Early development and innervation of taste bud‐bearing papillae on the rat tongue

Abstract

Early development of fungiform papillae on the fetal rat tongue was examined: (1) to determine whether morphogenesis of the taste bud-bearing fungiform papillae is induced by nerve and (2) to study the growth pattern of the two sensory nerves that innervate the papilla. The papillae first appear on the 15th day of gestation (E15; E1 is the day when the dam is sperm positive) in rows parallel to the midline sulcus. There appears to be a medial-lateral and an anterior-posterior gradient in the sequence of papilla differentiation. The epithelium of the early papilla resembles a multilayered placode topped by a flattened surface periderm. Close examination of the peridermal cells at the apex of the papillae reveals that the cells have fewer surface microvilli and their cytoplasm is more electron opaque than that of similar cells in interpapillary regions. The basal cells in the placode-like epithelium differ from those in interpapillary regions in that they are postmitotic and have more mitochondria. At later stages, the papilla acquires a mesenchymal core and nerves grow into the core. Results from organ culture experiments of tongue fragments taken from E14 fetuses indicate that morphogenesis of fungiform papillae is initiated in the absence of sensory nerve influence, but the nerve exerts a trophic effect on their maintenance. The two sensory nerves of the tongue, the chorda tympani and the lingual branch of the trigeminal nerve, enter the tongue mesenchyme at E14 and grow toward the epithelium. By E15 the chorda tympani branches have reached the developing fungiform papillae, by E16 many have entered the papilla, and by E17 they have penetrated the epithelium at the papilla apex. Their fibers are associated exclusively with the cells at the papilla apex, where the taste bud will develop. The trigeminal nerve ramifies beneath the surface of the entire epithelium by E15. Later, it, too, sends branches into fungiform papillae; these ascend along the trunk of the chorda tympani and at E17 terminate in the connective tissue core around the chorda tympani field. The results are compatible with the notion that the tongue epithelium exerts a general tropic effect on growing axons of both sensory nerves, and the epithelial cells of the fungiform papilla apex exert a similar effect to which only the chorda tympani axons are responsive.

Induction of ectopic taste buds by SHH reveals the competency and plasticity of adult lingual epithelium

“…Thus, it is possible that misexpression of SHH in lingual epithelium attracted gustatory and/ or somatosensory neurites, and hence ectopic taste bud formation would be secondary to SHH-directed innervation. This was decidedly not the case for gustatory innervation, as these nerves did not stray from their taste bud targets, consistent with the highly targeted development of taste bud innervation (Farbman and Mbiene, 1991;Lopez and Krimm, 2006). The anterior tongue is densely innervated by trigeminal somatosensory fibers, which in cross-innervation studies support taste buds in situ (Kinnman and Aldskogius, 1988).…”

ß-Catenin signaling regulates temporally discrete phases of anterior taste bud development

“…Thus, the increase in taste papilla size driven by stabilized β-catenin is associated with increases in taste bud precursors (Shh + , Prox1 + ) and taste papilla epithelium (Ptch1 + ). During normal development, taste placodes are mitotically quiescent, whereas the adjacent taste papilla epithelium is highly proliferative (Farbman and Mbiene, 1991;Liu et al, 2013;Mbiene and Roberts, 2003;Okubo et al, 2006). Hence, we next addressed whether β-catenin activation expands embryonic taste papillae in part by triggering proliferation of mitotically silent placodes cellautonomously.…”

Psychophysics of taste lateralization on anterior tongue

“…The first hypothesis posits a neural brain map that relates gustatory receptors to their orolingual position, enabling localization of stimulated taste receptors, analogous to the somatotopic or retinotopic neural maps. The second hypothesis posits that when a taste receptor cell is activated by a taste stimulus, it in turn activates adjacent tactile fibers, and the induced secondary tactile signal enables one to localize the stimulated region (Farbman & Mbiene, 1991;Whitehead & Kachele, 1994). The third hypothesis recognizes that most taste fibers are also mechanically and thermally sensitive (Hanamori, Hirota, & Ishiko, 1990;Matsuo et al, 1995;Ogawa, Hayama, & Yamashita, 1986;Ogawa, Imoto, & Hayama, 1984;Robinson, 1988;Travers & Norgren, 1995).…”