comparative morphological study on the lingual papillae

57Comparative morphological study on the lingual papillae and their connective tissue cores in rabbits

Introduction There are many reports concerning the lingual papillae

of mammals, and it has been shown that the lingual pa-pillae of each of these animal species has a characteristic structure (Sonntag, 1922, 1923, 1925). It is also accepted that not only the external form of lingual papillae but also the stereo structure of their CTCs retain a structure that is characteristic of each animal species (Kobayashi and Iwasaki, 1989). The morphological characteristics of lingual papillae have been studied in some animals such as rodents (rats, mice, hamster, bank vole, beaver) (Kutuzov and Sicher, 1951; Iino and Kobayashi, 1988; Kobayashi et al., 1989c; Kitajima et al., 1992; Jack-owiack and Godynicki, 2005; Shindo et al., 2006), insectivores (moles, suncus) (Kobayashi et al., 1989b; Miyata et al., 1990), carnivores (raccoon dog, fox, silver fox, tiger) (Emura et al, 2004, 2006; Jackowiack and Godynicki 2004), artiodactyl (Asami et al., 1995; Agung-priyono et al., 1995; Zheng et al., 2006), and primates (Kobayashi et al., 1989a; Kobayashi and Wanichanon,

1992). Rabbit tongues have been useful for morphologi-cal studies. The majority of studies, however, have been restricted to epithelial cells or to the gustatory epithe-lium, particularly the taste buds of well-developed foliate papillae (Tuckerman, 1890; Omar Trujillo-Cenoz, 1957; Scalzi, 1967; Toyoshima and Shimamura, 1981; Liu and Lee, 1982; Iwasaki, 1987; Kobayashi, 1992). Stereo structure of both the lingual papillae and their CTC of rabbits is provided by Silva et al. (2002), but more de-tailed study has been demonstrated herein. Particularly these structures of the rabbit are compared to those of other animals from a comparative anatomical point of view.

Material and methods The tongues of eight healthy adult domestic rabbits

(Oryctolagus cuniculus var. doesticus) were used in this study. Two tongues were fixed in a 10% formalin solution for light microscopy and six tongues were in

Okajimas Folia Anat. Jpn., 85(2): 57–66, August, 2008

Comparative morphological study on the lingual papillae and their connective tissue cores in rabbits

By

Kouji NONAKA1, Jin Hua ZHENG2 and Kan KOBAYASHI1

1 Department of Anatomy, School of Life Dentistry at Niigata, The Nippon Dental University, Niigata, Japan 2 Department of Anatomy, Harbin Medical University, China

–Received for Publication, May 8, 2008–

Key Words: Comparative Anatomy, Lingual Papillae, Connective Tissue Core (CTC), Rabbit, Scanning Electron Microscopy (SEM)

Summary: The morphological structure of the lingual papillae and their connective tissue cores (CTC) in a rabbit were studied using LM and SEM and were compared to that of other animal species. Externally, the filiform papillae distributed on the anterior surface of the dorsal tongue were short and conical with a round base and had a flat area on their anterior upper half. The CTC of the conical filiform papillae had a roughly triangular plate-like structure with a round top. Several small round protrusions were found on both inclined planes of the triangle. Spearhead-like filiform papillae were distrib-uted on the anterior edge of the lingual prominence and branched filiform papillae were on the posteriorly wide area of the prominence. These papillae on the prominence had a slightly ramified CTC that differed from that of the CTC of the coni-cal filiform papillae distributed on the anterior tongue. Dome-like fungiform papillae were distributed among the conical filiform papillae of the anterior tongue and had a CTC with a roundish structure that was almost but, not quite spherical in appearance with 1 to 10 small round concave indentations for taste buds on their upper surface. The foliate papillae had approximately 15 parallel ridges separated by grooves. These ridges contained a parallel thin plate-like CTC exhibited af-ter removal of the epithelium. The vallate papilla was comprised of a spherical central papilla and had a circular wall with a flower-like CTC almost resembling a carnation.

