Volume 9
Issue 3
Veterinary Medicine
JOURNAL OF
POLISH
AGRICULTURAL
UNIVERSITIES
Available Online: http://www.ejpau.media.pl/volume9/issue3/art-19.html
FOLIATE PAPILLAE ON THE TONGUE IN THE DOMESTIC RABBIT (ORYCTOLAGUS CUNICULUS F. DOMESTICA)
Mirosława Kulawik1, Szymon Godynicki2
1 Institute of Zoology, Department of Animal Anatomy, Poznań University of Life Sciences
2 Department of Histology and Embryology, Institute of Zoology, Poznań University of Life Sciences
In the posterior part of the body of the tongue there are two foliate papillae located on the dorsal-lateral part. Individual folia of foliate papillae are arranged parallel to one another and are separated by deep furrows. Numerous excretory ducts of posterior serous lingual glands (Ebner’s glands) open on the fundus of furrows of each foliate papilla. The epithelium covering foliate papillae varies in thickness as it forms epithelial streaks. In each folium of a foliate papilla there are two epithelial streaks. Sometimes in one folium papillae 3, 4 or 5 epithelial streaks were found. Some epithelial streaks divide. The connective tissue core of foliate papillae is formed by parallel folds of connective tissue separated by groove-like depressions. In each folium of a foliate papilla there is one central fold and two lateral folds. It is known from observations under a light microscope that folds of connective tissue area arranged between epithelial streaks. Some folds divide. Taste buds are found in the epithelium covering folia of foliate papillae from the side of the furrows, as well as in the epithelium directly surrounding papillae. Observations of the surface of foliate papillae confirmed the parallel arrangement of folia and furrows of papillae. Moreover, these observations showed that some folia papillae divide to form two secondary folia.
Key words: rabbit, tongue, foliate papillae.
INTRODUCTION
Foliate papillae are one of the three types of taste papillae found on the tongue in the rabbit, next to fungiform and vallate papillae [3, 4]. Foliate papillae have also been identified on the tongues of other animal species, e.g. in the albino rat [15], hamster [12, 13], mouse [18, 19], flying squirrel [5], bats [2], as well as the dog, cat, horse and the pig [10]. Moreover, foliate papillae have been also found in Primates, such as the tamarin, crab-eating monkey, mandrill [9], including the human [9, 14]. There are no foliate papillae on the tongue in ruminants [1, 7, 10, 11].
The aim of this study was to describe the structure of foliate papillae in adult rabbits, being popular laboratory animals [4, 20], based on observations under a light as well as a scanning electron microscope, used to investigate the surface of foliate papillae and their connective tissue core.
MATERIAL AND METHODS
Tongues for analyses were collected from 11 adult domestic rabbits, Oryctolagus cuniculus f. domestica, of both sexes. The material was obtained from an abattoir.
Samples of lingual tissue with foliate papillae were prepared for observations under a light microscope (LM) and a scanning electron microscope (SEM).
Samples for observations under a light microscope were fixed in 10% neutralized formalin or Bouin solution, embedded in paraffin and sliced into sections with the thickness ranging from 3 to 5 µm, in three planes, i.e. in the median, transverse and dorsal planes. Sections were stained according to Masson-Goldner or using H+E.
Specimens for observations under a scanning electron microscope were fixed in the Karnovski fixing solution, critical point dried and sputtered with gold.
For the purpose of observations of the connective tissue core of foliate papillae, some samples after being fixed in the Karnovski fixing solution were placed in a 10% NaOH solution for 20 days at room temperature (21-24°C). After the epithelium was removed samples were dehydrated, critical point dried and sputtered with gold.
Such prepared specimens were observed under a scanning electron microscope Hitachi S-4200 and LEO 435VP.
RESULTS
In the posterior part of the body of the tongue, on the dorsal-lateral side there are two foliate papillae. Foliate papillae are oval in shape and are composed of 15-21 parallel folia papillae, separated by deep furrows. Some folia of foliate papillae are divided into two secondary folia (Fig. 1).
