An investigation into the distributive pattern, classification and functional role of the conical papillae on the posterodorsal surface of the cat tongue using SEM

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An investigation into the distributive pattern, classification and functional role of the conical papillae on the posterodorsal sudace of the cat tongue using SEM Koei Ojima, Mamoru Takeda, Shigeji Matsumoto and Isao Nakanishi Department of Physiology, School of Dentistry at Tokyo, The Nippon Dental University, 1-9-20, Fujimi, Chiyoda-ku, Tokyo 102, Japan

Summary. In order to examine the relationship between their distributive patterns, classification and functional roles, three-dimensional structures in the microvascular network of the conical papillae (CoP) on the posterior third of the central dorsal surface of the cat tongue were observed by the corrosion cast method under a scanning electron microscope (SEM). CoP can be classified into two types: small conical papillae (SCoP) and large conical papillae (LCoP), according to their shape, size and distributive pattern. On the posterior third of the central dorsal surface of the tongue, SCoPs are arranged in the form of six - eight straight lines running regularly from the posterior third of the central zone towards the pharynx. LCoPs are also arranged in the form of a V, with the point directed posteriorly, in oblique lines running in an orderly fashion from both the antero-peripheral zones to the central zone. To summarize CoPs play an important role in the drinking of milk and water, after mixing the food with saliva, in the transport of the food mass towards the pharynx and in swallowing it. Key words: Cat - Tongue - Conical papillae (CoP) - Microvascular cast specimens (MVCS) - Scanning electron microscope (SEM)

papillae (CoP) are located on the dorsal surface of the cat tongue (Boshell et al. 1982; Chamoro et al. 1987; Crouch 1969; Iwasaki et al. 1987 a; Iwasaki 1990 a, b; Ojirna et al. 1996 a). There have been a relatively large number of studies on the three-dimensional fine anatomy of the lingual papillae of the cat tongue by scanning electron microscopy, including the FiP (Boshell et al. 1982; Chamoro et al. 1987; Crouch 1969; Iwasaki et al. 1987 a; Iwasaki 1992, 1993; Kobayashi 1992; Ojima and Lowe 1995; Ojima et al. 1996b; Ojima et al. 1996g, h), FuP (Chamora et al. 1987; Crouch 1969; Iwasaki et al. 1987 b; Kobayashi 1992; Ojima et al. 1996b, c), of YaP (Crouch 1969; Kobayashi et al. 1988; Kobayashi and Iwasaki 1988; Kobayashi 1992; Ojima 1995 b, c; Ojima et al. 1996 a, f), FoP (Crouch 1969; Iwasaki et al. 1987b; Kobayashi 1992) and CoP (Chamoro et al. 1987; Crouch 1969; Iwasaki et al. 1987 a, b; Iwasaki 1992, 1993; Kobayashi et al. 1988; Kobayashi and Iwasaki 1988; Kobayashi 1992). However, little is known about the relationships between the distributive patterns, classification and functions of the three-dimensional structures of CoPs in microvascular cast specimens (MVCS). One aim of this study was to extend our previous work (Ojima et al. 1996 g, i).

Introduction

Materials and methods

Various types of lingual papillae, such as filiform (FiP) , fungiform (FuP), vallate (VaP), foliate (FoP) and conical

Tongues from 55 crossbred Japanese domestic cats, Felis catus domestica, were used in the present study. Cats of both sexes (19 females and 36 males) were obtained from a commercial supplier. All were adults of unknown age. Each cat weighed be-

Correspondence to: Koei Ojima

Ann Anat (1997) 179: 505-510 © Gustav Fischer Verlag

tween 2.5 and 5.0 kg. They were anaesthethized with an overdose of Nembutal solution (Pentobarbital sodium injection) by intraperitoneal injection and killed. Their tongues were immediately removed and both lingual arteries cannulated and prepared for macroscopic, stereomicroscopic and SEM observation. For general SEM observation, each tongue surface was rinsed with 0.9% physiological saline solution or Ringer's solution at 35-37°C, and after cannulation with an injection needle (27 G) connected to a silicone-tube. Vascular perfusion with the solution was continued until all the blood in the jugular veins had been replaced. 5% glutaraldehyde solution in phosphate buffer (pH 7.4) was then injected into both lingual arteries in order to fix the vessels and their tributaries. Both lingual arteries were filled with synthetic resin (Mercox CL-2R 5, CL-2B 5, CL-2C 5, Dainippon Inki Chemical Co., Ltd., Tokyo, Japan) under manual pressure. The injected specimens of the tongue were fixed for 0.5 hr at room temperature and incubated for 0.5 hr at 55°C. The specimens mere then polymerized completely and immersed in 20% KOH or NaOH solution for over 3 hr at room temperature until the soft tissues had been dissolved away. The finest macerated vascular samples were carefully washed 2-3 times with warm water at 45-55°C and gently dried for 2-3 days at 55°C in an incubator. The MVCS of the whole tongue were mounted on specimen stubs and coated by gold-palladium sputtering. The specimens were then examined with on S-4000 seanning electron microscope (HITACHI, Tokyo, Japan) at an accelerating voltage of SkY.

