Quantitative study of fungiform papillae and taste buds on the cat's tongue

The number of fungiform papillae has been counted on the tongues of six adult cats and of kittens both at birth and aged 2 and 4 months. Papillae were sampled from different regions of the tongue, and their size and the number of taste buds they contained were determined using histological sections taken parallel to the tongue surface. There were approximately 250 fungiform papillae on the tongues of the adult cats, the papillae were most numerous at the tip of the tongue, and there was no significant difference between the number of papillae on each side. The size of the papillae increased from a mean maximum diameter of 0.28 mm at the tip of the tongue to 0.48 mm at the back; the mean number of taste buds increased correspondingly from 6.9 to 16.6. The kitten tongues had a number and distribution of fungiform papillae similar to that found in the adults. In the neonate, papillae were smaller and contained fewer taste buds; these parameters increased with the corresponding increase in tongue size in the 2- and 4-month-old kittens.     

Age does not affect numbers of taste buds and papillae in adult rhesus monkeys

Taste buds and papillae in tongues of rhesus monkeys were examined and counted to determine if there are age-related differences in general morphology or numbers of receptor organs. Tongues from 15 monkeys in five groups aged 4-31 years were studied with light microscopy. Fungiform, circumvallate, and foliate papillae were examined and taste buds in each papilla type were counted. Numbers of papillae did not differ with age through 31 years; however, at 24 years and older, fungiform papillae were reduced in number in some animals that had lost tongue tips due to trauma. There were no age-related differences in numbers of taste buds in any of the three gustatory papilla types, nor did taste bud diameter alter with age. From data on each papilla type, estimates were made of total numbers of lingual taste buds. Totals ranged from about 8,000 to 10,000 and there were no age-related differences. These results support other recent reports that taste buds are not decreased in number in old rats or humans. Since taste bud numbers and general morphology are maintained even in old age, any age-related differences in taste behavior cannot be attributed to gross degenerative changes in lingual taste buds.     

Maturation of taste buds on the soft palate of the postnatal rat

Taste bud distribution on the soft palate and within three types of tongue papillae (fungiform, foliate, and circumvallate) were examined histologically in the rat at different postnatal ages. After paraffin embedding, serial sections (10 microm) were made and stained by HE, and digitized images of each section were examined. The existence of a taste pore was used to identify mature taste buds. At birth, 53% (68 of 127 observed) of the taste buds on the soft palate, but only 14% (14 of 110 observed) within fungiform papillae, contained a taste pore. One week after birth, the number of mature taste buds increased rapidly, resulting in 90% of soft palate taste buds and 80% of fungiform taste buds containing taste pores. In contrast, no taste buds with pores were observed at birth within foliate and circumvallate papillae; however, at two weeks after birth 52% (71 of 132 observed) of the foliate and 68% (180 of 267 observed) of the circumvallate taste buds examined contained taste pores. These results suggest that taste buds within the soft palate play an important role in the detection of nutrients in the neonatal rat.     

Spatial distribution of rat fungiform papillae

The objective of this study was to determine the spatial distribution of fungiform papillae on the rat's tongue. Since each fungiform papilla in the rat has a single taste bud, the spatial distribution of fungiform papillae is equivalent to the location of taste buds on the anterior tongue. A mean total number of 187 fungiform papillae per tongue were found which were about equally divided between the two lateral halves of the tongue. Over 50% of the total number of fungiform papillae were located on the tongue tip for an average density of 3.4 papillae/mm², while the dorsal surface of the tongue had an average density of 1.3 papillae/mm² of tongue surface. Papillae were absent on the dorsal midline, but a paracentral line of papillae running from anterior to posterior was a consistent finding. Though not identical, the distribution of papillae was essentially the same on different tongues. The functional significance of the papilla distribution is not understood, but electrophysiological experiments show evidence of neural interaction of papillae which are clustered together. The distribution of papillae and the distribution of nerve fibers which innervate them must be evaluated together in order to appreciate the significance of the distribution of fungiform papillae and their associated taste bunds.     

