Skip to main content
SpringerLink
Log in

Cerebellar connections in Xenopus laevis

An HRP study

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

In the present study the cerebellar afferents in the clawed toad Xenopus laevis have been analysed with the horseradish peroxidase (HRP) technique. In addition, data on the efferent connections of the cerebellum could be gathered, based on the phenomenon of anterograde transport of HRP.

Cerebellar afferents in Xenopus laevis appear to arise mainly in the vestibular nuclear complex, in a primordial inferior olive and in the spinal cord. Both primary (arising in the ipsilateral vestibular ganglion) and secondary vestibulocerebellar projections were found. A distinct crossed olivocerebellar projection to the molecular layer of the cerebellum was found. Two spinocerebellar pathways are present in Xenopus laevis, as in other anurans, viz. an ipsilateral dorsal spinocerebellar tract, presumably arising in dorsal root ganglion cells, and a larger ventral pathway, bilaterally arising in the spinal gray matter. The latter tract mainly originates in the ventrolateral and ventromedial spinal fields. Furthermore, a secondary trigeminocerebellar projection arising in the descending trigeminal nucleus, a cerebellar projection arising in the dorsal column nucleus, a small projection arising in a possible primordium of the mammalian nucleus prepositus hypoglossi, a raphecerebellar projection, and a small cerebellar projection originating in the ipsilateral mesencephalic tegmentum were demonstrated.

Cerebellar efferents in Xenopus laevis are mainly aimed at the vestibular nuclear complex. A distinct ipsilateral cerebellovestibular projection present throughout the vestibular nuclear complex presumably arises in Purkyně cells, a smaller contralateral projection in the cerebellar nucleus. In addition, a small primordial brachium conjunctivum, projecting to the red nucleus, was noted.

The basic pattern of cerebellar connections as suggested for terrestrial vertebrates (ten Donkelaar and Bangma 1984) is also found in the permanently aquatic anuran Xenopus laevis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams JC (1981) Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775

    Google Scholar 

  • Altman JS, Dawes AE (1983) A cobalt study of medullary sensory projections from lateral line nerves, associated cutaneous nerves, and the VIIIth nerve in adult Xenopus. J Comp Neurol 213:310–326

    Google Scholar 

  • Ansorge K, Grüsser-Cornehls U (1978) Visual and visual-vestibular responses in frog cerebellar and spinal cord neurons. Neurosci Lett Suppl 1:S 350

    Google Scholar 

  • Antal M, Tornai I, Székely G (1980) Longitudinal extent of dorsal root fibers in the spinal cord and brain stem of the frog. Neuroscience 5:1311–1322

    Google Scholar 

  • Bangma GC (1983) Cerebellar connections in some reptiles. Thesis, University of Nijmegen

  • Bangma GC, ten Donkelaar HJ (1982) Afferent connections of the cerebellum in various types of reptiles. J Comp Neurol 207:255–273

    Google Scholar 

  • Bangma GC, ten Donkelaar HJ, Dederen, J, de Boer-van Huizen R (1983) Efferent connections of the cerebellum in the lizard Varanus exanthematicus. Neurosci Lett Suppl 14:S 16

    Google Scholar 

  • Barnard JW (1936) A phylogenetic study of the visceral afferent areas associated with the facial, glossopharyngeal, and vagus nerves, and their fiber connections. The efferent facial nucleus. J Comp Neurol 65:503–602

    Google Scholar 

  • Brecha N, Karten HJ, Hunt SP (1980) Projections of the nucleus of the basal optic root in the pigeon: an autoradiographic and horseradish peroxidase study. J Comp Neurol 189:615–670

    Google Scholar 

  • Brodal A (1981) Neurological anatomy in relation to clinical medicine. 3rd ed. Oxford University Press, New York

    Google Scholar 

  • Brown-Gould B (1980) Organization of afferents from the brain stem nuclei to the cerebellar cortex in the cat. Adv Anat embryol Cell Biol, Vol 62, Springer, Berlin Heidelberg New York

    Google Scholar 

  • Clarke PGH (1977) Some visual and other connections to the cerebellum of the pigeon. J Comp Neurol 174:535–552

    Google Scholar 

  • Cochran SL, Hackett JT (1977) The climbing fiber efferent system of the frog. Brain Res 121:362–267

    Google Scholar 

  • Corvaja N, D'Ascanio P (1981) Spinal projections from the mesencephalon in the toad. Brain Behav Evol 19:205–213

    Google Scholar 

  • Donkelaar HJ ten (1982) Organization of descending pathways to the spinal cord in amphibians and reptiles. In: Kuypers HGJM, Martin GF (eds) Progress in brain research, Vol 57: Descending pathways to the spinal cord. Elsevier Biomedical Press, Amsterdam: pp 25–67

