Anatomical and neurohistological observations on the tongue of the India goat, Capra aegagrus.

The anatomy and neurohistology of the tongue of the Indian goat, Capra aegagrus, have been described. The apex linguae is notched in the centre. The foramen caecum is found to be absent. The sublingua could not be traced. The filiform papillae are the most common and divided into three types: the simple, giant, and true filiform papillae. The true filiform papillae are the most developed of the three types. The foliate papillae are absent. There are 13--14 circumvallate papillae arranged in two rows in a V-shaped pattern. The fungiform papillae are large and could easily be seen with the naked eye. They are scattered over the entire dorsum, being in abundance at the tip. The tongue of the goat is richly innervated. On the dorsum, the lamina propria is innervated by thick nerve fibres. In the fungiform papillae quite a large number of nerve fibres could be seen. The circumvallate papillae are also abundantly provided with nerves. A few ganglion cells are found below the circumvallate papillae. Thick nerve fibres are seen across the numerous glands and their ducts. Muscle fibres and connective tissue are also richly innervated.     

Cyclopamine and jervine in embryonic rat tongue cultures demonstrate a role for Shh signaling in taste papilla development and patterning: fungiform papillae double in number and form in novel locations in dorsal lingual epithelium

From time of embryonic emergence, the gustatory papilla types on the mammalian tongue have stereotypic anterior and posterior tongue locations. Furthermore, on anterior tongue, the fungiform papillae are patterned in rows. Among the many molecules that have potential roles in regulating papilla location and pattern, Sonic hedgehog (Shh) has been localized within early tongue and developing papillae. We used an embryonic, tongue organ culture system that retains temporal, spatial, and molecular characteristics of in vivo taste papilla morphogenesis and patterning to study the role of Shh in taste papilla development. Tongues from gestational day 14 rat embryos, when papillae are just beginning to emerge on dorsal tongue, were maintained in organ culture for 2 days. The steroidal alkaloids, cyclopamine and jervine, that specifically disrupt the Shh signaling pathway, or a Shh-blocking antibody were added to the standard culture medium. Controls included tongues cultured in the standard medium alone, and with addition of solanidine, an alkaloid that resembles cyclopamine structurally but that does not disrupt Shh signaling. In cultures with cyclopamine, jervine, or blocking antibody, fungiform papilla numbers doubled on the dorsal tongue with a distribution that essentially eliminated inter-papilla regions, compared with tongues in standard medium or solanidine. In addition, fungiform papillae developed on posterior oral tongue, just in front of and beside the single circumvallate papilla, regions where fungiform papillae do not typically develop. The Shh protein was in all fungiform papillae in embryonic tongues, and tongue cultures with standard medium or cyclopamine, and was conspicuously localized in the basement membrane region of the papillae. Ptc protein had a similar distribution to Shh, although the immunoproduct was more diffuse. Fungiform papillae did not develop on pharyngeal or ventral tongue in cyclopamine and jervine cultures, or in the tongue midline furrow, nor was development of the single circumvallate papilla altered. The results demonstrate a prominent role for Shh in fungiform papilla induction and patterning and indicate differences in morphogenetic control of fungiform and circumvallate papilla development and numbers. Furthermore, a previously unknown, broad competence of dorsal lingual epithelium to form fungiform papillae on both anterior and posterior oral tongue is revealed.     

Sonic hedgehog exerts distinct, stage-specific effects on tongue and taste papilla development

