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Quantal nature of neuromuscular transmission in crayfish phasic abdominal flexors

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Summary

  1. 1.

    The electrophysiology and structure of the crayfish (Procambarus clarkii) deep abdominal flexor neuromuscular system were studied at several stages of development for the purpose of establishing and analyzing the quantal nature of synaptic transmission in these muscles.

  2. 2.

    In adult crayfish we were unable to obtain evidence for quantized neurotransmitter release in this system; spontaneous miniature synaptic potentials were never observed and evoked synaptic potential amplitude fluctuations suggested a mean quantal size of no more than a few microvolts. By recording from very young crayfish, so as to select fibers of higher input resistance, we were able to reveal the existence of a population of miniature potentials with a mean amplitude of less than 100 μV. Their amplitude distributions were always positively skewed, with the mode buried in the background noise. The time intervals between successive events were approximately exponentially distributed.

  3. 3.

    The extremely small quantal size was accounted for in terms of the input resistance (R N ) of the muscle fibers. The exceptionally lowR N resulted from a low specific membrane resistivity combined with an unusual organization of the muscle fibers into a system of electrically coupled subunits. Thus the total membrane area of each fiber is disproportionately large for its diameter. The developmental origin and functional significance of this form of neuromuscular organization are discussed.

  4. 4.

    The mean quantal content per muscle fiber was estimated to be several thousand in adult animals, an order of magnitude higher than has been reported for other crayfish muscles. The large quantal content appears to result from a greater than usual total number of synaptic contacts.

  5. 5.

    Synapses formed by the motor giant (MoG) and non-giant (NG) motor neurons displayed the same use-dependent labilities in young crayfish as previously reported in adults. With repetitive stimulation at low to moderate rates the NG synapses facilitated mildly due to an increase in mean quantal content, while the MoG synapses depressed even at rates of once per minute or less.

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Abbreviations

MoG :

motor giant

NG :

non giant

References

  • Anderson, M.: Electrophysiological studies on initiation and reversal of the heartbeat inCiona intestinalis. J. Exp. Biol.49, 363–385 (1968)

    Google Scholar 

  • Atwood, H.L.: Crustacean neuromuscular mechanisms. Am. Zool.7, 527–551 (1967)

    Google Scholar 

  • Atwood, H.L.: Crustacean muscle. In: The structure and function of muscle, Vol. 1, 2nd ed. Bourne, G.H. (ed.), pp. 421–489. New York: Academic Press 1972

    Google Scholar 

  • Atwood, H.L.: An attempt to account for the diversity of crustacean muscles. Am. Zool.13, 357–378 (1973)

    Google Scholar 

  • Atwood, H.L.: Organization and synaptic physiology of crustacean neuromuscular systems. Prog. Neurobiol.7, 291–391 (1976)

    Google Scholar 

  • Atwood, H.L.: Crustacean neuromuscular systems: Past, present and future. In: Identified neurons and behavior of arthropods. Hoyle, G. (ed.), pp. 9–29. New York: Plenum Press 1977

    Google Scholar 

  • Atwood, H.L., Bittner, G.D.: Matching of excitatory and inhibitory inputs to crustacean muscle fibers. J. Neurophysiol.34, 157–170 (1971)

    Google Scholar 

  • Atwood, H.L., Dorai Raj, B.S.: Tension development and membrane responses in phasic and tonic muscle fibers of a crab. J. Cell. Comp. Physiol.64, 55–72 (1964)

    Google Scholar 

  • Atwood, H.L., Jahromi, S.S.: Fast-axon synapses of a crab leg muscle. J. Neurobiol.9, 1–15 (1978)

    Google Scholar 

  • Atwood, H.L., Parnas, I.: Synaptic transmission in crustacean muscle with dual motor innervation. Comp. Biochem. Physiol.27, 381–404 (1968)

    Google Scholar 

  • Bittner, G.D.: Differentiation of nerve terminals in the crayfish opener muscle and its functional significance. J. Gen. Physiol.51, 731–758 (1968)

    Google Scholar 

  • Bittner, G.D., Harrison, J.: A reconsideration of the Poisson hypothesis for transmitter release at the crayfish neuromuscular junction. J. Physiol.206, 123 (1970)

    Google Scholar 

  • Bittner, G.D., Kennedy, D.: Quantitative aspects of transmitter release. J. Cell Biol.47, 585–592 (1970)

    Google Scholar 

  • Bittner, G.D., Sewell, V.L.: Facilitation at crayfish neuromuscular junctions. J. Comp. Physiol.109, 287–308 (1976)