Fig. 1. Dorsal section of a foliate papilla: Fp – folia of foliate papilla, arrows indicate furrows of foliate papilla, lines indicate the division of folia of papilla into two secondary folia. LM, x 3, Masson-Goldner staining |
 |
The epithelium covering foliate papillae is nonkeratinized stratified squamous epithelium, varying in thickness and forming epithelial streaks ingrown into connective tissue. In each folium papillae there are 2 epithelial streaks (Figs. 2, 3).
Fig. 2. Dorsal section of folia of foliate papilla: lines – epithelial streaks, red asterisks – lateral connective tissue folds, black asterisk – central connective tissue fold, arrows indicate taste buds, Sp – furrows of papilla. LM, x 12.5, Masson-Goldner staining |
 |
Fig. 3. Median cross-section of the tongue in the area of foliate papilla: Fp – folia papillae, arrows indicate furrows of papilla, lines – epithelial streaks, Cg – taste buds, black asterisks – central connective tissue folds, red asterisks – lateral connective tissue folds, Lp – lamina propria mucosae, Ps – secretory part of glands, De – excretory duct of glands, Ml – muscles of tongue. LM, x 5, Masson-Goldner staining |
 |
Studies showed that in individual cases in one folium papillae there are from 3 to 5 epithelial streaks (Figs. 4, 5) and some epithelial streaks branch off (Fig. 5.).
Numerous and densely distributed taste buds are located both in the epithelium covering individual folia papillae and in the epithelium directly surrounding foliate papillae from the side of furrows (Figs. 2, 3, 4, 5).
Fig. 4. Median cross-section of tongue in the area of foliate papilla: lines – epithelial streaks, arrows indicate furrows of papilla, Lp – lamina propria mucosae, De – excretory duct of glands, Ps – secretory part of glands, Ml – muscles of tongue. LM, x 5, Masson-Goldner staining |
 |
Fig. 5. Median cross-section of tongue with one folium of foliate papilla visible: lines – three epithelial streaks, of which one divides, arrows – taste buds, asterisks – connective tissue core of folium of foliate papilla divided into folds. LM, x 12.5, Masson-Goldner staining |
 |
Numerous excretory ducts of posterior serous lingual glands open on the fundus of furrows of each foliate papilla (Figs. 3, 4). Secretory parts of these glands are found primarily among muscles of the tongue. Sometimes they were observed on the lamina propria mucosae in the immediate vicinity of foliate papillae (Fig. 4).
In the site where foliate papillae are located lamina propria mucosae forms folds arranged between epithelial streaks. In each folium of a foliate papilla there is one central and two lateral folds (Figs. 2, 3). When the number of epithelial streaks is more than two in one folium papillae, the number of connective tissue folds increases (Figs. 4, 5). Numerous blood vessels are located in lamina propria mucosae. Many of them extend towards the area of connective tissue of foliate papillae.
SEM observations of foliate papillae on the tongue in the rabbit showed that individual folia papillae run parallel and are separated by distinct furrows. Some folia papillae divide to form two secondary folia. The longest folia are arranged in the central part of each foliate papilla, while the shortest at the anterior and posterior end of the papilla. Desquamate cells were observed on the surface of the epithelium of foliate papillae (Fig. 6).
Fig. 6. Surface of foliate papilla: Fp – folia papillae, red lines – dividing folia papillae, Sp – furrows of papilla. SEM |
 |
Results of observations of the connective tissue core of foliate papillae are consistent with the results of SEM observations. The connective tissue core of foliate papillae is formed by parallel folds, separated by groove-like hollows, in which prior to the removal of the epithelium there were epithelial streaks and the epithelium lining furrows of foliate papillae. In each folium of a foliate papilla there are two lateral folds and one central fold (Fig. 7). It was known from previous observations under a light microscope that the central fold is found in the central part of each folium of a foliate papilla, between two epithelial folds. Each lateral fold is found between one epithelial streak and the epithelium covering the folium papillae from the side of the furrow. Impressions left by taste buds can be seen on lateral folds contacting with the epithelium of lateral surfaces of folia of foliate papillae. Moreover, the observations showed that some lateral folds divide to form 2 or 3 secondary connective tissue folds, which as it is known from observations under a light microscope are arranged between the divided epithelial streaks. On the fundus of groove-like hollows located between two lateral folds there are numerous openings of excretory ducts of posterior serous lingual glands (Fig. 7).
