Okajima Folia Anat., Jpn., 58(4-6): 535-542, March 1982

Distribution and Development of Taste Buds on the Incisive Papillae of Mice and Rats

By

KUMIKO OHTA-YAMAKITA, IKUO YOSHIOKA, HIROSHI MUTO and NORIO OZEKI

Department of Anatomy, Aichi Medical University, Nagakute, Aichi, 480-11, Japan

-Received for Publication, November 6, 1981-

Key words : Hard , Incisive papilla, Taste bunds, Mouse, Rat.

Summary : The mouse and rat have been shown to have many taste buds on the incisive papillae of the . In the rat incisive papilla, taste buds were more numerously observed than in the mouse. They were most densely distributed in both animals on the anteromedial wall of the lower part of the nasopalatine ducts. The taste buds on the mouse incisive papilla appeared at 4 or 5 days of age, and after 20 days of age the number of taste buds was almost constant. The rat taste buds also showed a tendency to continue their development after 10 weeks of age. An active role for the taste buds on the incisive papilla in the mouse and rat is suggested in that the taste buds are more numerously distributed in the nasopalatine ducts than on the oral surface.

After Ponzo (1907) reported the pre- of the incisive papilla of several primates, sence of taste buds on the posterior part such as Nycticebus coucang (Hofer, 1977, near the in the human fetus, 1978), Tupaia glis (Wohrman-Repenning, several workers investigated the taste 1978), Galago crassicaudatus, Perodicticus buds in the rat hard palate (Kolmer, 1927 ; potto and Microcebus murinus (Hofer, Kutuzov & Sicher, 1952) and mouse 1980). The present study was undertaken (Kutuzov & Sicher, 1953). In 1929, Kolmer, to assess the distribution and postnatal first described the taste buds of the rat changes in occurrence of the taste buds incisive papilla, and Kutuzov and Sicher on the incisive papillae of the mouse and (1952) reported that the wall of the naso- rat. palatine ducts of the mouse carried taste buds. In 1967, Yoshioka found taste buds Materials and Methods in the epithelium of the oral surface of the mouse incisive papilla, and Ozeki et The materials used for this study were al. (1976) minutely described the occurrence 26 SMA mice aged 1 to 30 days and 1 and morphology of the mouse taste buds and 2 years, and 6 Wistar rats aged 9 to based on light and scanning electron 13 weeks and 36 weeks. They were microscopy. Recently, Hofer (1977) noted sacrificed under chloroform anesthesia. that taste buds occurred in the epithelium The incisive papillae and their surrounding

535 536 K. Ohta-Yamakita, I. Yoshioka, H. Muto and N. Ozeki

tissues were taken from all cases and fixed Thble 1. The number of taste buds on in 10% formalin. After decalcification in the mouse incisive papillae. 5% nitric acid, the specimen were passed through a graded ethanol series and em- bedded in paraffin. They were serially cut into frontal and sagittal sections at a thickness of about 20 pm and stained with hematoxylin-eosin.

Observations

1. Mouse The mouse hard palate around the inci- sive papilla is without bone tissue. A pair of incisive foramina, the lower end of the nasopalatine ducts, open into the rather medial side of the lateral margin of the incisive papilla, covered with kera- tinized stratified squamous epithelium. Between the incisive foramina, the lamina. propria mucosae contains a Merkal's pa- Merkel's papillary cartilage and a pair of pillary cartilage, its major axis being openings to the nasopalatine ducts (Fig. situated towards the transverse direction. 6). The taste buds in the incisive papilla The taste buds in the mouse incisive are more numerous than in the mouse. papilla are abundantly distributed on the Taste buds are most frequently found in anteromedial wall of the lower part of the anteromedial wall of the lower part the nasopalatine ducts and a few are of the nasoplatine ducts, and also often present on the oral surface, just in the in the oral surface around the incisive anterior part of the incisive foramina foramina (Fig. 7). Further, a few taste (Fig. 2). However, no taste buds are ob- buds are present in the posterolateral wall served in other parts of the papilla. of the lower part of the nasopalatine ducts The taste buds in the incisive papilla and in the oral surface of the anterior develop after birth. That is to say, taste part of the incisive papilla. Table 2 shows buds are found at 4 days after birth (Fig. an increasing tendency in number 3), and this stage is followed by a gradual at 9 to 13 weeks of age, and adult rats increase in the number of taste buds at generally contain over 70 taste buds per least from 5 to 15 days of age (Fig. 4). incisive papilla. At 20 days to 30 days of age, the number of taste buds appears constant, at 21 to Discussion 27 per incisive papilla, and after this stage, no increase in the number of taste bud Many investigators have studied the is recognized (Table 1, Fig. 1). Multi- taste buds in the soft palate, , pored taste buds (Bradley et at., 1980) are epiglottis and other mucous membranes. sometimes observed at 10 to 30 days of However, there has been no study on the age. number and postnatal development of the 2. Rat incisive papilla except for that indicating The rat incisive papilla also contains a the presence of about 20 taste buds in the Distribution and Development of Taste Buds 537

Fig. 1. Graph showing the number of taste buds in the developing mouse incisive papilla.

