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Distribution of serotonin-containing neurons in the central nervous system of the snail Helix pomatia

Comparison of immunocytochemical and 5,6-dihydroxytryptamine labelling

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Summary

The distribution of serotonin (5HT)-containing neurons in the central nervous system of the snail Helix pomatia has been determined in whole-mount preparations by use of immunocytochemical and in vivo 5,6-dihydroxy-tryptamine labelling. 5HT-immunoreactive neuronal somata occur in all but the buccal and pleural ganglia. Immunoreactive fibres are present throughout the central nervous system. The 5HT-immunoreactive neuronal somata characteristically appear in groups, located mainly in the cerebral, pedal, visceral and right parietal ganglia. The majority of 5HT-immunoreactive neurons is located in the pedal ganglia. Additionally a dense network of 5HT-immunoreactive varicose fibres is found in the neural sheath of the central nervous system including all the nerves and ganglia. The number and distribution of 5HT-immunoreactive neurons correlates with that demonstrated by 5,6-dihydroxytryptamine labelling method.

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References

  • Balaban PM, Vehovszky A, Maximova DA, Zakharov IS (1987) Effect of 5,7-dihydroxytryptamine on the food-aversive conditioning in the snail Helix lucorum. Brain Res 404:201–210

    Google Scholar 

  • Barber A (1982) Monoamine-containing varicosities in the neural sheath of a gastropod mollusc demonstrated by glyoxylic acid histofluorescence. Cell Tissue Res 226:267–273

    Google Scholar 

  • Beltz BA, Kravitz EA (1983) Mapping of serotonin-immunoreactivity in the lobster nervous system. J Neuroscience 3:585–602

    Google Scholar 

  • Benjamin PR, Elliott CJH (1988) Snail feeding oscillator: The central pattern generation and its control by modulatory interneurons. In: Jacklet J (ed) Cellular and Neuronal Oscillators. Marcel Dekker, New York (in press)

    Google Scholar 

  • Benjamin PR, Peat A (1968) Myoneural junctions in the connective tissue sheath of a molluscan ganglion. Nature 219:1371–1372

    Google Scholar 

  • Cottrell GA (1970) Direct postsynaptic response to stimulation of serotonin-containing neurones. Nature 225:1060–1062

    Google Scholar 

  • Cottrell GA (1977) Identified amine-containing neurons and their synaptic connections. Neuroscience 2:1–18

    Google Scholar 

  • Croll RP (1987) Distribution of monoamines in the central nervous system of the nudibranch gastropod, Hermissenda crassicornis. Brain Res 405:337–347

    Google Scholar 

  • Davis NT (1985) Serotonin-immunoreactive visceral nerves and neurohaemal system in the cockroach Periplaneta americana (L). Cell Tissue Res 240:593–600

    Google Scholar 

  • Dryer RF, Cowden RP (1973) Electron microscopy of the esophageal ganglion complex of the gastropod pulmonate Triodopsis divesta. I. Ultrastructure of the epineurium. J Morphol 139:125–154

    Google Scholar 

  • Flores V, Brusco A, Pecci Saavedra J (1986) Serotonergic system in Cryptomphalus aspersa. Immunocytochemical study with an anti-5-HT antiserum. J Neurobiol 17:547–561

    Google Scholar 

  • Gerschenfeld HM (1973) Chemical transmission in invertebrates central nervous system and neuromuscular junctions. Physiol Rev 53:1–119

    Google Scholar 

  • Gerschenfeld HM, Hamon M, Paupardin-Tritsch D (1978) Release of endogenous serotonin from two identified serotonin-containing neurones and the physiological role of serotonin uptake. J Physiol (Lond) 274:265–278

    Google Scholar 

  • Gerschenfeld HM, Paupardin-Tritsch D, Deterre P (1981) Neuronal responses to serotonin: a second view. In: Jacobs BL, Gelperin A (eds) Serotonin neurotransmission and behaviour. MIT Press, Cambridge Mass., pp 105–130