Fig. 7. Connective tissue core of foliate papilla: red asterisks – lateral connective tissue folds, black asterisks – central connective tissue folds, white asterisks – impressions left by taste buds, arrow indicates the opening of excretory duct of posterior serous lingual glands (Ebner’s glands). SEM |
 |
DISCUSSION
Foliate papillae in the rabbit and in the other analyzed animal species are located similarly, as they are always found on the dorsal-lateral part in the posterior part of the body of the tongue [5, 9, 18]. As it was shown, foliate papillae in the rabbit are formed from 15-21 folia papillae, arranged parallel and separated by deep furrows. Kobayashi [8] reported in his study on the rabbit an observation of 15 to 20 ridge-like protrusions, forming foliate papillae, while Emura et al. [5] in the flying squirrel observed 34 crests separated by deep furrows. The parallel arrangement of structures forming foliate papillae is a characteristic trait of these papillae, with their number varying in individual animal species [2, 5, 9, 18].
The epithelium covering foliate papillae is nonkeratinized stratified squamous epithelium, forming epithelial streaks, ingrown between connective tissue folds of individual folia papillae. Similar observations were reported by Kobayashi [8].
Numerous and densely arranged taste buds of foliate papillae in the rabbit are located in the epithelium of individual folia papillae from the side of the furrow, as well as the epithelium directly surrounding foliate papillae, which confirms the observations by Fujimoto et al. [6]. A similar arrangement of taste buds in the epithelium of folia of foliate papillae was shown by other authors in different animal species, e.g. in the hamster [12, 13] and in bats [2]. However, it needs to be added that during morphogenesis of foliate papillae in the rabbit taste buds were also observed in the superficial epithelium of papillae, as it was reported by Fujimoto et al. [6]. They are the so-called fetal taste buds, which later disappear. Their presence during the development of vallate papillae was also reported by Tichý [16, 17].
As it was shown by studies on the fundus of deep furrows of foliate papillae in the rabbit excretory ducts of posterior serous lingual glands (Ebner’s glands) open there, as it was also reported by other authors [6, 8, 13, 15].
Folia of foliate papillae sometimes branch off forming two secondary folia, which was shown in observations under a light and a scanning electron microscope. Sometimes epithelial streaks and connective tissue folds also branch off in individual folia of foliate papillae. There are no available literature sources describing the above findings in the rabbit and in other animal species, as well as the human, which makes it impossible to confront these observations.
CONCLUSIONS
Foliate papillae on the tongue in the rabbit are formed from 15-21 folia of foliate papillae.
Foliate papillae are covered by the nonkeratinized stratifies squamous epithelium, generating two epithelial streaks in each folium papillae. Only occasionally 3, 4 or 5 epithelial streaks were observed.
The connective tissue core of foliate papillae is formed from parallel folds, separated by groove-like hollows. In each folium papillae one central fold and two lateral folds are distinguished. Some folds divide to form two secondary folds.
Some folia of foliate papillae divide to form two secondary folia.