among the stretches of FiPs arranged in the form of a V pointing towards the pharynx (Ojima et a1. 1996 i) (Fig. 1). On the other hand, CoPs cover the posterior third of the dorsal surface of the tongue densely and are classified into two types; small conical papillae (SCoP) and large conical papillae (LCoP), according to their shape, size and distributive pattern. SCoPs are round or elliptical in shape, and are half the size of LCoPs. SCoPs inclined posteriorly are arranged in the form of six-eight straight lines running regularly from the central zone of the posterior third to the pharynx. LCoPs are, as a rule, round or elliptical in shape, similar to SCoP but double the size. LCoPs inclined from both antero-peripheral zones towards the postero-median

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The relationships between the distributive patterns, classification and functions of three-dimensional structures in the microvascular network of CoPs on the posterior third of the centro-dorsal surface of the tongue were then investigated under SEM, microphotographs being made of the whole tongue surface. In general, as shown Fig. 1, the anterior two-thirds of the centro-dorsal surface of the tongue are covered mainly by the various types of FiP and the different types of FuP, each with some regional variations. The posterior third of the centro-dorsal surface of the tongue is covered by CoPs. As deseribed in previous reports, there are five types of FiP; types I-V (Ojima and Lowe 1995), and four types of FuP; types I-IV (Ojima et a1. 1996 b) on the anteropostero-dorsal surface. On the front half of the anterior two-thirds of the dorsal surface, each FiP type is arranged in a geometrically ordered fashion, in the form of a A and in an oblique line from the antero-median zone to the postero-peripheral zone iti both directions, and each FuP type is also scattered among the stretches of FiPs arranged in the form of a A pointing towards the apex (Ojima et a1. 1996 g). On the rear half of the anterior two-thirds of the dorsal surface, each FiP type is arranged in a geometrically ordered fashion, in the form of a V and in an oblique line from both antero-peripheral zones to the postero-median zone or the pharynx, and each FuP type is scattered

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rn Pig. 1. A schematic diagram showing the distribution of the variouskinds of lingual papillae on the antero-posterior two thirds of the central dorsal surface of the cat tongue. From the central zone to the peripheral zone in both directions, and from the apical zone to the posterior zone, types I-V of PiP and types I-IV of FuP are arranged geometrically and comparatively symmetrically. On the posterior third of the centro-dorsal surface, SCoPs are regularly arranged from the central zone to the posterior zone (pharynx). LCoPs are arranged from the central zone to both peripheral zones in oblique lines geometrically and symmetrically. Fig. 2. corresponds to the square inset of this diagram. Indication mark: • = type I of Pip, 0 = type II, @ = type III, @ = type IV, 0 = type V and @ = type I of FuP, ~ = type II, ® = type III, • = type IV, ..:.... = SCoP, :. = LCoP, = nonlingual papillae zone.

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direction are arranged in a geometrically ordered fashion in the form of a V, and in an oblique line from the antero-peripheral zone in both directions to the postero-median zone or the pharynx (Fig. 2-4).

Discussion It may be reasonable to think that the blood supply to the tongue is more plentiful than that to most other tissues of the body (Hellekant 1971), and that MVCS of blood vessels inside the lingual papillae of the tongue form its basic structural core (Ojima 1995 a, b; Ojima and Lowe 1995; Ojima et al. 1996 a-i). The MVCS applied in this study provided an ideal, practical method for studying the three-dimensional angioarchitectural images of the microvascular network structure of the lingual papillae. Compared with other previous vascular perfusion methods, this novel technique offers an advantage in obtaining fine imprints of the walls of the small blood vessels of the lingual papillae and makes it possible to distinguish between arterioles and venules in terms of shape, size and anastomoses. In the present study, the re-

sin cast methods used in previous studies (Ojima 1995 a, b; Ojima and Lowe 1995; Ojima et al. 1996a, b) were modified and improved by injecting Mercox into tongue vessels that had first been twice treated with glutaraldehyde. In this way, we achieved better results in preserving the walls of blood vessels and preventing the extravasation of the injected Mercox. At the same time, we could observe the MVCS under better conditions (Ojima et al. 1996c-i). There are many fine morphological studies of CoP by SEM (Chamoro et al. 1987; Crouch 1969; Iwasaki et al. 1987 a, b; Iwasaki 1992, 1993; Kobayashi et al. 1988; Kobayashi and Iwasaki 1998; Kobayashi 1992). Chamoro et al. (1987) reported that in both species (cat and rabbit) there are three forms of mechanical papillae (smooth, scaly conical and filiform). As described by Crouch (1969) in his book, a great number of CoPs are distributed on the postero-dorsal surface of YaP, but they do not have taste buds. Iwasaki et al. (1987 a, b) wrote that CoP, without twigs, are distributed clearly, and distinctly on the posterior area of the marginal region between the anterior and posterior areas. Kobayashi et al. (1988) and Kobayashi (1992) reported that LCoPs are distributed on the root of the cat, dog and pig tongue.

