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

Abstract

A B S T R A C T 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 NaCI than to Na acetate over a wide range of concentrations. Iontophoretic presentation of CI-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 IxM anthracene-O-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 NaCI 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 NaCI and Na acetate, with spiking activity increasing with increasing stimulus concentration (0.01-I.0 M). H fibers, however, respond more strongly to NaC1 than to Na acetate. Furthermore, H fibers increase spiking with increases in NaCI 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.

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

“…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.…”

“…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.…”

Amiloride-Insensitive Salt Taste Is Mediated by Two Populations of Type III Taste Cells with Distinct Transduction Mechanisms

“…The amiloride-sensitive (AS) pathway responds selectively to sodium (and lithium) salts and is mediated by the epithelial sodium channel (Heck et al, 1984;Chandrashekar et al, 2010;Roper, 2015). The amiloride-insensitive (AI), or high-salt pathway, responds to a broad range of sodium and non-sodium salts (Ninomiya and Funakoshi, 1988;Halpern, 1998), yet the underlying receptor(s) remain unknown.…”

“…AI salt responses have been reported in two distinct populations of taste bud cells: (1) a subpopulation of bitterresponsive type II taste cells; and (2) the polycystic kidney disease 2-like 1 (PKD2L1)-expressing type III taste cells critical for sour taste (Oka et al, 2013). Because of the prevalence of cell-to-cell communication in the taste bud (Roper, 2013), it is unclear to what degree sour and AI salt responses co-occur in type III taste cells.…”

“…In the AI salt pathway, larger anion salts produce smaller responses, a phenomenon known as the "anion effect" (Beidler, 1967;Elliott and Simon, 1990;Ye et al, 1991Ye et al, , 1993Rehnberg et al, 1993;Kitada, 1995;Kitada et al, 1998). When the taste bud is exposed to a large anion salt, smaller cations diffuse through tight junctions at the taste pore, leaving their less permeable anions behind.…”