 microM anthracene-9-carboxylate, diphenylamine-2-carboxylate, 4-acetamido-4'-isothiocyanatostilbene-2,2'-disulfonate, and furosemide) that interfere with movements of Cl- across epithelial cells were ineffective in altering chorda tympani responses to 0.03 M of either NaCl or Na acetate. Anion inhibition related to movements of anions across epithelial membranes therefore seems unlikely. The chorda tympani contains a population of nerve fibers highly selective for Na+ (N fibers) and another population sensitive to Na+ as well as other salts and acids (H fibers). We found that N fibers respond similarly to NaCl and Na acetate, with spiking activity increasing with increasing stimulus concentration (0.01-1.0 M). H fibers, however, respond more strongly to NaCl than to Na acetate. Furthermore, H fibers increase spiking with increases in NaCl concentration, but generally decrease their responses to increasing concentrations of Na acetate. It appears that anion inhibition applies to taste cells innervated by H fibers but not by N fibers. Taste cells innervated by N fibers use an apical Na+ channel, whereas those innervated by H fibers may use a paracellularly mediated, basolateral site of excitation.

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