Shin-ichi Iwasaki

Evolution of the structure and function of the vertebrate tongue

Studies of the comparative morphology of the tongues of living vertebrates have revealed how variations in the morphology and function of the organ might be related to evolutional events. The tongue, which plays a very important role in food intake by vertebrates, exhibits significant morphological variations that appear to represent adaptation to the current environmental conditions of each respective habitat. This review examines the fundamental importance of morphology in the evolution of the vertebrate tongue, focusing on the origin of the tongue and on the relationship between morphology and environmental conditions. Tongues of various extant vertebrates, including those of amphibians, reptiles, birds and mammals, were analysed in terms of gross anatomy and microanatomy by light microscopy and by scanning and transmission electron microscopy. Comparisons of tongue morphology revealed a relationship between changes in the appearance of the tongue and changes in habitat, from a freshwater environment to a terrestrial environment, as well as a relationship between the extent of keratinization of the lingual epithelium and the transition from a moist or wet environment to a dry environment. The lingual epithelium of amphibians is devoid of keratinization while that of reptilians is keratinized to different extents. Reptiles live in a variety of habitats, from seawater to regions of high temperature and very high or very low humidity. Keratinization of the lingual epithelium is considered to have been acquired concomitantly with the evolution of amniotes. The variations in the extent of keratinization of the lingual epithelium, which is observed between various amniotes, appear to be secondary, reflecting the environmental conditions of different species.

Comparative studies of the dorsal surface of the tongue in three mammalian species by scanning electron microscopy

Comparative features of the dorsal tongue epithelia in musk shrews, mongooses and rats were described. The shapes of the filiform papillae were different in each of the species. The distribution pattern of filiform papillae was similar both in the musk shrews and mongoose, in that the form of filiform papillae changed gradually from the lingual apex to the posterior part of the lingual body. By contrast, the different types of filiform papillae were distributed on definite areas of the dorsal lingual surface in the rat. Microridges on the interpapillar surface in the musk shrew and mongoose presented a clear outline, but those of the rat were not so distinct. In all species, the upper surface of filiform papillae did not show any distinct microridges.

Ultrastructural study of the relationship between the morphogenesis of filiform papillae and the keratinisation of the lingual epithelium in the rat

Tongues were removed from rat fetuses on d 16 of gestation (E16) and from newborn (P0) and juvenile rats on d 7 (P7) and d 21 (P21) postnatally for examination by light and transmission electron microscopy. In the fetuses at E16, no rudiments of filiform papillae were visible on the dorsal surface of the tongue. No evidence of keratinisation could be recognised over the entire dorsal lingual epithelium. At P0, rudiments of filiform papillae showed a similar distribution to that seen in the adult, but had a more rounded appearance. The columnar structure of cells in the epithelium, with the different degrees of keratinisation as observed in the mature adult, was indistinct, but a keratinised layer was clearly located at the tip of each filiform papilla. In juveniles at P7, the filiform papillae on the anterior part of the tongue were long and slender, and the anterior and posterior cell columns of the filiform papillae and the interpapillary cell columns were clearly distinguishable. In juveniles at P21, the structure of filiform papillae was identical to that in the adult. These results indicate that, in rats, the morphogenesis of filiform papillae advances in parallel with keratinisation of the lingual epithelium from just before birth to a few weeks after birth.

Scanning-Electron-Microscopic Study of the Dorsal Lingual Surface of the Squirrel Monkey

The structure of the lingual papillae and the ultrastructure of the surface of the lingual dorsal epithelial cells of squirrel monkeys were observed by scanning electron microscopy. Filiform papillae were distributed over the entire dorsal surface of the tongue, except for the radix zone. Fungiform papillae were scattered among these filiform papillae. In the middle of the posterior end of the lingual body, a single vallate papilla was located. Higher magnification of the lingual dorsal epithelium revealed that prominent microridges and elevated intercellular borders occurred widely in the basofrontal area of the filiform papillae, interpapillar area and lingual radix zone. On the surface of the upper part of the filiform papillae, fine pits and hollows were observed. Indistinct microridges were distributed over the surface of the fungiform papillae.