The stereostructure of the rabbit's filiform CTC are comparatively described as being morphologically in between those of rodents and those of the guinea pig and Japanese serow. Such evolution has probably occurred due to the species unique masticatory and gustatory needs and functions.

57

58 K. NONAKA, J. ZHENG and K. KOBAYASHI

Karnowsky’s fixative (Karnowski, 1965) for scanning electron microscope (SEM) .

In preparation for light microscopy, paraffine embe-ded specimens were cut and stained with Hematoxylin-Eosin, Azocarmin (Masson-trichrome), and Aldehyde-fuchsin. In preparation for SEM, fixed specimens were immersed in a 3.5 N-HCl solution for about 10 days at room temperature (23~26°C) in order to exfoliate the epithelial cell layer. After exfoliation of the epithelial layer, both of the exposed sides (the connective tissue side and the epithelial cell side) were immersed in a 0.5% tannic acid solution for 60 min at 4°C and were postfixed for 60 minutes in 1% OsO4. Thereafter, they were frozen and dried using the t-butylalcohol method (Inoue and Osatake, 1988).

After evaporation of the platinum-palladium, the specimens were observed under a scanning electron mi-croscope (S-800 Hitachi, Japan) at an acceleration volt-age ranging from 5 to 15 kV.

Results

General description and lingual papillae of the rabbit tongue

The dorsal surface of the tongue of the rabbit can be divided into three parts: the anterior, the middle and the posterior parts. The anterior part contains the lingual apex and makes up almost half of the tongue. The middle part has a lingual prominence located at the intermolar region close to the posterior half area of the tongue. The posterior part is a narrow region located at the lingual root. Four types of lingual papillae were recognized: filiform, fungiform, foliate and vallate papillae. The fol-lowing three subtypes were used to delineate differing filiform papillae: non-branched conical filiform papillae (which were densely distributed on the surface of the an-terior part of the tongue from the apex to the anterior bor-der of the lingual prominence), spearhead-like filiform papillae (which were distributed on the anterior margin of the lingual prominence), and small branched filiform papille (which were distributed on the posteriorly wide area of the lingual prominence).

Multiple dome-like fungiform papillae were distrib-uted sporadically among conical filiform papillae of the anterior part of the tongue. Two foliate papillae that were oval-shaped with numerous parallel ridges and grooves were located on each side of the lateral margin of the lingual prominence. Two vallate papillae were located slightly lateral to the mid-line of the lingual prominence. The surface of the posterior part (the lingual root) of the tongue was narrow and smooth (Fig. 1).

(1) Anterior dorsal part of the tongueSEM figures of conical filiform papillae

Externally the conical filiform papillae distributed on

the dorsal surface of the anterior tongue were short and conical- shaped with a round base. There was a flat area at the anterior upper surface of the papilla, and a blunt tip was bent toward the posterior. The width of the round base was approximately 80–120 µm and its height was 150–200 µm (Fig. 2). After removal of the epithelium, the CTC of the conical filiform papillae resembled ser-rated arrowheads with several small rounded protrusions on both inclined edges of the arrowhead-like CTC of the papillae (Fig. 3). The basal length of the CTC was ap-proximately 50 to 100 µm, and the height was 100 to 150 µm. This arrowhead-like CTC had a slight concave ante-rior surface, while the posterior surface was bent towards the rear.

SEM figures of fungiform papillaeThe upper hemispheres of the fungiform papillae vary

in diameter from approximately 200 to 400 µm and their height from 300 to 500 µm (Fig. 4). Fungiform papillae were distributed among the conical filiform papillae and were especially densely distributed at the superior mar-ginal area of the anterior dorsal part of the tongue and

Fig. 1. The dorsal view of a rabbit tongue. The lingual prominence (LP) consists of an anterior edge (LP: ant) with large spearhead-like filiform papillae and a large posterior area (LP: post) with branched filiform papillae. AP: The apex of the tongue. BD: The body of the tongue, fi: conical filiform papilla, fu: fungiform papilla, fo: foliate papilla, va: vallate papilla, RX: root of the tongue.


for a short distance on the inferior marginal surface of the lingual apex. The CTC of the fungiform papillae had a spherical-like shape with about 15 to 20 vertical stria-tions on the lateral surface. Small round depressions for

taste buds were found on the narrow top of these fungi-form papillae. Each depression measured about 20 to 40 µm and there were between 1 to 10 of these depressions on the top of each of the fungiform papillae (Fig. 5 and 6).