    Google Scholar 

  • Bittner, G.D., Traut, D.L.: Growth of crustacean muscles and muscle fibres. J. Comp. Physiol.124, 277–285 (1978)

    Google Scholar 

  • Brown, T.H.: Structure and function of the crayfish phasic flexor neuromuscular system. Doctoral Dissertation, Stanford University (1977)

  • Bruner, J., Kennedy, D.: Habituation: Occurrence at a neuromuscular junction. Science169, 92–94 (1970)

    Google Scholar 

  • Castillo, J. del, Katz, B.: Quantal components of the end-plate potential. J. Physiol.124, 560–573 (1954)

    Google Scholar 

  • DeRosa, R.A., Govind, C.K.: Transmitter output increases in an identifiable lobster motoneurone with growth of its muscle fibre. Nature273, 676–678 (1978)

    Google Scholar 

  • Dudel, J.: Nonlinear voltage dependence of excitatory synaptic current in crayfish muscle. Pflügers Arch.352, 227–241 (1974)

    Google Scholar 

  • Dudel, J., Kuffler, S.W.: The quantal nature of transmission and spontaneous miniature potentials at the crayfish neuromuscular junction. J. Physiol.155, 514–529 (1961)

    Google Scholar 

  • Dudel, J., Orkand, R.K.: Spontaneous potential changes at crayfish neuromuscular junctions. Nature186, 476–477 (1960)

    Google Scholar 

  • Edwards, F.R., Redman, S.J., Walmsley, B.: Statistical fluctuations in charge transfer at Ia synapses on spinal motoneurones. J. Physiol.259, 665–688 (1976)

    Google Scholar 

  • Eisenberg, R.S.: The equivalent circuit of single crab muscle fibres as determined by impedance measurements with intracellular electrodes. J. Gen. Physiol.50, 1785–1806 (1967)

    Google Scholar 

  • Falk, G.: Predicted delays in the activation of the contractile system. Biophys. J.8, 608–625 (1968)

    Google Scholar 

  • Falk, G., Fatt, P.: Linear electrical properties of striated muscle fibres observed with intracellular electrodes. Proc. R. Soc. (London), Ser. B160, 69–123 (1964)

    Google Scholar 

  • Frank, E.: Matching of facilitation at the neuromuscular junction of the lobster: A possible case for influence of muscle on nerve. J. Physiol.233, 635–658 (1973)

    Google Scholar 

  • Franzini-Armstrong, C.: Freeze-fracture of excitatory and inhibitory synapses in crayfish neuromuscular junctions. J. Microsc. Biol. Cell.25, 217–222 (1976)

    Google Scholar 

  • Gage, P.W.: Generation of end-plate potentials. Physiol. Rev.56, 177–247 (1976)

    Google Scholar 

  • Gage, P., Helden, D. Van: Effects of permeant monovalent cations on end-plate channels. J. Physiol.288, 509–528 (1979)

    Google Scholar 

  • Hatt, H., Smith, D.O.: Synaptic depression related to presynaptic axon conduction block. J. Physiol.259, 367–393 (1976)

    Google Scholar 

  • Iansek, R., Redman, S.J.: The amplitude, time course and charge of unitary excitatory postsynaptic potentials evoked in spinal motoneurone dendrites. J. Physiol.234, 665–688 (1973)

    Google Scholar 

  • Jack, J.J.B., Noble, D., Tsien, R.W.: Electric current flow in excitable cells. Oxford: Clarendon Press 1975

    Google Scholar 

  • Jahromi, S.S., Atwood, H.L.: Electrical coupling and growth in lobster muscle fibres. Can. J. Zool.49, 1029–1034 (1971)

    Google Scholar 

  • Jahromi, S.S., Atwood, H.L.: Three-dimensional ultrastructure of the crayfish neuromuscular apparatus. J. Cell Biol.63, 599–613 (1974)

    Google Scholar 

  • Katz, B.: Neuromuscular transmission in invertebrates. Biol. Rev.24, 1–20 (1949)

    Google Scholar 

  • Katz, B., Miledi, R.: Propagation of electric activity in motor nerve terminals. Proc. R. Soc. (London), Ser. B161, 453–482 (1965)

    Google Scholar 

  • Katz, B., Thesleff, S.: On the factors which determine the amplitude of the “miniature end-plate potential”. J. Physiol.137, 267–278 (1957)

    Google Scholar 

  • Kennedy, D., Takeda, K.: Reflex control of abdominal flexor muscles in the crayfish. I. The twitch system. J. Exp. Biol.43, 211–227 (1965)

    Google Scholar 

  • Kuno, M., Miyahara, J.T.: Analysis of synaptic efficacy in spinal motoneurones from “quantum” aspects. J. Physiol.201, 479–493 (1969)

