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

Abstract

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.

Fig. 1.

Trial structure used for behavioral testing.

Fig. 2.

Overall performance for experiment 1 control sessions. Mean overall percentage correct (+SE or ±SE) in NaCl vs. KCl discrimination by group for presurgical control sessions (left), initial postsurgical testing (weeks 1–4; middle), and postsurgical control sessions (right). Sham-Int, rats that were subjected to sham surgery but served as a stimulus intensity control; CTx, chorda tympani nerve transection; GLx, glossopharyngeal nerve transection; GSPx, greater superficial petrosal nerve transection; sham, subjected to sham surgery.

Fig. 3.

Overall performance for experiment 1 amiloride sessions. Mean overall percentage correct (+SE) in NaCl vs. KCl (dissolved in 100 μM amiloride) discrimination by group for presurgical (left) and postsurgical (right) amiloride sessions. *Significantly higher than chance (50% overall) during amiloride sessions.

Fig. 4.

Overall performance for experiment 2 control sessions. Mean overall percentage correct (+SE or ±SE) in NaCl vs. KCl discrimination by group for presurgical control sessions (left), initial postsurgical testing (weeks 1–4; middle), and postsurgical control sessions (right).

Fig. 5.

Overall performance for experiment 2 amiloride sessions. Mean overall percentage correct (+SE) in NaCl vs. KCl (dissolved in 100 μM amiloride) discrimination by group for presurgical (left) and postsurgical (right) amiloride sessions. *Significantly higher than chance (50% overall) during amiloride sessions.