From the Anat. Labor. of Prof. H. SETO, Tohoku University, Innervation of Radical Part of Tongue of Hedgehog.

Transcription

1 From the Anat. Labor. of Prof. H. SETO, Tohoku University, Sendai. Innervation of Radical Part of Tongue of Hedgehog. Many histological studies on the innervation, especially on the sensory innervation, of the mucous membrane of the tongue have been reported in the past, e. g., by CIVALLERI (1908), KOLMER (1921), ABRAHAM (1930), SZYMONOWICZ (1937), HASHIZUME (1938) and KADOTA (1939) among others. Recently, OKANO (1953) has made an especially exhaustive study, with dog tongue as material, giving a good illumination on the subject. ABE et al. (1954) also reported on their study on the innervation of the apex linguae of hedgehog. The innervation of human tongues was thoroughly elucidated by the recent studies by KUMAGAWA (1941), NAKAYAMA (1943), INAZAWA (1949) and OHGAKI (1953). However, the above studies mostly were related to the fore and middle parts of the tongue, only INAZAWA (1949) being accredited with a study on the posterior part of a human tongue. In consideration of such a lack in the study of the innervation of the radix linguae, I took the material of my study from that part of hedgehog tongues, and utilizing the latest improvement in the silver method, undertook to make a study to throw light on the innervation in this part, to clarify its biological significance in collation with the results obtained in the study of human tongues. The materials were fixed for a long time in 10% neutral formol and cut into series of frozen sections, which were stained with SETO's impregnation. These series of beautifully stained preparations I subjected to minute microscopic examination and arrived at the observations outlined in the following. I. Individual Observations. There have been very little written on the fine structure of the posterior part of the hedgehog tongue, but as such a figure has a very close bearing on the elucidation of its innervation, I will preface my observations on its innervation with a histological picture thereof. The posterior part of the tongue to the back of the sulcus terminalis, that is, the radix linguae, is smoothly surfaced with a noncornified stratified flat epithelium, which increases in height as the lateral edges are approached starting from the median line. In hedgehog,

2 72 N. OHTOMO: as in man and other mammals, the epithelium of the papillae vallatae and foliatae, and in special frequency of the papillae fungiformes in the posterior part of the tongue is psovided with taste-buds. In a far smaller number, taste-buds are also found in the epithelium of the radix linguae, as is the case with the human tongue (INAZAWA 1949). No lingual papilla is found in the radix linguae and the common mucous papillae into the epithelium are also worse developed as we go farther back, being represented by small sporadic existence in the hindermost part. The glandular formation consists of purely serous glands beneath the vallate and foliate papillae and purely mucous glands in the radical part. It is of deep iuterest that the radix linguae of hedgehog is very poor in the development of the lymphatic tissue. No formation of lingual follicles as seen in human tongue is found by hedgehog, only sporadic lymphocytes being observed in the lamina propria. The nerve elements entering the above described histological figure of the posterior part of the tongue consist of sensory nerves coming from the rami isthmi faucium of the third branch of the n. trigeminus, the rami linguales of the n. glossopharyngicus and the rami pharyngici of the n. vagus, of motor nerves from the n. hypoglossus and of vegetative nerves, in particular, of sympathetic nerves originating chiefly in the ganglion sphenopalatinum. These nerve elements run into the muscular and glandular layers from the adventitia in bundles of various sizes and penetrate into the propria mucosae to form proprial plexus there, forming also rather gross plexus in their course. Such gross plexus is most typically formed in the mucous glandular layer of the radix linguae. The proprial plexus is composed of thick medullated sensory fibres and fine unmedullated vegetative fibres. In this plexus are found small groups of ganglion cells, but such groups are more abundant in the nerve bundles running through the muscular and glandular layers. These ganglion cells are very small and spherical in shape, and are multipolar, having very hard-to-stain processes, clearly belonging to sympathetic nerve system in nature, quite alike those found in human lingua (NAKAYAMA 1943; INAZAWA 1949), larynx (SASAKI 1943), pharynx (SATO 1952), and canine tongues (OKANO 1953), as shown in Fig. 1. That the termination of the vegetative fibres consists of a widespread terminalreticulum (STOHR) formed by reticular cords of extremely fine fibrils, as STOHR (1932), REISER (1932), SETO (1935) and other modern meurologists have demonstrated, and not of free endings, as has been presumed hitherto, has been proved beyond doubt in my specimens of hedgehog tongue too. Here, the vegetative nerve bundles composed of sympathetic fibres coming into the posterior part of the tongue, the