The nature of the substance P-containing nerve fibres in taste papillae of the rat tongue

The nature of the association of substance P (SP) with taste buds in the rat tongue was investigated by immunohistochemical and radioimmunoassay techniques. Both the circumvallate and fungiform papillae were found to receive a rich innervation by substance P-containing fibres. Although these fibres were closely associated with the taste buds in these structures, they assumed a perigemmal rather than an intragemmal location. Bilateral lesions of the glossopharyngeal nerve resulted in the depletion of taste buds from the vallate papilla and a large reduction in substance P immunoreactive fibres in this area. Lesions of the chorda tympani, which led to the degeneration of taste buds in fungiform papillae, had no effect on the immunohistochemical appearance of substance P in these papilla or on the substance P levels in the anterior part of the tongue. Lesions of the mandibular division of the trigeminal nerve or neonatal capsaicin treatment had no effect on the structural integrity of taste buds in fungiform papillae but led to the depletion of substance P-immunoreactive fibres from these papillae. Both of these procedures caused a 71% reduction in the substance P content of the anterior tongue, ipsilaterally after the nerve lesion and bilaterally after capsaicin treatment. The results are discussed in relation to the possible functional role of substance P-containing fibres within nerves supplying taste structures of the tongue.     

Neural control of ectopic filiform spines in adult tongue

The tongue surface directly above a fungiform taste bud is flat, thinly keratinized, and free of filiform spines. We examined fungiform papillae in serial sections of rat and gerbil tongues after unilateral transection of the chorda-lingual nerve had caused many fungiform taste buds to degenerate. Such empty fungiform papillae often formed a solitary keratinized outgrowth that closely resembled the spine of an ordinary filiform papilla. By six months an ectopic spine was found on 61% of empty fungiform papillae, but never on fungiform papillae that contained a taste bud. Experimental innervation of the tongue reduced the incidence of ectopic filiform spines in proportion to the cross-sectional area of the trigeminal nerve branches tested (the mylohyoid nerve, the lingual nerve, lingual + mylohyoid or lingual + auriculotemporal nerves). The chorda tympani nerve was 60 times more effective than trigeminal nerves in preventing ectopic filiform spines. We suggest that positive and negative trophic actions are normal characteristics of taste axons, for they promote the formation of taste buds and prevent the expression of ectopic filiform spines. By preventing the outgrowth of ectopic spines on fungiform papillae, taste axons maintain a thinly keratinized apical surface that can be breached by the taste receptor cells.     

Morphological characteristics of the tongue and its papillae in the donkey (Equus asinus): a light and scanning electron microscopical study

The morphology of the donkey tongue and its papillae were investigated by macroscopy and by light and scanning electron microscopy in ten adult animals (six males and four females). The spatula-shaped tongues measured about 28 cm in length, 4.5 cm in breadth and 3.5 cm in thickness. Samples from different areas of four tongues were grossly examined and pieces were processed for light and scanning electron microscopy. Filiform papillae were distributed mainly on the dorsum of the tongue, being thin and relatively short at the apex, conical and scaly in the main part (triangular zone) of the body, and thin and longer at the caudal part of the body. Few of them were found on the lateral surfaces. Fungiform papillae appeared scattered mainly on the lateral surfaces. They were mostly rounded (about 1.0 mm in diameter), but lobulated forms were also observed. Filiform and fungiform papillae were both completely devoid of taste buds, indicating a more mechanical function. The vallate papillae were 2-3 in number, located at the most caudal part of the body. They were three to four times as large as the fungiform papillae (about 5.6 mm in diameter) each with a wide circular groove around the central bulbous projection. Secondary grooves originating from the primary one were also demonstrated. The vallate papillae contained many taste buds with taste pores opening deeply into the papillary groove. Fine filiform papillae were demonstrated on the bulb-like part of the vallate papillae. The donkey tongue had sinister and dexter well-developed sets of foliate papillae close to the basis of the palatoglossal arch. They were arranged in the form of numerous leaves separated by deep, variably wide grooves and contained a very large number of taste buds. It is believed that the existence of well developed foliate papillae in donkey may substitute the comparatively few vallate papillae in this species.     

