of the mucous membrane of the oral cavity [Gairns, 1951, 1953, 1954; Gairns and Aitchison, 1950; Gairns and Garven, 1952], and deals with
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1 THE SENSORY NERVE ENDINGS OF THE HUMAN PALATE. By F. W. GAIRNS. From the Histology Division, Institute of Physiology, University of Glasgow. (Received for publication 10th August 1954) THE present study extends an earlier investigation into the innervation of the mucous membrane of the oral cavity [Gairns, 1951, 1953, 1954; Gairns and Aitchison, 1950; Gairns and Garven, 1952], and deals with the sensory nerve endings of the human hard and soft palates, including the uvula. There is little precise information about these tissues, especially in human material. The presence of a rich plexus of nerve fibres in the dermal tissue and of touch menisci (Merkel's discs) in the epithelium of the cat's palate was noted by Botezat [1901]. He also described [Botezat, 1906] the sensory endings found in the avian palate. Kadanoff [1927] has shown drawings of two types of dermal ending in the human palate, one of which exhibits straight unbranched fibrils (" ultraterminal ") entering the epidermis and passing to the outer layers of epithelial cells. Stohr [1951] stated that the human palate contains Meissner corpuscles, Krause end-bulbs and other endings which he left unspecified, but he has not given any illustrations of actual nerve endings observed in the palate. METHODS The tissues were obtained at early autopsies on 26 human subjects in whom the mucous membrane of the mouth appeared normal. The ages ranged from 17 to 62 years. After removal of the hard palate, soft palate and uvula in one piece, the specimens were partially divided by a series of transverse incisions and placed in 12 per cent neutral formalin. Fixation was for a minimum of 4 days: pieces of tissue were then washed for 5 min. in running tap water and sections, 15-20,u thick, cut on a freezing microtome. These sections were then carried through a modified Bielschowsky-Gros silver diammine ion method [Garven and Gairns, 1952] with varying time intervals to give different impregnations. Some of the tissue was embedded in paraffin, sections cut and stained with haemalum and eosin. 40
2 The Sensory Nerve Endings of the Human Palate 41 RESULTS Characteristic differences in the epithelium, dermis and associated glands occur in the three regions of the palate. The differences lie mainly in the number, size and form of the dermal papillke and in the distribution of the nerve endings associated with them: these are diagrammatically illustrated in text-fig. 1. HARD PALATE SOFT PALATE UVULA TEXT-FIG. 1.-The mucous membranes of the hard palate, soft palate and uvula as seen in transverse section. The epithelium is stippled, and the position and relative number of the organized endings are indicated by black ovals in the unstippled dermis. In the anterior part of the hard palate the numerous papille lie closely spaced: they are usually long, narrow and irregular in form. Towards the posterior part of the hard palate they become fewer, shallower and more regular in shape. In the soft palate they are even fewer and shallower and sometimes wider. In the uvula the pattern is similar to that of the soft palate though some of the papillae are narrower. The papillse of the uvula are the most vascular and those of the hard palate the least vascular. The number of "organized" nerve endings varies approximately with the number of papillae, and thus many more are to be found in the
3 42 Gairns hard palate than in the soft palate and uvula. The term "organized" is used here to mean "... any closely-knit and well-localized nerve termination (other than a simple terminal bead) whether or not it is surrounded by a connective tissue capsule " [Sinclair, Weddell and Zander, 1952]. Some of the nerve endings are formed from fibres that are thickly myelinated until the final node which lies very close to the ending; others are formed from fibres which are non-myelinated as far back from the ending as they can be traced. The thick myelinated fibre can be recognized when the myelin is stained, as well as the axon, as it is in many of the impregnations. In these instances the nodes can be seen and the Schwann cell nuclei do not bulge out from the side of the myelin sheath. The thinner myelinated fibre may, in light impregnations, not reveal its myelin or its nodes, but in a deeper impregnation these become obvious. Non-myelinated fibres are of smaller diameter, show no nodes even in deep impregnations, and the Schwann cell nuclei bulge out from the side of the fibre. A thick myelinated fibre near its termination changes its diameter abruptly and is continued on in one or more fibres, which are without nodes and decrease in diameter on branching; all these latter are regarded as non-myelinated branches. According to their position in the mucosa, the endings will be described in four groups: (1) Endings in the epithelium. (2) Endings in the dermal papillae. (3) Endings in the dermal papillae with extensions into the epithelium. (4) Endings in the dermis deep to the papillae. Hard Palate (1) In the epithelium, endings of the "free nerve ending" type have been found. Most commonly these arise from myelinated fibres which pass through the dermis almost to the epithelium before they divide into two or more non-myelinated lateral branches (P1. I, fig. 1). These branches may run closely applied to the basal edge of the epithelium for some distance and send fine short twigs into the epithelium. Here they become extremely delicate and finally ramify freely among the epithelial cells (P1. I, figs. 2a and b). On other occasions fine branches from non-myelinated fibres, which give rise to the dermal free endings, pass into the epithelium to form free endings there. In a few instances only have fine beaded fibres been observed in the epithelium. (2) The organized endings in the dermal papillwe vary in size and structure: they appear to have the same essential characters as those found in the human gum [Gairns and Aitchison, 1950] and in the human tongue [Gairns, 1953]. Typical Meissner corpuscles are only occasionally seen: the main myelinated fibre supplying these corpuscles is often accompanied by fine accessory fibres (P1. I, fig. 3). Another type of ending resembles the Meissner corpuscle but is less