3 Innervation of Radical Part of Tongue of Hedgehog. 73 Fig. 1. Multipolar ganglion cells in a nerve bundle running through the mucous glands layer of radix linguae of a hedge- parasympathetic fibres originating in the glossopharyngeal nerve, and the vegetative fibres represented by the long processes from the nerve cells in the radix linguae, ramifying and mutually anastomosing here and there, gradually divide into smaller and smaller branches, and nerve fibres therein finally through preterminal fibres end in the vegetative terminalreticulum, which exercises tactile control over the various cells and tissues with which it comes into contact. Such a figure was clearly observed also in my tongues of hedgehogs. Next I will give a description on the sensory nerve fibres and their terminations distributed in the posterior part of the tongue. To begin with the nerves for the circumvallate and foliate papillae, the fine structure of the circumvallate papillae on the tongue of hedgehog shows that their epithelium is a non-cornified, stratified flat epithelium, somewhat taller on the surface facing the oral cavity than on the sides facing the circumvallating fissure, and that the former surface epithelium contains taste-buds in rare cases, resembling the case in canine tongue (OKANO 1953), as shown in Fig. 2. The scarcity of taste-buds is even greater in hedgehog than in dog. In the circumvallate papillae in dog there are found a few rather deep fissures cut into the central part of the papillar trunk from the top surface of the papilla, but in hedgehog, these fissures are shallow, the epithelium lining these fissures, however, being far thicker than the so-called gemmal epithelium and devoid of taste-buds, similar to the case in dog. In human tongue, the epithelium of the wall facing the circumvallating fissure is always provided with taste-buds but neither in dog nor in hedgehog the epithelium of the wall has taste-buds. In the foliate papillae, taste-buds are found in the gemmal epithelium lining the side fissure and also that facing the oral

4 74 N. OHTOMO: Fig. 2. A papilla circumvallata of hedgehog. Vertical section. The distribution of the nerve fibres from the basal plexus into the papillar trunk is represented in cavity. The structure of the deeper parts of these two kinds of papillae is similar in man, dog and hedgehog. Serous glands are well developed in the muscular layer beneath the papillae, with their ducts generally opening into the bottom of the fissure. Interesting enough, some serous glands are also found in the papillar trunk. At the base of the circumvallate and the foliate papillae is formed well-developed basal plexus (Fig. 2), consisting of medullated sensory fibres of various sizes and much thinner unmedullated vegetative fibres of a smaller number. In this plexus are found REMAK's semi-ganglion cells similar to those in human and canine counterparts. The development of the plexus is much weaker than that in human and a little poorer than that in canine tongue. The sensory fibres from the basal plexus in most cases run into the papillar trunk in company with vegetative fibres and thence into the subepithelial layer, to end there in unbranched or simple branched terminations with a few terminal branches. All the terminal branches end in sharp points (Figs. 3 and 4). It is noteworthy that the terminal formation is somewhat more complex in a foliate papilla than in a circumvallate papilla. No such corpuscular terminations as NAKAYAMA (1943) has found in the secondary papillae in the large tongue papillae in man were observable in the hedgehog tongue. According to NAKAYAMA (1943), intraepithelial fibres formed in the epithelium of the surface facing the oral cavity by fibres running up from the subepithelial connective tissue are provable in human circumvallate papillae only in embryonic specimens, in human foliate

5 Innervation of Radical Part of Tongue of Hedgehog. 75 Fig. 3. Unbranched and simple branched sensory terminations ending directly beneath the epithelium facing the oral cavity of a papilla circumvallata of hedgehog. t vegeta- taste-buds in these papillae are far poorer in development in hedgehog than in man and somewhat below that in dog. Sometimes reduced to 2/3. no sensory temination is formed at all underneath a taste-bud. In man and dog, the development of sensory terminations seems to be somewhat better in foliate than in cicumvallate papillae, but in hedgehog I found no appreciable difference between the two. The terminal formation in hedgehog is in most cases of unbranched or extremely simple branched types, in rarer cases of somewhat more complex plexuslike type (Fig. 6). located near the basis of the tastebuds, no such typical glomepapillae, none, either in adults or embryos, and frequently found in the two kinds of papillae in dog (OKANO 1953), but in my tongues of hedgehogs, I often found them in the rather thin epithelium lining the oral cavity with a cornified plate of the foliate papillae, but none in the circumvallate papillae (Fig. 5). These intraepithelial fibres always terminate in simple unbranched endings. The vegetative fibres running into the papillae come into frequent complicated anastomosis and finally go over into the STOHR's terminalreticulum (Fig. 3). The sensory fibres to the Fig. 4. Unbranched and branched sensory terminations found beneath the epithelium facing the oral cavity of a papilla foliata of a hedgehog. Same staining.