Patterns of immunoreactivity specific for gustducin and for NCAM differ in developing rat circumvallate papillae and their taste buds

α-Gustducin and neural cell adhesion molecule (NCAM) are molecules previously found to be expressed in different cell types of mammalian taste buds. We examined the expression of α-gustducin and NCAM during the morphogenesis of circumvallate papillae and the formation of their taste buds by immunofluorescence staining and laser-scanning microscopy of semi-ultrathin sections of fetal and juvenile rat tongues. Images obtained by confocal laser scanning microscopy in transmission mode were also examined to provide outlines of histology and cell morphology. Morphogenesis of circumvallate papillae had already started on embryonic day 13 (E13) and was evident as the formation of placode. By contrast, taste buds in the circumvallate papillae started to appear between postnatal day 0 (P0) and P7. Although no cells with immunoreactivity specific for α-gustducin were detected in fetuses from E13 to E19, cells with NCAM-specific immunoreactivity were clearly apparent in the entire epithelium of the circumvallate papillary placode, the rudiment of each circumvallate papilla and the developing circumvallate papilla itself from E13 to E19. However, postnatally, both α-gustducin and NCAM became concentrated within taste cells as the formation of taste buds advanced. After P14, neither NCAM nor α-gustducin was detectable in the epithelium around the taste buds. In conclusion, α-gustducin appeared in the cytoplasm of taste cells during their formation after birth, while NCAM appeared in the epithelium of the circumvallate papilla-forming area. However, these two markers of taste cells were similarly distributed within mature taste cells.     

Mice lacking the p75 receptor fail to acquire a normal complement of taste buds and geniculate ganglion neurons by adulthood

Brain-derived neurotrophic factor and neurotrophin-4 are required for normal taste bud development. Although these neurotrophins normally function via the tyrosine kinase receptor, trkB, they also bind to the pan-neurotrophin receptor, p75. The goal of the present study was to determine whether the p75 receptor is required for the development or maintenance of a full complement of adult taste buds. Mice with p75 null mutations lose 34% of their circumvallate taste buds, 36% of their fungiform papillae, and 26% of their fungiform taste buds by adulthood. The reduction of taste buds in the adult circumvallate papilla was similar to that observed previously at postnatal day 7 (Fan et al. Brain Res Dev Brain Res 2004;150:23-39). Taken together, these findings indicate that the p75 receptor is critical for the development of a full complement of taste buds, but is not required for maintenance of circumvallate taste buds in adulthood. Immunolabeling for p75 was not observed in taste buds, indicating that p75 signaling influences taste bud number indirectly. Geniculate ganglion neurons, which provides innervation to fungiform taste buds, express the p75 receptor. Mice with p75 null mutations also have fewer neurons in the geniculate ganglion. Together, these results suggest that the p75 receptor is important for the survival of geniculate neurons and geniculate neuron survival is required for the development of a full complement of taste buds by adulthood.     

Development of fungiform papillae: patterned lingual gustatory organs

The fungiform papilla is a gustatory organ that provides a specific tissue residence for taste buds on the anterior tongue. Thus, during development there must be a progressive differentiation to acquire papilla epithelium, then taste cell progenitor epithelium, and finally taste cells within the papilla apex. Arranged in rows, the patterned distribution of fungiform papillae requires molecular regulation not only to induce papillae, but also to suppress papilla formation in the between-papilla tissue. Intact sensory innervation is not required to initiate papilla development or pattern. However, members of several molecular families have now been identified with specific localization in developing papillae. These may participate in papilla development and pattern formation, and subsequently in taste progenitor and taste cell differentiation. This review focuses on development of fungiform papillae in embryonic rat and mouse. Basic morphology, cell biology and molecular phenotypes of developing papillae are reviewed. Regulatory roles for molecules in several families are presented, and a broad schema is proposed for progressive epithelial differentiation to form taste cell progenitors in parallel with the temporal course, and participation of lingual sensory innervation.     

