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The Differentiation of Membrane Properties of Spinal Neurons

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Cellular and Molecular Biology of Neuronal Development

Abstract

Studies of neural induction involve assessments of neuronal differentiation following experimental manipulations. These studies have in the past relied principally on neuroanatomical descriptions of neurite outgrowth, which assess an important neuronal phenotype. In recent years, it has become possible to analyze the differentiation of key cytoplasmic specializations of neurons, such as their neurotransmitter synthetic capacity, as well as the differentiation of their characteristic membrane properties. Some of the recent progress in understanding the development of neuronal-membrane properties will be reviewed. These assays are likely to be useful in studies of neural induction for several reasons: (1) The increasing ease of application of the techniques involved invites their general use. (2) Acquisition of neuronal membrane properties occurs very early in normal embryonic development, recommending them for rapid evaluation of neuronal induction. (3) As Fig. 1 illustrates, different neurons exhibit different constellations of properties that appear in particular sequences (Spitzer and Lamborghini, 1981). A broader characterization of neuronal development affords the opportunity to distinguish the induction of different neuronal types.

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References

  • Anglister, L., Farber, I.C., Shahar, A., and Grinvald, A., 1982, Localization of voltage sensitive calcium channels along developing neurites: Their possible role in regulating neurite elongation, Dev. biol. 94:351–365.

    Article  PubMed  CAS  Google Scholar 

  • Baccaglini, P.I., 1978, Action potentials of embryonic dorsal root ganglion neurones in Xenopustadpoles, J. Physiol. 283: 585 – 604.

    PubMed  CAS  Google Scholar 

  • Baccaglini, P.I., and Spitzer, N.C., 1977, Developmental changes in the inward current of the action potential of Rohon—Beard neurones, J. Physiol. 271: 93 – 117.

    PubMed  CAS  Google Scholar 

  • Baud, C., Kado, R.T., and Marcher, K., 1982, Sodium channels induced by depolarization of the Xenopus laevisoocyte, Proc. Nat’I. Acad. Sci. 79: 3188 – 3192.

    Article  CAS  Google Scholar 

  • Bergey, G.K., Fitzgerald, S.C., Schrier, B.K., and Nelson, P.G., 1980, Neuronal maturation in mammalian cell culture is dependent on spontaneous electrical activity, Brain Res. 207:49–58.

    Article  Google Scholar 

  • Berwald-Netter, Y., Martin-Moutot, N., Koulakoff, A., and Couraud, F., 1981, Na+-channel- associated scorpion toxin receptor sites as probes for neuronal evolution in vivoand in vitro, Proc. Natl. Acad. Sci. U.S.A. 78: 1245 – 1249.

    Google Scholar 

  • Bixby, J.L., and Spitzer, N.C., 1982a, The appearance and development of chemosensitivity in Rohon–Beard neurones of the Xenopusspinal cord, J. Physiol. 330: 513 – 536.

    CAS  Google Scholar 

  • Bixby, J.L., and Spitzer, N.C., 1982b, Enkephalin shortens Ca++-spikes at early stages of embryonic spinal neurons in vivo, Soc. Neurosci. Abstr. 8: 229.

    Google Scholar 

  • Blackshaw, S., and Warner, A., 1976a, Onset of acetylcholine sensitivity and endplate activity in developing myotome muscles of Xenopus, Nature (London) 262: 217 – 218.

    Article  CAS  Google Scholar 

  • Blackshaw, S.E., and Warner, A.E., 1976b, Low resistance junctions between mesoderm cells during development of trunk muscles, J. Physiol. 255: 209 – 230.

    CAS  Google Scholar 

  • Blair, L., 1981, The timing of protein synthesis necessary for the acquisition of the Na+ action potential during development, Soc. Neurosci. Abstr.7: 245.

    Google Scholar 

  • Bloom, E.M., and Black, E.B., 1979, Metabolic requirements for differentiation of embryonic sympathetic ganglia cultured in the absence of exogenous nerve growth factor, Dev. Biol. 68: 568 – 578.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, M.W., and Kullberg, R.W., 1974, Temporal relationship between innervation and appearance of acetylcholine receptors in embryonic amphibian muscle, Proc. Can. Fed. Biol. Soc. 17: 176.

