Skip to main content
Log in

The septum of the lateral axon of the earthworm: A thin section and freeze-fracture study

  • Published:
Journal of Neurocytology

Summary

Septa occur between the axonal segments in the lateral giant septate axon of the nerve cord of the earthworm. This septum is demonstrated here to be permeable to fluorescein and to exhibit a negligible time delay for impulse transmission. Periodic anastomoses between the two lateral axons of the nerve cord are revealed by fluorescein. The permeability of the septum is correlated with the demonstration that nexuses occur along the septum. In thin sections, the nexuses may appear as long septilaminar or pentalaminar membrane appositions, but most frequently appear as a series of short or punctate membrane appositions. In freeze-fracture replicas, the nexuses appear as particles 10–12 nm in diameter on the PF face and as pits on the EF face. The particles and pits are arranged in plaques, in anastomosing strands, or most frequently in small plaques with strands of particles or pits emerging from the periphery. In addition to the nexuses, a junction characterized by the presence of 31 nm diameter hemispherical densities on the cytoplasmic surfaces of the septal membranes is revealed in thin sections. The densities are paired on the adjacent septal membranes, and most frequently are shown by optical diffraction to be arranged on the membrane surfaces in hexagonal or rhomboidal lattices with a centre-to-centre spacing of 34.8 nm. In freeze-fracture replicas, an array of particles and pits with a similar lattice symmetry and spacing to the arrays of hemispherical densities is demonstrated.

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

  • Azarnia, R., Larsen, W. J. andLoewenstein, W. (1974) The membrane junctions in communicating and non-communicating cells, their hybrids and segregants.Proceedings of the National Academy of Sciences (U.S.A.) 71, 880–4.

    Google Scholar 

  • Baerwald, R. J. (1975) Inverted gap and other cell junctions in cockroach hemocyte capsules. A thin-section and freeze-fracture study.Tissue and Cell 7, 575–85.

    Google Scholar 

  • Barr, L., Berger, W. andDewey, M. M. (1968) Electrical transmission at the nexus between smooth muscle cells.Journal of General Physiology 51, 347–68.

    Google Scholar 

  • Barr, L., Dewey, M. M. andBerger, W. (1965) Propagation of action potentials and the structure of the nexus in cardiac muscle.Journal of General Physiology 48, 797–823.

    Google Scholar 

  • Bennett, M. V. L. (1973) Function of electrotonic junctions in embryonic and adult tissues.Federation Proceedings 32, 65–75.

    Google Scholar 

  • Bennett, M. V. L., Nakajima, Y. andPappas, G. D. (1967) Physiology and ultrastructure of electrotonic junctions. 1. Supramedullary neurons.Journal of Neurophysiology 30, 161–79.

    Google Scholar 

  • Branton, D., Bullivant, S., Gilula, N. B., Karnovsky, M. J., Moor, H., Muhlethaler, K., Northcote, D. H., Packer, L., Satir, B., Satir, P., Speth, V., Staehelin, L. A., Steere, R. L. andWeinstein, R. S. (1975) Freeze-etching nomenclature.Science 190, 54–6.

    Google Scholar 

  • Brightman, M. andReese, T. (1969) Junctions between intimately apposed ceil membranes in the vertebrate brain.Journal of Cell Biology 40, 648–77.

    Google Scholar 

  • Brink, P. andBarr, L. (1977) The resistance of the septa of the median giant axon of the earthworm.Journal of General Physiology 69, 517–36.

    Google Scholar 

  • Brink, P. andDewey, M. (1978) Nexal membrane permeability to anions.Journal of General Physiology 72, 67–86.

    Google Scholar 

  • Brink, P., Kensler, R. andDewey, M. (1977) Structure of the septa of the median and lateral giant axons ofLumbricus terrestris.Journal of Cell Biology 75, 110a.

    Google Scholar 

  • Bullock, T. H. (1945) Functional organization of the giant fiber system ofLumbricus.Journal of Neurophysiology 8, 55–71.

    Google Scholar 

  • Caspar, D. L. D., Goodenough, D. A., Makowski, L. andPhillips, W. C. (1977) Gap junction structures. 1. Correlated electron microscopy and x-ray diffraction.Journal of Cell Biology 74, 605–28.