Cholinergic innervation of the tongue of the one humped camel, Camelus dromedarius

Distribution of adrenergic and cholinergic nerve profiles in the tongue of camel has been studied by histochemical methods. The tongue is richly innervated by cholinergic nerve profiles as is evidenced by the presence of numerous nerve fibres at different levels. There is noted strong cholinesterase positive reaction close to the lateral border of the circumvallate papillae (in the region of the taste buds) and the upper border of the fungiform papillae. Numerous nerve fibres have been observed in the connective tissue core of all the lingual papillae. Adrenergic nerve terminals could not be observed in the taste buds though numerous adrenergic nerve fibres could be seen in and around the blood vessels. Rich cholinergic innervation of the blood vessels has also been noted in the tongue.     

Comparative anatomical and neurohistological observations on the tongues of elephants (Elephas indicus and Loxodonta africana)

Frozen sections from Indian and African elephant tongues were investigated neurohistologically. On the dorsum there are 3 to 5 vallate papillae. Foliate papillae consisting of 18 to 27 clefts are observed in the posterolateral region of the tongue. Wart-like papillae are distributed along the lateral border of the tongue from the foliate papillae region to the apex. Vallate and foliate papillae contain serous glands but have no taste buds. They are supplied with abundant lamellated corpuscles of Pacinian type in their upper mucosa. The wart-like papillae are composed of two or more papillae, each of which has many secondary papillae supplied with plexiform thin and thick nerves. They bear a few taste buds and contain lamellated corpuscles of Pacinian type. From these neurohistologic characteristics wart-like papillae should be regarded as a receptive organ for secretion of the lingual glands. Lamellated corpuscles of Pacinian type are widely distributed over the whole surface of the tongue. The histologic location of these two structures is of interest in suggesting that they together play important roles as receptors of taste and tactile sensations during mastication of food. Double motor end plates are found on single muscle fibers. The mixed glands which are plentiful in the inferolateral area of the tongue are in close topographic relation with the wart-like papillae.     

Histological pattern of the tongue in the Japanese weasels, Mustela itatsi, with special reference to the morphology and distribution of papillae, taste buds and lingual glands

Light and scanning electron microscopical demonstrations were carried out on the tongues of adult Japanese weasels (Mustela itatsi). Four types of papillae are present on the mucous membrane of the tongue; filiform, fungiform, vallate and foliate papillae. The vallate and foliate papillae are furnished with taste buds. Three types of lingual glands are present in the tongue; mucous (Weber's), serous (Ebner's) and mixed glands. Weber's glands are compound tubular glands which are well developed near the radix. Ebner's glands are compound tubular glands connected with the vallate papillae. Mixed glands are compound tubulo-alveolar glands and present in the lower half of the tongue, near the apex.     

Light and scanning electron microscopic study on the lingual papillae and their connective tissue cores of the Cape hyrax Procavia capensis

We examined the epithelial surface and connective tissue cores (CTCs) of each lingual papilla on the Paenungulata, Cape hyrax (Procavia capensis), by scanning electron microscopy and light microscopy. The tongue consisted of a lingual apex, lingual body and lingual root. Filiform, fungiform and foliate papillae were observed on the dorsal surface of the tongue; however, fungiform papillae were quite diminished on the lingual prominence. Moreover, no clearly distinguishable vallate papillae were found on the tongue. Instead of vallate papillae, numerous dome-like large fungiform papillae were arranged in a row just in front of the rather large foliate papillae. Foliate papillae were situated in the one-third postero-lateral margin of the lingual body. The epithelium of filiform papillae was covered by a keratinized layer with kerato-hyaline granules, whereas weak keratinization was observed on the interpapillary epithelium. The external surface of the filiform papillae was conical in shape. CTCs of the filiform papillae were seen as a hood-like core with a semicircular concavity in the anterior portion of each core. Large filiform papillae were distributed on the lingual prominence. The CTCs of large filiform papillae after exfoliation of their epithelium consisted of a concave primary core and were associated with several small protrusions. The surface of fungiform papillae was smooth and dome-like. After removal of the epithelium, CTCs appeared as a flower bud-like primary core and were associated with several protrusions that were arranged on the rim of the primary core. Several taste buds were found on the top of the dorsal part of the epithelium of both fungiform and large fungiform papillae. Well-developed foliate papillae were seen and numerous taste buds could be observed in the lateral wall of the epithelium in a slit-like groove. The morphological characteristics of the tongue of the Cape hyrax had similarities with other Paenungulata such as Sirenia. However, three-dimensional characteristics, especially CTCs of lingual papillae, exhibited multiple similarities with rodents, insectivores and artiodactyls.     