Fig. 2. An SEM figure showing the external form of the conical filiform papillae distributed at the dorsal surface of the anterior tongue. Bar: 50 µm

Fig. 3. An SEM figure of the CTC of conical filiform papillae distributed at the dorsal surface of the anterior tongue. Bar: 30 µm

Fig. 4. An SEM figure of the surface of the lingual apex. Fungiform papillae(fu) are distributed among small conical filiform papillae.Bar: 200 µm

Fig. 5. An SEM figure showing CTCs of several fungiform papillae after removal of the epithelium among small conical filiform papillae on the lingual apex. Bar: 200 µm

Fig. 6. An SEM figure of the CTC of a fungiform papilla on the lingual apex. It has 10 or more vertical striations on the lateral wall and several round depressions for taste buds on its top. Bar: 100 µm


Fig. 7. An SEM figure showing the external form of large spearhead like filiform papillae distributed on the anterior edge of the lingual promi-nence. Bar: 150 µm

Fig. 8. An SEM figure of the CTC of large spearhead-like filiform papillae. Each papilla is long and most have apical branches. Bar: 100 µm

Fig. 9. An SEM figure showing the external form of branched filiform papillae distributed at the posterior large area of the lingual prominence. Each papilla consists of a main process with several small accessory processes. Bar: 100 µm

Fig. 10. An SEM figure of the CTC of branched filiform papillae distributed at the large posterior area of the lingual prominence. Each papilla consists of a bundle of several rod-shaped protrusions. Bar: 100 µm


(2) Lingual prominencea. Spearhead-like filiform papillae

There is a lingual prominence on the dorsal surface towards the posterior half of the tongue. At the anterior edge of the prominence, particularly large spearhead-like filiform papillae were distributed, each with a base of about 150 µm in diameter, and about 400 µm in height (Fig. 7). These had a spearhead-like main process with a pointed tip and often some small accessory processes on both sides of the process. After removal of the epithelium the CTC of these spearhead-like filiform papillae had a long columnar base and the upper quarter area several slender rod-shaped protrusions branched (Fig. 8).

b. Small branched filiform papillaeSmall branched filiform papillae were distributed on

the posteriorly wide area of the prominence behind a group of spearhead-like filiform papillae on the lingual prominence. On the surface epithelium, these small branched filiform papillae were thicker than the conical filiform papillae that were distributed across the dorsal portion of the anterior tongue. These small branched fi-liform papillae consisted of a central main process with some accessory processes on both sides of the upper part of the papillae (Fig. 9).

The CTC of the small branched filiform papillae con-sisted of a large main process and several rod-shaped ac-cessory processes extending upwards on both sides from the main process. These main and accessory processes terminated with rounded top (Fig. 10).

c. Vallate papillaeTwo vallate papillae were situated behind the lingual

prominence, and were located at the posterior one fifth of the tongue. The vallate papillae consisted of a round central bulb surrounded by a deep groove and a circular wall (Fig. 11). Numerous taste buds were located in the epithelium of the grooved side. Epithelial exfoliation of the CTC of the central papilla revealed a flower-like structure similar to that of a carnation (Fig. 12).

d. Foliate papillaeThe foliate papillae were oval-shaped and located on

each side of the postero- lateral margin of the lingual prominence. Each foliate papilla was approximately 3 mm long and 2.5 mm wide. The foliate papillae pos-sessed approximately 15 ridges and grooves. Light mi-croscopy of the lingual mucosa revealed parallel arranged ridges with numerous taste buds on the epithelium of the grooves. Each ridge was approximately 220 µm wide and each groove had a depth of about 300 µm (Fig. 13). Fig-ure 14 shows a SEM figure of some ridges whose surface epithelium was partially removed and each ridge had 3 corresponding parallel folds where the CTC was exposed and this observation has been previously reported by Kobayashi (1992). Numerous tast buds were regularly

distributed in the grooved epithelium. Each taste bud was approximately 30 µm long and about 25 µm wide. Their pores faced toward the surface of the groove (Fig. 15). The pores of the taste buds opened perpendicular to the grooved epithelium.

