The Anion Paradox in Sodium Taste Reception: Resolution by Voltage-Clamp Studies

Ye, Qing; Heck, Gerard L.; DeSimone, John A.

doi:10.1126/science.1948054

Cited by 169 publications

(113 citation statements)

References 26 publications

(28 reference statements)

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“…In fact, this anion effect was so pronounced that despite having twice the number of cations in (NH 4 ) 2 SO 4 , responses were still less than those to NH 4 Cl. This pronounced anion effect was also apparent in K+ responses and ENaC-independent Na+ responses, consistent with our studies as well as others in rats (Elliott and Simon 1990;Ye et al 1991;Lundy and Contreras 1997;Breza and Contreras 2012b), and hamsters (Rehnberg et al 1993) demonstrating that the function of the ENaC-independent pathway for salts is a highly conserved mechanism across several species of rodents.…”

Section: Discussionsupporting

confidence: 79%

“…We used 0.5 M sodium and potassium salts bound to 1 of 4 anions (chloride, acetate, sulfate, and gluconate), as well as 0.5 M CaCl 2 , MgCl 2 , NH 4 Cl, and (NH 4 ) 2 SO 4 . We used high salt concentrations so that we could analyze salt responses with large anions, which are known to suppress the nonselective pathway in rats (Ye et al 1991;Lundy and Contreras 1999;Breza and Contreras 2012b) and hamsters (Rehnberg et al 1993). Sodium chloride is the archetypal stimulus for saltiness and more highly preferred than the other salts.…”

Section: Chemical Stimuli and Solution Deliverymentioning

confidence: 99%

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Temperature Influences Chorda Tympani Nerve Responses to Sweet, Salty, Sour, Umami, and Bitter Stimuli in Mice

Lü

Breza

Contreras

2016

CHEMSE

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Temperature profoundly affects the perceived intensity of taste, yet we know little of the extent of temperature's effect on taste in the peripheral nervous system. Accordingly, we investigated the influence of temperature from 23 °C to 43 °C in 4 °C intervals on the integrated responses of the chorda tympani (CT) nerve to a large series of chemical stimuli representing sweet, salty, sour, bitter, and umami tastes in C57BL/J6 mice. We also measured neural responses to NaCl, Na-gluconate, Na-acetate, Na-sulfate, and MSG with and without 5 µM benzamil, an epithelial sodium channel (ENaC) antagonist, to assess the influence of temperature on ENaC-dependent and ENaC-independent response components. Our results showed that for most stimuli (0.5 M sucrose, glucose, fructose, and maltose; 0.02 M saccharin and sucralose; 0.5 M NaCl, Na-gluconate, Na-acetate, Na-sulfate, KCl, K-gluconate, K-acetate, and K-sulfate; 0.05 M citric acid, acetic acid, and HCl; 0.1 M MSG and 0.05 M quinine hydrochloride: QHCl), CT response magnitudes were maximal between 35 °C and 39 °C and progressively smaller at cooler or warmer temperatures. In contrast, the weakest responses to NH 4 Cl, (NH 4 ) 2 SO4, and K-sulfate were at the lowest temperature, with response magnitude increasing monotonically with increasing temperature, while the largest responses to acetic acid were at the lowest temperature, with response magnitude decreasing with increasing temperature. The response to sweet and umami stimuli across temperatures were similar reflecting the involvement of TRPM5 activity, in contrast to bitter stimuli, which were weakly affected by temperature. Temperature-modulated responses to salts and acids most likely operate through mechanisms independent of ENaC and TRPM5.

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Section: Discussionsupporting

confidence: 79%

Section: Chemical Stimuli and Solution Deliverymentioning

confidence: 99%

Temperature Influences Chorda Tympani Nerve Responses to Sweet, Salty, Sour, Umami, and Bitter Stimuli in Mice

Lü

Breza

Contreras

2016

CHEMSE

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“…In fact, the amplitude of the rat chorda-tympani nerve response to sodium was progressively smaller as the size of the anion became larger (Beidler 1954;Elliott and Simon 1990;Ye et al 1991;. Rehnberg, et al (1993) showed that this "anion effect" may be a characteristic of the nonselective salt-sensing pathway.…”