Fig. 2. Upper view of the composite photograph of scanning electron micrographs of MVCS of SCoPs and LCoPs of the posterior third of the centro-dorsal surface of the cat tongue corresponding to the square inset of Fig. l. From the posterior third of the central dorsal surface to the pharynx, six-eight white arrow straight lines of SCoP inclined posteriorly run regularly to the posterior zone or the pharynx. LCoP inclined from the antero-peripheral towards the postero-median direction are arranged in the form of a V, and in the white oblique lines running from both peripheral zones to the central zone.

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From the results of the present study, CoP can be classified into two types; small conical papillae (SCoP) and large conical papillae (LCoP) according to their shape, size and distributive patterns. In Fig. 2-4, the 6-8 white arrowheads indicate straight lines regularly running from the median zone posteriorly on the postero-median portion, and the white arrow lines indicate straight arranged obliquely from both antero-

peripheral zones to the postero-median portion in a geometrically ordered fashion on the posterior third of the central dorsal surface of the tongue. These arrangements of SCoPs and LCoPs indicate the paths taken by the masticated food mass for swallowing. LCoPs together with SCoPs on the posterior third of the lingual root may, as its most important role, facilitate the swallowing of the masticated food mass.

Fig. 3. Upper view of the composite photograph of a scanning electron micrographs of MVCS of SCoPs and LCoPs on the posterior third of the left dorsal surface of the tongue. In a white arrow, oblique lines from the left antero-peripheral zone to the postero-median zone, at the central zone, eight straight lines of SCoPs inclined posteriorly are regularly arranged from the posterior third portion to the pharynx. LCoPs inclined from the antero-peripheral towards the postero-median direction are arranged in oblique lines and in a geometrically ordered fashion.

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However, more detailed comparative observations of CoPs are required to clarify the fine relationships between their shape, size, distributive patterns and their functional role in other carnivora. Acknowledgment. The authors are grateful to Mrs. Fusako Mitsuhashi, Dental Research Institute, School of Dentistry at Tokyo, for assistance with SEM photography.

References Boshell JL, Wilborn WH, Singh BB (1982) Filiform papillae of cat tongue. Acta Anat 114: 95-105 Chamoro CA, Sandoval J, Fernandez JG, Fernandez M, de Paz P (1987) Comparative study of the lingual papillae of cats (Felis catus) and rabbits (Oryctolargus cuniculus) using the scanning electron microscope. Anat Hist Embryol16: 37-47

Fig. 4. Upper view of the composite photograph of scanning electron micrographs of MVCS of SCoPs and LCoPs on the posterior third of the right dorsal surface of the tongue. In a white arrow, oblique lines from the right antero-peripheral zone to the posteromedian zone, LCoPs inclined from the antero-peripheral to the postero-median direction are arranged in oblique lines and in a geometrically ordered fashion. The arrow in the upper left corner in Fig. 1-4 indicates the anterior (apical) direction of the tongue. Each bar in Fig. 2-4 = 1 mm.

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Crouch JE (1969) Text-atlas of cat anatomy. Lea & Febiger, Philadelphia, pp 128, 279-280 Hellekant G (1971) Circulation of the tongue. In: Emmelin N, Zotterman Y (eds) Oral Physiology. Oxford, Pergamon Press, pp 127-137 Iwasaki S, Miyata K, Kobayashi K (1987 a) Scanning electron microscopic studies of the surface of the dorsal tongue of the cat. Jpn J Oral Bioi 29: 94-101 Iwasaki K, Miyata T, Kobayashi K (1987 b) Comparative studies of the dorsal surface of the tongue in three mammalian species by scanning electron microscopy. Acta Anat 128: 140--146 Iwasaki S (1990a) Surface structure and keratinization of the mucosal epithelium of the domestic cat tongue. J Mamm Soc Japan 15: 1-13 Iwasaki S (1990 b) Fine structure of the dorsal lingual epithelium of the domestic, newborn kitten, Felis catus. Ann Anat 174: 293-300 Iwasaki S (1993) A study of the filiform papillae of the newborn domestic · kitten Felis catus by scanning electron microscopy. J Mamm Soc Japan 18: 33-38 Kobayashi K, Miyata K, Iwasaki S, Takahashi K (1988) Three dimensional structure of the connective tissue papillae of cat lingual papillae. Jpn J Oral Bioi 30: 719-731 Kobayashi K, Iwasaki S (1988) Comparative studies on the stereo architecture of the connective tissue papillae in some mammalian tongues. Prog Clin Bioi Res 295: 303-308 Kobayashi K (1992) Comparative anatomical studies on the tongues with special reference to the connective tissue of the lingual papillae. Shigaku (Odontology) 80: 661--678 Ojima K (1995 a) Numerical study of vallate papillae by SEM figure in cat tongue. Shigaku (Odontology) 82: 1006-1017 Ojima K (1995 b) Additional study of number and arrangement of vallate papillae in cat tongue. Shigaku (Odontology) 82: 1393-1499 Ojima K, Lowe AA (1995) Microvascular structural study of the filiform papillae in cat tongue. Shigaku (Odontology) 82: 1325-1336

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