Skip to main content
Log in

The role of cations in conduction in the central nervous system of the herbivorous insect Carausius morosus

  • Published:
Zeitschrift für vergleichende Physiologie Aims and scope Submit manuscript

Summary

  1. 1.

    The role of cations in nervous conduction in the central nervous system of the herbivorous insect Carausius morosus was studied with external electrodes.

  2. 2.

    The size of the compound action potential in axons (totally desheathed connectives) depends on the sodium concentration of the bathing medium (Fig. 2), the relationship roughly approximating that predicted by the Nernst formula (Table 4).

  3. 3.

    Sodium-free bathing medium reversibly blocks conduction in axons (totally desheathed connectives) within 1 min (Fig. 2).

  4. 4.

    At low concentrations in the perfusion solution, both tetrodotoxin and procaine reversibly block conduction in axons within a few minutes.

  5. 5.

    Lithium ions replace sodium ions in the maintenance of action potential size in axons for about 10 min, but then action potentials gradually decline. The action potential size is restored when the nerve cord is perfused once again with a medium containing the initial sodium concentration (Fig. 3).

  6. 6.

    External sodium concentrations either higher than 180 mM or lower than 150 mM significantly decrease the viability of axons (Fig. 4); we concluded that the sodium concentration of the extracellular fluid of the nerve cord is probably between 150 and 180 mM.

  7. 7.

    The order of effectiveness of potassium, rubidium and cesium ions in suppressing compound action potentials in axons is K+= Rb+>Cs+ (Fig. 5).

  8. 8.

    The action potentials in axons perfused with a solution containing 27 mM K+ are reversibly suppressed by approximately 37%; we concluded that the potassium concentration in the extracellular fluid of the ventral nerve cord is less than 27 mM.

  9. 9.

    When the calcium concentration in the external medium is reduced from 7.5 to 1 mM, repetitive firing and progressive conduction blockage are produced after nearly 4 hr in connectives in the absence of a fat-body sheath (Fig. 6).

  10. 10.

    When manganous ions (16 mM) are added to the bathing medium, there is little change in the level of axonal electrical activity (Fig. 7). Since manganous ions have been shown to suppress the increase in membrane conductance to calcium during the so-called calcium spikes of some irritable tissues, we concluded that calcium ions do not contribute significantly to the inward current during the action potential.

  11. 11.

    Axonal viability increases with the external magnesium concentration in the range from 0 to 50 mM Mg++ (Fig. 8). However, the actual magnesium concentration of the extracellular fluid may be between 10 and 25 mM.

  12. 12.

    When axons are perfused with magnesium-free solution, the action potentials are reduced to one-half of their initial size only after 2.36±0.42 hr; we concluded that magnesium ions are not carriers of inward current during action potentials.

  13. 13.

    Comparing our data with published data obtained from other animals, we concluded that nervous conduction in Carausius conforms to the classical membrane theory despite the unusual cationic levels in the hemolymph and that a yet undefined homeostatic mechanism maintains extracellular cationic concentrations at favorable levels in the nerve cord.

  14. 14.

    Viability studies indicate that an active transport mechanism is probably located in the fat-body sheath and that this mechanism probably maintains the extracellular sodium concentration at a high level (Table 2). These studies also indicate that the neural lamella and perineurium form a diffusion barrier which is only slightly permeable to the common cations (Tables 2, 3 and Fig. 6).

  15. 15.

    A model (Fig. 9), explaining the regulation of cationic concentrations in the extracellular fluid of Carausius nerve cord, is proposed from available data.

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

  • Adelman, W. J., Jr.: The effect of external calcium and magnesium depletion on single nerve fibers. J. gen. Physiol. 39, 753–772 (1956).

    Google Scholar 

  • Bishop, G. H.: The form of the record of the action potential of vertebrate nerve at the stimulated region. Amer. J. Physiol. 82, 462–477 (1927).

