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The development of the static vestibulo-ocular reflex in the Southern Clawed Toad,Xenopus laevis

I. Intact animals

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Summary

In the clawed toad,Xenopus laevis, the static vestibulo-ocular reflex appears in 3 days old tadpoles (developmental stage 42) (Fig. 2). The amplitude and gain of this reflex increase up to stage 52, and then decrease to an almost constant value at stage 60 and older tadpoles (Fig. 3). The most effective roll angle gradually increases during development (Fig. 4).

The size of the sensory epithelia reaches the final value at the end of the premetamorphic period (stage 56) (Fig. 5). The small-cellular medial ventral vestibular nucleus (VVN) reaches its maximal number of neurons before the large-cellular lateral VVN. Cell death is more pronounced in the medial than in the lateral part of the VVN. In the dorsal vestibular nucleus (DVN), the numerical development of the small and large neurons is similar to that in the small-cellular medial and large-cellular lateral portion of the VVN (Fig. 7).

The results demonstrate that labyrinth and oculomotor centres are anatomically connected before the labyrinth and the vestibular nuclei are fully developed. We discuss the possibility that the ciliary polarity pattern of the sensory epithelium is radial during the first period of life, and changes to the vertebrate fan-type pattern during the second week of life. According to the increase of gain during the first three weeks of life, an increase of the spontaneous activity of vestibular neurons may occur during this period.

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Abbreviations

α :

eye angle

γ :

roll angle

α(γ) :

response characteristic

A :

response amplitude

G :

response gain

VOR :

vestibulo-ocular reflex

VVN :

ventral vestibular nucleus

DVN :

dorsal vestibular nucleus

References

  • Anniko M (1983) Embryonic development of vestibular sense organs and their innervation. In: Romand R (ed) Development of auditory and vestibular systems. Academic Press, New York London, pp 375–423

    Google Scholar 

  • Budelmann B-U (1970) Die Arbeitsweise der Statolithenorgane vonOctopus vulgaris. Z Vergl Physiol 70:278–312

    Google Scholar 

  • Budelmann B-U (1979) Hair cell polarization in the gravity receptor systems of the statocysts of the cephalopodsSepia officinalis andLoligo vulgaris. Brain Res 160:261–270

    Google Scholar 

  • Cohen B (1974) The vestibulo-ocular reflex arc. In: Kornhuber HH (ed) The vestibular system. Part 1: Basic mechanisms. (Handbook of sensory physiology, vol VI/1). Springer, Berlin Heidelberg New York, pp 477–540

    Google Scholar 

  • Corwin JT (1983) Postembryonic growth of the macula neglecta auditory detector in the ray,Raja clavata: continual increases in hair cell number, neural convergence, and physiological sensitivity. J Comp Neurol 217:345–356

    Google Scholar 

  • Curthoys JS (1983) The development of function of primary vestibular neurons. In: Romand R (ed) Development of auditory and vestibular systems. Academic Press, New York London, pp 425–461

    Google Scholar 

  • Dieringer N, Precht W (1982) Compensatory head and eye movements in the frog and their contribution to stabilization of gaze. Exp Brain Res 47:394–406

    Google Scholar 

  • Ginzberg RD, Gilula NB (1980) Synaptogenesis in the vestibular sensory epithelium of the chick embryo. J Neurocytol 9:405–424

    Google Scholar 

  • Graf W, Baker R (1983) Adaptive changes of the vestibuloocular reflex in flatfish are achieved by reorganization of central nervous pathways. Science 221:777–779

    Google Scholar 

  • Gregory KM (1972) Central projection of the eight nerve in frogs. Brain Behav Evol 5:70–88

    Google Scholar 

  • Hess BJM, Knöpfel T, Precht W (1984) Dynamics of maculo-ocular reflexes in the frog. Neuroscience 11:645–650

    Google Scholar 

  • Holst E von (1950) Die Arbeitsweise des Statolithenapparates bei Fischen. Z Vergl Physiol 32:60–120

    Google Scholar 

  • Horn E, Rayer B (1978) Compensation of vestibular lesions in relation to development. Naturwissenschaften 65:441

    Google Scholar 

  • Horn E, Rayer B (1980) A hormonal component in central vestibular compensation. Z Naturforsch 35c:1120–1121

    Google Scholar 

  • Jacobson M (1978) Developmental neurobiology. Plenum Press, New York London

    Google Scholar 

  • Knöpfel T, Hess BJM, Precht W (1984) Responses of frog trochlear motoneurons to linear acceleration. J Comp Physiol A 154:233–240

    Google Scholar 

  • Konigsmark BW (1970) Methods for counting neurons. In: Nauta WJH, Ebbesson SOE (eds) Contemporary research methods in neuroanatomy. Springer, Berlin Heidelberg New York, pp 315–340

