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Dense-core vesicles and non-synaptic exocytosis in the central body of the crayfish brain

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Summary

The central body in the median protocerebrum of the brain of the crayfish Cherax destructor is a distinctive area of dense neuropile, the nerve fibres of which contain three main types of vesicles: electronlucent vesicles (diameter 35 nm), dense-core vesicles (diameter 64 nm), and large structured dense-core vesicles (diameter 98 nm, maximum 170 nm). Different vesicle types were found together in the same neurons. Electronlucent vesicles were seen at presynaptic sites and rarely observed in the state of exocytosis. Exocytosis of densecore and structured dense-core vesicles was a regular feature on non-synaptic release sites either close to, or at some distance from pre- and subsynaptic sites. Non-synaptic exocytotic sites are more often observed than chemical synapses. Different forms of exocytosis seen at non-synaptic sites included the release of single densecore vesicles, packets of dense-core vesicles, and rows of dense-core vesicles lined up along cell membranes and around fibre invaginations. Swelling and the enhanced electron density of extracellular non-synaptic spaces may mark the positions of prior exocytotic events. In vitro treatment of the brain with tannic acid buffer solution followed by conventional double fixation resulted in the augmentation of non-synaptic exocytosis. Electron microscopy of proctolin- and serotonin-immunoreactive nerve fibres shows them to contain dense-core and electron-lucent vesicles and to be surrounded by many unlabelled profiles similarly laden with dense-core vesicles and electron-lucent vesicles, indicating the presence of other, not yet identified, neuroactive compounds.

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References

  • Abbott N (1972) Access of ferritin to the interstitial space of Carcinus brain from intracerebral blood vessels. Tissue Cell 4:99–104

    Google Scholar 

  • Andrews PM (1973) Ultrastructural study of the pericardial organanterior ramifications with complex neurosecretory terminals. Z Zellforsch 144:309–324

    Google Scholar 

  • Aramant R, Elofsson R (1976) Monoaminergic neurons in the nervous system of crustaceans. Cell Tissue Res 170:231–251

    Google Scholar 

  • Atwood HL, Luff AR, Morin WA, Sherman RE (1971) Dense cored vesicles at neuromuscular synapses of arthropods and vertebrates. Experientia 27:816

    Google Scholar 

  • Buma P, Roubos EW (1986) Ultrastructural demonstration of non-synaptic release sites in the central nervous system of the snail Lymnaea stagnalis, the insect Periplaneta americana, and the rat. Neuroscience 17:867–879

    Google Scholar 

  • Cuadras J (1989) Non-synaptic release from dense-cored vesicles occurs at all terminal types in crayfish neuropile. Brain Res 477:332–335

    Google Scholar 

  • Cuzin-Roudy J, Ashton ML, Saleuddin ASM (1988) Neurosecretory centers from the eyestalk of Siriella armata M.Edw. (Crustacea: Mysidacea): ultrastructural variations during normal and experimentally inhibited molt cycle. Cell Tissue Res 254:381–391

    Google Scholar 

  • Dircksen H, Keller R (1988) Immunocytochemical localization of CCAP, a novel crustacean cardioactive peptide, in the nervous system of the shore crab, Carcinus meanas L. Cell Tissue Res 254:347–360

    Google Scholar 

  • Elekes K, Florey E (1987) New types of synaptic connections in crayfish stretch receptor organs: an electron microscopic study. J Neurocyto 16:613–626

    Google Scholar 

  • Heitler WJ, Cobb JLS, Fraser K (1985) Ultrastructure of the segmental giant neuron of crayfish. J Neurocytol 14:921–941

    Google Scholar 

  • Homberg U (1985) Interneurons of the central complex in the bee brain (Apis mellifera L.). J Ins Physiol 31:251–264

    Google Scholar 

  • Kerwien P, Schürmann FW (1990) Nonsynaptic exocytosis after tannic acid in vitro treatment in the brain and corpora cardiaca of an insect. In: Elsner N (ed) Proceedings of the 18th Göttingen Neurobiology Conference. Thieme, Stuttgart, p 312

    Google Scholar 

  • Killmann F, Schürmann FW (1985) Both electrical and chemical transmission between the ‘lobula giant movement detector’ and the ‘descending contralateral movement detector’ neurons of locusts are supported by electron microscopy. J Neurocytol 14:637–652