    Google Scholar 

  • Boné, G.: Le rapport sodium/potassium dans le liquide coelomique des insectes. I. Ses relations avec le régime alimentaire. Ann. Soc. roy. zool. Belg. 75, 123–132 (1944).

    Google Scholar 

  • Brink, F., Jr., and D. W. Bronk: Rhythmic activity of single nerve fibers induced by low calcium. Proc. Soc. exp. Biol. (N. Y.) 37, 94–95 (1937).

    Google Scholar 

  • Cowan, S. L.: The action of potassium and other ions on the injury potential and action current in Maia nerve. Proc. roy. Soc. B 115, 216–260 (1934).

    Google Scholar 

  • Dalton, J. C.: Effects of external ions on membrane potentials of a lobster giant axon. J. gen. Physiol. 41, 529–542 (1958).

    Google Scholar 

  • Duchâteau, G., M. Florkin, and J. Leclerq: Concentrations des bases fixes et types de composition de la base totale de l'hémolymphe des insectes. Arch. int. Physiol. 61, 518–549 (1953).

    Google Scholar 

  • Fatt, P., and B. L. Ginsborg: The ionic requirements for the production of action potentials in crustacean muscle fibres. J. Physiol. (Lond.) 142, 516–543 (1958).

    Google Scholar 

  • Feng, T. P., and Y. M. Liu: The concentration-effect relationship in the depolarization of amphibian nerve by potassium and other agents. J. cell. comp. Physiol. 34, 33–42 (1949).

    Google Scholar 

  • Frankenhaeuser, B.: The effect of calcium on the myelinated nerve fibre. J. Physiol. (Lond.) 137, 245–260 (1957).

    Google Scholar 

  • —, and A. L. Hodgkin: The action of calcium on the electrical properties of squid axons. J. Physiol. (Lond.) 137, 218–244 (1957).

    Google Scholar 

  • Gallego, A., and R. Lorente de Nó: On the effect of several monovalent ions upon frog nerve. J. cell. comp. Physiol. 29, 189–206 (1947).

    Google Scholar 

  • —: On the effect of ammonium and lithium ions upon frog nerve deprived of sodium. J. gen. Physiol. 35, 227–244 (1951).

    Google Scholar 

  • Gordon, H. T., and J. H. Welsh: The role of ions in axon surface reactions to toxic organic compounds. J. cell. comp. Physiol. 31, 395–419 (1948).

    Google Scholar 

  • Greengard, P., and R. W. Straub: Restoration by barium of action potentials in sodium-deprived mammalian B and C fibres. J. Physiol. (Lond.) 145, 562–569 (1959).

    Google Scholar 

  • Guttman, R., J. A. Dowling, and S. M. Ross: Resting potential and contractile system changes in muscles stimulated by cold and potassium. J. cell. comp. Physiol. 50, 265–276 (1957).

    Google Scholar 

  • Hagiwara, S., S. Chichibu, and K. Naka: The effects of various ions on resting and spike potentials of barnacle muscle fibers. J. gen. Physiol. 48, 163–179 (1964).

    Google Scholar 

  • —, and K. Naka: The initiation of spike potential in barnacle muscle fibers under low intracellular Ca++. J. gen. Physiol. 48, 141–162 (1964).

    Google Scholar 

  • —, and S. Nakajima: Differences in Na and Ca spikes as examined by application of tetrodotoxin, procaine and manganese ions. J. gen. Physiol. 49, 793–806 (1966).

    Google Scholar 

  • Hodgkin, A. L.: The effect of potassium on the surface membrane of an isolated axon. J. Physiol. (Lond.) 106, 319–340 (1947).

    Google Scholar 

  • —: The ionic basis of electrical activity in nerve and muscle. Biol. Rev. 26, 339–409 (1951).

    Google Scholar 

  • —: Ionic movements and electrical activity in giant nerve fibres. Proc. roy. Soc. B 148, 1–37 (1958).

