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.