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Second-order vestibular neuron morphology of the extra-MLF anterior canal pathway in the cat

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Abstract

Second-order vestibular neurons form the central links of the vestibulo-oculomotor three-neuron arcs that mediate compensatory eye movements. Most of the axons that provide for vertical vestibulo-ocular reflexes ascend in the medial longitudinal fasciculus (MLF) toward target neurons in the oculomotor and trochlear nuclei. We have now determined the morphology of individual excitatory second-order neurons of the anterior semicircular canal system that course outside the MLF to the oculomotor nucleus. The data were obtained by the intracellular horseradish peroxidase method. Cell somata of the extra-MLF anterior canal neurons were located in the superior vestibular nucleus. The main axon ascended through the deep reticular formation beneath the brachium conjunctivum to the rostral extent of the nucleus reticularis tegmenti pontis, where it crossed the midline. The main axon continued its trajectory to the caudal edge of the red nucleus from where it coursed back toward the oculomotor nucleus. Within the oculomotor nucleus, collaterals reached superior rectus and inferior oblique motoneurons. Some axon branches recrossed the midline within the oculomotor nucleus and reached the superior rectus motoneuron subdivision on that side. Since these neurons did not give off a collateral toward the spinal cord, they were classified as being of the vestibulo-oculomotor type and are thought to be involved exclusively in eye movement control. The signal content and spatial tuning characteristics of this anterior canal vestibulo-oculomotor neuron class remain to be determined.

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References

  • Baker R, Highstein SM (1978) Vestibular projections to medial rectus subdivision of oculomotor nucleus. J Neurophysiol 41:1629–1646

    Google Scholar 

  • Berthoz A, Droulez J, Vidai PP, Yoshida K (1989) Neural correlates of horizontal vestibulo-ocular reflex cancellation during rapid eye movements in the cat. J Physiol (Lond) 419:717–751

    Google Scholar 

  • Ezure K, Graf W (1984a) A quantitative analysis of the spatial organization of the vestibulo-ocular reflexes in lateral and frontal-eyed animals. I. Orientation of semicircular canals and extraocular muscles. Neuroscience 12:85–93

    Google Scholar 

  • Ezure K, Graf W (1984b) A quantitative analysis of the spatial organization of the vestibulo-ocular reflexes in lateral and frontal-eyed animals. II. Neuronal networks underlying vestibulooculomotor coordination. Neuroscience 12:95–109

    Article  CAS  PubMed  Google Scholar 

  • Glover JC, Pétursdóttir G (1988) Pathway specificity of reticulospinal and vestibulospinal projections in the 11-day chicken embryo. J Comp Neurol 270:25–38

    Google Scholar 

  • Graf W, Ezure K (1986) Morphology of vertical canal related sec ond order vestibular neurons in the cat. Exp Brain Res 63:35–48

    CAS  PubMed  Google Scholar 

  • Graf W, Wilson VJ (1989) Afferents and efferents of the vestibular nuclei. The necessity of context-specific interpretation. Prog Brain Res 80:149–157

    Google Scholar 

  • Graf W, McCrea RA, Baker R (1983) Morphology of posterior canal related secondary vestibular neurons in rabbit and cat. Exp Brain Res 52:125–138

    CAS  PubMed  Google Scholar 

  • Graf W, Simpson JI, Leonard CS (1988) Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells. J Neurophysiol 60:2091–2121

    Google Scholar 

  • Graf W, Baker J, Peterson BW (1993) Sensory-motor transformation in the cat's vestibulo-ocular reflex system. I. Neuronal signals coding spatial coordination of compensatory eye movements. J Neurophysiol Vol 70, No 6

  • Hirai N, Uchino Y (1984a) Superior vestibular nucleus neurones related to the excitatory vestibulo-ocular reflex of anterior canal origin and their ascending course in the cat. Neurosci Res 1:73–79

    Article  CAS  PubMed  Google Scholar 

  • Hirai N, Uchino Y (1984b) Floccular influence on excitatory relay neurons of vestibular reflexes of anterior semicircular canal origin in the cat. Neurosci Res 1:327–340

    Google Scholar 

  • Ishizuka N, Mannen H, Sasaki S-I, Shimazu H (1980) Axonal branches and terminations in the cat abducens nucleus of secondary vestibular neurons in the horizontal canal system. Neurosci Lett 16:143–148

    Google Scholar 

  • Isu N, Yokota J (1983) Morphophysiological study on the divergent projection of axon collaterals of medial vestibular nucleus neurons in the cat. Brain Res 53:151–162

    Google Scholar 

  • Isu N, Uchino Y, Nakashima H, Satoh S, Ichikawa T, Watanabe S (1988) Axonal trajectories of posterior canal-activated secondary vestibular neurons and their coactivation of extraocular and neck flexor motoneurons in the cat. Exp Brain Res 70:181–191

    Google Scholar 

  • Isu N, Sakuma A, Hiranuma K, Ichikawa T, Uchino Y (1990) Localization and synaptic effects of inhibitory vestibulo-collic neurons activated by the posterior semicircular canal nerve in the cat. Neurosci Lett 119:163–166

    Google Scholar 

  • Ito M (1982) Cerebellar control of the vestibulo-ocular reflex: around the flocculus hypothesis. Annu Rev Neurosci 5:275–296