Functional Morphology of the Tongue in the Domestic Goose (Anser Anser f. Domestica)

Using LM and SEM methods, the study describes microstructures in particular areas of the tongue of the goose. A thick multilayered keratinized epithelium forms the “lingual nail” and covers small and giant conical papillae, whereby the first functions as an exoskeleton of the tongue apex, and the latter are arranged along the lingual and well‐developed connective tissue cores, and together with the bill lamellae are involved in cutting. The row of conical papillae on the lingual prominence prevents regurgitation of transported food. In the area of the “lingual nail” and in the anterior part of the lingual prominence, Herbst corpuscles are accumulated, which allow to recognize food position. Filiform papillae, as widely distributed between the conical papillae of the body, are responsible for filtering. They can be explained as long keratinized processes of the epithelium and are devoid of connective tissue cores. During food transport, the flattened areas of the lingual body and the lingual prominence are protected by a parakeratinized epithelium, but the root is covered by a nonkeratinized epithelium. The presence of adipose tissue in the tongue probably reduces pressure during food passage, but also promotes mucus evacuation from the lingual glands, thus facilitating food transport. An entoglossal bone with a continuation as cartilage is the stable structural basis of the tongue system. Anat Rec, 2011.

Function-related morphological characteristics and specialized structures of the avian tongue

As a reflection of different life styles and environment, the tongue of vertebrates, which plays a major role in the intake and swallowing of food, displays significant morphological differences. The gross form and microscopic structure of the avian tongue differ greatly according to lifestyle. The avian tongue plays a fundamental role in many functions such as capturing, filtering, sucking and manipulating food in order to compensate absence of subsidiary organs like teeth in the oropharyngeal cavity. Variations in lingual papillae play an important role in feeding of birds, as they represent a structure similar to teeth in the upper and lower beaks and can be used to hold and direct food in the oropharyngeal cavity. Tongues of birds exhibit common as well as varying anatomical characteristics in terms of surface morphology, structure and topographical distribution of lingual papillae as well as distinct specialized structures, epithelial layers, taste buds and lingual glands. This review evaluates the important morphological peculiarities of the tongue in birds, focusing on the relationship between anatomical features and feeding functions.

Immunohistochemical detection of the expression of keratin 14 in the lingual epithelium of rats during the morphogenesis of filiform papillae

An immunofluorescence study of the expression of keratin 14 (K14) during the formation of filiform papillae was performed and the progress of keratinization of the epithelium of the rat tongue was monitored on semi-ultrathin sections by laser-scanning microscopy. Differential interference contrast (DIC) images were also examined to provide details of histology and cell morphology. No cells with immunoreactivity specific for K14 were detected on the lingual epithelium of foetuses on embryonic days 12 and 16 (E12 and E16), when the lingual epithelium was composed of a single layer or several layers of cuboidal cells. Immunoreactivity specific for K14 was detected first on basal and suprabasal keratinocytes of the dorsal epithelium of the tongue of new-borns on postnatal day 0 (P0) and was conspicuous in juveniles on P14. The immunoreactivity was particularly strong on the basal and suprabasal keratinocytes along the connective tissue papillae. The immunoreactivity extended over the entire cytoplasm but was not detected in the nucleus. The lingual epithelium was composed of stratified squamous cells and the rounded rudiments of filiform papillae were compactly arranged at equal intervals, for the most part, and the spaces between them were narrow and indistinct. Immunostaining of K14 was distinct on basal and suprabasal keratinocytes of the filiform papillar area of tongues of juveniles on P21, when the filiform papillae were conical. The spaces between them were relatively wide and, as a result, interpapillar cell columns were clearly visible. Immunoreactivity specific for K14 in the basal and suprabasal keratinocytes of the interpapillar cell columns was recognizable but was weaker than that in cells of papillar cell columns. The thickness of the epithelium in papillar and interpapillar areas increased gradually with the development of filiform papillae. However, sizes of basal and suprabasal keratinocytes remained almost unchanged during this process. These results suggest that the basal and suprabasal keratinocytes of the filiform papillar area proliferate with the initiation of the morphogenesis of filiform papillae and the keratinization of the epithelium. In addition, it appears that, after P14, the basal and suprabasal keratinocytes of the interpapillar area proliferate to supply the keratinocytes of the expanding interpapillar regions.