(3) Lingual rootThe surface of the lingual root was relatively flat with

some openings for the posterior salivary glands (Fig. 16). After removal of the epithelium, small fibrous strands and the openings of the ducts were revealed (Fig. 17).

Discussion Externally, the conical filiform papillae on the ante-

rior part of the rabbit tongue including the tip area have a relatively simple and short conical shape, with a flat anterior plane in the upper portion of the filiform pa-pilla bending towards the upper posterior direction. The simple structure of these filiform papillae on the anterior dorsal area is very similar to those found rodents such as; rats (Iino et al., 1988), mice (Kobayashi et al., 1989c), hamsters (Kitajima et al., 1992) and bank vole (Jackowi-ack and Godynicki, 2005) as well as insectivores such as moles (Miyata et al., 1990), and the suncus murinus (Kobayashi et al., 1989b). In contrast, the filiform papil-lae of artiodactyla, carnivores and primates vary in shape and consist of a main process and on average have be-tween 10 to 20 accessory processes (Asami et al., 1995; Inatomi and Kobayashi, 1999; Yamaguchi et al., 2002; Kobayashi et al., 1988a, 1988b; Emura et al., 2004, 2006, 2007; Kobayashi et al., 1989a, 1994, 1995, 1997). The CTC of the filiform papillae found in rats and mice looks like a small asymmetrical lump with narrow con-cave indentations on both of their anterior and posterior sides with a slender central protrusion. The hamster and suncus murinus have a spoon-like structure with a round concavity on the anterior. Rodents and insectivora have relatively simply shaped filiform CTC. In rabbits, how-ever, the filiform CTCs have roughly serrated arrowhead-like shapes with several small rounded protrusions on both inclined sides of the CTC. The filiform CTC of guinea pigs (Kobayashi, 1990) and most artiodactyls (Asami et al., 1995; Kobayashi et al., 1997; Yamaguchi et al., 2002) have slender protrusions, numbering three in the case of guinea pigs and with greater complexity of six or more in the case of most artiodactyls. The stereo structure of filiform CTCs on the anterior part of the rab-bits tongue are therefore comparatively described as be-ing morphologically in beween those of rodents (includ-ing insectivora) and those of the guinea pig and Japanese serow (artiodactyla) (Fig. 18).

The external form of the different types of filiform papillae distributed at the anterior margin of the lingual prominence of the rabbit’s tongue showed large spear-


Fig. 11. An SEM figure showing the external view of a rabbits vallate papilla surrounded by round gloove. Bar: 200 µm

Fig. 12. An SEM figure of the CTC of a vallate papilla after removal of the epithelium, it resembles petals of a carnation-like flower. Bar: 300 µm

Fig. 13. SEM figure showing the external view of a foliate papilla consisting of ridges (r) and grooves. Bar: 300 µm

Fig. 14. SEM figure showing the surface ridges (r) of a foliate papilla of the rabbit whose epithelium is partially removed, and corresponding folds (s: septal fold, g: groove side fold) of CTC are exposed. Bar: 300 µm

Fig. 15. SEM figure showing an enlarged cross-section of groove-side of a foliate papilla, there are several round taste buds (t) in the epithelial cell layer of the groove side. Bar: 30 µm


head-like filiform papillae and on the posterior part of the lingual prominence had numerous branched filiform pa-pillae. The spearhead-like filiform papillae distributed at the anterior margin of the lingual prominence of the rab-bit are similar in morphology to those of carnivores (cat, dog). The rabbit branched filiform papillae of the lingual prominence closely resemble those present in most artio-dactyl, unlike the rabbit tongue’s conical filiform papillae on the anterior dorsal tongue. From the morphological

differences discussed in this paper it is suggested that fi-liform papillae have evolved progressively from the sim-ple small masses found in rodents to that of those found in animals such as rabbits to the more complex bundles of numerous protrusions present in most artiodactyls.

