Elsevier

Neuroscience

Volume 93, Issue 1, June 1999, Pages 155-170
Neuroscience

Ultrastructure of vestibular commissural neurons related to velocity storage in the monkey

https://doi.org/10.1016/S0306-4522(99)00142-6Get rights and content

Abstract

The angular vestibulo-ocular reflex maintains gaze during head movements. It is thought to be mediated by two components: direct and velocity storage pathways. The direct angular vestibulo-ocular reflex is conveyed by a three neuron chain from the labyrinth to the ocular motoneurons. The indirect pathway involves a more complex neural network that utilizes a portion of the vestibular commissure. The purpose of the present study was to identify the ultrastructural characteristics of commissural neurons in the medial vestibular nucleus that are related to the velocity storage component of the angular vestibulo-ocular reflex. Ultrastructural studies of degenerating medial vestibular nucleus neurons were conducted in monkeys following midline section of rostral medullary commissural fibers with subsequent behavioral testing. After this lesion, oculomotor and vestibular functions attributable to velocity storage were abolished, whereas the direct angular vestibulo-ocular reflex pathway remained intact. Since this damage was functionally discrete, degenerating neurons were interpreted as potential participants in the velocity storage network. Ultrastructural observations indicate that commissural neurons related to velocity storage are small and medium sized cells having large nuclei with deep indentations and relatively little cytoplasm, which are located in the lateral crescents of rostral medial vestibular nucleus. The morphology of degenerating dendritic profiles varied. Some contained numerous round or tubular mitochondria in a pale cytoplasmic matrix with few other organelles, while others had few mitochondria but many cisterns and vacuoles in dense granular cytoplasm. The commissural nature of these cells was further suggested by the presence of two different types of degenerating axon terminals in the rostral medial vestibular nucleus: those with a moderate density of large spherical synaptic vesicles, and those with pleomorphic, primarily ellipsoid synaptic vesicles. The recognition of two types of degenerating terminals further supports our interpretation that at least two morphological types of commissural neurons participate in the velocity storage network. The degenerating boutons formed contacts with a variety of postsynaptic partners. In particular, synapses were observed between degenerating boutons and non-degenerating dendrites, and between intact terminals and degenerating dendrites. However, degenerating pre- and postsynaptic elements were rarely observed in direct contact, suggesting that additional neurons are interposed in the indirect pathway commissural system.

On the basis of these ultrastructural observations, it is concluded that vestibular commissural neurons involved in the mediation of velocity storage have distinguishing ultrastructural features and synaptology, that are different from those of direct pathway neurons.

Section snippets

Experimental animals

Brainstem tissue from one rhesus (M. mulatta; M9316) and two cynomolgus (M. fasicularis; M1190 and M1194) monkeys was used to characterize the ultrastructural anatomy of the monkey MVN under the tissue fixation and processing protocols used in our laboratory. In addition, one cynomolgus (M9210) and two rhesus (M502 and M613) monkeys received midline brainstem lesions and had oculomotor and vestibular testing after the midline medullary section. Animals were obtained from the Charles River

Velocity storage

Velocity storage was affected in both M502 and M613. Divergent strabismus due to bilateral paresis of adduction and gaze paresis precluded further testing of M9210. In both M502 and M613, the pre-operative velocity storage time-constants were initially asymmetric. They were 78 s for rightward and 22 s for leftward slow phases during steps of velocity in M502 (Fig. 1A), and 8 and 19 s for rightward and leftward eye velocities in M613. After the lesion, these values fell to approximately 4 and 6 s,

Discussion

Following the midline medullary section in M613, all oculomotor and vestibular functions attributable to velocity storage were abolished, while the direct aVOR pathway remained unaltered. OCR was also intact, indicating that pathways responsible for this otolith-ocular tilt reflex do not course in the region of the midline lesion. These observations suggest that the lesion-induced vestibular and oculomotor damage was functionally discrete, localized to the production of velocity storage. On the