    Google Scholar 

  • Chalcroft, J. andBullivant, S. (1970) An interpretation of liver cell membrane and junction structure based on observation of freeze-fracture replicas of both sides of the fracture.Journal of Cell Biology 47, 49–60.

    Google Scholar 

  • Coggeshall, R. E. (1965) A fine structural analysis of the ventral nerve cord and associated sheath ofLumbricus terrestris L.Journal of Comparative Neurology 125, 393–438.

    Google Scholar 

  • Decker, R. andFriend, D. S. (1974) Assembly of gap junctions during amphibian neurulation.Journal of Cell Biology 62, 32–48.

    Google Scholar 

  • Dewey, M. M. andBarr, L. (1962) Intercellular connections between smooth muscle cells: the nexus.Science 137, 670–72.

    Google Scholar 

  • Dewey, M. M. andBarr, L. (1964) A study of the structure and distribution of the nexus.Journal of Cell Biology 23, 553–85.

    Google Scholar 

  • Dewey, M. M. andBarr, L. (1970) Some considerations about the structure of cell membranes.Current Topics in Membranes and Transport 1, 1–33.

    Google Scholar 

  • Eccles, J. C., Granit, R. andYoung, J. Z. (1933) Impulses in the giant fibers of earthworms.Journal of Physiology (London) 77, 23P-24P.

    Google Scholar 

  • Epstein, H. andGilula, N. B. (1977) A study of communication specificity between cells in culture.Journal of Cell Biology 75, 769–787.

    Google Scholar 

  • Filshie, B. K. andFlower, N. E. (1979) Junctional structures inHydra.Journal of Cell Science 23, 151–72.

    Google Scholar 

  • Flower, N. E. (1971) Septate and gap junctions between the epithelial cells of an invertebrate, the molluscCominella maculosa.Journal of Ultrastructure Research 37, 259–68.

    Google Scholar 

  • Flower, N. E. (1977) Invertebrate gap junctions.Journal of Cell Science 25, 163–71.

    Google Scholar 

  • Fraser, R. D. B. andMillward, G. R. (1970) Image averaging by optical filtering.Journal of Ultrastructure Research 31, 203–11.

    Google Scholar 

  • Fry, G., Devine, C. andBurnstock, G. (1977) Freeze-fracture studies of nexuses between smooth muscle cells. Close relationship to sarcoplasmic reticulum.Journal of Cell Biology 72, 26–34.

    Google Scholar 

  • Furshpan, E. J. andPotter, D. D. (1959) Transmission at the giant motor synapses of the crayfish.Journal of Physiology 145, 289–325.

    Google Scholar 

  • Gilula, N. B. (1974) Junctions between cells. In:Cell Communication (edited byCox, R. P.), pp. 1–29. New York: John Wiley and Sons.

    Google Scholar 

  • Gilula, N. B., Reeves, D. andSteinbach, A. (1972) Metabolic coupling, ionic coupling, and cell contacts.Nature 235, 262–5.

    Google Scholar 

  • Gilula, N. B. andSatir, A. (1971) Septate and gap junctions in molluscan gill epithelium.Journal of Cell Biology 51, 869–72.

    Google Scholar 

  • Goodenough, D. A. andRevel, J. P. (1970) A fine structural analysis of intercellular junctions in the mouse liver.Journal of Cell Biology 45, 272–90.

    Google Scholar 

  • Gunther, J. (1975) Neuronal syncytia in the giant fibers of earthworm.Journal of Neurocytology 4, 55–62.

    Google Scholar 

  • Hama, K. (1959) Some observations on the fine structure of the giant nerve fibers of the earthwormEisenia foetida.Journal of Biophysical and Biochemical Cytology 6, 61–6.

    Google Scholar 

  • Issidorides, M. (1956) Ultrastructure of the synapse in the giant axon of the earthworm.Experimental Cell Research 11, 423–36.

    Google Scholar 

  • Johnson, R., Herman, W. S. andPreus, D. M. (1973) Homocellular and heterócellular gap junctions inLimulus; a thin section and freeze-fracture study.Journal of Ultrastructure Research 43, 298–312.

