Responses of gustatory cells in the nucleus of the solitary tract of the hamster after NaCl or amiloride adaptation

Abstract

1. The responses of single nucleus of the solitary tract (NST) neurons in the hamster were recorded to an array of Na+ and non-Na+ stimuli under each of three adaptation conditions: distilled H2O, 0.032 M NaCl, and 10 microM amiloride. Each adapting solution flowed for 60 s before delivery of one of seven test stimuli: 0.032 M NaCl, NaNO3, and Na-gluconate, 0.1 M KCl and sucrose, 1 mM HCl, and 3 mM quinine hydrochloride (QHCl). Stimuli were dissolved in distilled H2O (H2O and NaCl adaptation conditions) or 10 microM amiloride (amiloride adaptation condition). 2. Both amiloride treatment and NaCl adaptation reduced responses to the Na+ stimuli. The effects of NaCl adaptation were generally greater than those of amiloride, and the responses to the Na+ salts were reduced by NaCl adaptation in every cell that responded to NaCl, regardless of its best-stimulus classification. Amiloride treatment suppressed the responses to Na+ salts with larger anions (NaNO3 and Na-gluconate) more than the response to NaCl. 3. Unlike amiloride treatment, NaCl adaptation also reduced responses to several non-Na+ stimuli (KCl, HCl, and QHCl). This effect occurred primarily in the NaCl-best neurons that were most highly responsive to NaCl and that showed a postexcitatory suppression after NaCl. This suppression has been observed in recordings from the chorda tympani nerve in both rats and hamsters and in taste receptor cell responses recorded in situ in the rat. If it is a receptor phenomenon, these data would imply that some NaCl-sensitive receptor cells are also responsive to these non-Na+ electrolytes. 4. The effects of amiloride on the responses to Na+ stimuli were not limited to NaCl-best neurons, but occurred in sucrose-best cells as well. These results suggest that the sucrose-best cells in the NST receive converging input from sucrose- and NaCl-best chorda tympani fibers, because there is little Na+ sensitivity in the peripheral sucrose-best fibers and the amiloride sensitivity is restricted to NaCl-best chorda tympani fibers. The responses to NaCl in the few HCl- and QHCl-best NST neurons were not affected by amiloride. 5. Rinsing the tongue with amiloride for 60 s resulted in a reduction in the baseline response rate of NST cells. This effect occurred primarily in NaCl- and sucrose-best NST neurons and implies that much of the spontaneous activity in these brain stem cells arises from amiloride-sensitive channel activity in the peripheral receptor cells. 6. The results of human psychophysical studies show very different effects of NaCl adaptation and amiloride treatment. Adaptation to NaCl produces a robust and specific reduction in the saltiness of all salts. The present results show that NaCl adaptation reduces the responses of all cells sensitive to NaCl. Treatment of the human tongue with amiloride produces a proportionately smaller reduction in the response to NaCl than it does in rodents, and it appears to have no effect on saltiness. Rather, amiloride has been shown to specifically reduce the sour side taste of NaCl, Nag...

Differential Gurmarin Suppression of Sweet Taste Responses in Rat Solitary Nucleus Neurons

“…In some respects, the distribution of gurmarin sensitivity across NST neuronal types relative to those in the periphery ) is similar to that observed for amiloride-sensitive salt input as the apparent restriction of information derived from a particular receptor process to a specific peripheral neuron class is not absolute in the CNS. However, amiloride is more effective at reducing responses to Na ϩ salts in those NST cells that respond maximally to these stimuli relative to the average gurmarin-induced attenuation of responding to sucrose observed in class S cells in the present study (see Boughter and Smith 1998;Boughter et al 1999;Giza and Scott 1991;Scott and Giza 1990;Smith et al 1996;St. John and Smith 2000).…”

“…Those fibers that are affected exhibit absolute or near absolute suppression, with responses to 0.5 M sucrose suppressed to ϳ10% of control on average. This differential effect is somewhat analogous to the influence of amiloride on the neural processing of salt information as lingual application of amiloride suppresses responses to salts only in NaCl-best CT fibers (Hettinger and Frank 1990;Ninomiya and Funakoshi 1988) and NaCl-best (Boughter and Smith 1998;Boughter et al 1999;Giza and Scott 1991;Scott and Giza 1990;Smith et al 1996; St. John and Smith 2000) and sucrose-best (Smith et al 1996; St. John and Smith 2000) neurons in the nucleus of the solitary tract (NST). Therefore it is possible that input arising from gurmarin-sensitive and -insensitive sweet transduction mechanisms is segregated to particular classes of taste-responsive neurons in the brain stem.…”

“…This segregation of amiloride-sensitive salt information to a particular type of CT neuron is similar to the observation that gurmarin-sensitive sweet information is selectively distributed to a particular type of sucrose-best CT fiber . Because amiloride-sensitive salt information is predominantly relayed to NaCl-best (Boughter and Smith 1998;Boughter et al 1999;Giza and Scott 1991;Scott and Giza 1990;Smith et al 1996;St. John and Smith 2000) and sucrosebest (Smith et al 1996;St.…”

“…Because amiloride-sensitive salt information is predominantly relayed to NaCl-best (Boughter and Smith 1998;Boughter et al 1999;Giza and Scott 1991;Scott and Giza 1990;Smith et al 1996;St. John and Smith 2000) and sucrosebest (Smith et al 1996;St. John and Smith 2000) NST neurons, it could be hypothesized that gurmarin-sensitive sweet information is also differentially distributed across physiologically defined NST neuronal types.…”

Behavior Analysis and Revaluation

“…Taste receptors in the tongue project to neurons in the solitary nucleus of the midbrain and, from there, to neurons in the VTA (among others). Neurons in the solitary nucleus respond differentially to the four basic tastes (salt, sweet, bitter, and sour; e.g., Smith, Liu, & Vogt, 1996). These neurons then project to neurons in the reinforcing system and motor-association area (among others) where they evoke differential neural responses (e.g., Delfs, Zhu, Druhan, & Aston-Jones, 1998;Rolls, 1997;Schoenbaum, Chiba, & Gallagher, 1998).…”