    Google Scholar 

  • King DG (1976) Organization of crustacean neuropil. I. Patterns of synaptic connections in lobster stomatogastric ganglion. J Neurocytol 5:207–237

    Google Scholar 

  • Klemm N (1976) Histochemistry of putative transmitter substances in the insect brain. Prog Neurobiol 7:99–169

    Google Scholar 

  • Kondoh Y, Hisada M (1986) Distribution and ultrastructure of synapses on a premotor local nonspiking interneuron of the crayfish. J Comp Neurol 254:259–270

    Google Scholar 

  • Livingstone MS, Schaeffer SF, Kravitz EA (1981) Biochemistry and ultrastructure of serotoninergic nerve endings in the lobster: serotonin and octopamine are contained in different nerve endings. J Neurobiol 12:27–54

    Google Scholar 

  • Mearow KM, Govind CK (1989) Stimulation-induced changes at crayfish (Procambarus clarkii) neuromuscular terminals. Cell Tissue Res 256:119–123

    Google Scholar 

  • Meiss DE, Govind CK (1980) Heterogeneity of excitatory synapses at the ends of single muscle fibres in lobster, Homarus americanus. J Neurobiol 11:381–395

    Google Scholar 

  • Nässel DR, Elekes K (1984) Ultrastructural demonstration of serotonin-immunoreactivity in the nervous system of an insect (Calliphora erythrocephala). Neurosci Lett 48:203–210

    Google Scholar 

  • Nässel DR, O'Shea M (1987) Proctolin-like immunoreactive neurons in the blowfly central nervous system. J Comp Neurol 265:437–454

    Google Scholar 

  • Nordmann JJ, Morris JF (1980) Depletion of neurosecretory granules and membrane retrieval in the sinus gland of the crab. Cell Tissue Res 205:31–42

    Google Scholar 

  • Nordmann TC (1976) Neurosecretion by exocytosis. Int Rev Cytol 46:1–77

    Google Scholar 

  • Sandeman DC (1967) Vascular circulation in the brain, optic lobes and thoracic ganglia of the crab Carcinus. Proc R Soc Lond (Biol) 168:82–90

    Google Scholar 

  • Sandeman DC (1982) Organization of the central nervous system. In: Atwood HA, Sandeman DC (eds) Biology of the crustacea, vol 3. Academic Press, New York, pp 1–61

    Google Scholar 

  • Sandeman DC, Luff SE (1973) The structural organization of glomerular neuropile in the olfactory and accessory lobes of an Australian freshwater crayfish, Cherax destructor. Z Zellforsch 142:37–61

    Google Scholar 

  • Sandeman DC, Sandeman RE, Aitken AR (1988) Atlas of serotonin-containing neurons in the optic lobes and brain of the crayfish, Cherax destructur. J Comp Neurol 269:465–478

    Google Scholar 

  • Schürmann FW (1987) Histology and ultrastructure of the onychophoran brain. In: Gupta AP (ed) Arthropod brain. Its evolution, development, structure and functions. Wiley, New York, pp 159–180

    Google Scholar 

  • Thureson-Klein A (1983) Exocytosis from large and small dense cored vesicles in noradrenergic nerve teminals. Neuroscience 10:245–252

    Google Scholar 

  • Thureson-Klein A, Klein RL, Zhu P-J, Kong J-Y (1988) Differential release of transmitters and neuropeptides co-stored in central and peripheral neurons. In: Zimmermann H (ed) Cellular and molecular basis of synaptic transmission. Springer, Berlin Heidelberg New York, pp 137–151

    Google Scholar 

  • Tsvileneva VA, Titova VA (1985) On the brain structures of decapods. Zool Jb Anat 113:217–266

    Google Scholar 

  • Wang-Bennett LT, Glantz RM (1985) Presynaptic inhibition in the crayfish brain. J Comp Physiol A 156:605–617

    Google Scholar 

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Schürmann, FW., Sandeman, R. & Sandeman, D. Dense-core vesicles and non-synaptic exocytosis in the central body of the crayfish brain. Cell Tissue Res 265, 493–501 (1991). https://doi.org/10.1007/BF00340872

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