Organization of geniculate and trigeminal ganglion cells innervating single fungiform taste papillae: a study with tetramethylrhodamine dextran amine labeling.

Single gustatory nerve fibers branch and innervate several taste buds. In turn, individual taste buds may receive innervation from numerous gustatory nerve fibers. To evaluate the pattern of sensory innervation of fungiform papilla-bearing taste buds, we used iontophoretic fluorescent injection to retrogradely label the fibers that innervate single taste papillae in the hamster. For each animal, a single taste papilla was injected through the gemmal pore with 3.3% tetramethylrhodamine dextran amine. Fungiform papillae either at the tongue tip (0.5-1.5 mm from the tip) or more posteriorly (1.5-3.0 mm from the tip) were injected. After one to seven days survival, the geniculate and trigeminal ganglia and the tongue were sectioned and examined for labeled cells and fibers, respectively. Analysis of the number and topographic distribution of geniculate cells innervating single taste papillae, shows that: (i) 15 +/- 4 (S.D.) ganglion cells converge to innervate a single fungiform taste bud; (ii) more ganglion cells innervate anterior- (range: 13-35 cells) than posterior-lying buds (range: five to 12 cells), which, in part, may be related to bud volume (microm3); and (iii) ganglion somata innervating a single taste bud are scattered widely within the geniculate ganglion. Analysis of labeled fibers in the tongue demonstrated that two to eight taste buds located within 2 mm of the injected taste bud share collateral innervation with the injected taste bud. Since all buds with labeled fibers were located in close proximity (within a 2-mm radius), widely dispersed geniculate ganglion cells converge to innervate closely spaced fungiform taste buds. Trigeminal ganglion (mandibular division) cells were also labeled in every case and, as with the geniculate ganglion, a dispersed cell body location and collateralization pattern among papillae were observed. This study shows that iontophoresis of tetramethylrhodamine dextran amine, selectively applied to individual peripheral receptor end-organs, effectively locates sensory ganglion cells in two different ganglia that project to these sites. Moreover, the marker demonstrates collateral branches of sensory afferents associated with the labeled fibers and the nearby receptor areas innervated by these collaterals. The labeling of single or clusters of receptor cells, as well as identified sensory afferents, affords future possibilities for combining this technique with immunocytochemistry to establish the relationships of innervation patterns with neurotransmitters and neurotropic substances within identified cells.     

Localization of Ulex europaeus agglutinin-I (UEA-I) in the developing gustatory epithelium of the rat

To understand the development of the gustatory structures necessitates a reliable marker for both immature and mature taste buds. It has been reported that the intragemmal cells within the taste buds of adult rats were bound to Ulex europaeus agglutinin-I (UEA-I), a specific lectin for alpha-linked fucose, but it has not been determined whether immature taste buds, i.e. taste buds without an apparent taste pore, are labeled with UEA-I. The present study was conducted to examine the UEA-I binding pattern during the development of the rat gustatory epithelium. In adult animals, UEA-I bound to the membrane of taste buds in all examined regions of the gustatory epithelium. Within the individual taste buds, UEA-I labeled almost all intragemmal cells. The binding of UEA-I was occasionally detected below the keratinized layer of the trench wall epithelium but could not be found in the lingual epithelium of the adult animal. During the development of circumvallate papilla, some cells within the immature taste buds were also labeled with UEA-I. The developmental changes in the UEA-I binding pattern in fungiform papillae were almost identical to those in the circumvallate papilla: both immature and mature taste buds were labeled with UEA-I. The present results indicate that UEA-I is a specific lectin for the intragemmal cells of both immature and mature taste buds and, thus, UEA-I can be used as a reliable marker for all taste buds in the rat.     