Conclusions

The behavioral results of this study indicate that vestibular commissural axons related to velocity storage cross the midline of the brainstem in the rostral medulla, just caudal to the abducens nuclei. The anatomical findings suggest that such axons originate from clusters of small and medium-sized neurons located in the lateral crescents of the rostral MVN. The ultrastructural observations support the contentions that two types of indirect pathway commissural cells, and two types of axon

Acknowledgements

Supported by National Institutes of Health research grants DC01705 (G.R.H.) from the National Institute on Deafness and Other Communication Disorders, NS00294 (B.C.) from the National Institute of Neurological Diseases and Stroke, EY11812 (B.C.) and EY1867 (B.C.) from the National Eye Institute. The authors thank Ms Rosemary Lang and Mr Victor Rodriguez for their invaluable assistance with various aspects of this work.

References (68)

  • E.L. Keller et al.

    Characteristics of head rotation and eye movement related neurons in alert monkey vestibular nucleus

    Brain Res.

    (1975)
  • G.E. Korte et al.

    The fine structure of the feline superior vestibular nucleus: identification and synaptology of the primary vestibular afferents

    Brain Res.

    (1979)
  • R. Ladpli et al.

    Experimental studies of commissural and reticular formation projections from the vestibular nuclei in the cat

    Brain Res.

    (1968)
  • F.A. Miles

    Single unit firing patterns in the vestibular nuclei related to voluntary eye movements and passive body rotation in concious monkeys

    Brain Res.

    (1974)
  • S.D. Newlands et al.

    A quantitative study of the vestibular commissures in the gerbil

    Brain Res.

    (1989)
  • B.F. Trump et al.

    Cellular ion regulation and disease: a hypothesis

    Curr. Top. Membranes Transport

    (1985)
  • U. Wüllner et al.

    Evidence for an active type of cell death with ultrastructural features distinct from apoptosis: the effects of 3-acetylpyridine neurotoxicity

    Neuroscience

    (1997)
  • S.M. Blair et al.

    Brainstem commissure and control of time constant of vestibular nystagmus

    Acta otolar.

    (1981)
  • D.E. Bredesen

    Neural apoptosis

    Ann. Neurol.

    (1995)
  • A. Brodal

    The vestibular nuclei in the macaque monkey

    J. comp. Neurol.

    (1984)
  • U.W. Büttner et al.

    Transfer characteristics of neurons in vestibular nuclei of the alert monkey

    J. Neurophysiol.

    (1978)
  • Büttner-Ennever J. A. (1992) Patterns of connectivity in the vestibular nuclei. In Sensing and Controlling Motion:...
  • S.C. Cannon et al.

    Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey

    J. Neurophysiol.

    (1987)
  • G. Cheron et al.

    Lesions in the cat prepositus complex: effects on the optokinetic system

    J. Physiol.

    (1986)
  • B. Cohen et al.

    Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus

    J. Physiol.

    (1977)
  • B. Cohen et al.

    Vestibular-only (VO) neurons and velocity storage

    Soc. Neurosci. Abstr.

    (1996)
  • J.D. Crawford et al.

    Axes of eye rotation and Listing's law during rotations of the head

    J. Neurophysiol.

    (1991)
  • M. Dai et al.

    Effects of spaceflight on ocular counter-rolling and spatial orientation of the vestibular system

    Expl Brain Res.

    (1994)
  • M. Dai et al.

    Spatial orientation of the vestibular system: dependence of optokinetic after-nystagmus on gravity

    J. Neurophysiol.

    (1991)
  • E.J. Engelken et al.

    A new approach to the analysis of nystagmus: an application for order statistic filters

    Aviat. Space Environ. Med.

    (1990)
  • Engelken E. J., Stevens K. W. and Enderle, J. D. (1991) Optimization of an adaptive nonlinear filter for the analysis...
  • A.H. Epema et al.

    Commissural and intrinsic connections of the vestibular nuclei in the rabbit: a retrograde labeling study

    Expl Brain Res.

    (1988)
  • A.F. Fuchs et al.

    Unit activity in the vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement

    J. Neurophysiol.

    (1975)
  • R. Gacek et al.

    Ultrastructural changes in vestibulo-ocular neurons following vestibular neurectomy in the cat

    Ann. Otol. Rhinol. Lar.

    (1988)
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