    Google Scholar 

  • Donkelaar HJ ten, Bangma GC (1984) The cerebellum. In: Gans C, Northcutt RG (eds) Biology of the reptilia, Vol 17: Neurology C. Academic Press, London, in press

    Google Scholar 

  • Donkelaar HJ ten, de Boer-van Huizen R (1982) Basal ganglia projections to the brain stem in the lizard Varanus exanthematicus as demonstrated by retrograde transport of horseradish peroxidase. Neuroscience 6:1567–1590

    Google Scholar 

  • Donkelaar HJ ten, de Boer-van Huizen R (1982) Observations on the development of descending pathways from the brain stem to the spinal cord in the clawed toad Xenopus laevis. Anat Embryol 163:461–473

    Google Scholar 

  • Donkelaar HJ ten, de Boer-van Huizen R, Schouten FTM, Eggen SJH (1981) Cells of origin of descending pathways to the spinal cord in the clawed toad (Xenopus laevis). Neuroscience 6:2297–2312

    Google Scholar 

  • Ebbesson SOE (1976) Morphology of the spinal cord. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg: pp 679–706

    Google Scholar 

  • Fuller PM (1974) Projections of the vestibular nuclear complex in the bullfrog (Rana catesbeiana). Brain Behav Evol 10:157–169

    Google Scholar 

  • Fuller PM, Ebbesson SOE (1973) Central projections of the trigeminal nerve in the bullfrog (Rana catesbeiana) J Comp Neurol 152:193–199

    Google Scholar 

  • Gilman S, Bloedel JR, Lechtenberg R (1981) Disorders of the cerebellum. FA Davis Co. Philadelphia

    Google Scholar 

  • Grant P, Rubin E (1980) Ontogeny of the retina and optic nerve in Xenopus laevis. II. Ontogeny of the optic fiber pattern in the retina J Comp Neurol 189:671–698

    Google Scholar 

  • Gregory KM (1972) Centra projections of the eighth nerve in frogs. Brain Behav Evol 5:70–88

    Google Scholar 

  • Griffin G, Watkins LR, Mayer DJ (1979) HRP pellets and slowrelease gels: two new techniques for greater localization and sensitivity. Brain Res 168:595–601

    Google Scholar 

  • Grover BG (1983) Topographic organization of cerebellar efferents in the frog (Rana esculenta) as revealed by retrograde transport of wheat germ agglutinin conjugated horseradish peroxidase. Neurosci Lett Suppl 14:S 146

    Google Scholar 

  • Grover BG, Grüsser-Cornehls U (1980) Some ascending and descending pathways in the frog revealed by horseradish peroxidase. Neurosci Lett Suppl 5:S 193

    Google Scholar 

  • Hayle TH (1973) A comparative study of spinocerebellar systems in three classes of poikilothermic vertebrates. J Comp Neurol 149:477–495

    Google Scholar 

  • Hillman DE (1969) Light and electron microscopical study of the relationship between the cerebellum and the vestibular organ of the frog. Exp Brain Res 9:1–15

    Google Scholar 

  • Hillman DE (1972) Vestibulocerebellar input in the frog: anatomy. In: Brodal A, Pompeiano O (eds) Progress in brain research, Vol 37: Basic aspects of central vestibular mechanisms. Elsevier. Amsterdam. pp 329–339

    Google Scholar 

  • Joseph BS, Whitlock DG (1968) Central projections of selected spinal dorsal roots in anuran amphibians. Anat Rec 160:279–288

    Google Scholar 

  • Joseph BS, King RB, Whitlock DG (1968) Central distribution of trigeminal primary afferent fibers in anuran amphibians. Anat Rec 160:719–727

    Google Scholar 

  • Katz MJ, Lasek RJ (1979) Substrate pathways which guide growing axons in Xenopus embryos. J Comp Neurol 183:817–832

    Google Scholar 

  • Kokoros JJ, Northcutt RG (1977) Telencephalic efferents of the tiger salamander Ambystoma tigrinum tigrinum (Green). J Comp Neurol 173:613–628

    Google Scholar 

  • Larsell O (1923) The cerebellum of the frog. J Comp Neurol 36:89–112

    Google Scholar 

  • Larsell O (1967) The comparative anatomy and histology of the cerebellum from myxinoids through birds: Univ Minnesota Press Mineapolis

    Google Scholar 

  • Levine RL (1980) an autoradiographic study of the retinal projection in Xenopus laevis with comparisons to Rana. J Comp Neurol 189:1–29

    Google Scholar 

  • Lowe DA, Russell IJ (1982) The central projections of lateral line and cutaneous sensory fibres (VII and X) in Xenopus laevis. Proc R Soc Lond B 216:279–297