    Google Scholar 

  • Kuno, M., Turkanis, S.A., Weakly, J.N.: Correlation between nerve terminal size and transmitter release at the neuromuscular junction of the frog. J. Physiol.213, 545–556 (1971)

    Google Scholar 

  • Lang, F., Atwood, H.L.: Crustacean neuromuscular mechanisms: Functional morphology of nerve terminals and the mechanism of facilitation. Am. Zool.13, 337–355 (1973)

    Google Scholar 

  • Martin, A.R.: Quantal nature of synaptic transmission. Physiol. Rev.46, 51–66 (1966)

    Google Scholar 

  • Miledi, R.: Spontaneous synaptic potentials and quantal release of transmitter in the stellate ganglion of the squid. J. Physiol.192, 379–406 (1967)

    Google Scholar 

  • Onodera, K., Takeuchi, A.: Ionic mechanism of the excitatory synaptic membrane of the crayfish neuromuscular junction. J. Physiol.252, 295–318 (1975)

    Google Scholar 

  • Parnas, I., Atwood, H.L.: Phasic and tonic neuromuscular systems in the abdominal extensor muscles of the crayfish and rock lobster. Comp. Biochem. Physiol.18, 701–723 (1966)

    Google Scholar 

  • Schrameck, I.E.: Crayfish swimming: alternating motor output and giant fiber activity. Science169, 698–700 (1970)

    Google Scholar 

  • Selverston, A.I., Remler, M.P.: Neural geometry and activation of crayfish fast flexor motoneurons. J. Neurophysiol.35, 797–814 (1972)

    Google Scholar 

  • Sherman, R.G., Atwood, H.L.: Synaptic facilitation: Long-term neuromuscular facilitation in crustaceans. Science171, 1248–1250 (1971)

    Google Scholar 

  • Sherman, R.G., Atwood, H.L.: Correlated electrophysiological and ultrastructural studies of a crustacean motor unit. J. Gen. Physiol.59, 586–615 (1972)

    Google Scholar 

  • Takeda, K.: Permeability changes associated with the action potential in procaine-treated crayfish abdominal muscle fibers. J. Gen. Physiol.50, 1049–1074 (1967)

    Google Scholar 

  • Williams, J.D., Bowen, J.M.: Effects of quantal unit latency on statistics of Poisson and binomial neurotransmitter release mechanisms. J. Theor. Biol.43, 151–165 (1974)

    Google Scholar 

  • Wine, J.J., Krasne, F.B.: The organization of escape behaviour in the crayfish. J. Exp. Biol.56, 1–18 (1972)

    Google Scholar 

  • Zucker, R.S.: Crayfish escape behavior and central synapses. II. Physiological mechanisms underlying behavioral habituation. J. Neurophysiol.35, 621–637 (1972)

    Google Scholar 

  • Zucker, R.S.: Synaptic plasticity at crayfish neuromuscular junctions. In: Identified neurons and behavior of arthropods. Hoyle, G. (ed.), pp. 49–65. New York: Plenum Press 1977

    Google Scholar 

  • Zucker, R.S., Bruner, J.: Long-lasting depression and the depletion hypothesis at crayfish neuromuscular junctions. J. Comp. Physiol.121, 223–240 (1977)

    Google Scholar 

  • Zucker, R.S., Kennedy, D., Selverston, A.I.: Neuronal circuit mediating escape responses in crayfish. Science173, 645–650 (1971)

    Google Scholar 

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Author notes

  1. Thomas H. Brown

    Present address: Division of Neurosciences, City of Hope Research Institute, 91010, Duarte, California, USA

  2. Nicki Ann Newby

    Present address: Biology Department, Lafayette College, 18042, Easton, Pennsylvania, USA

Authors and Affiliations

  1. Department of Biological Sciences, Stanford University, 94305, Stanford, California, USA

    Thomas H. Brown & Nicki Ann Newby

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  1. Thomas H. Brown
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  2. Nicki Ann Newby
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Additional information

We thank Peter Getting, Donald Kennedy, Jeffrey Wine and Robert Zucker for reading versions of this manuscript and Russell Fricke for assistance in some of the anatomical studies. This research was supported by NIH Grant NS 02944-18 to Donald Kennedy and was completed during the tenure of research fellowships of the Muscular Dystrophy Association of America awarded to T.H.B. and N.A.N.

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Brown, T.H., Newby, N.A. Quantal nature of neuromuscular transmission in crayfish phasic abdominal flexors. J. Comp. Physiol. 136, 89–101 (1980). https://doi.org/10.1007/BF00656905

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