4 The Sensory Nerve Endings of the Human Palate compact and less symmetrical; they usually occur in groups of up to five or six, all lying within one single large papilla (P1. I, fig. 4). Endings unencapsulated and simpler in structure are very common. They consist of the prolongation of one or two non-myelinated fibres which form a loose ending by simply turning and twisting on themselves several times (P1. I, figs. 5 and 6). In some instances the supplying fibre forms a complete ring on itself before the ending proper (P1. I, figs. 7 and 8). Other variations of this kind of ending show long flattened dispersions of their constituent neurofibrils. These netlike dispersions appear to be in fact the final termination of the ending (P1. II, figs. 9, 10, 11). Occasionally neurofibrillar elements occur in the coils of an ending (P1. II, fig. 12), or even in the course of the supplying fibre. Larger types of endings often take the form of whorls supplied by thick myelinated fibres (P1. II, figs. 13 and 14). The component fibres of these whorls are always thick and impregnate heavily with the silver. Endings of still another type are shown (P1. II, figs. 15 and 16). Fine accessory fibres are often seen accompanying the main fibres to these organized endings in the dermal papillhe. In some papillae no organized endings are present at all, but instead, numbers of nerve fibres of different calibres turn and twist in a complex pattern (P1. II, fig. 17). Still other papillae have fibres which run to their apices and loop back on themselves to re-enter the dermis below, without any break in their continuity (P1. III, figs. 18a and b). (3) Some endings in the dermal papillae are characterized by one or several fine unbranched extensions, "ultra-terminal" fibrils, which pass into the epithelium. Fibrils of this type have been observed in the human gum [Gairns and Aitchison, 1950] and tongue [Gairns, unpublished work]. So far as I am aware they have not been described for any other part of the body surface and they appear to be characteristic of the mouth. Endings which show these "ultra-terminal" fibrils belong to all the types of organized endings described in (2) above except Meissner corpuscles. Examples are shown in P1. III, figs In figs. 22 and 23 the fibrils show terminal beads. It is of interest that none of these fibrils appear to branch and that all take a direct course towards the oral surface. Some end at a point just short of the outer surface itself, and are only covered by the outermost layers of epithelium which are beginning to flake off. (4) In the connective tissues below the papillse fewer nerve endings occur. All those observed in this region are Krause end-bulbs and exhibit the usual features of such endings (P1. III, fig. 24, and P1. IV, figs. 25 and 26). Often several fine accessory fibres accompany the main myelinated nerve fibre to the bulb. One or two of these fibres may enter the bulb while some travel around the outside of the capsule, remaining in close association with it; others again pass upwards towards the epithelium or run perhaps up into the nearest papillae above the bulb. 43
5 44 Gairns Soft Palate Associated with the smaller number of papille in this region, organized endings are correspondingly fewer in number than in the hard palate. Those present resemble the endings of the hard palate except that none of them showed "ultra-terminal" fibrils passing from the ending up through the epithelial cells to the surface. This may be of functional significance. There is probably a relative increase in the number of Krause end-bulbs. Uvula This part of the palate has undoubtedly a pattern of innervation peculiar to itself. Very large numbers of small nerve bundles are present in the dermis, though not all of them are sensory. Many of them are the motor nerve fibres supplying the subjacent skeletal muscle. The sensory endings are different from those in the hard and soft palates, as almost all of them are supplied by nerve fibres which are of finer calibre, and within the ending the component fibrils are nearly always markedly beaded. Again, the uvula is much more vascular than the other regions of the palate, and with this is associated a correspondingly larger number of autonomic fibres. 1. The free endings in the epidermis covering the uvula are numerous. The fibres from which they arise are non-myelinated and show clearly the cells of Schwann. The fibre, before it branches to form the endings, either runs along parallel to the dermal-epidermal junction or arrives more directly from the deeper tissues. It then splits into several divisions which branch again frequently. The branches intertwine with one another over an extensive area but do not extend far up into the epithelium. From the point of their first branching they are beaded throughout (P1. IV, figs. 27a and b). 2. In the uvula practically all the organized endings are of the endbulb type. They lie close to the basal epithelial edge. Many of them do not lie in typical papille but in small indentations in the dermalepidermal junction. These endings vary little in structure and are usually small, but on occasions may be extremely large. Often they occur in clusters of two, three or more (P1. IV, figs. 28, 29, 30). The fibres supplying these bulbs are not of such large diameter as those supplying the organized endings of the hard palate. Inside the end bulbs the fibres are numerous and fine. They show in their most delicate branches a typical beaded appearance. The close application of the bulb to the basal surface of the epithelium makes it clear that these endings have little or no capsule. Some fibres from them may pass into the surrounding tissue and also into the epithelium.
