Angioarchitectural structure of the fungiform papillae on the anterodorsal surface of the rat tongue

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AngioarchitecturaI structure of the fungiform papillae on the anterodorsal sudace of the rat tongue Koei Ojima, Chikako Saiki, Toshiaki Takahashi, Shigeji MatsUDIoto, Mamoru Takeda Department of Physiology, School of Dentistry at Tokyo, The Nippon Dental University, 1-9-20, Fujimi, Chiyoda-ku, Tokyo 102, Japan

SUDIIDary. To ascertain whether the microvascular mor-

phological differences of fungiform papillae (FuP) on the anterodorsal surface of the rat tongue are location ally and functionally related, this study aimed at examining and comparing, in greater detail, the comparative morphological characteristics of FuP. FuP were sporadically and consistently scattered among numerous filiform papillae (PiP) in three parts: the apical, central and in front of the intermolar eminence on the anterodorsal surface. We studied these by means of the microvascular cast specimen (MVCS) of FuP using scanning electron microscopy (SEM). The results obtained in this study showed that in all three parts on the anterodorsal region, the capillary bed of FuP presented as a netbasket-like and cylindrical figure with a central hole consisting of 4-5 horizontal rings of several ascending and descending roots. FuP in the central part on the anterodorsal region were relatively larger in size and more cylindrical in shape than those of both the other parts, and they play the leading part as sensory organs for the taste sense and were regarded as taste receptive organs. Key words: Rat - Fungiform papillae - Microvascular cast specimen - Scanning electron microscopy

Introduction As described by Iwasaki et al. (1984), Ohshima et al. (1990), Ojima et al. (1996 e), four types of papillae, namely, filiform, fungiform, foliate and circumvallate papillae are located on the dorsal surface and three types of Correspondence to: K. Ojima

Ann Anat (1997) 179: 399-403 © Gustav Fischer Verlag

PiP: small conical papillae (ScP), giant conical papillae (GcP) and true filiform papillae (TfP) are distributed in a restricted area of the rat tongue dorsal surface (Yoshioka et al. 1975; Iwasaki et al. 1984; lino et al. 1988; Nagata et al. 1989 a, b; Ohshima et al. 1990; Okada et al. 1994). Kutuzov et al. (1951) conducted the first detailed gross and light microscopic examinations of PiP on the rat lingual dorsum. They subdivided these papillae into three types of PiP : ScP on the anterior portion, GcP on the oval field of the anterior portion and TfP on the posterior portion of the body of the tongue. Numerous studies on the whole surface structure (Kato et al. 1965; Yukino et al. 1967; Farbman 1970, 1973; Svejda et al. 1971; Yoshioka et al. 1975; Baratz et al. 1975; Kesse et al. 1979; lida et al. 1985), many reports on connective tissue core (Toyoshirna et al. 1982; Iwasaki et al. 1984; lino et al. 1988; Kobayashi et al. 1989; Kobayashi 1992) and many studies on the microvasculature of PiP in the rat (Nagato et al. 1989 a, b; Ohshima et a1.1990; Ojima et aI.1996e), in the cat (Ojima and Lowe 1995), in the cat and rabbit (Ojima et al. 1996), of PiP and FuP in the cat (Ojima et al. 1996), YaP in the cat (Ojima 1995 b, c; Ojima et al. 1996 a), FuP in the rat (Iwasaki et al. 1984; Kobayashi and Iwasaki 1989; Kobayashi 1992; Miller and Presslar 1951; Mistretta and Baum 1984), of FuP in the bullfrog (Ojima 1995 a), in the cat (Ojima et al. 1996b) have been done using SEM. Okada et al. (1994) reported that rat PiP were classified into 6 types ScP, digitiform, giant conical, forked and true filiform. In particular, observations concerning ScP were made on types I and II of ScP in the lingual apex of the rat tongue. Recently, Ojima et al. (1996 e) have been made a classification of the three types of ScP I, II, III. There are, however, very few reports available concerning the pattern of distribution and positional form, and the functional relationship of FuP on the anterodorsal surface of the rat tongue. Therefore, the purpose of this

fied corrosive resin cast method (Kishi et al. 1990; Murakami 1971; Nagato et al. 1989; Ojima 1995 a, b, c; Ojima and Lowe 1995). The injected specimens of the tongue were kept at room temperature for 2 hr. After the specimens had been completely polymerized, they were immersed in 5% NaOH or KOH solution at 40 °C for one day, the medium being renewed twice and then the soft tissues of the tongue were dissolved. The finest macerated vascular samples were carefully washed in slowly flowing water and gently dried for one day at 55°C in an incubator. MVCS of the whole rat tongues were mounted on specimen stubs, sputter-coated with gold-palladium and then examined under a S-4000 type scanning electron microscope (HITACHI, Tokyo, Japan) at an accelerating voltage of 5 kV

study was to examine, in further detail, the clearer information from MVCS of FuP by means of SEM, the distributive pattern and form of FuP and to elucidate the close comparative relationship between the positional morphological characteristics and functional role of FuP on the anterodorsal part of the rat tongue.

Materials and methods Thirty-five adult Wistar white rats of both sexes, weighing 300400 g, were used in this study. The animals were anaesthetized with an intraperitoneal injection of sodium pentobarbital (50 mgt kg of body weight). For perfusion, an injection needle (27 G) connected to a silicone tube was carefully inserted into the ascending aorta under an optical stereomicroscope. Vascular perfusing with 0.9% physiological saline solution or Ringer's solution at 38°C was done until the efflux of the superior vena cava became clear, and 0.25% glutaraldehyde solution in phosphate buffer (pH 7.4) was immediately injected into the aorta for fixation of the vessels and their tributaries twice. After fixation for MVCS, the synthetic resin (Mercox CL2R 5, CL-2B 5, CL-2C 5, Dainippon Inki Chemical Co., Ltd., Tokyo, Japan) was injected under manual pressure by the modi-

Results On macroscopical observation, as schematically shown in Fig. 1, the rat tongue was relatively long, running from the anterior (apex) to the posterior (radix), and narrow, and had the median sulcus (MS) along the midline of the anterior half of the tongue. This was itself subdivided into the three regions: the anterior part, the intermolar eminence and the posterior part.