    Google Scholar 

  • Goldstein R, Kistler HB Jr, Steinbusch HWM, Schwartz JH (1984) Distribution of serotonin-immunoreactivity in the juvenile Aplysia. Neuroscience 11:535–547

    Google Scholar 

  • Hernádi L, Kemenes G, S.-Rózsa K (1987) Selective in vivo labelling of serotonergic neurones by 5,6-dihydroxytryptamine in the snail Helix pomatia L. In: Boer HH, Geraerts WPM, Joosse J (eds) Neurobiology, Molluscan Models. Mon Kon Ned Akad Wetensch, North Holland Publ Co, Amsterdam Oxford New York, pp 22–25

    Google Scholar 

  • Hiripi L, Salánki J (1973) Seasonal and activity-dependent changes of the serotonin level in the CNS and heart of the snail (Helix pomatia L.). Comp Gen Pharmacol 4:285–292

    Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) The use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP) procedures. J Histochem Cytochem 29:577

    Google Scholar 

  • Jahan-Parwar B, S-Rózsa K, Salánki J, Evans ML, Carpenter DO (1987) In vivo labelling of serotonin-containing neurons by 5,7- ihydroxytryptamine in Aplysia. Brain Res 426:173–178

    Google Scholar 

  • Kandel ER (1976) The Cellular Basis of Behavior. Freeman and Co, San Francisco

    Google Scholar 

  • Kandel ER, Schwartz JH (1982) Molecular biology of learning: modulation of transmitter release. Science 218:433–443

    Google Scholar 

  • Kandel ER, Klein M, Bailey CH, Hawkins RD, Castellucci VF, Lubit BV, Schwartz JH (1981) Serotonin, cyclic AMP, and the modulation of the calcium current during arousal. In: Jacobs BL, Gelperin A (eds) Serotonin neurotransmission and behavior. MIT Press, Cambridge, Mass., pp 211–254

    Google Scholar 

  • Kemenes G, S.-Rózsa K (1987) The role of serotonergic mechanisms in food-induced arousal of the snail Helix pomatia L. In: Boer HH, Geraerts WPM, Joosse J (eds) Neurobiology, Molluscan Models. Mon Kon Ned Akad Wetensch, North Holland Publ Co, Amsterdam Oxford New York, pp 277–286

    Google Scholar 

  • Kemenes G, Benjamin PR, Hiripi L (1988) 5,6-Dihydroxytryptamine-induced changes in the serotonergic modulation of feeding in Lymnaea. In: Salánki J, S.-Rózsa K (eds) Neurobiology of Invertebrates: Transmitters, Modulators and Receptors. Manchester Univ Press and Akadémiai Kiadó Budapest, pp 415–431

    Google Scholar 

  • Kistler HB, Jr, Hawkins RD, Koester J, Steinbusch HWM, Kandel ER, Schwartz JH (1985) Distribution of serotonin-immunoreactive cell bodies and processes in the abdominal ganglion of mature Aplysia. J Neuroscience 5:72–80

    Google Scholar 

  • Kupferman I, Castellucci V, Pinsker H, Kandel ER (1970) Neuronal correlates of habituation and dishabituation of the gillwithdrawal reflex in Aplysia. Science 167:1743–1745

    Google Scholar 

  • Longley RD, Longley AJ (1986) Serotonin immunoreactivity of neurons in the gastropod Aplysia californica. J Neurobiol 17:339–358

    Google Scholar 

  • Marsden C, Kerkut GA (1970) The occurrence of monoamines in Planorbis corneus: A fluorescence microscopic and microspectrometric study. Comp Gen Pharmacol 1:101–116

    Google Scholar 

  • McCaman MW, Ono JK, McCaman RE (1984) 5-Hydroxytryptamine measurements in molluscan ganglia and neurons using a modified radioenzymatic assay. J Neurochem 43:91–99

    Google Scholar 

  • Meng K (1958) 5-Hydroxytryptamin und Acetylcholin als Wirkungsantagonisten beim Helix-Herzen. Naturwissenschaften 19:470–481

