Cell and Tissue Research

, Volume 277, Issue 1, pp 189–198 | Cite as

Distribution and anatomy of GABA-like immunoreactive neurons in the central and peripheral nervous system of the snail Helix pomatia

  • L. Hernádi


Gamma-aminobutyric acid (GABA)-like immunoreactive neurons were studied in the central and peripheral nervous system of Helix pomatia by applying immunocytochemistry on whole-mount preparations and serial paraffin sections. GABA-immunoreactive cell bodies were found in the buccal, cerebral and pedal ganglia, but only GABA-immunoreactive fibers were found in the viscero-parietal-pleural ganglion complex. The majority of GABA-immunoreactive cell bodies were located in the pedal ganglia but a few could be found in the buccal ganglia. Varicose GABA-ir fibers could be seen in the neuropil areas and in distinct areas of the cell body layer of the ganglia. The majority of GABA-ir axonal processes run into the connectives and commissures of the ganglia, indicating an important central integrative role of GABA-immunoreactive neurons. GABA may also have a peripheral role, since GABA-immunoreactive fibers could be demonstrated in peripheral nerves and the lips. Glutamate injection did not change the number or distribution of GABA-immunoreactive neurons, but induced GABA immunoreactivity in elements of the connective tissue ensheathing the muscle cells and fibers of the buccal musculature. This shows that GABA may be present in different non-neural tissues as a product of general metabolic pathways.

Key words

GABA Glutamate Immunocytochemistry Nervous system, central Nervous system, peripheral Helix pomatia (Mollusca) 