    Google Scholar 

  • Crepel, F., Dupont, J.L., and Gardette, R., 1982, Connectivity and chemosensitivity of Purkinje cells in the immature rat cerbellum: An in vitrostudy, J. Physiol. 332: 62.

    Google Scholar 

  • Curtis, D.R., Hosli, L., Johnston, G.A.R., and Johnston, I.H., 1968, The hyperpolarization of spinal motoneurones by glycine and related amino acids, Exp. Brain Res. 5: 235 – 258.

    Article  PubMed  CAS  Google Scholar 

  • Dennis, M. J., Ziskind-Conhaim, L., and Harris, A.J., 1981, Development of neuromuscular junctions in rat embryo, Dev. Biol. 81: 266 – 279.

    Article  PubMed  CAS  Google Scholar 

  • Dixon, J.S., and Cronly-Dillon, J.R., 1972, The fine structure of the developing retina in Xenopus laevis, J. Embryol. Exp. Morphol. 28: 659 – 666.

    PubMed  CAS  Google Scholar 

  • Dunlap, K., and Fischbach, D.G., 1978, Neurotransmitters decrease the calcium component of sensory neurone action potentials, Nature (London) 276:837–839.

    Article  CAS  Google Scholar 

  • Duprat, A.-M., Zalta, J.-P., and Beetschen, J.-C., 1966, Action de l’actinomycine D sur la differentiation de divers types de cellules embryonnaires de l’amphibien Pleurodeles waltliien culture in vitro, Exp. Cell Res. 43: 358 – 366.

    Google Scholar 

  • Fambrough, D., and Rash, J.E., 1971, Development of acetylcholine sensitivity during myogenesis, Dev. Biol. 26: 55 – 68.

    Article  PubMed  CAS  Google Scholar 

  • Fischbach, G.D., 1972, Synapse formation between dissociated nerve and muscle cells in low density cell cultures, Dev. Biol. 28: 407 – 429.

    Article  Google Scholar 

  • Fukuda, J., and Kameyama, M., 1979, Enchancement of Ca spikes in nerve cells of adult mammals during neurite growth in tissue culture, Nature (London)279: 546 – 548.

    Article  CAS  Google Scholar 

  • Gilula, N.B., Reeves, O.R., and Steinbach, A., 1972, Metabolic coupling, ionic coupling and cell contacts, Nature (London) 235:262–265.

    Google Scholar 

  • Goodman, C.S., and Spitzer, N.C., 1979, Embryonic development of identified neurones: Differentiation from neuroblast to neurone, Nature (London) 280:208–214.

    Google Scholar 

  • Goodman, C.S., and Spitzer, N.C., 1980, Embryonic development of neurotransmitter receptors in grasshoppers, in: Receptors for neurotransmitters, Hormones and Pheromones in Insects( D.B. Satelle Hildebrand, J.G., and Hall, L.M., eds.), Elsevier/North–Holand, Amsterdam, pp. 195 – 207.

    Google Scholar 

  • Goodman, C.S., and Spitzer, N.C., 1981, The development of electrical properties of identified neurones in grasshopper embryos, J. Physiol. 313: 385 – 403.

    Google Scholar 

  • Hagiwara, S., and Jaffe, L.A., 1979, Electrical properties of egg cell membranes, Annu. Rev. Biophys. Bioeng. 8: 385 – 416.

    Google Scholar 

  • Harris, W.A., 1980, The effect of eliminating impulse activity on the development of the retino- tectal projection in salamanders, J. Comp. Neurol.194: 303 – 317.

    Article  PubMed  CAS  Google Scholar 

  • Harris, W.A., 1981, Neural activity and development, Annu. Rev. Physiol43: 689 – 710.

    Article  PubMed  CAS  Google Scholar 

  • Heathcote, R.D., 1981, Differentiation of an identified sensory neuron (SR) and associated structures (CTO) in grasshopper embryos, J. Comp. Neurol202: 1 – 18.

