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Morphology of posterior canal related secondary vestibular neurons in rabbit and cat

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Summary

  1. 1.

    The morphology of secondary vertical vestibular neurons was investigated by injection of horseradish peroxidase (HRP) into cells connected to the posterior canal system in rabbits (lateral-eyed animals) and cats (frontal-eyed animals). Vestibular neurons were identified by stimulation with bipolar electrodes implanted into the ampullae of the anterior and posterior (PC) semicircular canals of pigmented rabbits; in the cat, these cells were identified by natural and electrical stimulation. Axons monosynaptically activated by PC stimulation were injected with HRP in the medial longitudinal fasciculus (MLF). These were later reconstructed by light microscopy after the brains had been processed with a DAB-CoCl2 method.

  2. 2.

    In the rabbit the majority of the axons bifurcated after crossing the midline with one branch ascending and the other descending in the MLF. The ascending branches gave rise to collaterals that terminated in both the trochlear nucleus and the inferior rectus subdivision of the oculomotor nucleus. In addition some axons also sent collaterals into the paramedian pontine reticular formation, the periaqueductal grey and the interstitial nucleus of Cajal. The descending branches were followed to the caudal part of the medulla in the MLF and gave rise to collaterals terminating in the vestibular nuclei, the medullary reticular formation, the perihypoglossal nuclei, the abducens nucleus, and the facial nucleus. In another cell type axons crossed the midline without giving off any collaterals and proceeded caudally in the caudal MLF. The synaptic effects of the two types of cells were concluded to be excitatory and inhibitory, respectively. Cell bodies of contralaterally projecting neurons were located in either the medial or ventro-lateral vestibular nuclei.

  3. 3.

    In the cat we observed two neuron classes, with contralaterally projecting axons, whose synaptic effects are presumably excitatory. Their cell somata were located in the medial vestibular nucleus. Termination patterns were similar to both the trochlear and oculomotor nuclei, but neither projected to the abducens nucleus. One class of neurons was almost identical to that found in the rabbit with the main axon bifurcating in the MLF. The second type lacked a descending branch in the MLF. Axon collaterals of the latter type crossed the midline within the oculomotor nucleus after terminating in the inferior rectus subdivision to reach a similar portion of the ipsilateral oculomotor nucleus. Collaterals of these axons also terminated bilaterally in the supraoculomotor region between trochlear and oculomotor nucleus, the interstitial nucleus of Cajal and prerubral loci (including the fields of Forel). In similarity to the rabbit, presumed inhibitory vestibular neurons were found with axons directed caudally in the MLF without brain stem collaterals.

  4. 4.

    Ipsilateral neurons with ascending axons considered to be inhibitory were only studied in the rabbit. Their cell bodies were located in the superior vestibular nucleus, the axon joining the rostral MLF with major termination sites in the superior rectus and in the inferior oblique subdivisions of the oculomotor nucleus. Other terminations were in the paramedian pontine reticular formation and in the medullary reticular formation.

  5. 5.

    These data indicate strong similarities in the morphology of PC linked secondary vestibular neurons in the two species suggesting paramount importance for this wiring pattern in the spatial organization of eye movements. Variations in the termination patern likely reflect different kinematic characteristics of extraocular muscles necessary for the appropriate, but different, type of compensatory eye movements in lateral-versus frontal-eyed animals. We conclude that the termination pattern of secondary vestibular neurons forms a basic part of the neuronal matrix for space-time coordinated eye-movements and other related vestibular functions. This neuronal network provides a morphological basis for a conversion factor for the transformation of vestibular into e.g. extraocular muscle coordinates.

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  1. W. Graf

    Present address: The Rockefeller University, 1230 York Avenue, 10021, New York, NY, USA

  2. R. A. McCrea

    Present address: Dept. Pharmacol. and Physiol. Sci., University of Chicago, 60637, Chicago, IL, USA

Authors and Affiliations

  1. Dept. of Physiology and Biophysics, New York University Medical Center, 10016, New York, NY, USA

    W. Graf, R. A. McCrea & R. Baker

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Supported by DFG grant Gr 688/1, NIH grants 13742 and EY02007

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Graf, W., McCrea, R.A. & Baker, R. Morphology of posterior canal related secondary vestibular neurons in rabbit and cat. Exp Brain Res 52, 125–138 (1983). https://doi.org/10.1007/BF00237157

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