    Google Scholar 

  • Kanno, Y. andLoewenstein, W. R. (1966) Cell to cell passage of large molecules.Nature 212, 629–30.

    Google Scholar 

  • Kao, C. Y. (1960) Postsynaptic electrogenesis in septate giant axons. II. Comparison of medial and lateral giant axons of crayfish.Journal of Neurophysiology 23, 618–35.

    Google Scholar 

  • Kao, C. Y. andGrundfest, H. (1957) Postsynaptic electrogenesis in septate giant axons. I. Earthworm median giant axon.Journal of Neurophysiology 20, 553–73.

    Google Scholar 

  • Karnovsky, M. (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy.Journal of Cell Biology 27, 137–8a.

    Google Scholar 

  • Kensler, R. W., Brink, P. andDewey, M. M. (1977a) The nexus of frog ventricle.Journal of Cell Biology 73, 768–81.

    Google Scholar 

  • Kensler, R. W., Brink, P. andDewey, M. M. (1977b) Glial cells in the earthworm ventral nerve cord make an A-type nexus.American Journal of Anatomy 149, 605–11.

    Google Scholar 

  • Kogon, M. andPappas, G. D. (1975) Atypical gap junctions in the ciliary epithelium of the albino rabbit eye.Journal of Cell Biology 66, 671–5.

    Google Scholar 

  • Larsen, W. J. (1977) Structural diversity of gap junctions. A review.Tissue and Cell 9, 373–94.

    Google Scholar 

  • Mazet, F. andCartaud, J. (1976) Freeze-fracture studies of frog atrial fibers.Journal of Cell Science 22, 427–34.

    Google Scholar 

  • McNutt, N. S. andWeinstein, R. S. (1970) The ultrastructure of the nexus. A correlated thin-section and freeze-cleave study.Journal of Cell Biology 47, 666–88.

    Google Scholar 

  • McNutt, N. S. andWeinstein, R. S. (1973) Membrane ultrastructure at mammalian intercellular junctions.Progress in Molecular Biology 26, 45–101.

    Google Scholar 

  • Mulloney, B. (1970) Structure of the giant fibers of earthworms.Science 167, 994.

    Google Scholar 

  • Oesterle, D. andBarth, F. G. (1973) Zur feinstruktur einer elektrischen synapse. Die septen der dorsalen riesenfasern von regenwurmen (Lumbricus terrestris, Eisenia foetida).Zeitschift für Zellforschung und mikroskopische Anatomie 136, 139–52.

    Google Scholar 

  • Pappas, G. D., Asada, Y. andBennet, M. V. L. (1971) Morphological correlates of increased coupling resistance at an electrotonic synapse.Journal of Cell Biology 49, 173–88.

    Google Scholar 

  • Payton, B., Bennett, M. V. L. andPappas, G. D. (1969) Permeability and structure of junctional membranes at an electrotonic synapse.Science 166, 1641–3.

    Google Scholar 

  • Peracchia, C. (1973a) Low resistance junctions in Crayfish. I. Two arrays of globules in junctional membranes.Journal of Cell Biology 57, 54–65.

    Google Scholar 

  • Peracchia, C. (1973b) Low resistance junctions in crayfish. II. Structural details and further evidence for intercellular channels by freeze-fracture and negative staining.Journal of Cell Biology 57, 66–76.

    Google Scholar 

  • Pollack, G. H. andHuntman, L. L. (1973) Intercellular pathways in the heart: Direct evidence for low resistance channels.Experientia 29, 1501–2.

    Google Scholar 

  • Pricam, C., Humbert, F., Perrelet, A. andOrci, L. (1974) Gap junctions in mesangial and lacis cells.Journal of Cell Biology 63, 349–54.

    Google Scholar 

  • Prosser, C. L. andBrown, F. A. (1950)Comparative Animal Physiology, p. 75. Philadelphia: Saunders.

    Google Scholar 

  • Quick, D. C. andJohnson, R. G. (1977) Gap junctions and rhombic particle arrays in planaria.Journal of Ultrastructure Research 60, 348–61.