6 The Sensory Nerve Endings of the Human Palate 3. In the uvula there are no endings with "ultra-terminal" fibrils running to the outer layers of the epidermis such as were observed in the hard palate. 4. No sensory endings were found in the deep part of the dermis corresponding to those found in this region of the hard palate. At this depth in the uvula large numbers of skeletal muscle bundles are present. In the silver-impregnated sections, throughout all regions of the palate, there is clear evidence of an autonomic ground plexus similar in pattern to that already described in the human nipple [Cathcart, Gairns and Garven, 1948] and in the human gum [Gairns and Aitchison, 1950]. In many cases the ground plexus is closely associated with the smaller blood vessels and capillaries (P1. IV, fig. 31). In all the sections of hard palate, soft palate and uvula prepared by the silver method, a careful search revealed no taste buds. This involved material from 22 individuals. As a control, four palates were imbedded in paraffin and serial sections made throughout their length. These hwemalum- and eosin-stained sections were systematically examined and not a single taste bud was found. One of the palates used for this serial sectioning was from a 21-year-old man. DIsCUSSION In the type and distribution of sensory endings the human hard and soft palates closely resemble the gum and also the tongue, except for the taste buds. The uvula, on the other hand, exhibits a different pattern. Here there is only one type of free nerve ending in the epithelium instead of two as in the hard palate; only one type of organized ending is found as opposed to a number of types; and the deeper layer of dermis has no organized sensory endings. The conventional correlation of the individual types of organized ending in the skin with the functions which they fulfil in cutaneous sensibility has in recent years been subjected to severe criticism. Sinclair et at. [1952] have shown that the four modalities, touch, pain, cold and warmth, are present in the hairy skin of the pinna of the human ear, and that the sensibility of this area of skin is of the same order as that of parts of the glabrous skin. They did not find, however, a single organized ending in the more than 30 sq. cm. of skin of the pinna, which they examined. Only free endings and peritrichial endings were found. In the palate, as in the mouth generally, very large numbers of organized endings are present. It would be easy to suggest a number of answers, but until more is known of the physiological behaviour of the various endings these can only be speculations. The plates show how varied and rich is the sensory innervation of the mnouth. In this investigation taste buds have not been found on the palate or uvula, either in the silver-impregnated sections or in the serial 45
7 46 Gairns hamalum- and eosin-stained sections. Schumacher [1927] also stated that von Ebner and Schaffer both searched through serial sections of the adult soft palate for taste buds but did not find any. Haycraft [1900] showed clearly that gustatory sensibility and areas where taste buds are present do not correspond. He actually mentions only the tongue and epiglottis as having taste buds. Hoffman [1875] and Ponzo [1907] worked on human foetal material and demonstrated a fairly wide distribution of taste buds on the palate. In the sevenmonth fcetus Tuckerman [1889] found rudimentary taste buds on the soft palate and uvula, but considered them smaller and more rudimentary than those of the tongue. I have, however, been unable to find any work showing illustrations of taste buds on the palate or uvula in the human adult. It is probable therefore that a wider distribution of taste buds is only present during early development. SUMMARY 1. The sensory nerve endings of the adult human hard and soft palates and of the uvula have been described. They consist of free nerve endings within the epithelium, of numerous organized endings mainly in the dermal papille, and of a few organized endings in the subpapillary region of the dermis. 2. The organized endings of the hard and soft palates show a general similarity in morphological character, but are more numerous in the former, where they also show "ultra-terminal" fibrils penetrating the epithelium. Those in the uvula are of one type, show no " ultraterminal" fibrils and exhibit fine beading in their component fibrils. 3. Most of the organized endings are of unnamed form. Typical Meissner corpuscles are infrequent, while Krause end-bulbs are relatively uncommon. Accessory fibres are found associated with all these types. No Pacinian corpuscles or endings of Ruffini or Golgi-Mazzoni types have been seen. 4. An autonomic ground plexus is present in the dermis of palate and uvula. 5. No taste buds have been found. ACKNOWLEDGMENTS My thanks are due to Professor R. C. Garry for his continued interest and helpful suggestions in this investigation. I am extremely grateful to Dr. H. S. D. Garven for so generously letting me have the benefit of his experience and guidance. To Mr. Donald McAllister my thanks are due for skilful co-operation in the preparation of the photomicrographs, also to Mr. R. Callander for the clarity of the text-figures and the photodiagrams. Expenses were defrayed by a grant from the Rankin Medical Research Fund of this University. The Carnegie Trust have kindly assisted in defraying the cost of the plates.
