Skip to main content
SpringerLink
Log in

Microtubule-associated smooth endoplasmic reticulum in the frog's brain

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

Electron microscopic studies of neural processes in the cerebellum, optic tectum, and cerebral hemisphere of the frog reveal a distinctive system of SER cisternae lying at intervals (commonly 1–2 μm apart) perpendicular to the long axis of axons and dendrites, interconnected by tubular, longitudinally orientated SER elements, and in direct continuity with the outer membrane of mitochondria. The transverse cisternae are fenestrated, with a single mierotubule (or rarely, two) passing through the centre of each 50–75 nm fenestration. Extensions of the SER-microtubule complex may be located parasynaptically in axon terminals and dendrites. The SER of dendritic spines also appears to be continuous with the fenestrated cisternae.

Possible roles for the specialized SER (particularly of the parasynaptic extensions), such as calcium ion sequestration and ATP or monoamine oxidase transport, are discussed.

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

  • Banks, P., Mangnall, D., Mayor, D.: The redistribution of cytochrome oxidase, noradrenaline and adenosine triphosphate in adrenergic nerves constricted at two points. J. Physiol. (Lond.) 200, 745–762 (1969).

    Google Scholar 

  • Bannister, L.: Personal communication (1970).

  • Barondes, S. H.: Axoplasmic transport. Neurosci. Res. Program Bull. 5, 307–419 (1967).

    Google Scholar 

  • Cavallito, C. J.: Some speculations on the chemical nature of postjunctional membrane receptors. Fed. Proc. 26, 1647–1654 (1967).

    Google Scholar 

  • De Iraldi, A. P., De Robertis, E.: The neurotubular system of the axon and the origin of granulated and non-granulated vesicles in regenerating nerves. Z. Zellforsch. 87, 330–344 (1968).

    Google Scholar 

  • De Lorenzo, A. J. D., Brzin, M., Dettbarn, W. D.: Fine structure and organization of nerve fibers and giant axons in Homarus americanus. J. Ultrastruct. Res. 24, 367–384 (1968).

    Google Scholar 

  • Düring, M. V.: Über die Feinstruktur der motorischen Endplatte von höheren Wirbeltieren. Z. Zellforsch. 81, 74–90 (1967).

    Google Scholar 

  • Fahrenbach, W. H.: The morphology of the eyes of Limulus II. Z. Zellforsch. 93, 451–483 (1969).

    Google Scholar 

  • Fawcett, D. W.: The cell: its organelles and inclusions. Philadelphia: Saunders 1966.

    Google Scholar 

  • Follenius, E.: Organisation scalariforme du réticulum endoplasmique dans certains processus nerveux de l'hypothalamus de Gasterosteus aculeatus L. Z. Zellforsch. 106, 61–68 (1970).

    Google Scholar 

  • Fox, C. A., Siegesmund, K. A., Dutta, C. R.: The Purkinje cell dendritic branchlets and their relation with the parallel fibres: light and electron microscopic observations. In: M. M. Cohen and R. S. Snider (eds.), Morphological & biochemical correlates of neural activity, p. 112–141. New York: Harper & Row 1964.

    Google Scholar 

  • Gabella, G.: Caveolae intracellulares and sarcoplasmic reticulum in smooth muscle. J. Cell Sci. (in press) (1971).

  • Gage, P. W.: Depolarization and excitation-secretion coupling in presynaptic terminals. Fed. Proc. 26, 1627–1632 (1967).

    Google Scholar 

  • Grafstein, B.: Axonal transport: communication between soma and synapse. In: E. Costa and P. Greengard (eds.), Recent advances in biochemical psychopharmacology, p. 11–26, New York: Raven Press 1969.

    Google Scholar 

  • Grainger, F., James, D. W.: Mitochondrial extensions associated with microtubules in outgrowing processes from chick spinal cord in vitro. J. Cell Sci. 4, 729–737 (1969).

    Google Scholar 

  • —: Association of glial cells with the terminal parts of neurite bundles extending from chick spinal cord in vitro. Z. Zellforsch. 108, 93–104 (1970).

    Google Scholar 

  • Gray, E. G.: Axosomatic and axodendritic synapses of the cerebral cortex: an electron microscope study. J. Anat. (Lond.) 93, 420–433 (1959).

    Google Scholar 

  • —: Tissue of the central nervous system. In: S. M. Kurtz (ed.), Electron microscopic anatomy, p. 369–417. London and New York: Academic Press 1964.

    Google Scholar 

  • —: The fine structure of nerve. Comp. Biochem. Physiol. 36, 419–448 (1970).

    Google Scholar 

  • Hámori, J., Szentágothai, J.: The “crossing over” synapse: an electron microscope study of the molecular layer in the cerebellar cortex. Acta biol. Acad. Sci. hung. 15, 95–117 (1964).

    Google Scholar 

  • Hendelman, W.: The effect of thallium on peripheral nervous tissue in culture: a light and electron microscopic study. Anat. Rec. 163, 198–199 (1969).

    Google Scholar 

  • Holtzman, E., Novikoff, A. B.: Lysosomes in the rat sciatic nerve following crush. J. Cell Biol. 27, 651–669 (1965).

    Google Scholar 

  • Kapeller, K., Mayor, D.: An electron microscopic study of the early changes proximal to a constriction in sympathetic nerves. Proc. roy. Soc. B 172, 39–51 (1969).

    Google Scholar 

  • Koketsu, K.: Calcium and the excitable cell membrane. Neurosciences Res. 2, 1–39 (1969).