    Google Scholar 

  • —: The conduction of the nervous impulse. Springfield: Ch. C. Thomas 1964.

    Google Scholar 

  • —, and B. Katz: The effect of sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. (Lond.) 108, 37–77 (1949).

    Google Scholar 

  • Höber, R.: Über den Einfluß der Salze auf den Ruhestrom des Froschmuskels. Pflügers Arch. ges. Physiol. 106, 599–635 (1905).

    Google Scholar 

  • Hoyle, G.: High blood potassium in insects in relation to nerve conduction. Nature (Lond.) 169, 281–282 (1952).

    Google Scholar 

  • —: Potassium ions and insect nerve muscle. J. exp. Biol. 30, 121–135 (1953).

    Google Scholar 

  • —: Changes in the blood potassium concentration of the African migratory locust (Locusta migratoria migratorioides R. & F.) during food deprivation, and the effect on neuromuscular activity. J. exp. Biol. 31, 260–270 (1954).

    Google Scholar 

  • Keynes, R. D., and R. C. Swan: The permeability of frog muscle fibres to lithium ions. J. Physiol. (Lond.) 147, 626–638 (1959).

    Google Scholar 

  • Kuffler, S. W.: Neuroglial cells: physiological properties and a potassium mediated effect of neuronal activity on the glial membrane potential. Proc. roy. Soc. B 168, 1–21 (1967).

    Google Scholar 

  • Loewenstein, W. R., C. A. Terzuolo, and Y. Washizu: Separation of transducer and impulse-generating processes in sensory receptors. Science 142, 1180–1181 (1963).

    Google Scholar 

  • Lorente de Nó, R.: Effect of an excess of magnesium ions. Stud. Rockefeller Inst. med. Res. 131, 118–122 (1947).

    Google Scholar 

  • Maddrell, S. H. P., and J. E. Treherne: A neural fat-body sheath in a phytophagous insect (Carausius morosus). Nature (Lond.) 211, 215–216 (1966).

    Google Scholar 

  • —: The ultrastructure of the perineurium in two insect species, Carausius morosus and Periplaneta americana. J. Cell Sci. 2, 119–128 (1967).

    Google Scholar 

  • Nakajima, S., S. Iwasaki, and K. Obata: Delayed rectification and anomalous rectification in frog's skeletal muscle membrane. J. gen. Physiol. 46, 97–115 (1962).

    Google Scholar 

  • Nakamura, Y., S. Nakajima, and H. Grundfest: Eel electroplaques: spike electrogenesis without potassium activation. Science 146, 266–268 (1964).

    Google Scholar 

  • Narahashi, T., T. Deguchi, N. Urakawa, and Y. Ohkubo: Stabilization and rectification of muscle fiber membrane by tetrodotoxin. Amer. J. Physiol. 198, 934–938 (1960).

    Google Scholar 

  • —, J. W. Moore, and W. R. Scott: Tetrodotoxin blockage of sodium conductance increase in lobster giant axons. J. gen. Physiol. 47, 965–974 (1964).

    Google Scholar 

  • Netter, H.: Über den Ruhestrom des Nerven und die Ionenpermeabilität seiner Hüllen. Pflügers Arch. ges. Physiol. 218, 310–330 (1928).

    Google Scholar 

  • Overton, E.: Beiträge zur allgemeinen Muskel- und Nervenphysiologie. II. Über die Unentbehrlichkeit von Natrium-(oder Lithium-)Ionen für den Contractionsact des Muskels. Pflügers Arch. ges. Physiol. 92, 346–386 (1902).

    Google Scholar 

  • Ramsay, J. A.: The excretory system of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. exp. Biol. 32, 183–199 (1955).

    Google Scholar 

  • Roeder, K. D.: The effect of potassium and calcium on the nervous system of the cockroach, Periplaneta americana. J. cell. comp. Physiol. 31, 327–338 (1948).

