Skip to main content
Log in

Synapses on motoneuron dendrites in the brachial section of the frog spinal cord: a computer-aided electron microscopic study of cobalt-filled cells

  • Published:
Journal of Neurocytology

Summary

Cobalt-labelled motoneuron dendrites of the frog spinal cord at the level of the second spinal nerve were photographed in the electron microscope from long series of ultrathin sections. Three-dimensional computer reconstructions of 120 dendrite segments were analysed. The samples were taken from two locations: proximal to cell body and distal, as defined in a transverse plane of the spinal cord. The dendrites showed highly irregular outlines with many 1–2 μm-long ‘thorns’ (on average 8.5 thorns per 100 μm2 of dendritic area). Taken together, the reconstructed dendrite segments from the proximal sites had a total length of about 250 μm; those from the distal locations, 180 μm. On all segments together there were 699 synapses. Nine percent of the synapses were on thorns, and many more close to their base on the dendritic shaft. The synapses were classified in four groups. One third of the synapses were asymmetric with spherical vesicles; one half were symmetric with spherical vesicles; and one tenth were symmetric with flattened vesicles. A fourth, small class of asymmetric synapses had dense-core vesicles. The area of the active zones was large for the asymmetric synapses (median value 0.20 μm2), and small for the symmetric ones (median value 0.10 μm2), and the difference was significant. On average, the areas of the active zones of the synapses on thin dendrites were larger than those of synapses on large calibre dendrites. About every 4 μm2 of dendritic area received one contact. There was a significant difference between the areas of the active zones of the synapses at the two locations. Moreover, the number per unit dendritic length was correlated with dendrite calibre. On average, the active zones covered more than 4% of the dendritic area; this value for thin dendrites was about twice as large as that of large calibre dendrites. We suggest that the larger active zones and the larger synaptic coverage of the thin dendrites compensate for the longer electrotonic distance of these synapses from the soma.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Antal, M. (1984) The application of cobalt labelling to electron microscopic investigations of serial sections.Journal of Neuroscience Methods 12, 69–77.

    PubMed  Google Scholar 

  • Antal, M. &Kraftsik, R. (1987) Synaptic organization of motoneuron dendritic trees in the frog spinal cord.Neuroscience (Suppl.)22, S793.

    Google Scholar 

  • Antal, M., Kraftsik, R., Székely, G. &Van Der Loos, H. (1986) Distal dendrites of frog motoneurons: a computer-aided electron microscopic study of cobalt-filled cells.Journal of Neurocytology 15, 303–10.

    PubMed  Google Scholar 

  • Bras, H., Destombes, J., Gogan, P. &Tyc-Dumont, S. (1987) The dendrites of single brain-stem motoneurons intracellularly labelled with horseradish peroxidase in the cat. An ultrastructural analysis of the synaptic covering and microenvironment.Neuroscience 22, 971–82.

    PubMed  Google Scholar 

  • Brookhart, J. M. &Kubota, K. (1963) Studies on the integrative function of the motor neurone.Progress in Brain Research 1, 38–61.

    Google Scholar 

  • Brown, A. G. &Fyffe, R. E. V. (1981) Direct observations on the contacts made between Ia afferent fibres and α-motoneurones in the cat's lumbosacral spinal cord.Journal of Physiology 313, 121–40.

    PubMed  Google Scholar 

  • Conradi, S., Kellerth, J. -O. &Berthold, C. -H. (1979a) Electron microscopic studies of serially sectioned cat spinal α-motoneurons. II. A method for the description of architecture and synaptology of the cell body and proximal dendritic segments.Journal of Comparative Neurology 184, 741–53.

    PubMed  Google Scholar 

  • Conradi, S., Kellerth, J. -O., Berthold, C. -H. &Hammarberg, C. (1979b) Electron microscopical studies of serially sectioned cat spinal α-motoneurons. IV. Motoneurons innervating slow-twitch (type S) units of the soleus muscles.Journal of Comparative Neurology 184, 769–82.

    PubMed  Google Scholar 

  • Corvaja, N., Grofova, I. &Pompeiano, O. (1973) The origin, course and termination of vestibulospinal fibres in the toad.Brain, Behavior and Evolution 7, 401–23.

    Google Scholar 

  • Cruce, W. L. R. (1974) A supraspinal monosynaptic input to hindlimb motoneurons in lumbar spinal cord of the frog,Rana catesbeiana. Journal of Neurophysiology 37, 691–704.

    Google Scholar 

  • Czéh, G. (1972) The role of dendritic events in the initiation of monosynaptic spikes in the frog motoneurons.Brain Research 39, 505–9.

    PubMed  Google Scholar 

  • D'Ascanio, P., Corvaja, N. &Grofova, I. (1979) Retrograde axonal transport from spinal cord to brain stem cell groups in the toad.Neuroscience Letters (Suppl.)3, S134.

    Google Scholar 

  • Dunn, O. J. &Clark, V. A. (1987)Applied Statistics: Analysis of Variance and Regression. 2nd ed. New York: J. Wiley & Sons.