6 76 N. OHTOMO: Fig. 5. Unbranched intraepithelial nerve Fig. 6. A plexus-like sensory termination fibres seen in the epithelium facing the composed of thick and thin fibres oral cavity of a papilla foliate of a formed in the basis of a taste-bud seen in the epithelium facing the oral cavity of a foliate papilla of a hedgehog. rular termination as frequently found in human tongue being ever observed. However. intra- or extragemmal fibres are not rare (Fig. 7). Fig. 7. Sensory nerve fibres for the taste-buds in a papilla circumvallata of a hedgehog. These penetrate into the epithelium of the taste-buds, to end in unbranched or branched terminations with a few branches. Same

7 Innervation of Radical Part of Tongue of Hedgehog. 77 These terminate in unbranched sharp endings but never in nodular form as is often the case in human tongue. The fungiform papillae in the posterior part of the tongue are larger than those in its anterior part (ABE et al. 1954) but in fine structure, the both are quite alike. Nothing different in essence from those in man (NAKAYAMA 1943) and dog (OKANO 1953), the papillar trunk protrudes strongly into the epithelium, extremely minute secondary papillae are formed and the epithelium is very thin. The surface layer of the epithelium consists of a thin cornified plate formed by nucleated flat epithelial cells. In the epithelium facing the oral cavity taste-buds are frequently found. The fungiform papillae are very similar in hedgehog and dog. The innervation of such papillae in the posterior part of the tongue of hedgehog is also very similar to that of dog and that in the anterior part of the tongue as described by ABE et al At their basis, basal plexus is formed, though in a considerably poorer development than in the case of circumvallate papillae. The medullated sensory fibres from this plexus, together with fine vegetative fibres, penetrate into the papillar trunk in bundles and spreading out fan-wise, terminate directly beneath the epithelium or oftener in the secondary papillae. The sensory terminations are here also represented by unbranched and simple branched endings of a few branches, corpuscular terminations, such as found in human tongue, being entirely absent. Intraepithelial fibres are more abundant in the fungiform papillae in the posterior part of the tongue than those in its anterior part (ABE et al. 1954) and are generally of very simple formation, almost without branches. The sensory innervation of the taste-buds found in their epithelium facing the oral cavity is poorer than in the cases of circumvallate and foliate papillae, though in rare cases, intra- and extragemmal fibres are observable. Finally, in the mucous membrane of the radix linguae lying posterior to the sulcus terminalis, sensory nerves are distributed as follows. In this part, the development of the common mucosal papillae being poorer in the hindermost part, the sensory innervation is expected to become weaker as the posterior extremity is approached. According to INAZAWA 1949, however, in human tongue, the sensory nerve terminations are rather well developed in spite of the poor formation of the mucosal papillae in this part. In my hedgehogs, however, the sensory terminations in the radix linguae were very small in number and very simple in formation in most cases, as could be anticipated from the weaker development of the mucosal papillae. Of all the sensory terminations found in the radix linguae of hedge-

8 78 N. OHTOMO: Fig. 8. A simple branched sensory termination seen directly beneath the epithelium of the hog, unbranched and simple branched terminations with a few branches (Figs. 8 and 9) represent the largest majority. The medullated sensory fibres that penetrate into the propria run thence into the papillae in most cases, and after losing their myelin, end sharply in unbranched or simple branched terminations, in rare cases sending out 4-5 branches. posterior part of radix linguae of a hedgehog. Since the mucosal papillae are taller in the anterior part of the tongue root, the sensory terminations are there better developed, rather complex branched endings with several branches being more frequent here. As a type of complex terminations I may name the special terminations of indeterminate shape. This is a sort of strongly developed very peculiar termination found only in a limited area around the foramen caecum in the anterior part of the tongue root, but never in other parts of the tongue. Such a termination was not found in canine tongue (OKANO 1953), but in human radix linguae some similar formations of plexus-like terminations were observed (INAZAWA 1940). What is of interest is that these terminations are morphologically more similar to the special sensory terminations found in a great number in the tarsus in human eye-lid by SETO 1954 than anything Fig. 9. A somewhat complex branched sensory termination seen in a mucous papilla of radix linguae of a hedgehog. Same stain-

9 Innervation of Radical Part of Tongue of Hedgehog. 79 else. In form, these terminations belong to the branched type, but there is utterly nothing definite about the number and arrangement of their branches. The nature of the fibres composing them is also very peculiar. The trunk fibres are especially stout and the branches show peculiar change in size in their meandering courses, showing fibril dissolution here and there. As exemplified in Figs. 10 and 11, a thick sensory fibre comes into Fig. 10. A special branched sensory termination composed of very strong nerve fibres found in the vicinity of the foramen caecum of a hedgehog tongue. Details in the text. Fig. 11. Ditto. the subepithelial connective tissue, especially in a part close to the glandular layer, which branches out into several. branches, the latter

