Morphology of single primary vestibular afferents originating from the horizontal semicircular canal in the cat

The central projections of physiologically characterized vestibular nerve fibers originating from the horizontal semicircular canal were studied in the vestibular nuclei of adult cats after intracellular staining with horseradish peroxidase (HRP). First, primary nerve fibers were physiologically classified as regular or irregular types on the basis of the regularity of the spontaneous discharge pattern. Then, these two types of fibers were morphologically analyzed and compared following HRP intraaxonal injection. The two types of axons showed a basically similar trajectory in the four major vestibular nuclei. They bifurcated into an ascending and a descending branch in the ventrolateral part of the lateral vestibular nucleus (LVN). The ascending branch extended rostrally and gave off one or two collaterals in the superior vestibular nucleus (SVN), although some of the ascending branches further ran rostrally into the cerebellum. The collaterals, while running medially, gave rise to fine terminal branches with en passant boutons in the SVN, and further coursing caudally, they entered the rostral part of the medial vestibular nucleus (MVN). The descending branch, while running caudally in the lateral part of the LVN and the inferior vestibular nucleus (IVN), gave off several thick collaterals to the MVN and extensive terminals were present in the IVN and MVN. In each primary axon, about one‐third of the total terminal boutons were distributed in each of the SVN, the MVN, and the IVN. In contrast to this similarity of the overall axonal trajectory within the vestibular nuclei, both types of axons exhibited several marked differences in diameter and in the mode of terminal arborization. In almost every part of the ramification, the irregular‐type fibers were thicker than the regular‐type fibers. In the regular‐type axons, many small terminal boutons (mean size, 2.4 × 1.4 μm, N = 2,739) were located in close proximity (100–150 μm) to the parent collateral. In the irregular‐type axons, slightly larger terminal boutons (mean size, 3.0 × 1.7 μm, N = 1,287), were spread more widely (200–300 μm) around their collaterals. These clear morphological differences between the regular‐type and the irregular‐type terminal axons were consistently observed in any vestibular nucleus.

[1]  Ramón y Cajal,et al.  Histologie du système nerveux de l'homme & des vertébrés , 1909 .

[2]  E. Rouiller,et al.  Central projections of intracellularly labeled auditory nerve fibers in cats: Morphometric correlations with physiological properties , 1988, The Journal of comparative neurology.

[3]  O. Pompeiano,et al.  The vestibular nuclei in cat. , 1957, Journal of anatomy.

[4]  A. Brodal,et al.  SITE AND MODE OF TERMINATION OF PRIMARY VESTIBULOCEREBELLAR FIBRES IN THE CAT. AN EXPERIMENTAL STUDY WITH SILVER IMPREGNATION METHODS. , 1964, Archives italiennes de biologie.

[5]  J. Goldberg,et al.  Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. 3. Variations among units in their discharge properties. , 1971, Journal of neurophysiology.

[6]  D. Bowsher,et al.  The termination of primary vestibular fibers in the vestibular nuclei in the cat. An experimental study with silver methods , 1958, The Journal of comparative neurology.

[7]  G. Korte,et al.  The brainstem projection of the vestibular nerve in the cat , 1979, The Journal of comparative neurology.

[8]  R. L. Nó The central projection of the nerve endings of the internal ear , 1933 .

[9]  E. Mugnaini,et al.  The cerebellar projection of the vestibular nerve in the cat , 1979, The Journal of comparative neurology.

[10]  T. Furukawa,et al.  Intra‐axonal labeling of saccular afferents in the goldfish, Carassius auratus: Correlations between morphological and physiological characteristics , 1987, The Journal of comparative neurology.

[11]  S. Highstein,et al.  IS TRANSMISSION BETWEEN THE VESTIBULAR TYPE I HAIR CELL AND ITS PRIMARY AFFERENT CHEMICAL? , 1981, Annals of the New York Academy of Sciences.

[12]  M. Carpenter,et al.  Distribution of primary vestibular fibers in the brainstem and cerebellum of the monkey , 1984, Brain Research.

[13]  N. Ishizuka,et al.  Central course and terminal arborizations of single primary vestibular afferent fibers from the horizontal canal in the cat , 1982, Neuroscience Letters.

[14]  M. S. Estes,et al.  Physiologic characteristics of vestibular first-order canal neurons in the cat. I. Response plane determination and resting discharge characteristics. , 1975, Journal of neurophysiology.

[15]  V. Honrubia,et al.  Central projections of primary vestibular fibers in the bullfrog. II. Nerve branches from individual receptors , 1985, The Laryngoscope.

[16]  N. Ishizuka,et al.  Trajectory of Primary Vestibular Fibers Originating from the Lateral, Anterior, and Posterior Semicircular Canals in the Cat , 1982 .

[17]  Jay M. Goldberg,et al.  Conduction times and background discharge of vestibular afferents , 1977, Brain Research.

[18]  N. Kiang,et al.  Spontaneous Activity In The Eighth Cranial Nerve of The Cat , 1972 .

[19]  J H Milsum,et al.  Characteristics of neural transmission from the semicircular canal to the vestibular nuclei of cats , 1970, The Journal of physiology.

[20]  G. L. Rasmussen,et al.  Fiber analysis of the statoacoustic nerve of guinea pig, cat, and monkey , 1961, The Anatomical record.

[21]  A K Moschovakis,et al.  Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the squirrel monkey. II. Correlation with output pathways of secondary neurons. , 1987, Journal of neurophysiology.

[22]  Naiphinich Kotchabhakdi,et al.  Primary vestibular afferent projections to the cerebellum as demonstrated by retrograde axonal transport of horseradish peroxidase , 1978, Brain Research.

[23]  Y. Shinoda,et al.  Dynamic characteristics of responses to horizontal head angular acceleration in vestibuloocular pathway in the cat. , 1974, Journal of neurophysiology.

[24]  M. Carpenter,et al.  Primary vestibulocerebellar fibers in the monkey: distribution of fibers arising from distinctive cell groups of the vestibular ganglia. , 1972, The American journal of anatomy.

[25]  M. Carpenter,et al.  Central projections of portions of the vestibular ganglia innervating specific parts of the labyrinth in the rhesus monkey , 1967 .