    Google Scholar 

  • Fifkova, E. (1985) A possible mechanism of morphometric changes in dendritic spines induced by stimulation.Cellular and Molecular Neurobiology 5, 47–63.

    PubMed  Google Scholar 

  • Fuller, P. M. (1974) Projections of the vestibular nuclear complex in the bullfrog (Rana catesbeiana).Brain, Behavior and Evolution 10, 157–69.

    Google Scholar 

  • Görcs, T., Antal, M., Olah, E. &Székely, G. (1979) An improved cobalt labeling technique with complex compounds.Acta Biologica Academiae Scientiarum Hungaricae 30, 79–86.

    PubMed  Google Scholar 

  • Grantyn, R., Shapovalov, A. I. &Shiriaev, B. I. (1982) Combined morphological and electrophysiological description of connections between single primary afferent fibres and motoneurones in the frog spinal cord.Experimental Brain Research 48, 459–62.

    Google Scholar 

  • Grover, B. G. &Grüsser-Cornehls, U. (1980) Some ascending and descending spinal pathways in the frog revealed by horseradish peroxidase.Neuroscience Letters (Suppl.)5, S193.

    Google Scholar 

  • Hornung, J. -P. &Kraftsik, R. (1988) Three-dimensional reconstruction procedure using GKS primitives and software transformations for anatomical studies of the nervous system. InNew Trends in Computer Graphics (edited byMagnenat-Thalmann, N. &Thalmann, D.) pp. 555–64. Berlin, Heidelberg: Springer-Verlag.

    Google Scholar 

  • Houser, D. R., Lee, M. &Vaughn, J. E. (1983) Immuno-cytochemical localization of glutamic acid decarboxylase in normal and deafferented superior colliculus: Evidence for reorganization of γ-aminobutyric acid synapses.Journal of Neuroscience 3, 2030–42.

    PubMed  Google Scholar 

  • Ihaveri, S. &Frank, E. (1983) Central projections of the brachial nerve in bullfrogs: muscle and cutaneous afferents project to different regions of the spinal cord.Journal of Comparative Neurology 221, 304–12.

    PubMed  Google Scholar 

  • Jack, J. J. B., Redman, S. J. &Wong, U. (1981) The components of synaptic potentials evoked in spinal motoneurones by impulses in single group Ia fibres.Journal of Physiology 321, 111–26.

    PubMed  Google Scholar 

  • Kellerth, J. -O., Conradi, S. &Berthold, C. -H. (1979) Electron microscopic studies of serially sectioned cat spinal α-motoneurons. III. Motoneurons innervating fast-twitch (type FR) units of the gastrocnemius muscle.Journal of Comparative Neurology 184, 755–67.

    PubMed  Google Scholar 

  • Kellerth, J. -O., Conradi, S. &Berthold, S. -H. (1983) Electron microscopic studies of serially sectioned cat spinal α-motoneurons. V. Motoneurons innervating fast twitch (type FE) units of the gastrocnemius muscle.Journal of Comparative Neurology 214, 451–8.

    Google Scholar 

  • Kisvárday, Z. F., Martin, K. A. C., Friedlander, M. J. &Somogyi, P. (1987) Evidence for interlaminar inhibitory circuits in the striate cortex of the cat.Journal of Comparative Neurology 260, 1–19.

    PubMed  Google Scholar 

  • Krzanowski, W. J., (1990)Principles of Multivariate Analysis. Oxford: Clarendon Press.

    Google Scholar 

  • Lagerbäck, P. -A. (1985) An ultrastructural study of cat lumbosacral α-motoneurons after retrograde labeling with horseradish peroxidase.Journal of Comparative Neurology 240, 256–64.

    PubMed  Google Scholar 

  • Lagerbäck, P. -A., Cullheim, S. &Ulfhake, B. (1986) Electron microscopic observations on the synaptology of cat sciatic α-motoneurons after intracellular staining with horseradish peroxidase.Neuroscience Letters 70, 23–7.

    PubMed  Google Scholar 

  • Lévai, G., Matesz, C. &Székely, G. (1982) Fine structure of dorsal root terminals in the dorsal horn of the frog spinal cord.Acta Biologica Academiae Scientiarium Hungaricae 33, 231–46.

    Google Scholar 

  • Magherini, P. C., Precht, W. &Richter, A. (1974) Vestibulospinal effects on hindlimb motoneurons of the frog.Pflügers Archiv 348, 211–23.

    Google Scholar 

  • Mclean, J. H. &Hopkins, D. A. (1985) Ultrastructural studies of the nucleus ambiguus in cat and monkey following injection of HRP into the vagus nerve.Journal of Neurocytology 14, 961–79.

    PubMed  Google Scholar 

  • Morales, M. &Fifková, E. (1989)In situ localisation of myosin and actin in dendritic spines with the immuno-gold technique.Journal of Comparative Neurology 279, 666–74.

    PubMed  Google Scholar 

  • Nakajima, Y. &Reese, T. S. (1983) Inhibitory and excitatory synapses in crayfish stretch receptor organs studied with direct rapid freezing and freeze substitution.Journal of Comparative Neurology 213, 66–73.