    Google Scholar 

  • Mouren-Mathieu, A.-M., Colonnier, M.: The molecular layer of the adult cat cerebellar cortex after lesion of the parallel fibres: an optic and electron microscope study. Brain Res. 16, 307–323 (1969).

    Google Scholar 

  • Nastuk, W. L.: Activation and inactivation of muscle postjunctional receptors. Fed. Proc. 26, 1639–1646 (1967).

    Google Scholar 

  • Novikoff, A. B.: Lysosomes in nerve cells. In: H. Hydén (ed.). The neuron, p. 319–377. Amsterdam-London-New York: Elsevier 1967.

    Google Scholar 

  • Peracchia, C.: A system of parallel septa in crayfish nerve fibers. J. Cell Biol. 44, 125–133 (1970).

    Google Scholar 

  • Peters, A., Palay, S. L., Webster, H. de F.: The fine structure of the nervous system. New York: Harper & Row 1970.

    Google Scholar 

  • —, Vaughn, J.: Microtubules and filaments in the axons and astrocytes of early postnatal rat optic nerves. J. Cell Biol. 32, 113–119 (1967).

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).

    Google Scholar 

  • Rodríguez Echandía, E. L., Zamora, A., Piezzi, R. S.: Organelle transport in constricted nerve fibers of the toad Bufo arenarum Hensel. Z. Zellforsch. 104, 419–428 (1970).

    Google Scholar 

  • Rubin, R. P.: The role of calcium in the release of neurotransmitter substances and hormones. Pharmacol. Rev. 22, 355–428 (1970).

    Google Scholar 

  • Sampson, H. W., Dill, R. E., Mathews, J. L., Martin, J. H.: An ultrastructural investigation of calcium-dependent granules in the rat neuropil. Brain Res. 22, 157–162 (1970).

    Google Scholar 

  • Sandborn, E. B.: Electron microscopy of the neuron membrane systems and filaments. Canad. J. Physiol. Pharmacol. 44, 329–338 (1966).

    Google Scholar 

  • Sandow, A.: Excitation-contraction coupling in skeletal muscle. Pharmacol. Rev. 17, 265–320 (1965).

    Google Scholar 

  • Schmitt, F. O., Sampson, F. E., Jr.: Neuronal fibrous proteins. Neurosci. Res. Program Bull. 6, 113–219 (1968).

    Google Scholar 

  • Schnaitman, C., Greenawalt, J. W.: Enzymatic properties of the inner and outer membranes of rat liver mitochondria. J. Cell Biol. 38, 158–175 (1968).

    Google Scholar 

  • Sétáló, G., Székely, G.: The presence of membrane specializations indicative of somatodendritic synaptic junctions in the optic tectum of the frog. Exp. Brain Res. 4, 237–242 (1967).

    Google Scholar 

  • Smith, D. S., Järlfors, U., Beránek, R.: The organization of synaptic axoplasm in the lamprey (Petromyzon marinus) central nervous system. J. Cell Biol. 46, 199–219 (1970).

    Google Scholar 

  • Sotelo, C.: Ultrastructural aspects of the cerebellar cortex of the frog. In: R. Llinás (ed.), Neurobiology of cerebellar evolution and development, p. 327–371. Chicago: AMA Education and Research Foundation 1969.

    Google Scholar 

  • —, Palay, S. L.: The fine structure of the lateral vestibular nucleus in the rat. I. Neurons and neuroglial cells. J. Cell Biol. 36, 151–179 (1968).

    Google Scholar 

  • Tennyson, V. M.: The fine structure of the axon and growth cone of the dorsal root neuroblast of the rabbit embryo. J. Cell Biol. 44, 62–79 (1970).

    Google Scholar 

  • Trujillo-Cenóz, O.: The fine structure of a special type of nerve fiber found in the ganglia of Armadillidium vulgare (Crustacea, isopoda). J. biophys. biochem. Cytol. 7, 185–196 (1960).

    Google Scholar 

  • —: Some aspects of the structural organization of the arthropod ganglia. Z. Zellforsch. 56, 649–682 (1962).

    Google Scholar 

  • Vollrath, L.: Über die Herkunft “synaptischer” Bläschen in neurosekretorischen Axonen. Z. Zellforsch. 99, 146–152 (1969).

    Google Scholar 

  • Weiss, P., Pillai, A.: Convection and fate of mitochondria in nerve fibers: axonal flow as vehicle. Proc. nat. Acad. Sci. (Wash.) 54, 46–56 (1965).

    Google Scholar 

  • Westrum, L. E.: A combination staining technique for electron microscopy. I. Nervous tissue. J. Microscopie 4, 275–278 (1965).

    Google Scholar 

  • Wisniewski, H., Shelanski, M. L., Terry, R. D.: Effects of mitotic spindle inhibitors on neurotubules and neurofilaments in anterior horn cells. J. Cell Biol. 38, 224–229 (1968).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, University College London, UK

    A. R. Lieberman

Authors
  1. A. R. Lieberman
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Thanks are due to Profs. E. G. Gray and J. Z. Young for helpful discussion and to Mrs. N. Morgan and Mr. R. Boddy for technical assistance.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lieberman, A.R. Microtubule-associated smooth endoplasmic reticulum in the frog's brain. Z. Zellforsch. 116, 564–577 (1971). https://doi.org/10.1007/BF00335058

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00335058

Key-Words

Search

Navigation