57. Trajectory o f Primary Vestibular Fibers Originating f rom the Lateral, Anterior, and Posterior Semicircular Canals in the Cat
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1 No. 7] Proc. Japan Acad., 58, Ser. B (1982) Trajectory o f Primary Vestibular Fibers Originating f rom the Lateral, Anterior, and Posterior Semicircular Canals in the Cat By Haj ime MANNEN, Sei-ichi SASAKI, and Norio ISHIZUKA Third Department of Anatomy, Faculty of Medicine, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113 (Communicated by Teizo OGAWA, M. J. A., Sept. 13, 1982) Introduction. Previous studies with Golgi methods or degeneration techniques have shown that primary vestibular fibers as a whole project to all the four major vestibular nuclei2~'9 and to a restricted region in the cerebellumj>>6~ It has also been reported that fibers originating from each semicircular canal-the lateral, anterior, and posterior-have different terminal distributions in the vestibular nuclei.2"7 > However, precise morphology of the course of each primary fiber and the pattern of its branching have not been investigated at the single neuronal level. A study combining the recently developed intracellular staining with horseradish peroxidase ( HRP ) with three-dimensional reconstruction in serial sections has made it possible to reveal the axonal trajectory of physiologically identified single neurons, as far as their terminals.4> In the present study this method has been applied to primary vestibular afferents originating from the lateral, anterior, and posterior semicircular canals. Methods. Experiments were performed on adult cats anesthetized with ketamine hydrochloride (initial dose of mg/kg, i.m. ) and additionally with pentobarbital sodium (15-20 mg/kg, i.p.). Stimulating electrodes were implanted on the ampullary nerve of each canal according to the techniques described by Suzuki et al.8 The animal was paralyzed with pancronium bromide under artificial respiration with room air. A glass microelectrode filled with a 10% solution of HRP (Toyobo, Grade I C Japan) in 0.2 M KCI, buffered to ph 8.0, was used for both intraaxonal recording and staining. The axons were penetrated in the region immediately lateral to the lateral vestibular nucleus and physiologically identified as primary vestibular afferents by observing their direct activation following stimulation of each ampullary nerve. HRP was injected into the identified axons by iontophoresis. The animals were sacrificed hr after HRP injection. The general procedures for HRP reaction and reconstruction of axonal trajectory were fully described in a previous paper.4~ Results and conclusion. Reconstructions of the axonal trajectory were made for nine successfully stained fibers: 4 from the
2 238 H. MANNEN, S. SASAKI, and N. ISHIzuKA [Vol. 58(B), horizontal canal, 2 from the posterior canal, and 3 from the anterior canal. In the root bundle within the brain stem, afferents from the horizontal and anterior canals were in the rostral part, and those from the posterior canal were in the caudal part. All fibers gave off one collateral to the interstitial nucleus of Cajal situated in the vestibular root bundle, and distributed terminals in the nucleus (Figs. 1-3). The afferents then entered the ventrolateral region of the lateral vestibular nucleus, where they bifurcated into ascending and descending branches, as described by Held,3~ Koelliker,5~ and Cajal. ~ The ascending branch ran rostrodorsally in the ventral part of the lateral nucleus and entered the superior vestibular nucleus. The descending branch turned caudally in the ventral part of the lateral nucleus and entered the inferior vestibular nucleus. In the superior nucleus the ascending branch issued several collaterals and from these fine terminal branches. When observed in the medio-lateral direction, all canal fibers distributed terminals mainly in the middle part of the nucleus. In the rostro-caudal direction, however, there was a difference in terminal distribution area among the three kinds of canal fiber : Terminals of fibers from the horizontal and anterior canals were distributed in the whole rostrocaudal extent of the nucleus, but those from the posterior canal were found only in the caudal half of the nucleus (Figs. 1-3). Each canal fiber issued a single collateral which