    Google Scholar 

  • Ito M (1984) The cerebellum and neural control. Raven, New York

    Google Scholar 

  • Ito M, Nisimaru N, Yamamoto M (1973) Specific neural connections for the cerebellar control of vestibulo-ocular reflexes. Brain Res 40:81–84

    Article  Google Scholar 

  • Iwamoto Y, Kitama T, Yoshida K (1990a) Vertical eye movement-related secondary vestibular neurons ascending in medial longitudinal fasciculus in the cat. I. Firing properties and projection pathways. J Neurophysiol 63:902–917

    Google Scholar 

  • Iwamoto Y, Kitama T, Yoshida K (1990b) Vertical eye movement-related secondary vestibular neurons ascending in medial longitudinal fasciculus in the cat. II. Direct connections with extraocular motoneurons. J Neurophysiol 63:918–935

    Google Scholar 

  • Lang W, Büttner-Ennever J, Büttner U (1979) Vestibular projections to the monkey thalamus: an autoradiographic study. Brain Res 177:3–17

    Google Scholar 

  • Lisberger SG, Sejnowski TJ (1992) Motor learning in a recurrent network model based on the vestibulo-ocular reflex. Nature 360:159–161

    Google Scholar 

  • McCrea RA, Yoshida K, Berthoz A, Baker R (1980) Eye movement related activity and morphology of second order vestibular neurons terminating in the cat abducens nucleus. Exp Brain Res 40:468–473

    Google Scholar 

  • Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4:273–299

    Google Scholar 

  • Mitsakos A, Reisine H, Highstein, SM (1983) The superior vestibular nucleus: an intracellular HRP study in the cat. I. Vestibuloocular neurons. J Comp Neurol 215:78–97

    Google Scholar 

  • Pellionisz A, Graf W (1987) Tensor network model of the “threeneuron vestibulo-ocular reflex arc” in cat. J Theor Neurobiol 5:127–151

    Google Scholar 

  • Pétursdóttir G (1990) Vestibulo-ocular projectionjs in the 11-day chicken embryo: pathway specificity. J Comp Neurol 297:283–297

    Google Scholar 

  • Reisine H, Highstein SM (1979) The ascending tract of Deiters conveys a head velocity signal to medial rectus motoneurons. Brain Res 170:172–176

    Google Scholar 

  • Szentágothai J (1943) Die zentrale Innervation der Augenbewegungen. Arch Psychiatr Nervenkr 116:721–760

    Google Scholar 

  • Szentágothai J (1950) The elementary vestibulo-ocular reflex arc. J Neurophysiol 13:395–407

    PubMed  Google Scholar 

  • Uchino Y, Hirai N (1984) Axon collaterals of anterior semicircular canal-activated vestibular neurons and their coactivation of extra-ocular and neck motoneurons in the cat. Neurosci Res 1:309–325

    Google Scholar 

  • Uchino Y, Isu N (1992a) Properties of vestibulo-ocular and/or vestibulocollic neurons in the cat. In: Berthoz A, Graf W, Vidai PP (eds) The head-neck sensory motor system. Oxford University Press, Oxford, pp 266–272

    Google Scholar 

  • Uchino Y, Isu N (1992b) Properties of inhibitory vestibulo-ocular and vestibulo-collic neurons in the cat. In: Shimazu H, Shinoda Y (eds) Vestibular and brain stem control of eye, head and body movements. Japan Scientific Societies, Tokyo; Karger, Basel, pp 31–43

    Google Scholar 

  • Uchino Y, Suzuki S, Watanabe S (1980) Vertical semicircular canal inputs to cat extraocular motoneurons. Exp Brain Res 41:45–53

    Google Scholar 

  • Uchino Y, Hirai N, Suzuki N, Watanabe S (1981) Properties of secondary vestibular neurons fired by stimulation of ampullary nerves of the vertical, anterior or posterior, semicircular canals in the cat. Brain Res 223:273–286

    Article  CAS  PubMed  Google Scholar 

  • Uchino Y, Hirai N, Suzuki S (1982) Branching pattern and properties of vertical and horizontal-related excitatory vestibuloocular neurons in the cat. J Neurophysiol 48:891–903

    Google Scholar 

  • Uchino Y, Isu N, Ichikawa T, Satoh S, Watanabe S (1988) Properties and localization of the anterior semicircular canal-activated vestibulocollic neurons in the cat. Exp Brain Res 71:345–352

    Google Scholar 

  • Uchino Y, Isu N, Sakuma A, Ichikawa T, Hirunuma K (1990) Axonal trajectories of inhibitory vestibulocollic neurons activated by the anterior semicircular canal nerve and their synaptic effects on neck motoneurons in the cat. Exp Brain Res 82:14–24

    Google Scholar 

  • Uchino Y, Sasaki M, Isu N, Hirai N, Imagawa M, Endo K, Graf W (1992) Morphology of the excitatory disynaptic extra-MLF anterior canal pathway in the cat. Soc Neurosci Abstr 18:216.11

    Google Scholar 

  • Yamamoto M, Shimoyama I, Highstein SM (1978) Vestibular nucleus neurons relaying excitation from the anterior canal to the oculomotor nucleus. Brain Res 148:31–42

    Google Scholar 

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Uchino, Y., Sasaki, M., Isu, N. et al. Second-order vestibular neuron morphology of the extra-MLF anterior canal pathway in the cat. Exp Brain Res 97, 387–396 (1994). https://doi.org/10.1007/BF00241532

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  • DOI: https://doi.org/10.1007/BF00241532

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