mentioning

confidence: 99%

Anion size modulates salt taste in rats

Breza

Contreras

2012

Journal of Neurophysiology

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Breza JM, Contreras RJ. Anion size modulates salt taste in rats. J Neurophysiol 107: 1632-1648, 2012. First published December 28, 2011 doi:10.1152/jn.00621.2011.-The purpose of this study was to investigate the influence of anion size and the contribution of the epithelial sodium channel (ENaC) and the transient receptor potential vanilloid-1 (TRPV1) channel on sodium-taste responses in rat chorda tympani (CT) neurons. We recorded multiunit responses from the severed CT nerve and single-cell responses from intact, narrowly tuned and broadly tuned, salt-sensitive neurons in the geniculate ganglion simultaneously with stimulus-evoked summated potentials to signal when the stimulus contacted the lingual epithelium. Artificial saliva served as the rinse and solvent for all stimuli (0.3 M NH 4 Cl, 0.5 M sucrose, 0.03-0.5 M NaCl, 0.01 M citric acid, 0.02 M quinine hydrochloride, 0.1 M KCl, and 0.03-0.5 M Na-gluconate). We used the pharmacological antagonist benzamil to assess NaCl responses mediated by ENaC, and SB-366791 and cetylpyridinium chloride to assess responses mediated by TRPV1. CT nerve responses were greater to NaCl than Na-gluconate at each concentration; this was attributed mostly to broadly tuned, acid-generalist neurons that responded with higher frequency and shorter latency to NaCl than Na-gluconate. In contrast, narrowly tuned NaCl-specialist neurons responded more similarly to the two salts, but with subtle differences in temporal pattern. Benzamil reduced CT nerve and single-cell responses only of narrowly tuned neurons to NaCl. Surprisingly, SB-366791 and cetylpyridinium chloride were without effect on CT nerve or single-cell NaCl responses. Collectively, our data demonstrate the critical role that apical ENaCs in fungiform papillae play in processing information about sodium by peripheral gustatory neurons; the role of TRPV1 channels is an enigma. chorda tympani; geniculate ganglion; epithelial sodium channel; transient receptor potential vanilloid-1; electrophysiology SALT-TASTE DETECTION DEPENDS upon two salt-sensing transduction pathways that involve specialized membrane channels on the surface of fungiform taste bud cells in rats. One is the well-documented epithelial sodium channel (ENaC) that is selective for the sodium cation and can be blocked pharmacologically by amiloride. The other is not well understood in the rodent taste system, but has recently been hypothesized to be a variant of the nonspecific-cation channel of the transient receptor potential (TRP) family, TRP vanilloid-1 (TRPV1t) (Lyall et al. 2004), which is broadly receptive to several cations, sodium as well as potassium, calcium, and ammonium. These two salt-sensing pathways in fungiform taste bud cells communicate with two divergent afferent neuron groups in the chorda tympani (CT) nerve. Narrowly tuned NaCl-specialist neurons respond selectively to sodium (and lithium) salts and little, if at all, to other salts or other basic taste stimuli. ENaC antagonists attenuate NaCl responses of NaCl-specialist neurons, but not...

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“…Three sodium salts with different sized anions were used to limit AI transduction (Elliot & Simon, 1990;Formaker & Hill, 1988;Kitada, Mitoh, & Hill, 1998;Ye et al, 1993). Sodium gluconate in particular was chosen on the basis of its ineffectiveness in stimulating AI transduction (Ye, Heck, & DeSimone, 1991;Ye et al, 1993). This experiment marks the first time to our knowledge that sodium gluconate has been presented to sodium-depleted rats.…”

mentioning

confidence: 99%

Anion Size Does Not Compromise Sodium Recognition by Rats After Acute Sodium Depletion.

Geran¹,

Spector²

2004

Behavioral Neuroscience

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Amiloride-insensitive sodium taste transduction is severely limited by large anions (i.e., gluconate). We found that in a brief-access taste test, sodium-depleted rats exhibited similar levels of increased licking to several sodium salts regardless of anion but did not increase licking to nonsodium salts compared with water. The enhanced licking of sodium salts was abolished in the presence of amiloride. These results suggest that the amiloride-sensitive taste transduction pathway is not only necessary but that it is also sufficient for sodium identification in rats. Sodium-depleted rats tested with amiloride initiated significantly more trials than nondepleted rats; hence, appetitive behavior was mildly potentiated by depletion, even in the absence of a sodium taste cue. Overall, these findings provide compelling support for the primacy of the amiloride-sensitive taste transduction mechanism and its associated neural pathway in the recognition of the sodium cation.

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The Anion Paradox in Sodium Taste Reception: Resolution by Voltage-Clamp Studies

Cited by 169 publications

References 26 publications

Temperature Influences Chorda Tympani Nerve Responses to Sweet, Salty, Sour, Umami, and Bitter Stimuli in Mice

Temperature Influences Chorda Tympani Nerve Responses to Sweet, Salty, Sour, Umami, and Bitter Stimuli in Mice

Anion size modulates salt taste in rats

Anion Size Does Not Compromise Sodium Recognition by Rats After Acute Sodium Depletion.

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