left the superior nucleus and entered the brachium conj unctivum. It passed caudally through the ventral part of this peduncle. Unfortunately, the faint staining prevented us from pursuing its final destination in the cerebellum. In the lateral nucleus, collaterals were issued from the ascending branch as well as the descending branch. These collaterals, on the way to the medial vestibular nucleus, gave off several fine branches which distributed terminals mainly in the border region between the lateral and medial nuclei. Few terminals were observed in the dorsal part of the lateral nucleus. The descending branch passed caudally through the ventral region of the inferior nucleus. Several collaterals emerged at various intervals from the descending branch, ran medially keeping parallel to one another, and reached the medial nucleus. In the inferior and medial nuclei, the descending branches and their collaterals of the posterior canal nerve ran dorsally, and those of the horizontal and anterior canal nerves were situated ventrally near the reticular formation. In the medial nucleus, collaterals reached the medial part of the nucleus and some of them turned their course caudalward. Terminal arborizations were most densely found in the medial part
3 No. 7] Trajectory of Primary Vestibular Fibers in th e Cat 239 Fig. 1. Reconstruction of the ramifications of a primary vestibular afierent originating from the horizontal canal. Horizontal view. Hatched ellipse represents the injection site of HRP. Arrowhead indicates the collateral towards the cerebellum. TNT, interstitial nucleus of Cajal; SV, superior vestibular nucleus; LV, lateral vestibular nucleus; IV, inferior vestibular nucleus; MV, medial vestibular nucleus; G, facial genu. of the inferior nucleus and the lateral part of the medial nucleus, although some of them were scattered widely in the two nuclei. Each collateral gave rise to a number of fine branches which distributed terminals in a relatively narrow region around the collateral, where axosomatic and axodendritic (proximal parts) contacts were observed between the stained terminals and a number of small and medium-sized neurons. Terminal regions of neighboring collaterals did not overlap each other.
4 240 H. MANNEN, S. SASAKI, and N. ISHIZUKA [Vol. 58(B), Fig. 2. Reconstruction of the rami afferent from the anterior canal. abbreviations as in Fig. 1. v fications of a primary vestibular Horizontal view. Symbols and In conclusion, the trajectories of single primary vestibular fibers originating from three different canals were very similar as to bifurcation into ascending and descending branches and the existence of terminals in the four major vestibular nuclei and the interstitial nucleus of Cajal. However, there were significant differences among fibers of different canals as to their axonal course in the brain stem and the sites of terminal distribution in each vestibular nucleus. Acknowledgements. We should like to thank Professor Shimazu for critically reading the manuscript, Mrs. Taguchi and Miss Koizumi for preparing the histological material, and Miss Higuchi for secretarial assistance. This study was supported by Grants-in-Aid for
5 No. 7] Trajectory of Primary Vestibular Fibers in the Cat 241 Fig. 3. Reconstruction of the afferent from the posterior abbreviations as in Fig. 1. ramifications of a primary vestibular canal. Horizontal view. Symbols and Scientific Research Nos and from the Japan Ministry of Education, Science, and Culture. References 1) 2) 3) 4) 5) Brodal, A., and Hoivik, B.: Arch. ital. Biol., 102, 1-21 (1964). Gacek, R. R.: Acta oto-laryng., suppl., 254, 1-66 (1969). Held, H.: Arch. Anat. Physiol., (1892). Ishizuka, N., Mannen, H., Hongo, T., and Sasaki, S.: J. Comp. Neuro., 1$6, (1979). Koelliker, A.: Handbuch der Gewebelehre des Menschen. Wilhelm Engel-
6 242 H. MANNEN, S. SASAKI, and N. ISHIZUKA [Vol. 58(B), man, Leipzig, Band II, pp (1896). 6) Ramon y Caj al, S.: Histologie du systeme nerveux de l'homme et des vertebras. Maloine, Paris, Tome I, pp (1909). 7) Stein, B. M., and Carpenter, M. B.: Am. J. Anat., 120, (1967). 8) Suzuki, J.-I., Goto, K., Tokumasu, K., and Cohen, B.: Ann. Otol., 78, (1969). 9) Walbe.rg, F., Bowsher, D., and Brodal, A.: J. Comp. Neur., 110, (1958).
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