Rabbits have numerous fungiform papillae particu-larly on the lingual apex and on the inferior margin at the tip of the tongue. After removal of the epithelium, small round depressions for taste buds were clearly recognized

Fig. 16. SEM figure of the external surface of a rabbit lingual root. Note the flat surface containing the openings of three small ducts (arrows) of the lingual posterior gland. Bar: 100 µm

Fig. 17. SEM figure of the connective tissue surface after removal of the epithelium of the rabbit lingual root, there are two openings (arrows) of the glandular duct. Bar: 100 µm

Fig. 18. Schematic comparative drawing of the CTC of the filiform papillae distributed on the dorsal surface of the anterior tongue of a rat (a), rabbit (b), guinea pig (c), and Japanese serow (d).


and easily countable on the upper part of the fungiform papillae. The number of taste buds on the upper part of the fungiform papillae varies between animal species. Animals which have one taste bud on each fungiform papilla include rodentia (rats (Iino et al., 1988), mice (Kobayashi et al., 1989c), hamsters (Kitajima and Ko-bayashi, 1992)) and the suncus murinus (Kobayashi et al., 1989b) (insectivora). Moles (Miyata et al., 1990) (insectivora) have one to three taste buds on each fun-giform papilla. Dogs and cats (carnivores) have several, and crab-eating monkeys (primate) have 10 to 20 taste buds on each fungiform papilla (Kobayashi et al., 1989a; Kobayashi et al., 1995). In the rabbits we studied, the number of taste buds on each fungiform papilla varied between one to ten. However, in most cases two to five taste buds were more commonly found on each of the rabbit’s fungiform papilla. It therefore appears that the number of taste buds increased with evolution

The number of taste buds found on the rabbit’s fun-giform papilla is much more numerous than in either rodents or insectivores, but significantly less than the number of taste buds observed on the fungiform papilla of the crab eating monkey (primate).

The presence of a lingual prominence is regarded as a characteristic structure of herbivores such as cattle, goats, deer (artiodactyla), rats, and mice (rodentia). Rabbits also have a conspicuous lingual prominence with large spear-head-like filiform papillae on the anterior edge of the lingual prominence and with branched filiform papillae on the posterior area of the prominence. This muscle rich prominence with spearhead-like and branched filiform papillae is an effective structure for herbivous animals to masticate food by grinding food between the tongue and the upper palate. The morphology and structure of filiform papillae has evolved according to the species masticatory requirements and functions.

Each animal species has a varying number of vallate papillae. Rats, mice, and hamsters have one vallate pa-pilla. Rabbits, moles, suncuses (insectivora) (Kobayashi et al., 1989d; Miyata et al., 1990), guinea pigs (Ko-bayashi, 1990), horses (perissodactyla) (Kobayashi et al., 2005) and pigs (artiodactyla) have two vallate papillae. Animals which have three vallate papillae include koa-las (Kobayashi et al., 2003), wallabies, kangaroos and koala (marsupials) (Kubota et al., 1963; Abe et al., 2001, Kobayashi et al. 2003), tupais, tamarins, and mandrills (primates) (Kobayashi and Wanichanon, 1992; Chun-habundit et al., 1992; Kobayashi et al, 2004). Japanese marten and tiger have four vallate papillae (Emura et al., 2004, 2007). Dogs, cats, and raccoon dogs (carnivores) all have several vallate papillae (Kobayashi et al., 1988a, b). Some animals such as cattle, goats, deer, and sheep (artiodactyla) (Asami et al., 1995; Inatomi et al., 1999; Yamaguchi et al., 2002; Zheng et al., 2006) have on av-erage 10 to 20 or more vallate papillae. It is thought that an increase in the number of vallate papillae corresponds