    Google Scholar 

  • Raviola, E. andGilula, N. B. (1973) Gap junctions between photoreceptor cells.Proceedings of the National Academy of Sciences (U.S.A.) 70, 1677–81.

    Google Scholar 

  • Raviola, E. andGilula, N. B. (1975) Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits.Journal of Cell Biology 65, 192–222.

    Google Scholar 

  • Revel, J. P. andKarnovsky, M. J. (1967) Hexagonal arrays of subunits in intercellular junctions of the mouse heart and liver.Journal of Cell Biology 33, C7-C12.

    Google Scholar 

  • Reynolds, E. (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy.Journal of Cell Biology 17, 208–12.

    Google Scholar 

  • Rosenbluth, J. (1963) Contrast between osmium-fixed and permanganate-fixed toad spinal ganglia.Journal of Cell Biology 16, 143–58.

    Google Scholar 

  • Rushton, W. A. H. (1945) Action potentials from the isolated nerve cord of the earthworm.Proceedings of the Royal Society of London B132, 423–37.

    Google Scholar 

  • Satir, P. andGilula, N. B. (1973) The fine structure of membranes and inter-cellular communication in insects.Annual Review of Entomology 18, 143–66.

    Google Scholar 

  • Simionescu, M., Simionescu, N. andPalade, G. E. (1976) Segmental differentiations of cell junctions in the vascular endothelium. Arteries and veins.Journal of Cell Biology 68, 705–23.

    Google Scholar 

  • Sommer, J. andWaugh, R. (1976) The ultrastructure of the mammalian cardiac muscle cell; with special emphasis on the tubular membrane systems.American Journal of Pathology 82, 192–217.

    Google Scholar 

  • Staehelin, L. A. (1972) Three types of gap junctions connect intestinal epithelial cells.Proceedings of the National Academy of Sciences (U.S.A.) 69, 1318–21.

    Google Scholar 

  • Staehelin, L. A. (1974) Structure and function of intercellular junctions.International Review of Cytology 39, 191–283.

    Google Scholar 

  • Stough, H. B. (1926) Giant nerve fibers of the earthworm.Journal of Comparative Neurology 40, 409–43.

    Google Scholar 

  • Stough, H. B. (1930) Polarization of the giant nerve fibers of the earthworm.Journal of Comparative Neurology 50, 217–29.

    Google Scholar 

  • Tani, E., Yamagata, S. andIto, Y. (1977) Cell membrane structure of vascular smooth muscle of the circle of Willis.Cell and Tissue Research 179, 131–42.

    Google Scholar 

  • Tsien, R. andWeingart, R. (1974) Cyclic-AMP: Cell to cell movement and inotropic effect in ventricular muscle studied by a cut end method.Journal of Physiology 242, 95P-96P.

    Google Scholar 

  • Weidmann, S. (1966) The diffusion of radiopotassium across intercalated discs of mammalian cardiac muscles.Journal of Physiology 187, 323–42.

    Google Scholar 

  • Weidmann, S. (1970) Electrical constants of trabecular muscle from mammalian heart.Journal of Physiology 210, 1041–54.

    Google Scholar 

  • Weingart, R. (1974) The permeability to TEA ions of the surface membrane and intercalated discs of sheep and calf myocardium.Journal of Physiology 210, 741–62.

    Google Scholar 

  • Wilson, D. M. (1961) The connections between the lateral giant fibers of earthworms.Comparative Biochemistry and Physiology 8, 274–84.

    Google Scholar 

  • Wood, R. L. (1977) The cell junctions ofHydra as viewed by freeze-fracture replication.Journal of Ultrastructure Research 58, 299–315.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Portions of this work were reported in abstract at the 30th Annual Meeting of the Society of General Physiologists 1976, and at the American Society for Cell Biology Meetings in November, 1977.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kensler, R.W., Brink, P.R. & Dewey, M.M. The septum of the lateral axon of the earthworm: A thin section and freeze-fracture study. J Neurocytol 8, 565–590 (1979). https://doi.org/10.1007/BF01208510

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01208510

Keywords

Navigation