Rewiring the gustatory system: Specificity between nerve and taste bud field is critical for normal salt discrimination

Abstract

Forty years have passed since it was demonstrated that a cross-regenerated gustatory nerve in the rat tongue adopts the stimulus-response properties of the taste receptor field it cross-reinnervates. Nevertheless, the functional consequences of channeling peripheral taste signals through inappropriate central circuits remain relatively unexplored. Here we tested whether histologically confirmed cross-regeneration of the chorda tympani nerve (CT) into the posterior tongue in the absence of the glossopharyngeal nerve (GL) (CT-PostTongue) or cross-regeneration of the GL into the anterior tongue in the absence of the CT (GL-AntTongue) would maintain presurgically trained performance in an operant NaCl vs. KCl taste discrimination task in rats. Before surgery all groups were averaging over 90% accuracy. Oral amiloride treatment dropped performance to virtually chance levels. During the first week after surgery, sham-operated rats, GL-transected rats, and rats with regenerated CTs displayed highly competent discrimination performance. In contrast, CTtransected rats were severely impaired (59% accuracy). Both the CT-PostTongue and the GLAntTongue groups were impaired to a similar degree as CT-transected rats. These initially impaired groups improved their performance over the weeks of postsurgical testing suggesting that the rats were capable of relearning the task with discriminable signals in the remaining taste nerves. This relearned performance was dependent on input from amiloride-sensitive receptors likely in the palate. Overall, these results suggest that normal competence in a salt discrimination task is dependent on the taste receptor field origin of the input as well as the specific nerve transmitting the signals to it associated circuits in the brain.

Learning-based recovery from perceptual impairment in salt discrimination after permanently altered peripheral gustatory input

“…There was no significant difference between groups, indicating that there was no increase in the number of taste buds in the NID after CTx. Similarly, these means are similar to those found previously by this laboratory in other experiments (1,52).…”

“…It has been known for some time that the CT is necessary for normal discrimination of sodium from nonsodium salts; CTx severely impairs salt discrimination but does not abolish it (27,51,52,54,60). Transection of the GL, leaving the CT and GSP intact, has been shown to have no effect in a range of salt-based gustatory tasks, including sodium detection and recognition, and salt discrimination (1,10,32,52).…”

“…However, it is unclear how amiloride is acting on the GSP; a systematic single-fiber analysis of the nerve that includes amiloride treatment has not been conducted, and the work done so far has not found N-fibers such as those found in the CT (50). In contrast to the collective gustatory branches of the seventh cranial nerve (i.e., CT and GSP), the lingual branch of the glossopharyngeal (GL) nerve, which innervates taste buds in the posterior tongue, is unnecessary for sodium detection and salt discrimination (10,45,52). It responds only modestly to NaCl and is refractory to the inhibitory effects of amiloride treatment on sodium responses (13,14,26,64; but see Ref.…”

“…We previously observed that after displaying severe initial impairments in the behavioral discrimination of NaCl from KCl as a function of permanent removal of the taste input from the anterior tongue resulting from CTx, some rats markedly improved their performance over weeks of repeated testing postneurotomy (52). The present study was conducted to 1) confirm this finding, 2) systematically determine the necessity and sufficiency of the anterior tongue taste receptors (innervated by the CT) in subserving salt taste discrimination, and 3) identify the source of the remaining peripheral taste signal that allows the rats to regain near-normal discriminative function after CTx.…”

The Perceptual Characteristics of Sodium Chloride to Sodium-Depleted Rats

“…Suggestively, amiloride seems to cause behavior toward NaCl to be more like that of KCl, which is consistent with the elimination of the transduction pathway that is most differentially sensitive to Na + and K + cations. This result is also consistent with the behavior of rats that are sodiumreplete who cannot discriminate NaCl and KCl (and other nonsodium salts) in the presence of amiloride (Spector et al 1996;Hill et al 1990;Spector et al 2010). Nonetheless, it must be noted that at 100 and 300 μM amiloride, rats were still licking concentrations around isotonic at greater rates than water mixed with amiloride, suggesting minimal recognition of sodium.…”