    Article  PubMed  CAS  Google Scholar 

  • Jacobson, M., 1981, Rohon–Beard neuron origin from blastomeres of the 16–cell frog embryo, J. Neurosci. 1: 918 – 922.

    Google Scholar 

  • Kano, M., and Suzuki, N., 1982, Inhibition by α-amanitin of development of tetrodotoxin-sensitive spike induced by brain extract in cultured chick skeletal muscle cells, Dev. Brain Res.3: 674 – 678.

    Article  CAS  Google Scholar 

  • Lamborghini, J.E., 1980, Rohon-Beard cells and other large neurons in Xenopusembryos originate during gastrulation, J. Comp. Neurol189: 323 – 333.

    Article  PubMed  CAS  Google Scholar 

  • Lo, C.W., and Gilula, N.B., 1979, Gap junctional communication in the postimplantation mouse embryo, Cell18: 411 – 422.

    Article  PubMed  CAS  Google Scholar 

  • Meiri, H., Spira, M.E., and Paranas, I., 1978, Membrane Conductance and action potential of a regenerating axonal tip, Science 211:709–712

    Article  Google Scholar 

  • Meiri, H., Spira, M.E., and Parnas, I., 1981, Membrane conductance and action potential of a regenerating axonal tip, Science 211:709–712.

    Google Scholar 

  • Miyake, M., 1978, The development of action potential mechanism in a mouse neuronal cell line in vitro, Brain Res. 143: 349 – 354.

    Article  PubMed  CAS  Google Scholar 

  • Mori–Okamoto, J., Ashida, H., Mara, E., and Tatsuno, J., 1983, The development of action potentials in cultures of explanted cortical neurons from chick embryos, Dev. Biol, 97: 408 – 416.

    Google Scholar 

  • Obata, K., 1977, Development of neuromuscular transmission in culture with a variety of neurons and in the presence of cholinergic substances and TTX, Brain Res. 119:141–153.

    Article  PubMed  CAS  Google Scholar 

  • O’Dowd, D.K., 1981, The timing of RNA synthesis necessary for the development of the Na+- dependent action potential in cultured neurons, Soc. Neurosci. Abstr.7: 245.

    Google Scholar 

  • Ohmori, H., and Sasaki, S., 1977, Development of neuromuscular transmission in a larval tunicate, J. Physiol 269: 221 – 254.

    PubMed  CAS  Google Scholar 

  • Palmer, J.F., and Slack, C., 1970, Some bioelectric parameters of embryos of Xenopus laevis, J. Embryol Exp. Morphol 24: 535 – 553.

    PubMed  CAS  Google Scholar 

  • Pappano, A.J., 1972, Sodium-dependent depolarization of noninnervated embryonic chick heart by acetylcholine, J. Pharmacol. Exp. Ther. 180: 340 – 350.

    PubMed  CAS  Google Scholar 

  • Potter, D.D., Furshpan, E.J., and Lennox E., 1966, Connections between cells of the developing squid as revealed by electrophysiological methods, Proc. Natl. Acad. Sci. U.S.A.55: 328 – 336.

    Article  PubMed  CAS  Google Scholar 

  • Rayport, S.C., and Kandel, E.R., 1980, Developmental modulation of an identified electrical synapse: Functional uncoupling, J. Neurophysiol. 44: 555 – 567.

    PubMed  CAS  Google Scholar 

  • Roberts, A., and Clarke, J.D.W., 1982, The neuroanatomy of an amphibian embryo spinal cord, Philos. Trans. R. Soc. London Ser. B 296: 195 – 212.

    Article  CAS  Google Scholar 

  • Seecof, R.L., 1977, A genetic approach to the study of neurogenesis and myogenesis, Am. Zool 17: 577 – 584.

    Google Scholar 

  • Sheridan, J.D., 1968, Electrophysiological evidence for low resistance electrical connections between cells of the chick embryo, J. Cell Biol.37: 650 – 659.