An ultrastructural study of the dorsal lingual epithelium of the rat snake, Elaphe quadrivirgata

The histological characteristics and ultrastructure of the dorsal lingual epithelium of the rat snake, Elaphe quadrivirgata, were investigated by light microscopy and scanning and transmission electron microscopy. Most of the surface of the bifurcated part of the tongue was relatively smooth. Dome-shaped, hemispherical bulges were compactly arranged on the epithelial cell surface of the basal area of this region. Intercellular borders were clearly recognizable as striations. Microridges were densely distributed on the epithelial cell surface of the lingual body. Intercellular borders were thickened. A keratinized layer was clearly visible in the epithelium of the anterior bifurcated area, namely, at the apex of the tongue. Although keratohyalin granules were not found in any layer of the epithelium in this area, the cells of the surface layer were filled with keratin filaments. The dorsal lingual epithelium of the posterior area, namely, the lingual body, did not show any evidence of keratinization. Each cell on the surface side still had a large, oval nucleus and intact organelles, such as mitochondria, rough endoplasmic reticulum, ribosomes, tonofibrils, and tonofilaments. Cellular interdigitation was evident between adjacent cells and clear microridges or microvilli were observed on the cell membranes on the free-surface side of cells located in the surface layer. The phylogenetic relevance of these findings is discussed.

Fine structure of the dorsal lingual epithelium of the domestic, newborn kitten, Felis catus.

The tip and the body of the tongue of the domestic kitten, Felis catus, were examined by light and transmission electron microscopy. On the tip of the tongue, no filiform papillae were observed, but the connective tissue papillae of the lamina propria were recognized. On the lingual body, there were filiform papillae composed of an anterior, a posterior and interpapillar epithelium. Under the transmission electron microscope, the epithelium on the tip of the kitten tongue was found to be of the stratified squamous type. The epithelium contained no cells filled with keratin fibers. In the lingual body, the interpapillar epithelium contained very few keratohyalin granules, and no cells with keratin fibers. In the epithelium on the anterior side of the filiform papillae, numerous keratohyalin granules appeared in the intermediate layer. In the surface layer, a thin layer of typical keratinized cells was visible. In the epithelium on the posterior side of the filiform papillae, a thick layer of keratinized cells was located on the surface layer.

Fine Structure of the Dorsal Lingual Epithelium of the Japanese Monkey Macaca fuscata fuscata

Filiform papillae, which were densely distributed all over the dorsal surface of the lingual body, were crown-shaped, with a central, circular area that sloped in the anterior direction and several branches that surrounded it in a semicircle from the back of the central area. Dome-shaped, fungiform papillae were scattered among these filiform papillae. At the posterior end of the lingual body, there were four circumvallate papillae. Prominent microridges and elevated intercellular borders were widely distributed in the central area of the filiform papillae and the interpapillar region. On the surface of the branches of the filiform papillae, microridges were rarely seen. On the surface of the fungiform papillae, indistinct microridges were observed. Histologically, the dorsal lingual epithelium revealed three different regions: the epithelium on the anterior side of the filiform papillae, the epithelium on the posterior side of the filiform papillae and the interpapillar epithelium. Whereas the basal and suprabasal cells are similar throughout, differences characterize the intermediate and surface layers. Keratohyalin granules appear predominantly in the intermediate layer in the epithelium on the anterior side of filiform papillae. In the epithelium on the posterior side of the filiform papillae, no keratohyalin granules occur and, instead, tonofibrils are prominent. The cells become significantly flattened. In the interpapillar epithelium, no keratohyalin granules are visible, and the tonofilaments occupy almost the entire cytoplasm of most cells in the intermediate and surface layers. The cells are larger in volume in these layers.