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Morphology and distribution of the synapses to the spinal motoneuron of the frog

With special reference to the subsurface cisterns

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Summary

The quantitative distribution of the different structural elements on the surface of the motoneurons (MN) in the spinal cord of the frog was studied in thin sections and freeze-fracture replicas.

In particular, the different synaptic types and their distribution on the MN soma and dendrites are described. In thin sections three types of synapses were discerned: the S-type with spherical vesicles, the F-type with flattened vesicles, and finally the C-type synapse with spherical vesicles and a subsynaptic cistern. The synaptic covering at the MN surface as determined by thin sections is about 36%. In freeze-fracture replicas we observed boutons with and without gap junctions, and C-type boutons. When using the latter technique the synaptic covering was found to be 43%.

With both techniques special attention was paied to the morphology of the C-type bouton and both the subsynaptic and extrasynaptic cisterns. The soma membrane over the sub- and extrasynaptic cisterns reveals characteristic and very similar morphological features with respect to both the distribution and size of the membrane particles. The possible functions of the two cisternal types are discussed.

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References

  • Araki T, Otani T, Furukawa T (1953) The electrical activities of single motoneurons in toad's spinal cord recorded with intracellular electrodes. Jp J Physiol 3:254–267

    Google Scholar 

  • Beux Y Le (1972) Subsurface cisterns and lamellar bodies: particular forms of the endoplasmic reticulum in neurons. Z Zellforsch 133:327–352

    Google Scholar 

  • Buschmann MB T (1979) Development of lamellar bodies and subsurface cisterns in pyramidal cells and neuroblasts of hamster cerebral cortex. Am J Anat 155:175–184

    Google Scholar 

  • Charlton BT, Gray EG (1965) Electron microscopy of specialized synaptic contacts suggesting possible electrical transmission in frog spinal cord. J Physiol 179:2–4P

    Google Scholar 

  • Charlton BT, Gray EG (1966) Comparative electron microscopy of synapses in the vertebrate spinal cord. J Cell Sci 1:67–80

    Google Scholar 

  • Conradi S (1970a) Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult rat. Acta physiol scand 78:Suppl 332:5–48

    Google Scholar 

  • Conradi S (1970b) Ultrastructure and distribution of neuronal and glial elements on the surface of the proximal part of a motoneuron dendrite, as analyzed by serial sections. Acta physiol scand 78, Suppl. 332:49–61

    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. J Comp Neurol 184:741–754

    Google Scholar 

  • Conradi S, Kellerth J-O, Berthold C-H, Hammarberg C (1979b) Electron microscopic studies of serially sectioned cat spinal α-motoneurons. IV. Motoneurons innervating slow-twitch (type S) units of the soleus muscle. J Comp Neurol 184:769–782

    Google Scholar 

  • Curtis DR, Phillis JW, Watkins JC (1961) Actions of amino acids on the isolated hemisected spinal cord of the toad. Br J Pharmacol 16:262–283

    Google Scholar 

  • Eccles JC (1946) Synaptic potentials of motoneurons. J Neurophysiol 9:87–120

    Google Scholar 

  • Eccles JC (1964) The physiology of synapses. Springer Verlag, Heidelberg, Germany

    Google Scholar 

  • Fadiga E, Brookhart JM (1960) Monosynaptic activation of two different portions of the motoneuron membrane. Am J Physiol 198:693–703

    Google Scholar 

  • Fisher SK, Goldman K (1975) Subsurface cisterns in the vertebrate retina. Cell Tissue Res 164:473–480

    Google Scholar 

  • Gray EG (1961a) The granule cells, mossy synapses and Purkinje spine synapses of the cerebellum, light and electronmicroscope observations. J Anat 95:345–356

    Google Scholar 

  • Gray EG (1961b) Ultrastructure of synapses of the cerebral cortex and of certain specialisations of neuroglial membranes. In: Boyd JD et al. (eds). Electron Microscopy in Anatomy, London, Arnold, pp 54–73

    Google Scholar 

  • Grinnell AD (1966) A study of the interaction between motoneurones in the frog spinal cord. J Physiol (Lond) 182:612–648

    Google Scholar 

  • Henkart M, Landis D, Reese TS (1976) Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons. J Cell Biol 70:338–347

    Google Scholar 

  • Kellerth J-O, Berthold D-H, Conradi S (1979) Electron microscopic studies of serially sectioned cat spinal α-motoneurons. III. Motoneurons innervating fast-twitch (type FR) units of the gastrocnemius muscle. J Comp Neurol 184:755–768

    Google Scholar 

  • Kennard DW (1959) The anatomical organisation of neurons in the lumbar region in the spinal cord of the frog (Rana temporaria). J Comp Neurophysiol 111:447–567

    Google Scholar 

  • McLaughlin BJ (1972a) The fine structure of neurons and synapses in the motor nuclei of the cat spinal cord. J Comp Neurol 144:429–460

    Google Scholar 

  • McLaughlin BJ (1972b) Dorsal root projections to the motor nuclei in the cat spinal cord. J Comp Neurol 144:461–474

    Google Scholar 

  • McLaughlin BJ (1972c) Propriospinal and supraspinal projections to the motor nuclei in the cat spinal cord. J Comp Neurol 144:475–500