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Fig. 1. A schematic diagram showing the distribution of the various types of lingual papillae on the anterodorsal surface of the rat tongue. The rat tongue had the median sulcus (MS) along the midline of the anterior half of the fore-tongue, subdivided into the three regions: the anterior part, the intermolar eminence and the posterior part. In these three different parts, four types of lingual papillae can be distinguished: filiform papillae (FiP) and fungiform papillae (FuP) (.) in the anterior part, foliate papillae (FoP) (I) on both peripheral sides and circumvallate papillae (CvP) (.,) along the central line of the posterior part. FiP were subdivided into three types: small conical papillae (ScP) (.), giant conical papillae (GcP) (e), true filiform papillae (TfP) (~) . ScPs were subdivided into three different types: ScP I (0), II (0) and III (.) according to the shape, size, distributive pattern and form from the apical-peripheral part to MS or the central portion on the apical part of the tongue (Ojima et al. 1996). A relatively small number of FuP were sporadically and consistently and almost uniformly scattered among the various types of ScPo

Fig. 2. Upper view scanning electron micrography of MVCS of the seven points of FuP on the anterodorsal surface correspond to the schema 8. FuP 1 and 2 in Fig. 2-8 are indicated as FuP 1 and 2 in Fig. 2 at the apical part, FuP 3 and 4 are indicated as FuP 3 and 4 at the central part and FuP 5-7 are indicated as FuP 5-7 at the front part of the intermolar eminence. The angioarchitectural figure of FuP of seven points in the three parts showed the long netbasket-like and a cylindrical shape with a central hole consisting of 4-5 horizontal rings of the capillary loops where the capillary bed of the papillae presented several ascending and descending capillary roots. FuP in the central part of the antero-dorsal region (Fig. 2: 3, 4, 6) were relatively larger in size and more cylindrical in shape than that of both the other parts (Fig. 2: 1, 2, 5, 7). All each bar = 200 Ilm. The arrow on the upper left side indicates the front of the tongue (Fig. 1 and Fig. 2: 8).

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In these three different parts, three different types of FiP were subdivided: small conical papillae (ScP) subdivided into three types: ScP I, II, III (Ojima et al. 1996) in the anterior part, giant cylindrical papillae (GcP) at the intermolar eminence and true filiform papillae (TiP) on the posterior part of the anterior portion. Like other lingual papillae, FuP were sporadically and consistently scattered among numerous ScPs in the anterior part, foliate papillae (FoP) on both side peripherally and circumvallate papillae (CvP) along the central line of the posterior portion of the rat tongue (Fig. 1). The scanning electron microscopical observations were carried out angio-architecturally on MVCS of FuPs at seven points in the three parts (Fig. 2: 8): two points on an apical (Fig. 2: 1, 2) and the central parts (Fig. 2: 3, 4) and three points on the front part of the intermolar eminence (Fig. 2: 5-7). They showed the long netbasket-like and cylindrical shape with a central hole consisting of 4-5 horizontal rings of the capillary loops where the capillary bed of the papillae presented several ascending and descending roots (Fig. 2: 1-7). FuPs on the central part of the anterodorsal region (Fig. 2: 3, 4, 6) were relatively larger and more cylindrical than those of the other two parts (Fig. 2: 1, 2, 5, 7).

Discussion It is known that the blood supply to the tongue is more

plentiful than to most other tissues of the body (Hellekant 1971), and the vascular structures of the rat tongue are the basic core of the these tissues which supply nutrition. We have in this study applied the corrosive resin cast method, modified from that of Kishi et al. (1990), Murakami (1971), Nagato et al. (1989a, b). The MVCS method (Ojima 1995 a, b, c; Ojima and Lowe 1995; Ojima et al. a, b, c, d, e) provided an ideally, practical method for studying three-dimensional images of the microvascular network structure of the FuP of the rat tongue. Concerning the comparative morphological observation of FuPs, clearer partial or positional differences cannot be found on MVCS of FuP using SEM, but FuPs of the central part on the anterior portion of the rat tongue were relatively larger than those of the apical part and the two sides. A spatial distribution of rat FuP showed that a mean total number of 187 FuPs per tongue were present on the tongue surface, and FuP were absent on the dorsal midline, but a paracentral line of papillae running from the anterior to the posterior parts was a consistent finding (Miller and Prestar 1975). On the other hand, a quantitative study of taste buds in FuP and YaP of young and aged rats showed no difference in the number or size of taste buds in papillae on anterior and posterior areas of the tongue from the two age groups, and both FuP and YaP were larger in older rats (Mistretta and Baum 1983).

In this study, all FuPs on the three parts of the anterodorsal surface were sporadically and consistently scattered among the three types of ScP: ScP I, II, III. The SEM's microvascular morphological observation by means of MVCS of FuP showed that these distributive patterns and number of FuPs agreed with the reports above described (Miller and Preslar 1975; Mistretta and Baum 1984), but differed with regard to the size of FuPs. FuPs, regarded as taste sensory organs, were the same size and shape (Fig. 2: 1, 2, 5, 7) at the seven points in the three parts of the anterodorsal surface, except that FuPs on the central parts (Fig. 2: 3, 4, 6) were relatively larger in size and more cylindrical in shape.

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