    Google Scholar 

  • Lang HG, Horn E (1980) The development of the static vestibulo-ocular reflex inXenopus. Z Naturforsch 35c:1122–1123

    Google Scholar 

  • Lannou J, Precht W, Cazin L (1983) Functional development of the central nervous system. In: Romand R (ed) Development of auditory and vetibular systems. Academic Press, New York London, pp 463–478

    Google Scholar 

  • Lowenstein O, Roberts DM (1949) The equilibrium of the otolith organs of the thornback ray (Raja clavata). J Physiol (Lond) 110:392–415

    Google Scholar 

  • Matesz C (1979) Central projection of the VIIIth cranial nerve in the frog. Neuroscience 4:2061–2071

    Google Scholar 

  • Mehler WR (1972) Comparative anatomy of the vestibular nuclear complex in submammalian vertebrates. Prog Brain Res 37:55–67

    Google Scholar 

  • Neil DM (1975) Statocyst control of eyestalk movements in mysid shrimps. In: Schöne H (ed) Mechanisms of spatial perception and orientation as related to gravity. Fortschr Zool 23. Gustav Fischer, Stuttgart, pp 98–109

    Google Scholar 

  • Nieuwkoop PD, Faber J (1975) Normal table ofXenopus laevis (Daudin). Hubrecht Laboratory, Utrecht

    Google Scholar 

  • Precht W (1974) Physiological aspects of the efferent vestibular system. In: Kornhuber HH (ed) The vestibular system. Part 1: Basic mechanisms. (Handbook of sensory physiology VI/1). Springer, Berlin Heidelberg New York, pp 221–236

    Google Scholar 

  • Precht W (1976) Physiology of the peripheral and central vestibular system. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 481–512

    Google Scholar 

  • Rayer B, Cagol E, Horn E (1983) Compensation of vestibular induced deficits in relation to the development of the Southern Clawed Toad,Xenopus laevis Daudin. J Comp Physiol 151:487–498

    Google Scholar 

  • Romand R, Dauzat M (1982) Modification of spontaneous activity in primary vestibular neurons during development in the cat. Exp Brain Res 45:265–268

    Google Scholar 

  • Romeis B (1968) Mikroskopische Technik. Oldenburg, München Wien

    Google Scholar 

  • Sachs L (1974) Angewandte Statistik. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Schöne H (1954) Statocystenfunktion and statische Lageorientierung bei decapoden Krebsen. Z Vergl Physiol 36:241–260

    Google Scholar 

  • Schöne H (1964) Über die Arbeitsweise der Statolithenapparate bei Plattfischen. Biol Jahresheft 4:135–156

    Google Scholar 

  • Schöne H (1975) On the transformation of the gravity input into reactions by statolith organs of the “fan” type. In: Schöne H (ed) Mechanisms of spatial perception and orientation as related to gravity. Fortschr Zool 23. Gustav Fischer, Stuttgart, pp 120–127

    Google Scholar 

  • Shelton PMJ (1970) The lateral line system at metamorphosis inXenopus laevis Daudin. J Embryol Exp Morphol 24:511–524

    Google Scholar 

  • Tegetmeyer H, Schwartze P (1982) Tonic vestibular control of eye position in postnatal developing rabbits. Acta Otolaryngol 94:289–297

    Google Scholar 

  • Thornhill RA (1972) The development of the labyrinth of the lamprey (Lampetra fluviatilis Linn. 1758). Proc R Soc Lond B 181:175–198

    Google Scholar 

  • Traill AB, Mark RF (1970) Optic and static contributions to ocular counter-rotation in carp. J Exp Biol 52:109–124

    Google Scholar 

  • Wersäll J, Bagger-Sjöbäck D (1974) Morphology of the vestibular sense organ. In: Kornhuber HH (ed) The vestibular system. Part 1: Basic mechanisms. (Handbook of sensory physiology, vol VI/1). Springer, Berlin Heidelberg New York, pp 123–170

    Google Scholar 

  • Will U, Luhede G, Görner P (1985a) The area octavo-lateralis inXenopus laevis. I. The primary afferent projections. Cell Tissue Res 239:147–161

    Google Scholar 

  • Will U, Luhede G, Görner P (1985b) The area octavo-lateralis inXenopus laevis. II. Second order projections and cytoarchitecture. Cell Tissue Res 239:163–175

    Google Scholar 

  • Young JZ (1960) The statocysts ofOctopus vulgaris. Proc R Soc Lond B 152:3–29

    Google Scholar 

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Horn, E., Lang, H.G. & Rayer, B. The development of the static vestibulo-ocular reflex in the Southern Clawed Toad,Xenopus laevis . J. Comp. Physiol. 159, 869–878 (1986). https://doi.org/10.1007/BF00603740

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