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Morphology of vertical canal related second order vestibular neurons in the cat

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Summary

The morphology of vertical canal related second order vestibular neurons in the cat was studied with the intracellular horseradish peroxidase method. Neurons were identified by their monosynaptic potentials following electrical stimulation via bipolar electrodes implanted into individual semicircular canal ampullae. Anterior and posterior canal neurons projected primarily to contralateral or ipsilateral motoneuron pools (excitatory and inhibitory pathways, respectively). The axons of contralaterally projecting neurons crossed the midline at the level of the abducens nucleus and bifurcated into an ascending and a descending main branch which travelled in the medial longitudinal fasciculus (MLF). Two types of anterior canal neurons were observed, one with unilateral and one with bilateral oculomotor projection sites. For both neuron classes, the major termination sites were in the. contralateral superior rectus and inferior oblique subdivisions of the oculomotor nucleus. In neurons which terminated bilaterally, major collaterals recrossed the midline within the oculomotor nucleus to reach the ipsilateral superior rectus motoneuron pool. Other, less extensive, termination sites of both neuron classes were in the contralateral vestibular nuclear complex, the facial nucleus, the medullary and pontine reticular formation, midline areas within and neighboring the raphé nuclei, and the trochlear nucleus. The ascending main axons continued further rostrally to reach the interstitial nucleus of Cajal and areas around the fasciculus retroflexus. The descending branches proceeded further caudal in the medial vestibulo-spinal tract but were not followed to their spinal target areas. In addition to two previously described posterior canal related neuron types (Graf et al. 1983), we found neurons with bilateral oculomotor terminals and a spinal collateral. Typical for posterior canal neurons, the major termination sites were in the trochlear nucleus (superior oblique motoneurons) and in the inferior rectus subdivision of the oculomotor nucleus. Axon collaterals recrossed the midline to reach ipsilateral inferior rectus motoneurons. The axons of ipsilaterally projecting neurons ascended through the reticular formation to join the MLF caudal to the trochlear nucleus. The main target sites of anterior canal related neurons were in the trochlear nucleus and the inferior rectus subdivision of the oculomotor nucleus. Minor collaterals reached the pontine reticular formation and areas in between the fiber bundles of the ipsilateral MLF. In some cases, small collaterals crossed the midline within the oculomotor nucleus to terminate in the inferior rectus subdivision on the contralateral side. The axon proceeded further rostral to project to the interstitial nucleus of Cajal and beyond. The main termination sites of posterior canal neurons were in the superior rectus and inferior oblique subdivisions of the oculomotor nucleus. Minor collaterals were also observed to reach the midline area within the oculomotor nucleus, however, prospective contralateral termination sites could not be identified. More rostral projections were found in the interstitial nucleus of Cajal. The described axonal arborization of second order vestibular neurons reflects the organization of intrinsic coordinate systems as exemplified by the geometry of the semicircular canal and the extraocular muscle planes. These neurons are interpreted to provide a matrix for coordinate system transformation, i.e. from vestibular into oculomotor reference frames, and to play a role in gaze control and related reflexes by distributing their signals to multiple termination sites.

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Abbreviations

DV:

descending vestibular nucleus

INC:

interstitial nucleus of Cajal

INT:

nucleus intercalatus

IQ:

inferior oblique subdivision

LV:

lateral vestibular nucleus

MLF:

medial longitudinal fasciculus

MRF:

medullary reticular formation

MV:

medial vestibular nucleus

nVII:

facial nerve

PH:

nucleus praepositus hypoglossi

PRF:

pontine reticular formation

RO:

nucleus Roller

SR:

superior rectus subdivision

SV:

superior vestibular nucleus

III:

oculomotor nucleus

IV:

trochlear nucleus

VI:

abducens nucleus

VII:

facial nucleus

XII:

hypoglossal nucleus

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Author notes

  1. K. Ezure

    Present address: Tokyo Metropolitan Institute for Neurosciences, 2-6 Musashidai, Fuchu-shi, 183, Tokyo, Japan

Authors and Affiliations

  1. The Rockefeller University, 1230 York Avenue, 10021, New York, NY, USA

    W. Graf & K. Ezure

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  1. W. Graf
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Supported by NIH grants EY04613 and NS02619

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Graf, W., Ezure, K. Morphology of vertical canal related second order vestibular neurons in the cat. Exp Brain Res 63, 35–48 (1986). https://doi.org/10.1007/BF00235644

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