    Google Scholar 

  • Pappas GD, Waxman SG, Bennett MVL (1975) Morphology of spinal electromotor neurons and presynaptic coupling in the gymnotid Sternarchus albifrons. J Neurocytol 4:469–478

    Google Scholar 

  • Peters A, Palay SL, Webster H (1976) The fine structure of the nervous system: The neurons and supporting cells. WB Saunders Comp. Philadelphia London Toronto

    Google Scholar 

  • Pfenninger K, Akert K, Moor H, Sandri C (1972) The fine structure of freeze-fractured presynaptic membranes. J Neurocytol 1:129–149

    Google Scholar 

  • Pullen AH, Sears TA (1978) Modification of “C” synapses following partial central deafferentation of thoracic motoneurones. Brain Res 145:141–146

    Google Scholar 

  • Ronnevi L-O (1979) Spontaneous phagocytosis of C-type synaptic terminal by spinal α-motoneurons in newborn kittens. An electron microscopic study. Brain Res 162:189–199

    Google Scholar 

  • Ronnevi L-O, Conradi S (1974) Ultrastructural evidence for spontaneous elimination of synaptic terminals on spinal motoneurons in the kitten. Brain Res 80:335–339

    Google Scholar 

  • Rosenbluth J (1962) Subsurface cisterns and their relationship to the neuronal plasma membrane. J Cell Biol 13:405–421

    Google Scholar 

  • Schwarke K (1980) Membranpartikel und Membranfunktion. Eine Gefrierbruchstudie an der Rattenniere und dem Froschruckenmark. Dissertation, Heidelberg

  • Silver ML (1942) The motoneurons of the frog spinal cord. J Comp Neurol 77:1–39

    Google Scholar 

  • Sonnhof U (1979) Elektrische und chemische Synapsen am Motoneuron des Frosches. Eine Untersuchung der ionalen Mechanismen von Erregung und Hemmung mit Hilfe intraund extrazellulärer lonenaktivitätsmessungen. Habilitationsschrift, Heidelberg

    Google Scholar 

  • Sonnhof U, Grafe P, Krumnikl G, Linder M, Schindler L (1973) Postsynaptic actions of GABA, glycine and glutamate on motoneurons of the isolated spinal cord of the frog. Pflügers Arch Ges Physiol 343:Suppl R136

  • Sonnhof U, Grafe P, Krumnikl G, Linder M, Schindler L (1975) Inhibitory postsynaptic actions of taurine GABA and other amino acids on motoneurons of the isolated frog spinal cord. Brain Res 100:327–341

    Google Scholar 

  • Sonnhof U, Linder M, Grafe P, Krumnikl G (1975b) Postsynaptic actions of glutamate on somatic and dendritic membrane areas of the lumbar motoneurons of the frog. Pflügers Arch 355:171

    Google Scholar 

  • Sonnhof U, Richter DW, Taugner R (1977) Electrotonic coupling between frog spinal motoneurons. An electrophysiological and morphological study. Brain Res 138:197–215

    Google Scholar 

  • Sotelo C, Palay SL (1967) Synapses avec des contacts étroits (tight junctions) dans le noyau vestibulaire latéral du rat. J Microsc 6:83a

    Google Scholar 

  • Sotelo C, Palay SL (1970) The fine structure of the lateral vestibular nucleus in the rat. II. Synaptic organization. Brain Res 18:93–115

    Google Scholar 

  • Sotelo C, Grofova I (1976) Ultrastructure features of the spinal cord. Frog Neurobiol. (R Llinas, W Precht, eds), Springer Verlag

  • Spoerri PE, Glees P (1977) Subsurface cisterns in the Cynomolgus retina. Cell Tissue Res 182:33–38

    Google Scholar 

  • Stensaas LJ, Stensaas SS (1971) Light and electron microscopy of motoneurons and neuropile in the amphibian spinal cord. Brain Res 31:67–84

    Google Scholar 

  • Streit P, Akert K, Sandri C, Livingston RB, Moor H (1972) Dynamic ultrastructure of presynaptic membranes at nerve terminals in the spinal cord of rats. Anesthetized and unanesthetized preparations compared. Brain Res 48:11–26

    Google Scholar 

  • Sumner BEH (1974) A quantitative study of subsurface cisterns and their relationships in normal and axotomized hypoglossal neurones. Exp Brain Res 22:175–183

    Google Scholar 

  • Taugner R, Sonnhof U, Richter DW, Schiller A (1978) Mixed (chemical and electrical) synapses on frog spinal motoneurons. Cell Tissue Res 193:41–59

    Google Scholar 

  • Uchizono R (1966) Excitatory and inhibitory synapses in the cat spinal cord. Jpn J Physiol 16:570–575

    Google Scholar 

  • Watanabe H, Burnstock G (1976) Junctional subsurface organs in frog sympathetic ganglion cells. J Neurocytol 5:125–136

    Google Scholar 

  • Werman R, Carlen PL (1976) Unusual behavior of the la EPSP in cat spinal motoneurons. Brain Res 112:395–401

    Google Scholar 

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Voss, C., Schiller, A. & Taugner, R. Morphology and distribution of the synapses to the spinal motoneuron of the frog. Cell Tissue Res. 213, 253–271 (1980). https://doi.org/10.1007/BF00234786

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  • DOI: https://doi.org/10.1007/BF00234786

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