An investigation was made of the precise origin of the efferent nerve terminals in the fungiform papillae of the bullfrog\u27s tongue. Some axonal enlargements originate from the parasympathetic postganglionic neurons in the glossopharyngeal nerve. Axonal enlargements containing large dense-cored vesicles (100-120 nm in diameter) and small, clear synaptic vesicles (50-60 nm in diameter) were in close contact with the supporting cell in the taste disk. These results seem to provide morphological evidence for the existence of an efferent control system in the taste disk of the bullfrog

INOUE KATSUHIRO

KITADA YASUYUKI

NAITO JUNPEI

OHKUBO YOSHINOBU

English

application/pdfAn investigation was made of the precise origin of the efferent nerve terminals in the fungiform papillae of the bullfrog's tongue. Some axonal enlargements originate from the parasympathetic postganglionic neurons in the glossopharyngeal nerve. Axonal enlargements containing large dense-cored vesicles (100-120 nm in diameter) and small, clear synaptic vesicles (50-60 nm in diameter) were in close contact with the supporting cell in the taste disk. These results seem to provide morphological evidence for the existence of an efferent control system in the taste disk of the bullfrog.journal articl

INOUE, KATSUHIRO

OHKUBO, YOSHINOBU

NAITO, JUNPEI

KITADA, YASUYUKI

Matsumoto Dental University Repository

(Original) Matsumoto Shigaku 20 : 274--279, 1994             key words:taste disk - frog - parasyrnpathetic inneryation - nerve terminalsExistence of the Parasympathetic Postganglionic Nerve Terminals in the Taste Disk of the Fungiform Papillae of the Bullfrog, Rana CatesbeianaLaborato7yKATSUHIRO INOUE and YOSHINOBU OHKUBOof Oral Structure and Function, Institute for Dental Science,Laborato7 y ofA ninzaJUNPEI NAITOl Stracture and Fzanction, SchoolDePartmentMatsumoto Dental Collegeof Agriculture, Nagoya UniversdyYASUYUKI KITADAof Oral Physiology, Ohayama University Dental SclaoolSummary       An investigation was made of the precise origin of the efferent nerve terminals in the    fungiform papillae of the bullfrog's tongue. Some axonal enlargements originate from the   parasympathetic postganglionic neurons in the glossopharyngeal nerve. Axonal enlarge-   ments containing large dense-cored vesicles (100-120 nm in diameter) and small, clear   synaptic vesicles (50-60 nm in diameter) were in close contact with the supporting cell in   the taste disk. These results seem to provide morphological evidence for the existence of   an efferent control system in the taste disk of the bullfrog.                                   Introduction   Efferent control of the gustatory system has been postulated from electron-physiologicalevidence (Brush and Halpern, 1970'), Chernetski, 19642), Esakov, 19614), Hellekant, 19715), Kimura,19619), Zaiko and Lokshima, 1962'5}), but there is inadequate morphological evidence for such aconclusion. The glossopharyngeal nerve of the frog consists of afferent nerve fibers originate fromthe jugular ganglion and efferent nerve fibers originate from the superior cervical ganglion (sympa-thetic nerve) or the medulla (parasympathetic nerve). After cutting of the glossopharyngeal nervetrunk above the jugular ganglion, degeneration nerve fibers were not found in the fungiformpapillae. On the other hand, when glossopharyngeal nerve trunk was cut under the jugular ganglion,most of the myelinated nerve fibers in the fungiform papillae were degenerating, but not unmyelinat-ed nerve fibers (Inoue and Kitada, 19917)). We also reported the existence of neurons within thelingual branch of the glossopharyngeal nerve and identified them to the parasympathetic postgang-lionic neurons (Inoue and Kitada, 1991')). These findings show that unmyelinated nerve fibers in the(accepted for publication on October 31, 1994)tE}Jztsitse}E 20(3) 1994 275fungiform papillae are efferent and originate from the parasympathetic postganglionic neurons.Furthermore, axonal enlargements of the remaining unmyelinated nerve fibers were in close contactwith the Merkel-like basal or supporting cells in the taste disk of the fungiform papillae (Inoue etal. 19928)). We examined experimentally whether remaining axonal enlargements in the taste diskare nerve terminals and originate from parasympathetic postganglionic neurons. We found that thenerve terminals originated from parasympathetic postganglionic neurons within the lingual branchof the glossopharyngeal nerve were present in the taste disk of the frog fungiform papillae.Materials and Methods   Fourteen