Summary
The synaptic input to crayfish (Orconectes limosus) stretch receptor neurons, and the synaptic interactions between the inhibitory and excitatory efferents were analysed by electron microscopy of serial sections. Several novel types of synaptic connections have been observed: (i) inhibitory synaptic input on the axon hillock and initial axon segment; (ii) serial synaptic terminals on the sensory cell body; (iii) simultaneous synaptic contacts of the same inhibitory terminal with sensory dendrites and muscle fibres; (iv) reciprocal synapses between the two types of inhibitory efferents; and (v) inhibitory synapses on the primary inhibitory axon. The possible functional significance of these synapses is discussed in the light of earlier electrophysiological and pharmacological findings.
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References
Alexandrowicz, J. S. (1951) Muscle receptor organs in the abdomen ofHomarus vulgaris andPalinurus vulgaris.Quarterly Journal of Microscopical Science 92, 163–203.
Alexandrowicz, J. S. (1967) Receptor organs in the thoracic and abdominal ganglion of Crustacea.Biological Reviews 42, 288–326.
Atwood, A. H. (1982) Synapses and neurotransmitters. InThe Biology of Crustacea, Vol. 3,Neurobiology: Structure and function (edited byBliss, D. E., Atwood, H. L. &Sandeman, D. C.), pp. 105–50. New York: Academic Press.
Atwood, H. L. (1976) Organization and synaptic physiology of crustacean neuromuscular systems.Progress in Neurobiology 7, 291–391.
Atwood, H. L. &Jones, A. (1967) Presynaptic inhibition in crustacean muscle: axo-axonal synapse.Experientia 23, 1036–8.
Bazemore, A. W., Elliot, K. A. &Florey, E. (1957) Isolation of Factor I.Journal of Neurochemistry 1, 334–9.
Beltz, B. S. &Kravitz, E. A. (1987) Physiological identification, morphological analysis, and development of identified serotonin-proctolin containing neurons in lobster ventral nerve cord.Journal of Neuroscience 7, 533–46.
Bishop, C. A., Nagy, F., Wine, J. J. &O'Shea, M. (1984) Neuropeptide proctolin in postural motoneurons of the crayfish.Journal of Neuroscience 4, 2001–9.
Burgen, A. S. &Kuffler, S. W. (1957) Two inhibitory fibers forming synapses with a single nerve cell in the lobster.Nature 80, 1490–1.
Craelius, W. &Fricke, R. A. (1981) Release of3H-gamma-amino-butyric-acid (GABA) by inhibitory neurons of the crayfish.Journal of Neurobiology 12, 249–58.
Deisz, R. A. &Lux, H. D. (1982) The role of intracellular chloride in hyperpolarizing post-synaptic inhibition of crayfish stretch receptor neurones.Journal of Physiology 326, 123–38.
Edwards, C. &Kuffler, S. W. (1959) The blocking effect of γ-amino-butyric acid (GABA) and the action of related compounds on single nerve cells.Journal of Neurochemistry 4, 19–30.
Elekes, K. &Florey, E. (1987) Immunocytochemical evidence for the GABAergic innervation of the stretch receptor neurons in crayfish.Neuroscience (in press).
Eyzaguirre, C. &Kuffler, S. W. (1955a) Processes of excitation in the dendrites and in the soma of single isolated sensory nerve cells of the lobster and crayfish.Journal of General Physiology 39, 87–119.
Eyzaguirre, C. &Kuffler, S. W. (1955b) Further study of soma dendrite and axon excitation in single neurons.Journal of General Physiology 39, 121–53.
Florey, E. &Florey, E. (1955) Microanatomy of the abdominal stretch receptors of the crayfish (Astacus fluvialitis L.)Journal of General Physiology 39, 69–85.
Florey, E. &Rathmayer, M. (1986) Erregende und hemmende Wirkungen von GABA und von Dopamin auf Streckrezeptor-Neurone von Flußkrebsen: ionale Mechanismen. InSensomotorik. Identifizierte Neurone (edited byElsner, N. &Rathmayer, W.), p. 57. Stuttgart, New York: Georg Thieme Verlag.
Hirosawa, K., Tao-Cheng, Y., Nakajima, Y. &Tisdale, A. D. (1981) Thin-section and freeze-fracture studies of crayfish stretch receptor synapses including the reciprocal inhibitory synapses.Journal of Comparative Neurology 200, 39–53.
Hökfelt, T., Lundberg, J., Skirboll, L., Johansson, O., Schultzberg, M. &Vincent, S. R. (1982) Co-existence of classical transmitters and peptides in neurones. InCo-transmission (edited byCuello, A. C.), pp. 77–126. London: Macmillan.
Iwasaki, S. &Florey, E. (1969) Inhibitory miniature potentials in the stretch receptor neurons of crayfish.Journal of General Physiology 53, 666–82.
Jansen, J. K. S., Njå, A., Ormstad, K. &Walloe, L. (1971) On the innervation of the slowly adapting stretch receptor of the crayfish abdomen. An electrophysiological approach.Acta physiologica scandinavica 81, 273–85.
