Behavioral Discrimination between Quinine and KCl Is Dependent on Input from the Seventh Cranial Nerve: Implications for the Functional Roles of the Gustatory Nerves in Rats

Abstract

The rat glossopharyngeal nerve (GL), which innervates posterior tongue taste buds, contains several physiologically defined taste fiber types; at least one type is primarily responsive to certain alkaloids (such as quinine), and another is primarily responsive to acids and salts. In contrast, the chorda tympani (CT), which innervates anterior tongue taste buds, does not appear to contain fibers that differentially respond to quinine relative to salts and acids. It was therefore predicted that GL transection should disrupt behavioral discriminations between quinine and either acids or salts. Water-restricted rats were trained to press one of two levers if a sampled taste stimulus was quinine (0.1-1.0 mM) and the second lever if the sampled stimulus was KCl (0.1-1.0 M). Sham surgery, GL transection, and sublingual and submaxillary salivary gland extirpation were found to have no effect relative to presurgical performance. Both CT transection and combined GL and CT transection caused a substantial and approximately equal decrement in discrimination performance. Removal of the gustatory branches of the seventh cranial nerve [CT and greater superficial petrosal (GSP)] nearly eliminated the discrimination of the taste stimuli, and combined transection of the CT, GL, and GSP unequivocally reduced performance to chance levels. Although these findings were not presaged by the known electrophysiology, they nonetheless compare favorably with other studies reporting little effect of GL transection on behavioral responses to quinine. These results, in the context of other discrimination studies reported in the literature, suggest that, in rats, the neural coding of taste quality depends primarily on the input of the facial nerve.

Comparison of the responses of the chorda tympani and glossopharyngeal nerves to taste stimuli in C57BL/6J mice

“…However, the size of electrophysiological responses does not necessarily reveal the relative importance of the taste nerves in taste-mediated behavior. Recent behavioral experiments in rats stress the prominence of the CT over the NG for the bitter taste [26-28]. We have found that mice with bilateral CT cut have a significantly impaired ability to discriminate water from the bitter stimulus denatonium benzoate in two bottle preference (TBP) tests, while mice with bilateral NG cut showed no difference from the sham surgery group (own unpublished observations).…”

Topographical representations of taste response characteristics in the rostral nucleus of the solitary tract in the rat

“…For example, the CT could provide a main cue discriminating NaCl from KCl, or KCl from quinine, while the IX may not play a critical role in the discriminations (Spector and Grill 1992;St John and Spector 1998). In contrast, the IX may be involved in an aversive behavior to toxic foods, because IX transections have been shown to reduce an aversive oromotor response induced by bitter tastants (Travers et al 1987).…”

Cracking taste codes by tapping into sensory neuron impulse traffic

“…T2R lineage specificity exaggerates the difficulty in identifying T2R, compared to T1R, ligands. CN VII fields, where T1Rs, specific Na + receptors and aversive-electrolyte receptors are located, focus on taste discrimination more than CN IX fields, where T2Rs predominate and reflexes are initiated (Adler et al ., 2000; St John and Spector, 1998; King et al ., 2000). A posterior lingual T2R locus is consistent with CN IX brainstem, projection sites for high-affinity, cycloheximide neural activity (Geran and Travers, 2006); activity that elicits sensations quite unlike quinine (Frank et al ., 2003) as well as protective reflexes (King et al .…”

“…In rodents, CN IX taste-bud containing receptive fields are more involved in ingesting/rejecting via brain-stem motor systems (Travers and Travers, 2005), and CN X receptive fields more involved in protecting the airway (Bradley, 2000) or participating in metabolic pathways in the gut, (Margolskee et al ., 2007) than sensing taste-stimulus quality. Although the CT assumes some GL reflexive functions when cross-wired to posterior fields (King et al ., 2008), it is not yet known that the GL can take over the well-documented CT-mediated discrimination of taste quality (St John and Spector, 1998; Geran et al ., 2002). …”