bullfrogs (Rana catesbeiana) weighing 250-470 g were anesthetized by immersing in asolution of MS-222 (tricaine methanesulfonate, 2 g/liter). The glossopharyngeal and hypoglossalnerves were cut at the level of the angle of the mouth (Fig. IA). After surgery, frogs were killed onday 28 or 56 (group A), or on day 28 after the surgery, the lingual branches of the left glossopharyn-geal nerve were cut in the body of the tongue (Fig. IB) and then frogs were killed 7 days afteradditional nerve transection (group B). For electron microscopy, frogs were anesthetized with MS-222 and perfused through the heart with 100 ml of a mixture of 1% glutaraldehyde and 4%paraformaldehyde in O.1 M phosphate buffer, pH 7.4, for 10 minutes. After perfusion, the tongue ofthe left side was removed and cut into small pieces. Tissues were then immersed for 2 hours in thesame fixative at 4 OC and postfixed for one hour at room temperature in 1% Os04 dissolved in O.1M phosphate buffer, pH 7.4. They were treated for conventional electron microscopy.Fig. 1:a  PNFl}"O'Eil)iili[Li-lii.GIE,i}iis,,Drw"A:The glossopharyngeal nerves were cut at the level of the angle of the mouth. B:On day28 after the surgery A, the lingual branches of the Ieft glossopharyngeal nerve were cut inthe body of the tongue. 1 and 2, positions of the cut in the glossopharyngeal nerve; IX,glossopharyngeal nerve;X, vagus nerve;F, fungiform papilla;JG, jugular ganglion;PN,postganglionic neuron; R, rhomben cephalon ; S, sympathetic trunk ; T, tongue.GResults   After cutting of position 1 in Fig. IA, no signs of the degeneration were found on the axons inthe taste disk of the fungiform papillae. In the taste disk, the persisted axons were transformed intoirregularly shaped enlargements of varying sized and more distinct features. Some axons madeclose contact with the supporting cells in the taste disk. The enlargements of the axoplasm,276 Inoue et al. : Parasympathetic Nerve Terminals in the Frog Taste Diskprobably nerve endings, were filled with large dense-cored vesicles (100-120 nm in diameter) andsmall, clear synaptic vesicles (50-60 nm in diameter) (Figs. 2 and 3).    After cutting of position 1 and 2 in Fig. IB, clear signs of the degeneration were observed inaxonal enlargements in just under the taste disk or in taste disk of the fungifornn papillae. A largedense body, the accumulation of large dense-cored vesicle, and dissolution of the microtubularstructure, and disappearance of the synaptic vesicles were found in the degenerative axonalenlargements. Degenerative axonal enlargements also made close contact with the supporting cells(Figs. 4-7).fig. 2 : Twenty-eight days after cutting position 1 (see Fig. IA). Intact axons (*) in the taste disk      of a fungiform papilla. M, Merkel-like basal cell ; S, supporting cell. Bar=500 nm.Fig.3: Fifty-six days after cutting position 1. Axoplasmic enlargements (*) containing small,      clear synaptic vesicles and Iarge dense-cored vesicles in close contact with a supporting (S)      or taste cell (T) in the taste disk of a fungiform papilla. Bar:= 500 nm.Figs. 4-7 : Seven days after cutting of position 2 on day 28 after section position 1 (see Fig. IB). Fig.        4. Degenerating axons (*) just under the taste disk in a fungiforrn papilla. M, Merkel-        like basal cell. Bar = 500nm. Figs.5-7. Degenerating axoplasmic enlargements (*)        containing small, clear synaptic vesicles and large dense-cored vesicles in close contact        with a supporting (S) in the taste disk of a fungiform papilla. T, taste cell. Bar=500 nm.za2ts dvntt,`; 20(3) 1994 277278 Inoue et al. : Parasympathetic Nerve Terminals in the Frog Taste Disk                                      Discussion    After cutting of the glossopharyngeal and hypoglossal nerves of each side at the level of theangle of the mouth, some unmyelinated nerve fibers in the near or in the taste disk remained intact.These remaining unmyelinated nerve fibers were transformed into irregularly shaped enlargementof varying sized and more distinct features just under and within the taste disk. This is goodagreement with our previous findings (Inoue et al., 19928)). It is not likely that these persistentunmyelinated nerve fibers are sympathetic, although the glossopharyngeal nerve contains sympa-thetic nerve fibers. Because adrenergic nerve fibers, considered sympathetic nerve in nature,disappear from the fungiform papillae within 14 days after cutting of the sympathetic trunk (Inoueand Kitada, 19886)). These remaining unmyelinated nerve fibers were not afferent, since