    Article  PubMed  CAS  Google Scholar 

  • Slack, C., and Warner, A.E., Properties of surface and junctional membranes of embryonic cells isolated from blastula stages of Xenopus laevis, J. Physiol. 248:97–120.

    Google Scholar 

  • Spitzer, N.C., 1970, Low resistance connections between cells in the developing anther of the lily, J. Cell Biol. 45: 565 – 575.

    Article  PubMed  CAS  Google Scholar 

  • Spitzer, N.C., 1982a, Voltage- and stage-dependent uncoupling of Rohon-Beard neurones during embryonic development of Xenopustadpoles, J. Physiol.330: 145 – 162.

    CAS  Google Scholar 

  • Spitzer, N.C., 1982b, The development of electrical excitability, in: Neuronal–Glial Cell Interrelationships( T.A. Sears, ed), pp. 77 – 91, Springer-Verlag, Berlin.

    Google Scholar 

  • Spitzer, N.C., and Bixby, J.L., 1982, Appearance and development of chemosensitivity of embryonic amphibian spinal neurons in vitro, Soc. Neurosci, Abstr. 8: 130.

    Google Scholar 

  • Spitzer, N.C., and Lamborghini, J.E., 1976, The development of the action potential mechanism of amphibian neurons isolated in culture, Proc. Natl. Acad. Sci. U.S.A.73: 1641 – 1645.

    Article  PubMed  CAS  Google Scholar 

  • Spitzer, N.C., and Lamborghini, J.E., 1981, Programs of early neuronal development, in: Studies in Developmental Neurobiology(W.M. Cowan, ed.), Oxford University Press, New York, pp. 261 – 287.

    Google Scholar 

  • Spray, D.C., Harris, A.L., and Bennett, M.V.L., 1979, Voltage-dependence of junctional conductance in early amphibian embryos, Science 204:432–434.

    Article  PubMed  CAS  Google Scholar 

  • Steinbach, J.H., 1975, Acetylcholine responses in clonal myogenic cells in vitro, J. Physiol. 247:393–405.

    Google Scholar 

  • Stocker, S., and Bride, M., 1980, Effects of α-amanitin and actinomycin D on Xenopus laevis(Daud.) heart in culture during cardiac differentiation, Cell. Mol. Biol.26: 303 – 317.

    CAS  Google Scholar 

  • Strichartz, G., Small, R., Nicholson, C., Pfenninger, K.H., and Llinas, R., 1980, Ionic mechanisms for impulse propagation in growing nonmyelinated axons: Saxitoxin binding and electrophy– siology, Soc. Neurosci, Abstr. 6: 660.

    Google Scholar 

  • Takahashi, K., and Yoshii, M., 1981, Development of sodium, calcium and potassium channels in the cleavage-arrested embryo of an ascidian, J. Physiol. 315: 515 – 529.

    Google Scholar 

  • Takahashi, K., Miyazaki, S., and Kidokoro, Y., 1971, Development of excitability in embryonic muscle cell membranes in certain tunicates, Science 171:415–418.

    Google Scholar 

  • Tarin, D., 1971, Histological features of neural induction in Xenopus laevis, J. Embryol. Exp. Morphol. 26: 543 – 570.

    CAS  Google Scholar 

  • Van Essen, D.C., 1982, Neuromuscular synapse elimination, in: Neuronal Development(N.,C. Spitzer, ed.), Plenum Press, New York, pp. 333 – 376.

    Google Scholar 

  • Willard, A.L., 1980, Electrical excitability of outgrowing neurites of embryonic neurones in cultures of dissociated neural plate of Xenopus laevis, J. Physiol 301: 115 – 128.

    Google Scholar 

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    Google Scholar 

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© 1984 Plenum Press, New York

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Spitzer, N.C. (1984). The Differentiation of Membrane Properties of Spinal Neurons. In: Black, I.B. (eds) Cellular and Molecular Biology of Neuronal Development. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2717-2_6

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  • DOI: https://doi.org/10.1007/978-1-4613-2717-2_6

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-9686-7

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