Taste papillae are ectodermal specializations that serve to house and distribute the taste buds and their renewing cell populations in specific locations on the tongue. We previously showed that Sonic hedgehog (Shh) has a major role in regulating the number and spatial pattern of fungiform taste papillae on embryonic rat tongue, during a specific period of papilla formation from the prepapilla placode. Now we have immunolocalized the Shh protein and the Patched receptor protein (Ptc), and have tested potential roles for Shh in formation of the tongue, emergence of papilla placodes, development of papilla number and size, and maintenance of papillae after morphogenesis is advanced. Cultures of entire embryonic mandible or tongues from gestational days 12 to 18 [gestational or embryonic days (E)12-E18] were used, in which tongues and papillae develop with native spatial, temporal, and molecular characteristics. The Shh signaling pathway was disrupted with addition of cyclopamine, jervine, or the 5E1 blocking antibody. Shh and Ptc proteins are diffuse in prelingual tissue and early tongue swellings, and are progressively restricted to papilla placodes and then to regions of developing papillae. Ptc encircles the dense Shh immunoproduct in papillae at various stages. When the Shh signal is disrupted in cultures of E12 mandible, tongue formation is completely prevented. At later stages of tongue culture initiation, Shh signal disruption alters development of tongue shape (E13) and results in a repatterned fungiform papilla distribution that does not respect normally papilla-free tongue regions (E13-E14). Only a few hours of Shh signal disruption can irreversibly alter number and location of fungiform papillae on anterior tongue and elicit papilla formation on the intermolar eminence. However, once papillae are well formed (E16-E18), Shh apparently does not have a clear role in papilla maintenance, nor does the tongue retain competency to add fungiform papillae in atypical locations. Our data not only provide evidence for inductive and morphogenetic roles for Shh in tongue and fungiform papilla formation, but also suggest that Shh functions to maintain the interpapilla space and papilla-free lingual regions. We propose a model for Shh function at high concentration to form and maintain papillae and, at low concentration, to activate between-papilla genes that maintain a papilla-free epithelium.     

Separate and distinctive roles for Wnt5a in tongue, lingual tissue and taste papilla development

Although canonical Wnt signaling is known to regulate taste papilla induction and numbers, roles for noncanonical Wnt pathways in tongue and taste papilla development have not been explored. With mutant mice and whole tongue organ cultures we demonstrate that Wnt5a protein and message are within anterior tongue mesenchyme across embryo stages from the initiation of tongue formation, through papilla placode appearance and taste papilla development. The Wnt5a mutant tongue is severely shortened, with an ankyloglossia, and lingual mesenchyme is disorganized. However, fungiform papilla morphology, number and innervation are preserved, as is expression of the papilla marker, Shh. These data demonstrate that the genetic regulation for tongue size and shape can be separated from that directing lingual papilla development. Preserved number of papillae in a shortened tongue results in an increased density of fungiform papillae in the mutant tongues. In tongue organ cultures, exogenous Wnt5a profoundly suppresses papilla formation and simultaneously decreases canonical Wnt signaling as measured by the TOPGAL reporter. These findings suggest that Wnt5a antagonizes canonical Wnt signaling to dictate papilla number and spacing. In all, distinctive roles for Wnt5a in tongue size, fungiform papilla patterning and development are shown and a necessary balance between non-canonical and canonical Wnt paths in regulating tongue growth and fungiform papillae is proposed in a model, through the Ror2 receptor.     

A scanning electron microscopic study of the dorsal surface of the human tongue

To study the dorsal surface of the human tongue using a scanning electron microscopy (SEM), tissue specimens were taken from the anterior part of the tongues of 15 individuals aged from 21- to 28-years-old. The formalin-fixed samples were processed routinely for SEM. With SEM the surface of the normal tongue mucosa was shown to be rather evenly covered by filiform papillae, with some fungiform papillae scattered among them. Filiform papillae consisted of two parts: the body and hairs. The mucosal surface of the body was smooth; the squamous epithelial cells were polygonal, and their boundaries were prominent. On the surface of the superficial epithelial cells were parallel or branching microplicae. Each filiform papilla had 6-10 hairs, which were scaled and covered by an extensive plaque of microorganism. The upper surface of the fungiform papillae was smooth; only a few desquamating cells were seen. The superficial cells had a pitted appearance and cell boundaries overlapped. Taste pores, up to 3 pores in a single papilla, were found on the upper surface. Desquamation was more pronounced on the base of the fungiform papillae than on the upper surface. In almost all fungiform papillae some hairs protruded from the base. Parallel microplicae were found on the surface of the superficial cells of the base. The structure and function of the human tongue, as well as the microplicae of its superficial cells, are compared to those of various species of animals.     