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12 The Sensory Nerve Endings of the Human Palate 47 REFERENCES BOTEZAT, E. (1901). Z. wi88. Zool. 69, 429. BOTEZAT, E. (1906). Z. wi88. Zool. 84, 205. CATHCART, E. P., GAIRNS, F. W. and GARVEN, H. S. D. (1948). Tran8. Roy. Soc. Edinb. 61, 699. GAIRNS, F. W. (1951). J. Physiol. 115, 70 P. GAIRNS, F. W. (1953). J. Physiol. 121, 33 P. GAIRNS, F. W. (1954). J. Phy8iol. 123, 26 P. GAIRNS, F. W. and AITCHISON, J. (1950). Dent. Ree. 70, 180. GARNS, F. W. and GARVEN, H. S. D. (1952). J. Physiol. 118, 53 P. GARVEN, H. S. D. and GAIRNS, F. W. (1952). Quart. J. exp. Phy8iol. 37, 131. HAYCRAFT, J. B. (1900). In SCHAFER, E. A. Textbook of Physiology, 2, Edinburgh and London: Pentland. HOFFMAN, A. (1875). Virchow's Arch. 62, 516. KADANOFF, D. (1927). Z. Zellforsch, 5, 615. PoNzo, M. (1907). Anat. Anz. 30, 529. SCHUMACHER, S. (1927). In MOLLENDORFF, W. Hand. Mik. Anat. 5, 1, 23. Berlin: Springer. SINCLAIR, D. C., WEDDELL, G. and ZANDER, E. (1952). J. Anat. Lond. 23, 402. STOHR, P. (1951). Lehrbuch der Histologie. Berlin: Springer. TUCKERMAN, F. (1889). J. Anat. Lond. 23, 559. DESCRIPTION OF PLATES PLATE I FIG. 1.-Myelinated nerve fibre dividing into two non-myelinated fibres which enter the epithelium and ramify around the epithelial cells. FIG. 2a.-Photomicrograph of thick non-myelinated branch of myelinated fibre running along the epidermal-dermal junction and giving off fine fibrils into the epithelium. FIG. 2b.-Photodiagram of same field to show full extent of fine fibrils ramifying between the epithelial cells. FIG. 3.-Meissner corpuscle in a dermal papilla. Note the fine accessory fibre accompanying the large myelinated fibre. FIG. 4.-Group of Meissner-like endings in a single dermal papilla. FIG. 5. A simple ending formed by a single nerve fibre. FIG. 6.-More extensive ending formed by two fibres but essentially the same type as fig. 5. FIGS. 7 and 8.-Single nerve fibres which coil on themselves before going on to form the actual endings. PLATE II FIGS. 9, 10, 11.-Nerve endings whose final termination is flattened dispersions of neurofibrillar elements. formed by long FIG. 12.-A large ending where the neurofibrillar elements have been cut transversely, forming little rosettes. FIGs. 13 and 14.-Examples of the whorl type of ending. FIGS. 15 and 16.-Endings of less compact form. FIG. 17.-A dermal papilla containing large numbers of fine non-myelinated fibres forming no discrete ending. Some of the fibres enter the epithelium and ramify among the cells. VOL. XL, NO. L
13 48 Gairns PLATE III FIG. 18a.-Photomicrograph to show non-myelinated fibres entering and leaving a papilla without forming any definite ending although branching may occur. Some branches pass into the epithelium. FIG. 18b.-Photodiagram of same field as fig. 18a. FIGs. 19, 20, 21.-Examples of "ultra-terminal" fibrils passing into the epithelium from endings in the dermal papillse. Fig. 21 shows the fibril apparently passing through an epithelial cell. FIGS. 22 and 23.-"Ultra-terminal" fibrils at greater magnification, to show terminal beads. FIG. 24.-A group of Krause end-bulbs in the dermis below the papillae. PLATE IV FIGs. 25 and 26.-Krause end-bulbs cut in different planes. In both instances fine accessory fibres can be seen accompanying the main supplying fibre. FIG. 27a.-Uvula. Photomicrograph of fine intra-epithelial beaded fibres. Schwann cell nuclei are prominent. FIG. 27b.-Uvula. Photodiagram of same field as fig. 27a. FIGS. 28, 29, 30.-Uvula. Examples of end-bulbs of varying sizes, lying in their typical site immediately below the epithelium. Note that their component nerve elements are markedly beaded. FIG. 31.-Uvula. Sympathetic ground plexus in close association with small blood vessels at the entrance to a dermal papilla.
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