Light and scanning electron microscopic study on the tongue and lingual papillae of the common raccoon, Procyon lotor

We observed the external surface and connective tissue cores (CTCs), after exfoliation of the epithelium of the lingual papillae (filiform, fungiform, foliate and vallate papillae) of the common raccoon (Procyon lotor) using scanning electron microscopy and light microscopy. The tongue was elongated and their two-third width was almost fixed. Numerous filiform papillae were distributed along the anterior two-thirds of the tongue and fungiform papillae were distributed between the filiform papillae. Eight vallate papillae that had a weak circumferential ridge were distributed in a V-shape in the posterior part of the tongue and numerous taste buds were observable in the circumferential furrows of vallate papillae. Weak fold-like foliate papillae were observable at the lateral edge in the posterior part of the tongue and a few salivary duct orifices were observable beneath the foliate papillae. An islet-like structure with numerous taste buds, was observable on the deep part of the salivary duct of foliate papillae. Large conical papillae were distributed at the posterior part and root of the tongue. After removal of epithelium, filiform papillae of CTCs were appeared to be a thumb or cone-like main core and associating several finger-like short accessory cores. These cores were surrounded an oval concavity. The main core was situated behind the concavity and associated with accessory cores. CTCs of fungiform papillae were cylinder-like with numerous vertically running ridges and with a few concavities seen at the top of the cores. CTCs of vallate papillae and their surrounded circumferential ridge were covered with numerous pimple-like protrusions. The lingual papillae of Common raccoon's tongue had morphological feature of carnivore species.     

Morphology of the lingual papillae in the Japanese marten

The dorsal lingual surfaces of two adult Japanese marten (Martes melampus) were examined by scanning electron microscopy (SEM). Filiform, fungiform, vallate and foliate papillae were observed. A small filiform papilla on the apical surface of the tongue had several pointed processes. A small filiform papilla contained the connective tissue core consisting of several small processes. A large filiform papilla of the lingual body consisted of a main papilla and some secondary papillae. A large filiform papilla contained the connective tissue core consisting of processes of various size. The fungiform papillae are round in shape. The connective tissue core of the fungiform papilla had a top with several round depressions. The four vallate papillae were located on both sides of the posterior end of the lingual body and each papilla was surrounded by groove and crescent pad. A zigzag surface structure appeared on the connective tissue core of the vallate papilla. The foliate papillae were seen on the dorsolateral aspect of the tongue and some ridges and grooves were exposed reciprocally. A zigzag surface structures appeared on the connective tissue cores of the ridges of the foliate papillae.     

Modulation of taste peripheral signal through interpapillar inhibition in hamsters

Single taste buds from fungiform papillae were iontophoretically stimulated with chemicals filling glass microelectrodes while a single unit was recorded in the taste pore of a neighbor papilla. High signal-to-noise ratio responses were observed in the recorded papilla as antidromic action potentials. These responses were possibly modulated by the simultaneous stimulation of another adjacent papilla. A decrease in the frequency of firing and/or both decrementing spikes were observed during such dual papillae stimulations. These inhibitory effects were not modified by the section of the chordo-lingual nerve, suggesting the tongue is able to process the gustatory information thanks to interpapillar negative feedback, prior to transmitting the signal to the central nervous system. Branched chorda tympani fibers can account for responses observed for single papillae stimulations; inhibitions and decrementing spikes may suggest the contribution of another mechanism of interaction between two different single fibers.