白暨豚的舌

在现代生存的四类淡水豚中,恒河豚(Platanista gangetica)和拉河豚(Pontoporia blain-villei)的舌已有详文报道(Arvy和Pilleri,1970;Yamasaki等,1976a)。亚河豚(Iniageoffrend)的舌也在Yamasaki的文章中作为和上述二种淡水豚舌的比较而述及。白暨豚(Liptes vexillifer)的舌除陈宜瑜等(1975)曾提及外,迄今未有其他报道。鉴此,作者对白暨豚的舌作了解剖学和组织学的观察,现将研究结果报告如下: 白暨豚舌的标本取自幼体、亚成体、成体和老年个体等七头个体。为了比较,还收集了亚河豚、其它海豚类和陆生哺乳类的舌。用10％甲醛固定保存,各项量度根据固定标本测量。白暨豚舌的外形描述以NNC 7909号标本为主,以其它个体的观察为辅。其组     

Taste bud density in circumvallate and fungiform papillae of the bovine tongue

Taste bud quantitation may provide useful parameters for interspecies comparisons of the gustatory system. The present study is a morphometric analysis of bovine taste papillae. Circumvallate and fungiform papillae from six bovine tongues were serially sectioned and, following staining, analyzed. Circumvallate papillae were found to have a mean volume of 3.66 +/- 2.82 mm3, a mean number of taste buds per papilla of 445 +/- 279, and a mean taste bud density of 155 +/- 112 buds/mm3. Values for lateral fungiform papillae for the same three parameters were 0.384 +/- 0.184 mm3, 13.2 +/- 13.4, and 40.8 +/- 46.6 buds/mm3, respectively. Values for dorsal fungiform papillae were 0.438 +/- 0.246 mm3, 4.39 +/- 4.78, and 14.0 +/- 17.1 buds/mm3, respectively. Circumvallate papillae were found to have a significantly greater volume, number of taste buds per papilla, and taste bud density than either type of fungiform papilla. These data should serve as background for biochemical, endocrinological, or neurological studies involving the bovine tongue.     

Sublingual structures of primates. II. Hominoidea, review, summary and literature

1. In Homo and the great apes (Pongidae) there occurs, besides the plica sublingualis a plica fimbriata at the ventral surface of the tongue. This duplicature of the mucosa does not occur in the Hylobytidae and in the other primates. 2. Some taste buds could be found in the epithelium of the plica sublingualis of the Pongidae. 3. There are many taste buds in the epithelium of the plica fimbriata of the Pongidae. On this sublingual structure there were counted 1776 taste buds in Pongo, 592 in Gorilla and 280 in Pan. A few taste buds could also be found on the plica fimbriata of a human newborn. 4. A glandula apicis linguae occurs in Homo, Pan, Gorilla and Pongo. 5. The fresh saliva of the glandula apicis linguae and the saliva on the floor of the mouth can be tested by the taste buds in the epithelium of the plica fimbriata, of papillae lenticulares and of areae gustatoriae at the ventral surface of the tongue. 6. It might be the function of the sublingual taste buds to taste the fresh saliva as a gradient for the central nervous comparison with the taste of the saliva on the dorsal surface of the tongue. 7. Because of the complete absence of a sublingua in the Platyrrhini and in the Cercopithecinae it is unlikely that the plica fimbriata of Homo and the great apes can be interpreted as a homalogon of the sublingua in the prosimians. 8. Because of the absence of a sublingua in other ordines of the Mammalia (Insectivora, Carnivora, Rodentia, Chiroptera, Ungulata) it is unlikely as well that the sublingua in the prosimians can be interpreted as a homologon of the tongues of the lower vertebrates. The sublingual structures occuring in the Marsupialia have to be investigated. 9. Because of these reasons the new development of the sublingua in the prosimians and the plica fimbriata in the Hominoidea, in complete independence from one another, seems to be a better explanation of the 2 structures and less contradictionary to anatomical and phylogenetic arguments. The different function of both structures in the recent primates gives a hint for the possible reason for their development during the process of evolution.     