REFERENCES
Atoji Y., Yamamoto Y., Suzuki Y., 1998: Morphology of the tongue of a male Formosan Serow (Capricornis crispus swinhoei). Anat. Histol. Embryol., 27: 17-19. Azzali G., Gabbi C., Grandi D., Arcani M.L., 1992: Comparative anatomical and ultrastructural features of the sensory papillae in the tongue of hibernating bats. Arch. Ital. Anat. Embriol., 97(3): 141-155. Barone R., Pavaux P.C., Blin C., Cuq P., 1973: Atlas D`Anatomie du Lapin. Atlas of rabbit anatomy. Masson & Cie Editeurs, Paris. Červený Č., Mísek I., 1993: Veterinární anatomie. Přehledná anatomie laboratorních savců. Ediční středisko Vysoké skoly veterinární a farmaceutické v Brně Emura S., Tamada A., Hayakawa D., Chen H., Jamali M., Taguchi H., Shoumura S., 1999: SEM study on the dorsal lingual surface of the flying squirrel, Petaurista leucogenys. Annals of Anatomy, 181: 495-498. Fujimoto S., Yamamoto K., Yoshizuka M., Yokoyama M., 1993: Pre- and postnatal development of rabbit foliate papillae with special reference to foliate gutter formation and taste bud and serous gland differentiation. Microscopy Research and Technique, 26: 120-132. Gupta S.K., Sharma D.N., Bhardwaj R.L., Singh I., 1990: Anatomy of the tongue of Gaddi goat with special reference to the papillae distribution. Indian Journal of Animal Sciences, 60(5): 560-562. Kobayashi K., 1992: Stereo Architecture of the interface of the epithelial cell layer and connective tissue core of the foliate papilla in the rabbit tongue. Acta Anatomica, 143: 109-117. Kobayashi K., Kumakura M., Yoshimura K., Takahashi M., Zeng J.H., Kageyama I., Kobayashi K., Hama N., 2004: Comparative morphological studies on the stereo structure of the lingual papillae of selected primates using scanning electron microscopy. Annals of Anatomy, 186: 525-530. Krysiak K., wieżyński K., 2001: Anatomia Zwierzšt. Wydawnictwo Naukowe PWN, Warszawa. Kumar P., Kumar S., Singh Y., 1998: Tongue papillae in goat: a scanning electron – microscopic study. Anat. Histol. Embryol., 27: 355-357. Miller R.L., Chaudhry A.P., 1976: Comparative ultrastructure of vallate, foliate and fungiform taste buds of golden Syrian hamster. Acta Anat., 95: 75-92. Miller I.J., Smith D.V., 1988: Proliferation of taste buds in the foliate and vallate papillae of postnatal hamsters. Growth, Development and Aging, 52: 123-131. Ostrowski K., 1995: Histologia. Wydawnictwo Lekarskie PZWL, Warszawa. State F.A., El-Eishi H.I., Naga I.A., 1974: The development of taste buds in the foliate papillae of the albino rat. Acta Anat., 89: 452-460. Tichý F., 1991a: The morphogenesis of circumvallate papillae and the differentiation of taste buds in the pig at 41 to 64 days of prenatal development. Acta Vet. Brno, 60: 99-110. Tichý F., 1991b: The morphogenesis of circumvallate papillae and the differentiation of taste buds in the porcine foetus from day 76 till birth and in the adult pig. Acta Vet. Brno, 60: 307-315. Utiyama C., Watanabe L., König B. Jr., Koga L.Y., Semprini M., Tedesco R.C., 1995: Scanning electron microscopic study of the dorsal surface of the tongue of Calomys callosus mouse. Annals of Anatomy, 177: 569-572. Watanabe I., Utiyama C., Koga L.Y., Motoyama A.A., Kobayashi K., Lopes R.A., König B. Junior, 1997: Scanning electron microscopy study of the interface epithelium-connective tissue surface of the lingual mucosa in Calomys callosus. Annals of Anatomy, 179: 45-48. Weisbroth S.H., Flatt R.E., Kraus A.L., 1974: The biology of the laboratory rabbit. Academic Press, INC.
The study was carried out within the framework of a grant for a Ph.D. thesis supervision no. 5P06D01719 financed by the Committee for Scientific Research.
Accepted for print: 14.09.2006
Mirosława Kulawik
Institute of Zoology, Department of Animal Anatomy, Poznań University of Life Sciences
ul. Wojska Polskiego 71 C
60-625, Poznań
tel: 48 61 8487625
email: kulawik@au.poznan.pl
Szymon Godynicki
Department of Histology and Embryology, Institute of Zoology, Poznań University of Life Sciences
ul. Wojska Polskiego 71 C
60-625, Poznań
email: gody@up.poznan.pl
Responses to this article, comments are invited and should be submitted within three months of the publication of the article. If accepted for publication, they will be published in the chapter headed 'Discussions' and hyperlinked to the article.