    PubMed  Google Scholar 

  • Pongrác, F. (1985) The function of dendritic spines: a theoretical study.Neuroscience 15, 933–46.

    PubMed  Google Scholar 

  • Purves, D. &Voyvodic, J. T. (1987) Imaging mammalian nerve cells and their connections over time in living animals.Trends in Neuroscience 10, 398–404.

    Google Scholar 

  • Ramon Y Cajal, S. (1933) (trans. 1954) Neuron Theory or Reticular Theory? (translated byUbeda Purkiss, M. &Fox, C. A.) Madrid: Consejo Superior de Investigationes Cientfficas.

    Google Scholar 

  • Redman, S. &Walmsley, B. (1983) Amplitude fluctuations in synaptic potentials evoked in cat spinal motoneurones at identified group Ia synapses.Journal of Physiology 343, 135–45.

    PubMed  Google Scholar 

  • SAS (1985a)User's Guide: Basics. 5th edition. Cary, NC: SAS Institute Inc.

    Google Scholar 

  • SAS (1985b)User's Guide: Statistics. 5th edition. Cary, NC: SAS Institute Inc.

    Google Scholar 

  • SAS/GRAPH (1985)User's guide. 5th edition. Cary, NC: SAS Institute Inc.

    Google Scholar 

  • Schwindt, P. C. (1976) Electrical properties of spinal motoneurons. InFrog Neurobiology (edited byLlinas, R. &Precht, W.) pp. 750–64. Berlin: Springer-Verlag.

    Google Scholar 

  • Shapovalov, A. I. (1975) Neuronal organization of synaptic mechanisms of supraspinal motor control in vertebrates.Review of Physiology, Biochemistry and Pharmacology 72, 1–54.

    Google Scholar 

  • Sokal, R. R. &Rohlf, F. J. (1981)Biometry. 2nd ed., New York: W. H. Freeman.

    Google Scholar 

  • Sotelo, C., Gotow, T. &Wassef, M. (1986) Localization of glutamic-acid-decarboxylase-immunoreactive axon terminals in the inferior olive of the rat, with special emphasis on anatomical relations between GABAergic synapses and dendrodendritic gap junctions.Journal of Comparative Neurology 252, 32–50.

    PubMed  Google Scholar 

  • Székely, G. (1976) The morphology of motoneurons and dorsal root fibers in the frog's spinal cord.Brain Research 103, 275–90.

    PubMed  Google Scholar 

  • Székely, G. &Antal, M. (1984) Segregation of muscle and cutaneous afferent fibre terminals in the brachial spinal cord of the frog.Journal für Hirnforschung 23, 671–5.

    Google Scholar 

  • Székely, G. &Gallyas, F. (1975) Intensification of cobaltous sulphide precipitate in frog nervous tissue.Acta Biologica Academiae Scientiarum Hungaricae 26, 175–88.

    PubMed  Google Scholar 

  • Székely, G. &Levai, G. (1981) Synaptic relations of dorsal root fibres in the frog spinal cord. InSpinal Cord Sensation (edited byBrown, A. G. &Rethelyi, M.) pp. 157–64. Edinburgh: Scottish Academic Press.

    Google Scholar 

  • Székely, G., Nagy, J., Wolf, E. &Nagy, P. (1989) Spatial distribution of pre- and postsynaptic locations of axon terminals in the dorsal horn of the frog spinal cord.Neuroscience 29, 175–88.

    PubMed  Google Scholar 

  • Ten Donkelaar, H. J., De Boer-Van Huizen, R., Schouten, F. T. M. &Eggen, S. J. H. (1981) Cells of origin of descending pathways to the spinal cord in clawed toad (Xenopus laevis).Neuroscience 6, 2297–312.

    PubMed  Google Scholar 

  • Triller, A., Cluzeaud, F., Pfeiffer, F., Betz, H. &Korn, H. (1985) Distribution of glycine receptors at central synapses: an immunoelectron microscopy study.Journal of Cell Biology 101, 683–8.

    PubMed  Google Scholar 

  • Triller, A., Seitanidou, T., Franksson, O., &Korn, H. (1990) Size and shape of glycine receptor clusters in a central neuron exhibit a somato-dendritic gradient.The New Biologist 7, 637–41.

    Google Scholar 

  • Uchizono, K. (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat.Nature 207, 642–3.

    PubMed  Google Scholar 

  • Walberg, F. (1966) Elongated vesicles in terminal boutons of the central nervous system, a result of aldehyde fixation.Acta Anatomica 65, 224–35.

    PubMed  Google Scholar 

  • Wang, C. L., Sakamoto, H. &Saito, K. (1989) Ultrastructure and synaptic architecture of spinal motoneurons in the frog (Rana catesbeiana).Acta Anatomica 134, 1–11.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Antal, M., Kraftsik, R., Székely, G. et al. Synapses on motoneuron dendrites in the brachial section of the frog spinal cord: a computer-aided electron microscopic study of cobalt-filled cells. J Neurocytol 21, 34–49 (1992). https://doi.org/10.1007/BF01206896

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01206896

Keywords

Navigation