Macroanatomic,light microscopic,and scanning electron microscopic studies of the tongue in the seagull (Larus fuscus) and common buzzard (Buteo buteo)

The tongues of ten seagulls and six common buzzards were examined. In both species, papillae linguales caudales were shaped like a letter “V” between the corpus linguae and the radix linguae. From these papillae, the length of the laterally placed papillae was greater compared with others in both species. Two or three secondary papillae were detected on these papillae in the seagull. In scanning electron microscope (SEM) examinations, in the seagull, the apex linguae was composed of multilayered desquamated cells, while in the buzzard, scalelike simple projections on the surface of desquamated cells were observed. In the buzzard, glandula (gll). linguales, and gll. mandibulares caudales were seen, while in the seagull, gll. cricoarytenoideae and gll. mandibulares caudales were present. In the seagull, apex linguae were bifurcated, and there were desquamating multilayered cells, particularly at the apex linguae. The number and location of salivary gland orifices are specific to this species. The common buzzard had similarities to many characteristics of the long‐legged buzzard. An absence of long and curly threadlike projections at the two lateral sides of the corpus linguae and an excessive number of salivary gland orifices at the corpus linguae were the main differences from the long‐legged buzzard.     

Filiform papillae of human, rat and swine tongue

In order to study the structure of filiform papillae (FP), tissue specimens were taken from the anterior part of the tongues of 8 humans, 8 rats and 8 swine. The formalin-fixed samples were processed routinely for scanning electron microscopy (SEM) and light microscopy. With SEM, FP of human tongue contained 5-12 hairs which were covered with a massive plaque of micro-organisms. FP of rat tongue, on the other hand, contained one papillary projection with smooth surface structure. Colonization of micro-organisms was seen on the anterior part of the body of FP, but not on the hairs. In the cross-section of FP of the rat tongue, the cells of the papilla were close to each other and no micro-organisms were seen within the papillae. On the contrary, the spaces between the squamous epithelial cells of the hairs of human FP contained numerous micro-organisms. The structure of FP of the swine tongue resembled that of the rat tongue. The hairs were smooth, and some micro-organisms were seen on the cell surface of the interpapillary areas. The structure of FP is discussed from the standpoint of different keratinization and colonization of micro-organisms.     

Scanning electron microscopic study on the structure of the lingual papillae of the Saanen goat

The morphology of lingual papillae of the ten male mature Saanen goats (11 months old, approximately 42 kg in weight and of a known pedigree) was examined by scanning electron microscopy. Tissues were taken from the dorsal and ventral surfaces of the apex, body and root of the tongue, and were prepared accordingly and observed under the scanning electron microscope. On the dorsal and ventro-lateral surfaces of the lingual mucosa, three types of mechanical papillae (filiform, lenticular, and conical) and two types of gustatory papillae (vallate and fungiform) were observed. The structure and density of the filiform papillae differentiated on the anterior, posterior and ventro-lateral aspects of the tongue. Two types of lenticular papillae, both possessing a prominent surrounding papillary groove, were determined. The pyramidal-shaped type I lenticular papilla had a pointed apex while the round-shaped type II lenticular papilla possessed a blunt apex. Certain number of the type I lenticular papillae had double apices. The larger conical papillae were hollow structures, differing structurally from the filiform papillae with their larger size, a tip without projections and lack of the secondary papillae. The vallate papillae were present on both rims of the torus linguae, were encircled by a prominent gustatory furrow which was also surrounded by a thick annular fold. The fungiform papillae were scattered among the filiform papillae in the anterior two-thirds of the dorsal and lateral surfaces, and each of them was highly protected by surrounding filiform papillae, yet encircled by a papillary groove. Our findings indicate that Saanen goat have profuse distribution of papillae on the tongue displaying morphological features characteristic of mechanical function.     

