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The first-order giant neurons of the giant fiber system in the squid: electrophysiological and ultrastructural observations

  • Published:
Journal of Neurocytology

Abstract

The giant fiber system controlling mantle contraction used for jet propulsion in squid consists of two sets of three giant neurons organized in tandem. The somata of the 1st- and 2nd-order giant cells are located in the brain, while the perikarya of the 3rd-order giant cells are encountered in the stellate ganglia of the mantle. The somata and dendrites of one fused pair of 1st-order giant cells are thought to receive synaptic input from the eye, statocyst, skin proprioceptors, and supraesophageal lobes. To define the cellular properties for integration of such an extensive synaptic load, especially given its diversity, intracellular recordings and electron microscopic observations were performed on 1st-order giant cells in an isolated head preparation. Spontaneous bursts of action potentials and spikes evoked by extracellular stimulation of the brachial lobe were sensitive to the Na+ channel blocker TTX. Action potentials were also abolished by recording with microelectrodes containing the membrane-impermeant, use-dependent Na+ channel blocker QX-314. The small action potential amplitude and the abundant synaptic input imply that the spike initiation zone is remotely located from the recording site. The high spontaneous activity in the isolated head preparation, as well as the presence of synaptic junctions resembling inhibitory synapses, suggest; that afferent synapses on 1st-order giant neurons might represent the inhibitory control of the giant fiber system. The characterization of the electroresponsive properties of the 1st-order giant neurons will provide a description of the single cell integrative properties that trigger the rapid jet propulsion necessary for escape behavior in squid.

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References

  • Bloom, F. E. & Aghajanian, G. K. (1966) Cytochemistry of synapses: selective staining for electron microscopy. Science 154, 1575- 7.

    Google Scholar 

  • CastejÓn, O. J. & Villegas, G. M. (1964) Fine structure of the synaptic contacts in the stellate ganglion of the squid. Journal of Ultrastructure Research 10, 585- 98.

    Google Scholar 

  • Charlton, M. P. & Bittner, G. D. (1978) Facilitation of transmitter release at squid synapses. Journal of General Physiology 72, 471- 86.

    Google Scholar 

  • Colonnier, M. (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscopy study. Brain Research 9, 268- 87.

    Google Scholar 

  • Corrie, J. T., de Santis, A., Katayama, Y., Khodakhah, K., Messenger, J. B., Ogden, D. C. & Trentham, D. R. (1993) Postsynaptic activation at the squid giant synapse by photolytic release of L-glutamate from a ″caged″ L-glutamate. Journal of Physiology 465, 1- 8.

    Google Scholar 

  • Froesch, D. & Martin, R. (1972) Heterogeneity of synaptic vesicles in the squid giant fibre system. Brain Research 43, 573- 9.

    Google Scholar 

  • Furukawa, T. (1966) Synaptic interaction at the Mauthner cell of goldfish. Progress in Brain Research 21A, 44- 70.

    Google Scholar 

  • Gervasio, A., Martin, R. & Miralto, A. (1971) Fine structure of synaptic contacts in the first order giant fiber system of the squid. Zeitschrift für Zellforschung 112, 85- 96.

    Google Scholar 

  • Gilly, W. F., Hopkins, B. & Mackie, G. O. (1991) Development of giant motor axons and neural control of escape responses in squid embryos and hatchlings. Biological Bulletin 180, 209- 20.

    Google Scholar 

  • Gray, E. G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscopic study. Journal of Anatomy 93, 420- 33.

    Google Scholar 

  • Gray, E. G. (1963) Electron microscopy of presynaptic organelles of the spinal cord. Journal of Anatomy 97, 101- 6.

    Google Scholar 

  • Hama, K. (1962) Some observations on the fine structure of the giant synapse in the stellate ganglion of the squid, Doryteuphis bleekeri. Zeitschrift für Zellforschung 56, 437- 44.

    Google Scholar 

  • Kehoe, J. (1972) Ionic mechanisms of a two-component cholinergic inhibition in Aplysia. Journal of Physiology (Cambridge) 225, 85- 114.

    Google Scholar 

  • Landis, D. M. D., & Reese, T. S. (1974) Differences in membrane structure between excitatory and inhibitory synapses in the cerebellar cortex. Journal of Comparative Neurology 155, 93- 126.

    Google Scholar 

  • Landis, D. M. D., Reese, T. S. & Raviola, E. (1974) Differences in membrane structure at excitatory and inhibitory components of the reciprocal synapse in the olfactory bulb. Journal of Comparative Neurology 155, 67- 92.

    Google Scholar 

  • Laverack, M. S. (1980) Electrophysiology of the isolated central nervous system of the northern octopus Elodone cirrhosa. Marine Behaviour and Physiology 7, 155- 69.

    Google Scholar 

  • LlinÁs, R., Steinberg, I. Z & Walton, K. (1981) Presynaptic calcium current in squid giant synapse. Biophysical Journal 33, 289- 322.

    Google Scholar 

  • LlinÁs, R. & Sugimori, M. (1995) Synaptic transmission in the squid stellate ganglion. In: Cephalopod Neurobiology (edited by Abbott, N. J., Williamson, R. & Maddock, L.), pp. 255- 70. Oxford: Oxford University Press.

    Google Scholar 

  • Martin, R. (1969) The structural organization of the intracerebral giant fiber system of cephalopods. Zeitschrift für Zellforschung 97, 50- 68.

