The gustatory competence of the lingual epithelium requires neonatal innervation

Abstract

The rat vallate papilla is bilaterally innervated by the IXth nerve whose axons are required for the normal development of its several hundred taste buds. Temporary denervation during the developmental sensitive period for taste buds prevented most vallate taste buds from forming. Specifically, removing one IXth nerve and crushing the other in 3 day old neonates eliminated axons from the vallate papilla for about 10 days and by adulthood resulted in a mean ± 1 S.E.M. of 48 ± 12 vallate taste buds. Two explanations for the shortfall of adult vallate taste buds were evaluated: either 10 days of neonatal denervation impaired the gustatory competence of the vallate papilla, or the IXth nerve's trophic support of taste buds failed to recover after nerve crush on day 3. In adults, it was found that a IXth nerve previously crushed on day 3 would support numerous vallate taste buds (183 ± 27), provided that the vallate papilla had been continuously innervated by the contralateral IXth nerve during neonatal development. Consequently, taste neurons, whose axons had been crushed on day 3, seemed to survive and retain their trophic capacity to support taste buds in adults. To test for diminished competence of the gustatory epithelium, one IXth nerve was crushed on day 3 while the contralateral IXth nerve was removed. Beginning on day 75, the chorda tympani nerve was substituted for the re-innervating axons of the crushed IXth nerve. The cross-innervating chorda tympani ultimately supported only 51 ± 10 vallate taste buds. In contrast, in vallate papillae that developed without interruption of the contralateral IXth nerve during the sensitive period, the cross-innervating chorda tympani by itself supported more than four times as many vallate taste buds (214 ± 22). Evidently, a neonatal period of denervation permanently restricts the gustatory competence of the vallate epithelium; nerve-dependent precursors of taste receptor cells probably died or gpermanently changed their fate.