Scanning electron microscopy of developing papillae on the tongue of human embryos and fetuses

The appearance and differentiation of papillae on dorsal andlateral surfaces of human embryonic and fetal tongues, at variousdevelopmental ages, were studied by scanning electron microscopy.Formaldehyde and phosphate buffer fixation provided satisfactorypreservation. At 8–9 weeks, the anterior two-thirds ofthe tongue showed no obvious signs of papillae. In contrast,just anterior to the sulcus terminalis rounded elevations wereseen, suggesting initial signs of circumvallate papillae. At10–13 weeks, the distribution and shape of elevationson the anterior two-thirds of the tongue indicated the beginningof fungiform papillae. Openings located on the dorsal surfaceof many of these fungiforms contained an amorphous central structureprojecting out of the papilla. First signs of foliate papillaewere seen at 10 weeks. At 15–18 weeks, fungiform and filiformpapillae were recognized, although sometimes their borders wereobscured by scaling epithelial cells. At 23–26 weeks,all papillae exhibited their adult form. ^*Presented, in part, at the VIth International Symposium onOlfaction and Taste, Gif-sur-Yvette, Paris, France, 15–17thJuly, 1977.     

Regeneration ability of fungiform papillae and taste-buds in rats

We have earlier shown that the taste-bud-bearing fungiform papillaeform a stable pattern on the tongue of rats. In this study theeffect of removal of the fungiform papillae in rats was investigated.The fungiform papillae on a 10 x 5-mm area on one side of thetongue were removed after mapping of both sides under an operatingmicroscope. Serial sections of five rat tongues within 1 dayof biopsy showed that all but one papilla were gone. After 4,6 and 12 months an average of seven papillae with taste-budswere found in the operated area, compared to 20, 26 and 23 inthe controls. Comparison of tongue maps before and after theseperiods showed that papillae had not migrated from areas outsidethe area of the biopsies. To test the assumption that the extentof biopsy determined the amount of regeneration, only the upperpart of the papillae with their taste buds were removed in 15rats. Complete regeneration of papillae and taste buds was obtainedwithin 14 days. The function of the regenerated taste buds wastested by bilateral recording from the chorda tympani propernerves. No difference in response amplitudes was observed betweenthe sides. When, however, the whole papilla including its basewas removed, neither the papilla nor the taste-bud regenerated.The results show that the ability of the fungiform papilla andthe taste-bud to regenerate after removal of the papilla isrelated to the extent of the biopsy. If the entire papilla includingits base is removed, it will not regenerate. If only the upperpart is removed, complete regeneration of both papilla and itstaste-bud will occur.     

Epithelial overexpression of BDNF or NT4 disrupts targeting of taste neurons that innervate the anterior tongue

Brain-derived neurotrophic factor (BDNF) and neurotrophin-4 (NT4) are essential for the survival of geniculate ganglion neurons, which provide the sensory afferents for taste buds of the anterior tongue and palate. To determine how these target-derived growth factors regulate gustatory development, the taste system was examined in transgenic mice that overexpress BDNF (BDNF-OE) or NT4 (NT4-OE) in basal epithelial cells of the tongue. Overexpression of BDNF or NT4 caused a 93 and 140% increase, respectively, in the number of geniculate ganglion neurons. Surprisingly, both transgenic lines had severe reduction in fungiform papillae and taste bud number, primarily in the dorsal midregion and ventral tip of the tongue. No alterations were observed in taste buds of circumvallate or incisal papillae. Fungiform papillae were initially present on tongues of newborn BDNF-OE animals, but many were small, poorly innervated, and lost postnatally. To explain the loss of nerve innervation to fungiform papillae, the facial nerve of developing animals was labeled with the lipophilic tracer DiI. In contrast to control mice, in which taste neurons innervated only fungiform papillae, taste neurons in BDNF-OE and NT4-OE mice innervated few fungiform papillae. Instead, some fibers approached but did not penetrate the epithelium and aberrant innervation to filiform papillae was observed. In addition, some papillae that formed in transgenic mice had two taste buds (instead of one) and were frequently arranged in clusters of two or three papillae. These results indicate that target-derived BDNF and NT4 are not only survival factors for geniculate ganglion neurons, but also have important roles in regulating the development and spatial patterning of fungiform papilla and targeting of taste neurons to these sensory structures.     