Komuro, T. (1981) Fine structural study of the abdominal muscle receptor organs of the crayfish (Procambarus clarkii). Sensory endings and synaptic structures.Journal of Neurocytology 10, 27–43.
Kosaka, K. (1969) Electrophysiological and electron microscopical studies on the neuromuscular junction of the crayfish receptors.Japanese Journal of Physiology 19, 160–75.
Kravitz, E. A., Kuffler, S. W. &Potter, D. D. (1963a) Gamma amino butyric acid and related compounds in crustacea. III. The relative concentrations in separated motor and inhibitory axons.Journal of Neurophysiology 26, 739–51.
Kravitz, E. A., Kuffler, S. W., Potter, D. D. &Van Gelder, N. M. (1963b) Gamma amino butyric acid and other blocking compounds in crustacea. II. Peripheral nervous system.Journal of Neurophysiology 26, 729–38.
Kuffler, S. W. (1954) Mechanisms of activation and motor control of stretch receptors in lobster and crayfish.Journal of Neurophysiology 17, 558–74.
Kuffler, S. W. &Edwards, C. (1958) Mechanism of gamma amino-butyric acid (GABA) action and its relation to synaptic inhibition.Journal of Physiology 21, 589–619.
Kuffler, S. W. &Eyzaguirre, C. (1955) Synaptic inhibition in an isolated nerve cell.Journal of General Physiology 39, 155–84.
McGeer, E. G., McGeer, P. L. &McLennan, H. (1961) The inhibitory action of 3-hydroxytryptamine, gamma-aminobutyric acid (GABA) and some other compounds towards crayfish stretch receptor neuron.Journal of Neurochemistry 8, 36–49.
Nadol, J. B. &De Lorenzo, A. J. D. (1968) Observations on the abdominal stretch receptor and the fine structure of associated axo-dendritic synapses and neuromuscular junctions inHomarus.Journal of Comparative Neurology 132, 419–44.
Nakajima, S., Tisdale, A. D. &Henkart, M. P. (1973) Presynaptic inhibition at inhibitory nerve terminals. A new synapse in the crayfish stretch receptor.Proceedings of the National Academy of Sciences USA 70, 2462–6.
Nakajima, Y. &Reese, T. S. (1983) Inhibitory and excitatory synapses in crayfish stretch receptor organs studied with direct rapid freezing and freeze-substitution.Journal of Comparative Neurology 213, 66–73.
Osborne, N. N., Cuello, A. C. &Dokray, G. J. (1982) Substance P and cholecystokinin-like peptides in Helix neurons and cholecystokinin and serotonin in a giant neuron.Science 216, 409–11.
Osborne, N. N. &Dockray, G. J. (1982) Bombesin-like immunoreactivity in specific neurones of the snailHelix aspersa and an example of the coexistence of substance P and serotonin in an invertebrate neurone.Neurochemistry International 4, 175–80.
Otsuka, M., Iversen, L. L., Hall, Z. W. &Kravitz, E. A. (1966) Release of gamma aminobutyric acid from inhibitory nerves of lobster.Proceedings of the National Academy of Sciences USA 56, 1110–15.
Peterson, R. P. &Pepe, F. A. (1961) The fine structure of inhibitory synapses in the crayfish.Journal of Biophysical and Biochemical Cytology 11, 157–69.
Reynolds, E. S. (1963) The use of lead citrate in electron-microscopy.Journal of Cell Biology 17, 208–12.
Siwicki, K. K., Beltz, B. S. &Kravitz, E. A. (1987) Proctolin in identified serotonergic, dopaminergic, and cholinergic neurons in lobster,Homarus americanus.Journal of Neuroscience 7, 522–32.
Spurr, A. R. (1969) A low viscosity expoxy resin embedding medium for electron-microscopy.Journal of Ultrastructure Research 26, 31–41.
Takeuchi, A. &Takeuchi, N. (1964) The effect on crayfish muscle of iontophoratically applied glutamate.Journal of Physiology 170, 296–317.
Takeuchi, A. &Takeuchi, N. (1965) Localized action of gamma-amino-butyric acid on the crayfish muscle.Journal of Physiology 177, 225–38.
Terzuolo, C. A. &Bullock, T. H. (1956) Measurement of imposed voltage gradient adequate to modulate neuronal firing.Proceedings of the National Academy of Sciences USA 42, 687–94.
Tisdale, A. D. &Nakajima, Y. (1976) Fine structure of synaptic vesicles in two types of nerve terminals in crayfish receptor organs: influence of fixation methods.Journal of Comparative Neurology 165, 369–86.
Uchizono, K. (1967) Inhibitory synapses on the stretch receptor neuron of the crayfish.Nature 214, 833–4.
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Fellow of the Alexander von Humboldt-Stiftung.
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Elekes, K., Florey, E. New types of synaptic connections in crayfish stretch receptor organs: an electron microscopic study. J Neurocytol 16, 613–626 (1987). https://doi.org/10.1007/BF01637654
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DOI: https://doi.org/10.1007/BF01637654