Table 2. The number of taste buds on of the rat incisive papilla revealed a the rat incisive papillae. tendency to continue taste buds formation over 10 weeks of age (Table 2). In the opossum (Elliott, 1945), it has been reported that taste bud formation in the fungiform papillae began at 16 days after birth, and the taste buds gradually increased in number until leaving the maternal pouch 70 days after birth. In the mouse and rat, the taste buds also develop after birth and continue with mouse incisive papilla (Ozeki et al., 1976). their development. In contrast, the sheep Based on the present results, the taste epiglottal taste buds increase in number buds of the mouse incisive papilla, which prenatally and continue to increase after are absent in the newborn, appear at 4 birth (Bradley et al., 1980). Concerning or 5 days after birth, and then continue the taste bud number, Bradley et al. sug- to increase in number at a slower rate gested that taste bud division occurred until about 20 days of age (Table 1, Fig. because of the increased number of taste 1). buds with multiple pores in the 100-day Srivastava and Vyas (1979), who studied fetus, although the mechanism was not the postnatal development of the rat soft clear. In the present study also, multi- palate, have stated that the taste buds, pored taste buds were sometimes seen which were absent in the newborn, de- between 10 to 30 days of age. veloped during the first 3 weeks of age As regards the function of the incisive and after this stage no new taste buds papilla, many investigators have supported appeared. In contrast, the present study Merkel's hypothesis that the papilla may 538 K. Ohta-Yamakita, I. Yoshioka, H. Muto and N. Ozeki

have some specialized sensory function through the nasopalatine ducts. The basis because of the dense innervation, the re- of their hypothesis is that in primates stricted distribution of different types of the taste buds were never found in the terminal and the presence of specialized palatal surface but may occur at the epithelial papillae (Yohro, 1980). However, ventrolateral edge of the incisive papilla. few investigators have discussed the func- However, in the rat incisive papilla, they tion of the taste buds of the incisive always occur in small numbers on the papilla. oral surface. Wilson (1905), who reviewed the early From their observations of the sheep literature on the taste buds of the larynx, epiglottis, Bradley et al (1980) have sup- suggested that the laryngeal taste buds ported the theory that the taste buds have were either a phylogenetic residue with a functional role in the upper aiway pro- no functional role, or served as chemo- tective reflexes, because of the large sensors. He stated that his own epiglottis number of taste buds and the maintenance could taste the 4 primary tastes although of their density on the epiglottis, adding the taste sensation was quantitatively and a review of the literature. qualitatively inferior to that of the tongue. Broman (1919, 1920) described a "trans- He therefore rejected the notion that the verse palatine muscle" between the incisors epiglottal taste buds are a phylogenetic and incisive papilla in the guinea pig, rat, residue and hypothesized that they re- mouse and rabbit, by which the naso- present part of a reflex mechanism pro- palatine ducts would be closed to protect tecting the airway. Johnson et al. (1973) the food mass from invading the nasal and Downing and Lee (1975) have also cavity. shown that the larynx is chemosensitive The incisive papilla of the rat contains in the newborn lamb. Electrophysiological more abundant taste buds than that of studies have demonstrated that the nerve the mouse. In both of them, the taste supply of the epiglottis contains chemo- buds are more numerously distributed in sensitive fibers (Storey, 1968 ; Storey and the lower part of the nasopalatine ducts Johnson, 1975 ; Harding et al., 1978). than on the oral surface around the inci- It is clear that the taste buds of the sive foramina. These findings appear to incisive papilla are not a phylogenetic suggest a functional role for the taste residue, since they developed after birth buds on the incisive papilla. and increased in number with the develop- ment of the mouse and were densely dis- References tributed at the nasopalatine ducts. Recently, Hofer (1977, 1978, 1980) and 1) Bradley, R. M., Cheal, M. L. and Kim, Wohrmann-Repening (1977) have discussed Y. H.: Quantitative analysis of develop- the role of the taste buds of the incisive ing epiglottal taste buds in sheep. J. papilla on the basis of their observations Anat., 130: 25-32, 1980. of the papillae of primates, mediating 2) Broman, I.: Ueber bisher unbekannte, sexual behavior gustatorily, as well as quergestreifte Muskeln im harten Gamen der Nagetiere. Anat. Anz., 52: 1-15, those of the olfactory epithelium of the 1919. . The anatomical situa- 3) Broman, I.: Das Organon vomelo-nasale tion of the taste buds indicates that they Jacobsoni — Ein Wassergeruchsorgan are functionally related to both the Anat. H., 58: 143-198, 1920. olfactory epithelium and the accessory 4) Downing, S. E. and Lee, J. C.: Laryngeal olfactory organ (vomeronasal organ) chemosensitivity : A possible mechanism Distribution and Development of Taste Buds 539