Light- and Scanning-Electron-Microscopic Analyses of the Plica glossoepiglottica lateralis of the neonate and adultPan troglodytes troglodytes — Blumenbach (1799)

A unique type of papillae is evident in the plicae glossoepiglotticae laterales of the tongue ofPan troglodytes troglodytes. Areas of occurrence show flat lobes of varying length with elongated miniature processes on their free tips. The function of these papillae is presumably the convection of liquid food into the pharynx (along with the lateral folds). Furthermore, it is assumed that the papillae are sensory organs which relay taste, temperature, pain, and pressure, similar to the papillae filiformes of the tongue of other mammalia (Kunze 1969). Free nerve fibres and nerve endings were found in both the epithelium and the connective-tissue. Nerve structures resembling the “Organs of Meissner” were also discovered in the subepithelial connective-tissue. Goblet cells are found in the surface layers in the epithelium of the papillae of the newborn. These are absent in the papillae of the adultPan troglodytes troglodytes. The secretion of the goblet cells functions as a mechanical and chemical protectant for the papillae.     

Comparative anatomy of the tongue of Pan troglodytes (Blumenbach, 1799) and other primates. II. Findings in other primates

This 2nd part of our studies shows that the papilla foliata is fully developed in Pan, Cebus, and Macaca; in Prosimians the papilla foliata is well developed in Lemur and Chirogaleus. In Galago crassicaudatus, this papilla is missing. Among 3 individuals of Microcebus, the papilla foliata was differently developed: in 2 cases, the tongue exhibited only 2 on both sides and a very low folia. Taste buds were found in the epithelium of only one side of each folium. In the 3rd case, the folia of the papilla were developed only on one side of the tongue, whereas, on the other side, a typical papilla was missing. Instead of the papilla, the tongue of the same animal exhibited a hillock-like structure; it is a gustatory hillock which exhibited many taste buds. There were 3 gustatory hillocks in all of the specimens of Tupaia glis; they are situated on both sides of the tongue.     

Observations on rhinoceros tongue morphology

The rhinoceros tongue is distinguished among perissodactyl organs by its sagittally divided intermolar eminence crowned by a dextral and a sinistral cluster of circumvallate papillae. These structures were originally noted in the Indian rhinoceros by Owen (1852) but have since remained unmentioned for this, or for any other rhinoceros form. They are here described for specimens of the Indian, African White and African Black rhinoceroses. The structural and functional nature of the intermolar eminence is established and this entity is distinguished from an hitherto unrecognized topographical component of the tongue, designated the pars elliptica linguae. The lingual morphology of the three rhinoceros forms is summarised and certain intergeneric differences are noted.     

Shh, Bmp-2, Bmp-4 and Fgf-8 are associated with initiation and patterning of mouse tongue papillae.

Spacing patterns are of fundamental importance in various repeated structures which develop at regular intervals such as feathers, teeth and insect ommatidia. The mouse tongue develops a regular papilla pattern and provides a good model to study pattern formation. We examined the expression patterns of the signalling molecules, sonic hedgehog (Shh), bone morphogenetic proteins -2 and -4 (Bmp-2 and Bmp-4), and fibroblast growth factor-8 (Fgf-8) in mouse embryos between E 10.5 and 15. We show that all four genes are expressed uniformly in the tongue epithelium between E 10.5 and 11. At E 13, before morphologically detectable gustatory papillae initiation, Shh, Bmp-2 and Bmp-4 expression segregates into discrete spots, whereas, Fgf-8 is downregulated. At E 14, small eminences in the anterior part of the tongue are the first morphological indications of fungiform papillae, and they express Shh and Bmp-2, whereas, Bmp-4 is almost absent in the tongue. We conclude that these conserved signalling molecules are associated with the initiation and early morphogenesis of the tongue papillae.