to greater sensitivity in the sense of taste. Pigs are exceptional among the numerous species

classified as artiodactyla for having a pair of foliate pa-pillae, unlike most other artiodactyls which have none. Dogs and cats, which are classified as carnivores, do not have any foliate papillae but, they do have several finger-like protrusions (lateral organs) arranged linealy. These finger-like lateral organs do not contain any taste buds and it is speculated that they act as some kind of me-chanical organ rather than as a taste organ (Boshell et al., 1982). Japanese bears, racoon dogs, and silver foxes (carnivores), however have well-developed foliate papil-lae with numerous taste buds in their epithelial cell layer.

It is noteworthy thought that the tupaia glis (Kobayashi and Wanichanon, 1992) (a primate) has finger-like lateral organs just like those found in cats (Boshell et al., 1982). Most primates however such as crab-eating monkeys, mandrills, and humans have well-developed foliate pa-pillae (Kobayashi et al., 1995, 2004). Considering the above observations, it is interesting to point out that foli-ate papillae have developed in omnivorous primates. On the other hand, rats, mice, hamsters (rodentia), as well as rabbits which are classified as herbivorous animals, also have foliate papillae. The significance of foliate papillae is therefore not easily determinable. Because lower order animals such as rodents, rabbits, and guinea pigs have foliate papillae, it may be considered that foliate papillae exist primarily as a set with other lingual papillae like filiform, fungiform, and vallate papillae. In animals like dogs and cats that became purely meat-eating animals, and in cattle and goats that became purely grass-eating animals, foliate papillae may have degenerated through evolutionary processes for unknown reasons. To ascer-tain the significance of the existence of foliate papillae in mammalian species, a wider variety of animal cases must be investigated.

This study has provided information that supports the idea that lingual papillae and their CTC evolved accord-ing to the species masticatory and gustatory needs and functions.

Acknowledgements

We are thankful to Dr. Zac Morse (Fiji School of Medicine) for valuable discussions on this manuscript.

References

1) Abe T, Koizumi K and Kobayashi K. Comparative morphologi-cal studies on the stereo structure of the lingual papillae and their connective tissue cores in the Swamp Wallaby Wallabia bicolar. Jpn J Oral Biol 2001; 43:292–309.

2) Agungpriyono S, Yamada J, Kitamura N, Nisa C and Sigit K. Morphology of the dorsal lingual papillae in the lesser mouse deer, Tragulus javanicus. J Anat 1995; 187:635–640.


3) Asami Y, Asami T and Kobayashi K. Light microscopic and scanning electron microscopic studies on the lingual papillae and stereo structure of their connective tissue cores in cattle. Shigaku (Odontology) 1995; 82:1223–1244.

4) Boshell JK, Wilborn WH and Singh BB. Filiform papillae of cat tongue. Acta Anat 1982; 114:97–105.

5) Chunhabundit P, Thongpila S and Somana R. SEM study on the dorsal lingual surface of the common tree shrew, Tupaia glis. Acta Anat 1992; 253:253–257.

6) Emura S, Hayakawa D, Chen H and Shoumura S. Morphology of the lingual papillae in the tiger. Okajimas Folia Anat Jpn 2004; 81:39–44.

7) Emura S, Okumura T and Chen H. Morphology of the lingual papillae in the Japanese marten. Okajimas Folia Anat Jpn 2007; 84:77–82.

8) Emura S, Okumura T, Chen H and Shoumura S. Morphology of the lingual papillae in the Raccoon dog and Fox. Okajimas Folia Anat Jpn 2006; 83:73–76.

9) Iino T and Kobayashi K. Morphological studies on the lingual pa-pillae and their connective tissue papillae of rat. Shigaku (Odon-tology) 1988; 75:1039–1060.