    Google Scholar 

  • Sandow, A., and H. Mandel: Effects of potassium and rubidium on the resting potential of muscle. J. cell. comp. Physiol. 38, 271–291 (1951).

    Google Scholar 

  • Shanes, A. M., W. H. Freygang, H. Grundfest, and E. Amatniek: Anesthetic and calcium action in the voltage clamped squid giant axon. J. gen. Physiol. 42, 793–802 (1959).

    Google Scholar 

  • Smith, D. S.: The trophic role of glial cells in insect ganglia. In: Insects and physiology (J. W. L. Beament and J. E. Treherne, eds.), p. 189–198. Edinburgh and London: Oliver & Boyd 1967.

    Google Scholar 

  • Steel, R. G. D., and J. H. Toreie: Principles and procedures of statistics with special reference to biological sciences. New York: McGraw-Hill 1960.

    Google Scholar 

  • Taylor, R. E.: Effect of procaine on electrical properties of squid axon membrane. Amer. J. Physiol. 196, 1071–1078 (1959).

    Google Scholar 

  • Tobias, J. M.: Potassium, sodium and water interchange in irritable tissues and haemolymph of an omnivorous insect, Periplaneta americana. J. cell. comp. Physiol. 31, 125–142 (1948).

    Google Scholar 

  • Treherne, J. E.: Some preliminary observations on the effects of cations on conduction processes in the abdominal nerve cord of the stick insect, Carausius morosus. J. exp. Biol. 42, 1–6 (1965a).

    Google Scholar 

  • —: The distribution and exchange of inorganic ions in the central nervous system of the stick insect Carausius morosus. J. exp. Biol. 42, 7–27 (1965 b).

    Google Scholar 

  • —: Axonal function and ionic regulation in insect central nervous tissues. In: Insects and physiology (J. W. L. Beament and J. E. Treherne, eds.), p. 175–188. Edinburgh and London: Oliver & Boyd 1967.

    Google Scholar 

  • —, and S. H. P. Maddrell: Membrane potentials in the central nervous system of a phytophagous insect (Carausius morosus). J. exp. Biol. 46, 413–421 (1967a).

    Google Scholar 

  • —: Axonal function and ionic regulation in the central nervous system of a phytophagous insect (Carausius morosus). J. exp. Biol. 47, 235–247 (1967b).

    Google Scholar 

  • Twarog, B. M., and K. D. Roeder: Properties of the connective tissue sheath of the cockroach abdominal nerve cord. Biol. Bull. 111, 278–286 (1956).

    Google Scholar 

  • Werman, R., F. V. McCann, and H. Grundfest: Graded and all-or-none electrogenesis in arthropod muscle. I. The effects of alkali-earth cations on the neuromuscular system of Romalea microptera. J. gen. Physiol. 44, 979–995 (1961).

    Google Scholar 

  • Wilbrandt, W.: The effect of organic ions on the membrane potential of nerves. J. gen. Physiol. 20, 519–541 (1937).

    Google Scholar 

  • Wood, D. W.: The effect of ions upon neuromuscular transmission in a herbivorous insect. J. Physiol. (Lond.) 138, 119–139 (1957).

    Google Scholar 

  • Yamasaki, T., and T. Narahashi: The effects of potassium and sodium ions on the resting and action potentials of the cockroach giant axon. J. Insect Physiol. 3, 146–158 (1959).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was supported by USPHS Grant NB-05188, USPHS Grant 2 TO1 GM 225 and USPHS Postdoctoral Fellowship 2 F2 NB 34, 531-03 NSRB to D.J.W.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weidler, D.J., Diecke, F.P.J. The role of cations in conduction in the central nervous system of the herbivorous insect Carausius morosus . Z. vergl. Physiologie 64, 372–399 (1969). https://doi.org/10.1007/BF00340433

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00340433

Keywords

Navigation