    Google Scholar 

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

    Google Scholar 

  • Matesz C, Székely G (1978) The motor colum and sensory projections of the branchial cranial nerves in the frog. J Comp Neurol 178:157–176

    Google Scholar 

  • Mehler WR (1972) Comparative anatomy of the vestibular nuclear complex in submammalian vertebrates. In: Brodal A, Pompeiano O (eds) Progress in brain research, Vol 37: Basic aspects of central vestibular mechanisms. Elsevier, Amsterdam, pp 55–67

    Google Scholar 

  • Mesulam M-M (1978) Tetramethylbenzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117

    Google Scholar 

  • Nieuwenhuys R, Opdam P (1976) Structure of the brain stem. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg, pp 811–855

    Google Scholar 

  • Nikundiwe AM, Nieuwenhuys R (1983) The cells masses in the brainstem of the South African clawed frog Xenopus laevis: a topographical and topological analysis. J Comp Neurol 213:199–219

    Google Scholar 

  • Nikundiwe AM, de Boer-van Huizen R, ten Donkelaar HJ (1982) Dorsal root projections in the clawed toad (Xenopus laevis) as demonstrated by anterograde labeling with horseradish peroxidase. Neuroscience 7:2089–2103

    Google Scholar 

  • Plassmann W (1980) Central neuronal pathways in the lateral line system of Xenopus laevis. J Comp Physiol 36:203–213

    Google Scholar 

  • Potter HD (1965) Mesencephalic auditory region of the bullfrog. J Neurophysiol 28:1132–1154

    Google Scholar 

  • Prior LJ, Cruce WLR (1982) Organization of frog mesencephalic tegmental nuclei. Soc Neurosci Abst 8:875

    Google Scholar 

  • Röthig P (1927) Beiträge zum Studium des Zentralnervensystems der Wirbeltiere. II Über die Faserzüge im Mittelhirn, Kleinhirn und der Medulla oblongata der Urodelen und Anuren. Z mikranat Forsch 10:381–472

    Google Scholar 

  • Rubinson K (1968) Projections of the tectum opticum of the frog. Brain Behav Evol 1:529–560

    Google Scholar 

  • Rushmer DS (1970) Electrophysiological evidence for primary somesthetic afferent connections in the frog cerebellum. Brain Res 18:560–564

    Google Scholar 

  • Stern TA, Rubinson K (1971) Efferent projections of the cerebellar cortex of Rana pipiens, Anat Rec 169:438

    Google Scholar 

  • Tohyama M, Maeda T, Shimizu N (1975) Comparative anatomy of the locus coeruleus. II Organization and projection of the catecholamine containing neurons in the upper rhombencephalon of the frog, Rana catesbeiana. J Hirnforsch 16:81–89

    Google Scholar 

  • Vesselkin NP, Ermakova TV, Kenigfest NB, Goiković M (1980) The striatal connection in frog Rana temporaria: an HRP study. J Hirnforsch 21:381–392

    Google Scholar 

  • Wilczynski W (1981) Afferents to the midbrain auditory center in the bullfrog Rana catesbeiana. Anat Rec 198:421–433

    Google Scholar 

  • Wilczynski W (1982) Brainstem afferents to the cerebellum in the leopard frog, Rana pipiens. Anat Rec 202:203A

  • Wilczynski W, Northcutt RG (1977) Afferents to the optic tectum of the leopard frog: an HRP study. J Comp Neurol 173:219–230

    Google Scholar 

  • Woodburne RT (1936) A phylogenetic consideration of the primary and secondary centers and connections of the trigeminal complex in a series of vertebrates. J Comp Neurol 65:403–502

    Google Scholar 

  • Yamamoto K, Tohyama M, Shimizu N (1977) Comparative anatomy of the topography of catecholamine containing neuron systems in the brain stem from birds to teleosts. J Hirnforsch 18:229–240

    Google Scholar 

Download references

Author information

Author notes

  1. A. Gonzalez

    Present address: Departamento de Morfologia Microscopia, Universidad Complutense, Madrid, (Spain)

Authors and Affiliations

  1. Department of Anatomy and Embryology, University of Nijmegen, P.O. Box 9101, 6500 HB, Nijmegen, The Netherlands

    A. Gonzalez, H. J. ten Donkelaar & R. de Boer-van Huizen

Authors
  1. A. Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. J. ten Donkelaar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. de Boer-van Huizen
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gonzalez, A., ten Donkelaar, H.J. & de Boer-van Huizen, R. Cerebellar connections in Xenopus laevis . Anat Embryol 169, 167–176 (1984). https://doi.org/10.1007/BF00303146

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00303146

Key words

Search

Navigation