Acetic acid modulates spike rate and spike latency to salt in peripheral gustatory neurons of rats

Abstract

Sour and salt taste interactions are not well understood in the peripheral gustatory system. Therefore, we investigated the interaction of acetic acid and NaCl on taste processing by rat chorda tympani neurons. We recorded multi-unit responses from the severed chorda tympani nerve (CT) 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, 0.1 M NaCl, 0.01 M citric acid, 0.02 M quinine hydrochloride (QHCl), 0.1 M KCl, 0.003-0.1 M acetic acid, and 0.003-0.1 M acetic acid mixed with 0.1 M NaCl]. We used benzamil to assess NaCl responses mediated by the epithelial sodium channel (ENaC). The CT nerve responses to acetic acid/NaCl mixtures were less than those predicted by summing the component responses. Single-unit analyses revealed that acetic acid activated acid-generalist neurons exclusively in a concentration-dependent manner: increasing acid concentration increased response frequency and decreased response latency in a parallel fashion. Acetic acid suppressed NaCl responses in ENaC-dependent NaCl-specialist neurons, whereas acetic acid-NaCl mixtures were additive in acid-generalist neurons. These data suggest that acetic acid attenuates sodium responses in ENaC-expressing-taste cells in contact with NaCl-specialist neurons, whereas acetic acid-NaCl mixtures activate distinct receptor/cellular mechanisms on taste cells in contact with acid-generalist neurons. We speculate that NaCl-specialist neurons are in contact with type I cells, whereas acid-generalist neurons are in contact with type III cells in fungiform taste buds.