    Google Scholar 

  • Nässel DR, Elekes K (1985) Serotonergic terminals in the neural sheath of the blowfly nervous system: electromicroscopical immunocytochemistry and 5,7-dihydroxytryptamine labelling. Neuroscience 15:293–307

    Google Scholar 

  • Osborne NN (1982) Biology of Serotonergic Transmission. John Wiley and Sons Ltd, Chichester

    Google Scholar 

  • Osborne NN, Dockray GJ (1982) Bombesin-like immunoreactivity in specific neurones of the snail Helix aspersa and an example of the coexistence of substance P and serotonin in an invertebrate neurone. Neurochem Int 4:175–180

    Google Scholar 

  • Osborne NN, Cuello AC, Dockray GJ (1982) Substance P and cholecystokinin and serotonin in a giant neuron. Science 216:160–178

    Google Scholar 

  • Ono JK, McCaman RE (1984) Immunocytochemical localization and direct assays of serotonin-containing neurons in Aplysia. Neuroscience 11:549–560

    Google Scholar 

  • Pentreath VW, Cottrell GA (1970) The blood supply to the central nervous system of Helix pomatia. Z Zellforsch 111:160–178

    Google Scholar 

  • Sawada M, Ichinose M, Ito I, Maeno T, McAdoo D (1984) Effect of 5-hydroxytryptamine on membrane potential, contractility, accumulation of cyclic AMP and Ca2+ movements in the anterior aorta and ventricle of Aplysia. J Neurophysiol 51:361–374

    Google Scholar 

  • Sakharov DA, Zs.-Nagy I (1968) Localization of biogenic monoamines in cerebral ganglia of Lymnaea stagnalis. Acta Biol Acad Sci Hung 19:145–157

    Google Scholar 

  • Sedden CB, Walker RJ, Kerkut GA (1968) The localization of dopamine and 5-HT in neurons of Helix aspersa. Symp Zool Soc Lond 22:19–32

    Google Scholar 

  • S.-Rózsa K (1976) Neural network underlying the regulation of heart beat in Helix pomatia. In: Salánki J (ed) Neurobiology of Invertebrates. Gastropoda Brain. Akadémiai Kiadó, Budapest, pp 597–613

    Google Scholar 

  • S.-Rózsa K (1979) Analysis of the neural network regulating the cardio-renal system in the central nervous system of Helix pomatia L. Am Zool 19:117–128

    Google Scholar 

  • S.-Rózsa K (1984) The pharmacology of molluscan neurons. Prog Neurobiol 23:79–150

    Google Scholar 

  • S.-Rózsa K, Hernádi L, Kemenes G (1986) Selective in vivo labelling of serotonergic neurones by 5,6-dihydroxytryptamine in the snail Helix pomatia L. Comp Biochem Physiol 85C:419–425

    Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry. John Wiley and Sons, New York

    Google Scholar 

  • Tuersley MD, McCrohan CR (1988) Serotonergic modulation of patterned motor output in Lymnaea stagnalis. J Exp Biol 135:473–486

    Google Scholar 

  • Weiss KP, Kupferman I, Koch UT, Koster J, Mandelbaum DE (1981) Neural and molecular mechanism of food-induced arousal in Aplysia californica. In: Salánki J (ed) Neurobiology of Invertebrates. Akadémiai Kiadó, Budapest, pp 305–344

    Google Scholar 

  • Welsh JH, Moorhead M (1960) The quantitative distribution of serotonin in invertebrates especially in their nervous system. J Neurochem 6:146–149

    Google Scholar 

  • Wendelaar Bonga SE (1970) Ultrastructure and histochemistry of neurosecretory cells and neurohaemal areas in the pond snail Lymnaea stanglis. Z Zellforsch 108:190–224

    Google Scholar 

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Hernádi, L., Elekes, K. & S.-Rózsa, K. Distribution of serotonin-containing neurons in the central nervous system of the snail Helix pomatia . Cell Tissue Res. 257, 313–323 (1989). https://doi.org/10.1007/BF00261835

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