of sudden infant death. Pediatrics, 55: and the palate of the laboratory mouse. 640-649, 1975. Anat. Rec., 116: 409-425, 1953. 5) Elliott, R.: Distribution of taste buds 14) Ozeki, N., Yoshioka, I., Ooishi-Iida, M. in fungiform papillae on tongue of the and Muto, H.: Morphological obser- opossum. J. Comp. Neurol., 82: 205-213, vations on the hard palate of mice, 1954. especially on the taste buds in the 6) Harding, R., Johnson, P. and McClelland, incisive papilla (in Japanese with English M. E.: Liquid-sensitive laryngeal recep- abstract) . J. Aichi Med. Univ. Ass., 4: tors in the developing sheep, cat and 178-182, 1976. monkey. J. Physiol., 277: 409-422, 1978. 15) Ponzo, M.: Sulla presenza di organi del 7) Hofer, H. 0.: The anatomical relations gusto nella parte laringea della faringem of the ductus vomeronasalis and the nel tratto cervicale dell' esofago e nel occurrence of taste buds in the papilla palato duro del feto umano. Anat. Anz., palatina of Nycticebus coucang (Primates, 31 : 570-575, 1907. Prosimiae) with remarks on strepsir- 16) Srivastava, H. C. and Vyas, D. C. : rhinism. Gegenbaurs Morph. Jahrb., Postnatal development of rat soft palate. 123: 836-856, 1977. J. Anat., 128: 97-105, 1979. 8) Hofer, H. 0.: The ductus nasopalatinus 17) Storey, A. T.: A functional analysis of and the ductus vomeronasalis and sensory units innervating epiglottis and occurrence of taste buds in the papilla larynx. Exp. Neurol., 20: 366-383, 1968. palatina in Nycticebus coucang (Primates, 18) Storey, A. T. and Johnson, P.: Laryngeal Prosimiae) . Verh. Anat. Ges., 72 : 649- water receptors initiating apnea in the 650, 1978. lamb. Exp. Neurol., 47: 42-55, 1975. 9) Hofer, H. 0.: Further observations on 19) Währmann- Repenning, A.: Geschma- the occurrence of taste buds in the cksknospen an der Papilla pallatina von papilla palatina of primates. Gegenbaurs Tupaia glis (Diard 1820) , ihr Vorkommen Morph. Jahrb., 126: 110-117, 1980. und ihre Beziehungen zum Jacobsonschen 10) Johnson, P., Robinson, J. S. and Salisbury, Organ. Gegenbaurs Morph. Jahrb., 124: D.: The onset and control of breathing 375-384, 1978. after birth. Foetal and neonatal physio- 20) Wilson, J. G.: The structure and logy (ed. Coline, K. S. et al.) , pp. 217- function of the taste buds on the larynx. 221, Cambridge Univ. Press, Cambridge, Brain, 28 : 339-351, 1905. 1973. 21) Yohro, T.: Structure and innervation 11) Kolmer, W.: Ueber das Vorkommen von. of the papilla incisiva (Papilla palatina) Geschmacksknospen im Ductus naso- of the shrew, Sorex unguiculatus. palatinus der Ratte. Anat. Anz., 63: Okajimas Fol. Anat. Jpn., 57: 321-336, 248-251, 1927. 1980. 12) Kutuzov, H. and Sicher, H.: Anatomy 22) Yoshioka, I.: Histology of the palate of and function of the palate in the mouse with special reference to distri- white rat. Anat. Rec., '114: 67-84, 1952. bution of elastic fibers (in Japanese with 13) Kutuzov, H. and Sicher, H.: Comparative English abstract) . Aichi-Gakuin J. Dent. anatomy of the mucosa of the tongue Sci., 4: 130-136, 1967. 540 K. Ohta-Yamakita, I. Yoshioka, H. Muto and N. Ozeki

Explanation of Figures

Plate I

Fig. 2. Sagittal section through the palatine duct of the incisive papilla of an adult mouse. Several taste buds can be seen (arrows) . x 120

Fig. 3 to 5. Frontal sections of the incisive papillae of mice.

Fig. 3. At 4 days of age. A taste bud appears. x 120

Fig. 4. At 5 deys of age. A few taste buds can be seen. x 290

Fig. 5. At 20 day of age. x 120

Fig. 6. Sagittal section through the middle part of the incisive papilla of an adult rat. x 120

Fig. 7. Sagittal section through the palatine duct of the incisive papilla of an adult rat. A few taste buds can be seen. x 120 541 Plate I

K. Ohta-Yamakita, et al.