Summary
The avascular ventral nerve cord of the moth, Manduca sexta, possesses an extensive dorsal mass of connective tissue in which lie fibroblasts that produce a collagen-like protein. The lateral and ventral surfaces of the nerve cord are ensheathed by an acellular neural lamella. Beneath this lies a layer of microtubule-laden perineurial cells which are separated from one another at their peripheral borders by lacunae containing electron-opaque material to which the cells are attached by hemi-desmosomes. Beyond these spaces, narrow intercellular clefts occur between the interdigitating perineurial plasma membranes; these are then connected by both gap and tight junctions. The axons beneath are surrounded by glia which also contain many microtubules and which are linked to one another by desmosomes and tight junctions.
When intact nerve cords are incubated in horseradish peroxidase, reaction product is subsequently found within the neural lamella as well as in the lacunae and clefts between perineurial cells, but not beyond this level. Desheathed preparations, however, contain peroxidase within the cytoplasm of the exposed glial cells. Lanthanum penetrates the neural lamella and the lacunae, clefts and gap junctions between adjacent perineurial cells, but no further. It therefore appears that the tight junctions in the perineurium may be the site of restriction to the entry of ions and molecules, the existence of which has been suggested previously by electrophysiological investigations.
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References
Ashhurst, D.E.: Fibrillogenesis in the wax-moth, Galleria mellonella. Quart. J. micr. Sci. 105, 391–403 (1964).
Ashhurst, D.E.: An insect desmosome. J. Cell Biol. 46, 421–425 (1970).
Ashhurst, D.E., Costin, N.M.: Insect mucosubstances. II. The mucosubstances of the central nervous system. Histochem. J. 3, 297–310 (1971a).
Ashhurst, D.E., Costin, N.M.: Insect mucosubstances. III. Some mucosubstances of the nervous systems of the wax-moth (Galleria mellonella) and the stick insect (Carausius morosus). Histochem. J. 3, 379–387 (1971b).
Baskin, D.G.: The fine structure of neuroglia in the central nervous system of Nereid polychaetes. Z. Zellforsch. 119, 295–308 (1971).
Brightman, M.W., Reese, T.S.: Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648–677 (1969).
Cotran, R.S., Karnovsky, M.J.: Ultrastructural studies on the permeability of the mesothelium to horseradish peroxidase. J. Cell Biol. 37, 123–137 (1968).
Goodenough, D.A., Revel, J.-P.: A fine structural analysis of intercellular junctions in the mouse liver. J. Cell Biol. 45, 272–290 (1970).
Goodenough, D.A., Revel, J.-P.: The permeability of isolated and in situ mouse hepatic gap junctions studied with enzymatic tracers. J. Cell Biol. 50, 81–91 (1971).
Hand, A.R., Gobel, S.: The structural organization of the septate and gap junctions of Hydra. J. Cell Biol. 52, 397–408 (1972).
Harper, E., Seifter, S., Scharrer, B.: Electron microscopic and biochemical characterization of collagen in blattarian insects. J. Cell Biol. 33, 385–393 (1967).
Hudspeth, A.J., Revel, J.P.: Coexistence of gap and septate junctions in an invertebrate epithelium. J. Cell Biol. 50, 92–101 (1971).
Johnson, R.G., Sheridan, J.D.: Junctions between cancer cells in culture. Ultrastructure and permeability. Science 174, 717–719 (1971).
Karnovsky, M.J.: A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27, 137A (1965).
Karnovsky, M.J.: The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol. 35, 213–236 (1967).
Lane, N.J., Treherne, J.E.: Peroxidase uptake by glial cells in desheathed ganglia of the cockroach. Nature (Lond.) 223, 861–862 (1969).
Lane, N.J., Treherne, J.E.: Uptake of peroxidase by the cockroach central nervous system. Tissue and Cell 2, 413–425 (1970a).
Lane, N.J., Treherne, J.E.: Lanthanum staining of neurotubules in axons from cockroach ganglia. J. Cell Sci. 1, 217–231 (1970b).
Lane, N.J., Treherne, J.E.: Accessibility of the central nervous connectives of Anodonta cygnea to a large molecular weight compound. J. exp. Biol. 56 (1972a).
Lane, N.J., Treherne, J.E.: Studies on perineurial junctional complexes and the sites of uptake of microperoxidase and lanthanum by the cockroach central nervous system. Tissue and Cell, in the press (1972b).
Moreton, R.B.: Electrophysiology and ionic movements in the central nervous system of the snail, Helix aspersa. J. exp. Biol. in press (1972).
Nicholls, J.G., Kuffler, S.W.: Extracellular space as a pathway for exchange between blood and neurons in the central nervous system of the leach: ionic composition of glial cells and neurons. J. Neurophysiol. 27, 645–671 (1964).
Payton, B.W., Bennett, M.V.L., Pappas, G.D.: Permeability and structure of junctional membranes at an electrotonic synapse. Science 166, 1641–1643 (1969).
Pentreath, V.W., Cottrell, G.A.: The blood supply to the central nervous system of Helix pomatia. Z. Zellforsch. 111, 160–178 (1970).
Pichon, Y., Sattelle, D.B., Lane, N.J.: Conduction processes in the nerve cord of the moth Manduca sexta in relation to its ultrastructure and haemolymph ionic composition. J. exp. Biol. 56, 1–18 (1972).
Revel, J.-P., Karnovsky, M.J.: Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33, C7-C12 (1967).
Sabatini, D.D., Bensch, K., Barrnett, R.J.: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 19–58 (1963).
Sattelle, D.B.: Potassium movements in a central nervous ganglion of Limnaea stagnalis (L.) (Gastropoda: Pulmonata). (In preparation) (1972).
Sattelle, D.B., Lane, N.J.: Architecture of gastropod central nervous tissues in relationto ionic movements. Tissue and Cell. In the press (1972).
Smith, D.S., Treherne, J.E.: Functional aspects of the organization of the insect nervous system, p. 401–484. In: Advances in insect physiology. (eds. J.W.L. Beament, J.E. Treherne and V.B. Wigglesworth), vol. 1. London and New York: Academic Press 1963.
Treherne, J.E., Lane, N.J., Moreton, R.B., Pichon, Y.: A quantitative study of potassium movements in the central nervous system of Periplaneta americana. J. exp. Biol. 53, 109–136 (1970).
Treherne, J.E., Mellon, D., Carlson, A.D.: The ionic basic of axonal conduction in the central nervous system of Anodonta cygnea (Mollusca: Eulamellibranchia). J. exp. Biol. 50, 711–722 (1969).
Treherne, J.E., Moreton, R.B.: The environment and function of invertebrate nerve cells. Int. Rev. Cytol. 28, 45–88 (1970).
Treherne, J.E., Pichon, Y.: The insect blood-brain barrier. In: Advances in insect physiology., in the press (1972).
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I am grateful to Miss Yvonne R. Carter for her invaluable technical assistance and to Dr. J.E. Treherne and Dr. D.B. Sattelle for helpful discussions.
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Lane, N.J. Fine structure of a lepidopteran nervous system and its accessibility to peroxidase and lanthanum. Z.Zellforsch 131, 205–222 (1972). https://doi.org/10.1007/BF00306928
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DOI: https://doi.org/10.1007/BF00306928