10) Inatomi M and Kobayashi K. Comparative morphological stud-ies on the tongue and lingual papillae of the Japanese Black Bear (carnivora) and the Mountain goat (artiodactyla). Shigaku (Odon-tology) 1999; 87:313–328.

11) Inoue T and Osatake H. A new drying method of biological speci-mens for scanning electron microscopy: the t-butylalcohol freeze-drying method. Arch Histol Cytol 1988; 51:53–59.

12) Iwasaki S. Morphological studies of the lingual mucosa of the rabbit. Shigaku (Odontology) 1987; 74:1235–1264.

13) Jackowiak H and Godynicki S. The scanning electron microscop-ic study of lingual papillae in the silver fox (Vulpes vulpes fulva, Desmarest, 1820). Ann Anat 2004; 186:179–183.

14) Jackowiak H and Godynicki S. The distribution and structure of the lingual papillae on the tongue of the bank vole Clethrionomys glareolus. Folia Morphol 2005; 64:326–333.

15) Karnovsky MJ. A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 1965; 27:137A–138A.

16) Kitajima K and Kobayashi K. Light and electron microscopic studies on the lingual papillae and their connective tissue cores in hamster. Jpn J Oral Biol 1992; 34:503–530.

17) Kobayashi K. Three-dimensional architecture of the connective tissue core of the lingual papillae in the guinea pig. Anat Embryol (Berl) 1990; 182:205–213.

18) Kobayashi K. Stereo architecture of the interface of the epithelial cell layer and connective tissue core of the foliate papillae in the rabbit tongue. Acta Anat 1992; 143:109–117.

19) Kobayashi K and Iwasaki S. Comparative studies on the stereo architecture of the connective tissue papillae in some mammalian tongue. In: Motta PM, editor. Cell and Tissue: a three-dimension-al approach by modern techniques on microscopy. New York: Alan R. Liss. 1989 (p 303–308).

20) Kobayashi K, Jackowiak H, Frackowiak H, Yoshimura K, Kuma-kura M and Kobayashi KI. Comparative morphological study on the tongue and lingual papillae of horses (perissodactyla) and selected ruminantia (artiodactyla). It J Anat Embryol 2005; 110 (suppl) n.1:55–63.

21) Kobayashi K, Kumakura M, Shinkai H and Ishii K. Ttree-dimen-sional fine structure of the lingual papillae and their connective tissue cores in the human tongue. Acta Anat Nippon 1994; 69:624–635.

22) Kobayashi K, Kumakura M, and Takahashi M. Comparative ob-servations on lingual papillae and their connective tissue cores in three primates. A scanning electron microscopic study. It J Anat Embryol 1995; 100 (suppl):349–358.

23) Kobayashi K, Kumakura M and Yoshimura K. Stereo structural

differences of lingual papillae and their connective tissue cores in three kinds of artiodactyla. In: Motta PM (ed) Recent Advances in microscopy of Cell, Tissues and Organs 1997, (p 357–361).

24) Kobayashi K, Kumakura M, Yoshimura K, Nonaka K and Hen-neberg M. Comparative morphological study of the lingual papil-lae and their connective tissue cores of the koala. Anat Embryol 2003; 206:247–254 .

25) Kobayashi K, Kumakura M, Yoshimura K, Takahashi M, Zheng JH, Kageyama I, Kobayashi KI and Hama N. Comparative mor-phological studies on the stereo structure of the lingual papillae of selected primates using scanning electron microscopy. Annals Anat 2004; 186:525–530 .

26) Kobayashi K, Miyata K, Asami T, Kitajima K, Iwasaki S and Sasagawa I. Three-dimensional structure of the connective tissue core of the lingual papillae in the crab-eating macaque, (Macaca- fascicularis). Shigaku (Odontology) 1989a; 77:1308–1317.

27) Kobayashi K, Miyata K, Iwasaki S and Takahashi K. Three di-mensional structure of the connective tissue papillae of cat lingual papillae. Jpn J Oral Biol 1988a; 30:717–731.

