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

Abstract

Breza JM, Contreras RJ. Acetic acid modulates spike rate and spike latency to salt in peripheral gustatory neurons of rats. J Neurophysiol 108: 2405-2418, 2012. First published August 15, 2012 doi:10.1152/jn.00114.2012.-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. chorda tympani; electrophysiology; epithelial sodium channel; geniculate ganglion MUCH IS KNOWN ABOUT TASTE BUD receptor proteins that initiate signal transduction and how individual peripheral neurons code information unique to each of the five basic taste qualities. Little is known, however, about how the peripheral nervous system processes information about two or more basic stimuli when presented together in a mixture. The purpose of this study was to investigate how the peripheral nervous system deciphers information about mixtures of NaCl and acetic acid in rat chorda tympani (CT) neurons.In rodents, two salt transduction pathways have been identified. The first is selective for the sodium cation detected by an epithelial sodium channel (ENaC) located on the apical membrane of taste bud receptor cells (Heck et al. 1984). The second pathway is cation nonselective, but the transduction mechanism is not well understood. Lyall et al. (2004) proposed that this pathway involved an apically located ...

Breadth of tuning in taste afferent neurons varies with stimulus strength

“…Moreover, 5 seconds closely matches the duration of licking bursts in mice (~6 sec 29 , recognizing that this varies with water deprivation, the tastant solution, and even with the size of the sipping spout 30 ). Last, 5 sec taste stimulation approximates what others have employed in electrophysiological recordings of geniculate ganglion neurons 31 , thereby facilitating comparisons of our findings with previous studies.…”

“…Sensory axons that synapse with presynaptic (Type III) cells would respond to many stimuli. Indeed, Breza et al 31. speculated that ‘generalist' (that is, broadly tuned) geniculate ganglion neurons they recorded with microelectrodes were synaptically coupled to Type III (Presynaptic cells).…”

“…( a – c ) Series of electrical pulses (grey lines) applied to the anterior tongue surface, modelled after trains of action potentials recorded from rat geniculate ganglion cells192031. Ganglion cell action potentials were evoked by applying 30, 100 and 300 mM MSG onto a rat tongue in a separate experiment (electrophysiological recordings kindly provided by R. Contreras and A. Nikonov).…”

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

“…We chose to examine the influence of temperature on an equimolar concentration (0.05 M) of HCl, citric acid, and acetic acid, as these acids are effective sour stimuli at these concentrations at our temperature range (Horio et al 2011), but are quite different from another in terms of solution pH (HCl = 1.3, citric acid = 2.24, and acetic acid = 3.03). Importantly, acid responses from the rat CT neurons are not directly correlated to solution pH, because weak acids are more effective stimuli than their pH would suggest (Lyall et al 2001;Breza and Contreras 2012a). A decrease in the intracellular pH appears to be the proximate stimulus in sour taste transduction (Lyall et al 2001), but weak acids, such as acetic acid and carbonic acid, are more effective (at the same solution pH) at decreasing intracellular pH than HCl, a strong mineral acid (Lyall et al 2001).…”

“…This may imply that the effects of temperature may have intracellular and extracellular sites of action or multiple receptor mechanisms, and warrants future investigation. It could also imply that the mechanisms of sour-taste transduction in rats and mice differ, since responses to acids in whole nerve and single cell recordings (Lyall et al 2001;Breza and Contreras 2012a) of rats are similar when matched for concentrations, despite differences in solution pH.…”