afferentnerve fibers originate from neurons in the jugular ganglion. They seemed to originate fromparasympathetic postganglionic neurons within the glossopharyngeal nerve under the jugularganglion (Inoue et al., 19928}). Axonal enlargements were found in the taste disk on 28 days aftercutting the glossopharyngeal nerve at the level of the angle of the mouth. Therefore, the characteris-tics of the remaining axonal enlargements are parasympathetic. Axonal enlargements containedlarge dense-cored and small, cleared synaptic vesicles. Axonal enlargements containing largedense-cored and small synaptic vesicles are similar to the synaptic endings, postulated to be efferentsynaptic endings from morphological criteria, in the taste organs of frogs (Nomura et al., 1975ii),Sbarbati et al., 1988i2), Witt, 1993i3}), mammals (Murray, 1971iO), Yoshie et al., 1990'`)) and fishes(Desgranges, 19663}). However, their characteristics were not described. Axonal enlargements of thepersistent unmyelinated fibers were filled with large dense-cored vesicle and small, clear synapticvesicles degenerated after cutting the lingual branches of the glossopharyngeal nerve in the body ofthe tongue. These findings show that axonal enlargements originate from parasympathetic postgan-glionic neurons within the lingual branch of the glossopharyngeal nerve. We found axonal enlarge-ments containing large sense-cored and small synaptic vesicles were in close contact with thesupporting cells in the taste disk. Therefore, our results strongly suggest that they are parasympa-thetic nerve terminals. These results seem to provide morphological evidence for the existence ofa parasympathetic efferent control system in the taste disk.                                      References1) Brush, A. D. and Halpern, B. P. (1970) Centrifugal control of gustatory responses. Physiol. Behav. 5:743   -746.2) Chernetski, K. E. (1964) Sympathetic enhancement of peripheral sensory input in the frog. J. Neuro-   physiol. 27 : 493-515.3 ) Desgranges, J. C. (1966) Sur la double innervation des cellules sensorielles des bourgeons du gout des   barbillons du Poisson-chat. C. R, Acad. Sc. Paris, 263 : 1103-1106.4 ) Esakov, A. I. (1961) Concerning the efferent control of receptors. Biull. Eksp. Biol. Med. USSR, 51 : 3-8.5 ) Hellekant, G. (1971) The effect of stomach distension on the efferent activity in the chorda tympani   nerve of the rat. Acta Physiol. Scand. 83 : 527-531.6 ) Inoue, K. and Kitada, Y. (1988) On the origin and course of sympathetic nerve fibers in the fungiform   papillae of the frog's tongue. Okajima Folia Anat. Jpn. 65 : 171-176.7) Inoue, K. and Kitada, Y. (1991) Parasympathetic postganglionic cells in the glossopharyngeal nerve   trunk and their relationship to unmyelinated nerve fibers in the fungiform papillae of the frog. Anat,   Rec. 230 :131-135.8) Inoue, K., Yamaai, T. and Kitada, Y. (1992) Parasympathetic postganglionic nerve fibers in theX!ZtJ4sitsE=iitl 20(3) 1994 279  fungiform papillae of the bullfreg, Rana catesbeiana. Brain Res. 596 : 299-304.9 ) Kimura, K. (1961) Factors affecting the response of taste receptors of rat. Kumamoto Med. J. 14 : 95  -99.10) Murray, R. G. (1971) Chapter 2. Ultrastructure of taste receptors. In L. M. Beidler (Ed.) Handbook of  SensoryPhysiology Vol.IV ChemicalSensesPart2 pp.31-50. Springer-VerlagBerlin, Heidel-  berg.11) Nomura, S., Muneoka, Y., and Kanno, Y. (1975) The ultrastructure of taste organs of a frog (Rana  Catesbeiana)-three types of synapse and junctions between taste cells. Jap. J. oral Biol. 17 : 371-384.12) Sbarbati, A., Franceschini, F., Zancanaro, C., Cecchini, T., Claroni, S. and Osculati, F. (1988) The fine morphology of the basal cell in the frog's taste organ. J. Submicrosc. Cytol. Pathol. 20 : 73-79.13) Witt, M. (1993) Ultrastructure of the taste disc in the red-bellied toad Bombina orientalis (Discoglos- sidae, Salientia). Cell Tissue Res. 272: 59-70.14) Yoshie, S., Wakasugi, C., Teraki, Y. and Fujita, T. (1990) Fine structure of the taste bud in guinea pigs. I. Cell characterization and innervation patterns. Arch. Histol. Cytol. 53 : 103-119.15) Zaiko, N.S. and Lokshima, E.S. (1962) The reflex reaction of gustatory receptors of the tongue in direct stimulation of gastric receptors (or receptors of the stomach). Bull. eksp. Biol. Med. 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Existence of the Parasympathetic Postganglionic Nerve Terminals in the Taste Disk of the Fungiform Papillae of the Bullfrog, Rana Catesbeiana

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