    Google Scholar 

  • Martin, R. (1977) The giant nerve fibre system of cephalopods. Recent structural findings. Symposium of the Zoological Society of London 38, 261- 75.

    Google Scholar 

  • Martin, R. & Miledi, R. (1986) The form and dimensions of the giant synapse of squids. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 312, 355- 77.

    Google Scholar 

  • Messenger, J. B., de Santis, A. & Ogden, D. C. (1995) Chemical transmission at the squid giant synapse. In: Cephalopod Neurobiology (edited by Abbott, N. J., Williamson, R. & Maddock, L.), pp. 283- 297. Oxford: Oxford University Press.

    Google Scholar 

  • Miledi, R. (1967) Spontaneous synaptic potentials and quantal release of transmitter in the stellate ganglion of the squid. Journal of Physiology (Cambridge) 192, 379- 406.

    Google Scholar 

  • Miledi, R. (1969) Transmitter action in the giant synapse of the squid. Nature 223, 1234- 5.

    Google Scholar 

  • Miyan, J. A. & Messenger, J. B. (1995) Intracellular recordings from the chromatophore lobes of Octopus. In: Cephalopod Neurobiology (edited by Abbott, N. J., Williamson, R. & Maddock, L.), pp. 415- 29. Oxford: Oxford University Press.

    Google Scholar 

  • Otis, T. S. & Gilly, W. F. (1990) Jet-propelled escape in the squid Loligo opalescens: Concerted control by giant and non-giant motor axon pathways. Proceedings of the National Academy of Sciences, USA 87, 2911- 5.

    Google Scholar 

  • Peters, A., Palay, S. L. & Webster, H. deF. (1991) The Fine Structure of the Nervous System. Neurons and Their Supporting Cells, 3rd edition. Oxford: Oxford University Press.

    Google Scholar 

  • Pfenninger, K. H., Sandri, C., Akert, K. & Engster, C. (1969) Contributions to the problem of structural organization of the presynaptic area. Brain Research 12, 10- 18.

    Google Scholar 

  • Pozzo-Miller, L. D., Moreira, J. E. & LlinÁs, R. R. (1996) Electrophysiological and ultrastructural observations on the first-order giant neuron of the giant fiber system of the squid. Society for Neurosciences Abstracts 22, 1081.

    Google Scholar 

  • Prosser, C. L. & Young, J. Z. (1937) Responses of muscles of the squid to repetitive stimulation of the giant nerve fibres. Biological Bulletin 73, 237- 41.

    Google Scholar 

  • Pumplin, D. W. & Reese, T. S. (1978) Membrane ultrastructure of the giant synapse of the squid Loligo pealei. Neuroscience 3, 685- 96.

    Google Scholar 

  • Ribak, C. E. & Roberts, R. C. (1990) The GABAergic synapses in the brain identified with antisera to GABA and its synthesizing enzyme, glutamate decarboxylase. Journal of Electron Microscopy Technique 15, 34- 48.

    Google Scholar 

  • Stanley, E. F. (1984) The action of cholinergic agonists on the squid stellate ganglion giant synapse. Journal of Neuroscience 4, 1904- 11.

    Google Scholar 

  • Stanley, E. F. (1990) The preparation of the squid giant synapse for electrophysiological investigation. In: Squid as Experimental Animals (edited by Gilbert, D. L., Adelman, W. J. Jr. & Arnold, J. M.), pp. 171- 92. New York: Plenum Press.

    Google Scholar 

  • Trueman, E. R. & Packard, A. (1968) Motor performances of some cephalopods. Journal of Experimental Biology 49, 495- 507.

    Google Scholar 

  • Uchizono, K. (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature 207, 642- 3.

    Google Scholar 

  • Uchizono, K. (1967) Inhibitory synapses on the stretch receptor neurone of the crayfish. Nature 214, 833- 4.

    Google Scholar 

  • Webb, G. D., Dettbarn, W. D. & Brzin, M. (1966) Biochemical and pharmacological aspects of the synapse of the squid stellate ganglia. Biochemistry and Pharmacology 15, 1813- 4.

    Google Scholar 

  • Williams, L. W. (1909) The Anatomy of the Common Squid Loligo pealei Lesueur. Leiden, Holland: Brill.

    Google Scholar 

  • Williamson, R. & Budelmann, B. U. (1991) Convergent inputs to Octopus oculomotor neurones demonstrated in a brain slice preparation. Neuroscience Letters 121, 215- 8.

    Google Scholar 

  • Young, J. Z. (1938) The functioning of the giant fibres of the squid. Journal of Experimental Biology 15, 170- 5.

    Google Scholar 

  • Young, J. Z. (1939) Fused neurons and synaptic contacts in the giant nerve fibers of cephalopods. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 229, 465- 503.

    Google Scholar 

  • Young, J. Z. (1973) The giant fibre synapse of Loligo. Brain Research 57, 457- 60.

    Google Scholar 

  • Young, J. Z. (1976) The nervous system of Loligo. II. Subesophageal centres. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 274, 101- 67.

    Google Scholar 

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Pozzo-Miller, L.D., Moreira, J.E. & Llinás, R.R. The first-order giant neurons of the giant fiber system in the squid: electrophysiological and ultrastructural observations. J Neurocytol 27, 419–429 (1998). https://doi.org/10.1023/A:1006984410908

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