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

Rats lacking input to the chorda tympani (CT) nerve, a facial nerve branch innervating anterior tongue taste buds, show robust impairments in salt discrimination demonstrating its necessity. We tested the sufficiency of the CT for salt taste discrimination and whether the remaining input provided by the greater superficial petrosal (GSP) nerve, a facial nerve branch innervating palatal taste buds, or by the glossopharyngeal (GL) nerve, innervating posterior tongue taste buds, could support performance after extended postsurgical testing. Rats presurgically trained and tested in a two-response operant task to discriminate NaCl from KCl were subjected to sham surgery or transection of the CT (CTx), GL (GLx), or GSP (GSPx), alone or in combination. While initially reduced postsurgically, performance by rats with an intact GSP after CTx + GLx increased to normal over 6 wk of testing. Rats with CTx + GSPx consistently performed near chance levels. In contrast, rats with GSPx + GLx were behaviorally normal. A subset of rats subjected to sham surgery and exposed to lower concentrations during postsurgical testing emulating decreased stimulus intensity after neurotomy showed no significant impairment. These results demonstrate that CTx changes the perceptual nature of NaCl and/or KCl, leading to severe initial postsurgical impairments in discriminability, but a “new” discrimination can be relearned based on the input of the GSP. Despite losing ∼75% of their taste buds, rats are unaffected after GSPx + GLx, demonstrating that the CT is not only necessary, but also sufficient, for maintaining salt taste discrimination, notwithstanding the unlikely contribution of the small percentage of taste receptors innervated by the superior laryngeal nerve.

Functional status of the regenerated chorda tympani nerve as assessed in a salt taste discrimination task

We tested whether the recovered ability of rats to discriminate NaCl from KCl after chorda tympani nerve transection (CTX) is causally linked to nerve regeneration or some other compensatory process. Rats were presurgically trained in an operant NaCl vs. KCl discrimination task. Rats with regenerated nerves, histologically confirmed by anterior tongue taste pore counts and tested 62 days after CTX (CTX-62R; n = 5), performed as well as those tested 62 days after sham surgery (Sham-62; n = 5), but both of these groups initially performed slightly worse than animals tested 7 days after sham surgery (Sham-7; n = 4). Performance of rats tested either 7 (CTX-7P; n = 5) or 62 (CTX-62P; n = 4) days after CTX in which nerve regeneration was prevented was severely disrupted. Adulteration of the stimuli with amiloride, an epithelial sodium channel blocker, impaired discrimination performance in a similar dose-dependent manner in the Sham-7 ( n = 2), Sham-62 ( n = 5), and CTX-62R ( n = 5) groups, suggesting that the functional status of the amiloride-sensitive transduction pathway returns to normal in rats with regenerated chorda tympani nerves. Performance of CTX rats without regenerated nerves (CTX-7P, n = 2; CTX-62P, n = 4) was further degraded by amiloride treatment, suggesting that taste receptors innervated by other nerves are sensitive to amiloride. In conclusion, nerve regeneration is an essential component underlying full recovery of salt discrimination function after CTX.

Salt taste discrimination after bilateral section of the chorda tympani or glossopharyngeal nerves

Gustatory deafferentation of the anterior tongue by bilateral section of the chorda tympani nerve, which removes only 15% of the total taste buds in the rat, severely impaired the rat's ability to discriminate NaCl from KCl. The discrimination deficit was selective. Denervated rats were able to discriminate sucrose from quinine. Despite eliminating four times as many taste buds by bilateral section of the glossopharyngeal nerve, posterior lingual deafferentation had no effect on NaCl vs. KCl discrimination performance. Collectively, these data suggest that afferents in the chorda tympani nerve provide the highest degree of disparity between the peripheral signals representing NaCl and KCl. Electrophysiological findings of others implicate the sodium-specific afferents that appear to exclusively exist in the chorda tympani nerve as the critical elements subserving the NaCl vs. KCl discrimination.