10 80 N. OHTOMO: again dividing out into numerous sub-branches, in an utterly irregular arrangement. The branches and sub-branches are represented by thick fibres showing remarkable change in size and end in blunt or sharp points. In their courses, these fibres sometimes show fibril swellings. II. Summary. The epithelium of the papilla circumvallata in hedgehog tongue is of noncornified stratified flat type, and is taller on the surface facing the oral cavity than on the sides lining the circumvallating fissure, being provided with occasional taste-buds. On this top surface are found a few grooves sunk into the papillar trunk. No taste-bud is found in the epithelium lining such grooves. These findings are similar to those in dog, but in proportions the former are somewhat smaller than the latter. No taste-bud is formed in the epithelium lining the wall of the circumvallate fissure, as is the case in dog. In the papilla foliata, taste-buds are found in the epithelium facing the oral cavity as well as in the gemmal epithelium lining the side fissure, as in dog. Nerve plexus consisting of thick medullated sensory fibres and thin unmedullated vegetative fibres is found at the basal part of the circumvallate and foliate papillae, as in human and canine tongues, but in development, that in hedgehog is poorer than that in dog. The sensory fibres enter the papillar trunk and go up close to the epithelium to end there in unbranched and simple branched terminations. Nowhere can be found anything resembling the complex corpuscular terminations found in human tongue. Intraepithelial fibres are found in a small number in the epithelium facing the oral cavity of papilla foliata but never in the same place of the papilla circumvallata. Such intraepithelial fibres are unbranched. The development of sensory fibres to the taste-buds in the two kinds of papillae above is somewhat lower in a hedgehog than in a dog. The terminations are generally unbranched or simple branched. Extraand intragemmal fibres are not very rare and are in general represented by unbranched terminations. The fungiform papillae in the posterior part of hedgehog tongue are morphologically similar in essence to those in man and the sensory innervation thereof resembles closely to the case in dog. Basal plexus of weak development is formed at the basis of the papillar trunk, from which sensory fibres reach out close to the epithelium and end there in unbranched or simple branched terminations. Intraepithlial fibres are often found in the epithelium facing the oral cavity provided with a thin corneate plate. The development of the sensory fibres for the tastebuds is somewhat weak, but intra- and extragemmal fibres are not rare

11 Innervation of Radical Part of Tongue of Hedgehog. 81 here also. In the mucous membrane of the radix linguae posterior to the sulcus terminalis, almost no lymphatic tissue as seen in human tongue is observable. The formation of mucosal papillae to the epithelium in this part is also very poor. The development of sensory fibres here is proportionately poor, their terminal formation being small in number and unbranched or simple branched in type. However, as the development of mucosal papillae is better in the anterior part of radix linguae, the sensory fibres are also richer in number and their terminations are more complex there. In particular, in the vicinity of the foramen caecum there are found very peculiarly shaped, strongly developed terminations of indefinite form deserving special mention. They are morphologically very near to the special sensory terminations found by SETO in the tarsus of human eye-lid. They belong to the branched type of endings, but the number and the arrangement of the branches is utterly undefinable. The fibres also show very peculiar characteristics, the trunk fibres being very stout in general, the branches showing peculiar change in size and frequent fibril dissolutions in their meandering courses, finally to end in sharp or blunt points.

12 82 N. OHTOMO. References. Abe, Endo a. Gotoh: Tohoku J. exp. Med. In press. -Abraham: Z. Zellforsch. 11 (1930). S Civalleri: Anat. Anz. 33 (1908). S Hashizume: Kaibo. Z. 12 (1938). P Inazawa: Tohoku Igaku Zassi. 42 (1949). P Kadota: Nihon Byori-Gakkaishi. (Jap.) 29 (1939). P Kolmer: Anat. Anz. 54 (1921). S Kumagawa: J. orient. Med. 34 (1941). P Nakayama: Tohoku Igakn Zassi. 33 (1943). P. 447 a. 473; 34 (1944). P Ohgaki: Tohoku J. exp. Med. 57 (1953). P Okano: Tohoku J. exp. Med. 57 (1953). P Reiser: Z. Zellforsch. 15 (1932). S Sasaki: Tohoku Igaku Zassi. 32 (1943). P a Sato: Tohoku Igaku Zassi. 46 (1952). P. 517 a Seto: Z. Zellforsch. 22 (1935). S Arch. hist. jap. 5 (1953). P Stohr: Z. Zellforsch. 16 (1932). S. 123; 29 (1939). S Szymonowicz: Z. Zellforsch. 25 (1937). S. 160.