28) Kobayashi K, Miyata K, Iwasaki S and Takahashi K. Three di-mensional structure of the connective tissue papillae of the tongue in Suncus murinus. Jpn J Oral Biol 1989b; 31:363–371.

29) Kobayashi K, Miyata K, Takahashi K and Iwasaki S. Develop-mental and morphological changes in dog lingual papillae and their connective tissue papillae. Proc 6th M. Singer Symposium. Eds S. Inoue et al. 1988b; pp 609–617.

30) Kobayashi K, Miyata K, Takahashi K and Iwasaki S. Three-dimensional architecture of the connective tissue papillae of the mouse tongue as viewed by scanning electron microscopy. Acta Anat Nippon 1989c; 64:523–538 .

31) Kobayashi K and Wanichanon C. Stereo architecture of the con-nective tissue cores of the lingual papillae in the tree shrew. Anat Embryol (Berl) 1992; 186:511–518.

32) Kobayashi S, Arai S, Tomo S, Shimoda T, Shimamura A and Yamada H. Scanning electron microscopic study on the lingual papillae of the Japanese insectivora. Okajimas Folia Anat Jpn 1989d; 65:413–428.

33) Kubota K, Kubota J, Fukuda N, Asakura S, Nakagawa S and Ma-sui M . Comparative anatomical and neurohistological observa-tions on the tongue of the marsupials. Anat Rec 1963; 147:337–353.

34) Kutuzov H and Sicher H. The filiform and the conical papillae of the tongue in the white rat. Anat Rec 1951; 110:275–288.

35) Liu HC and Lee JC. Scanning electron microscopic and histo-chemical studies of foliate papillae in the rabbit, rat and mouse. Acta Anat 1982; 112:310–320.

36) Miyata K, Iwasaki S and Kobayashi K. Fine morphological stud-ies on the connective tissue core and the epithelial cells of the lingual papillae in Mogella wogura wogura. Shigaku (Odontology) 1990; 78:553–574.

37) Omar Trujillo-Cenoz. Electron micrope study of the rabbit gusta-tory bud. Zeitschrift Zellforschung 1957; 46:272–280.

38) Scalzi HA. The cytoarchitecture of gustatory receptors from the rabbit foliate papillae. Z Zellforshung 1967; 80:413–435.

39) Shindo J, Yoshimura K and Kobayashi K. Comparative morpho-logical study on the stereo-structure of the lingual papillae and their connective tissue cores of the American beaver (Castor canadensis). Okajimas Folia Anat Jpn 2006; 82:127–138 .

40) Silva MCP, Watanabe I and Kronka MC. Three-dimensional ar-chitecture of the connective tissue core and surface structures of the lingual papillae in the rabbit. Histol Histopathol 2002; 17:455–461.

41) Sonntag CF. The comparative anatomy of the tongues of the mammalia VII. Cetacea, Sirenia and Ungulata. Proc. Zool Soc Lond 1922; 92:639–657.

42) Sonntag CF. The comparative anatomy of the tongues of the mammalia. VIII, Carnivora, Proc Zool Soc Lond 1923; 93:129–


153.43) Sonntag CF: The comparative anatomy of the tongues of the

mammalia. XII. Summary, classification and phylogeny. Proc Zool Soc Lond 1925; 95:701–762.

44) Toyoshima K and Shimamura A. A scanning electron microscopic study of taste buds in the rabbit. Biomed Res 1981; 2:459–464.

45) Tuckerman F. On the gustatory organs of some of the mammalia. J Morph 1890; 4:151–193.

46) Yamaguchi T, Asami T and Kobayashi K. Comparative anatomi-cal studies on the stereo structure of the lingual papillae and their connective tissue cores in the Japanese Serow and Bighorn Sheep. Jpn J Oral Biol 2002; 44:127–141.

47) Zheng JH and Kobayashi K. Comparative morphological study on the lingual papillae and their connective tissue cores (CTC) in reeves’ muntjac deer (Muntiacus reevesi).

Ann Anat 2006; 188:555–564.

comparative morphological study on the lingual papillae

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