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  1. Arshavsky YI, Deliagina TG, Gamkrelidze GN, Orlovsky GN, Panchin YV, Popova LB, Shupliakov OV (1993) Pharmacologically induced elements of the hunting and feeding behavior in the pteropod mollusk Clione limachina. I. Effects of GABA. J Neurophysiol 69:512–521Google Scholar
  2. Atwood HL (1982) Synapses and neurotransmitters. In: Atwood HL, Sandeman DC (eds) The biology of Crustacea, vol 3, Neurobiology: structure and function. Academic Press, New York, pp 105–150Google Scholar
  3. Bagust J, Fitzsimos JTR, Kerkut GA (1979) Evidence for integrating activity in the isolated intestinal nerve of Helix aspersa. Comp Biochem Physiol [A] 62:397–408Google Scholar
  4. Bailey CH, Castellucci VF, Koester J, Kandel ER (1979) Cellular studies of peripheral neurons in siphon skin of Aplysia californiaca. J Neurophysiol 42:530–557Google Scholar
  5. Bokisch AJ, Walker RJ (1986) The ionic mechanism associated with action of putative transmitters on identified neurons of the smail, Helix aspersa. Comp Biochem Physiol [C]84:231–241Google Scholar
  6. Bullock TH, Horridge GA (1965) Structure and function in the nervous systems of invertebrates. Freeman, San Francisco, LondonGoogle Scholar
  7. Cline H, Nushbaum MP, Kristan WB Jr (1985) Identified GABAergic inhibitory motor neurons in the leech nervous system take up GABA. Brain Res 348:359–362Google Scholar
  8. Cooke IRC, Gelperin A (1988) Distribution of GABA-like immunoreactive neurons in the slug Limax maximus. Cell Tissue Res 253:77–81Google Scholar
  9. Cooke IRC, Delaney K, Gelperin A (1985) Complex computation in a small neural network. In: Weinberger NM, McGaugh JL, Lynch G (eds) Memory systems of the brain. Guilford, New York, pp 173–191Google Scholar
  10. Cottrell GA (1974) Serotonin and free amino acid analysis of ganglia and isolated neurones of Aplysia dactylomela. J Neurochem 22:557–559Google Scholar
  11. Dolezalova JJ, Gaicombini E, Stepita-Klaco M (1973) An attempt to identify putative neurotransmitter molecules in the central nervous system of the snail. Int J Neurosci 5:53–59Google Scholar
  12. Elekes K (1991) Serotonin-immunoreactive varicosities in the cell body region and neural sheath of the smail, Helix pomatia ganglia: an electron microscopic immunocytochemical study. Neuroscience 42:583–591Google Scholar
  13. Elekes K, Florey E (1987) Immunocytochemical evidence for the GABAergic innervation of the stretch receptor neurons in crayfish. Neuroscience 33:1111–1122Google Scholar
  14. Elekes K, Nässel DR (1990) Distribution of FMRFamide-like immunoreactive neurons in the central nervous system of the snail Helix pomatia. Cell Tissue Res 262:177–190Google Scholar
  15. Elekes K, S-Rózsa K, Vehovsky Á, Hernádi L, Salánki J (1985) Nerve cells and synaptic connections in the intestinal nerve of the snail Helix pomatia L. An ultrastructural and HRP study. Cell Tissue Res 239:611–620Google Scholar
  16. Enna SJ (1983) The GABA receptors. Humana Press, Clifton, NJGoogle Scholar
  17. Gerschenfeld HM, Lasansky A (1964) Action of glutamic acid and other naturally occurring amino acids on snail central neurons. Int J Neuropharmacol 3:301–314Google Scholar
  18. Gorman ALF, Mirolli M (1969) The input-output organization of a pair of giant neurons in the mollusc, Anisodoris nobilis (McFarland). J Exp Biol 51:615–634Google Scholar
  19. Hernádi I (1992) General and immunocytochemical organization of the peripheral nervous system in the lips and its connection with the CNS of the snail Helix pomatia. In: Elsner N, Richter DW (eds) Rhythmogenesis in neurons and networks. Proceedings of the 20th Göttingen Neurobiology Conference. Thieme, Stuttgart New York, p 147Google Scholar
  20. Hernádi L (1993) Somatotopic representation of the head areas in the cerebral ganglion of the snail Helix pomatia. Acta Biol Hung 43:221–230Google Scholar
  21. Hernádi L, Elkes K (1993) Peptidergic and aminergic centers in the Helix cerebral ganglia: somatotopy and immunocytochemistry. Acta Biol Hung 44:89–92Google Scholar
  22. Hernádi L, Kemenes GY, Salánki J (1984) Central representation and functional connections of afferent and efferent pathways of Helix pomatia L. lip nerves. Acta Biol Hung 35:49–69Google Scholar
  23. Hernádi L, Elekes K, S-Rózsa K (1989) Distribution of serotonincontaining neurons in the central nervous system of the snail Helix pomatia. Comparison of immunocytochemical and 5,6-dihydroxytryptamine labelling. Cell Tissue Res 257:313–323Google Scholar
  24. Hodgson AJ, Penke B, Erdei A, Chubb IW, Somogyi P (1985) Antisera to amino butyric acid: I. Production and characterization using a new model system. J Histochem Cytochem 33:229–239Google Scholar
  25. Johnson CD, Stretton AOW (1987) GABA-immunoreactivity in inhibitory motor neurons of the nematode Ascaris. J Neurosci 7:223–235Google Scholar
  26. Kerkut GA, Walker RJ (1961) The effects of drugs on neurons of the snail Helix aspersa. Comp Biochem Physiol 3:143–160Google Scholar
  27. Leak LD, Walker RJ (1980) Invertebrate neuropharmacology. Blackie, GlasgowGoogle Scholar
  28. Mugnani E, Oertel WH (1985) An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunocytochemistry. In: Björklund A, Hökfelt T (eds), Handbook of chemical neuroanatomy, vol 4. Elsevier, Amsterdam, pp 436–608Google Scholar
  29. Nässel DR, Elekes K (1984) Ultrastructural demonstration of serotonin-immunoreactivity in the nervous system of an insect (Calliphora erythrocephala). Neurosci Lett 48:203–210Google Scholar
  30. Osborne NN (1971) Occurrence of GABA and taurine in the nervous system of the dogfish and some invertebrates. Comp Gen Pharmacol 2:433–438Google Scholar
  31. Osborne NN, Briel G, Neuhoff V (1971) Distribution of GABA and other amino acids in different tissues of the gastropod mollusc Helix pomatia, including in vitro experiments with 14C glucose and 14C glutamic acid. Int J Neurosci 1:263–272Google Scholar
  32. Osborne NN, Szczpaniak AC, Neuhoff V (1973) Amines and amino acids in identified neurones of Helix pomatia. Int J Neurosci 5:125–131Google Scholar
  33. Peretz B, Jacklet JW, Lukowiak K (1976) Habituation of reflexes in Aplysia: contribution of the peripheral and central nervous system. Science 191:396–399Google Scholar
  34. Richmond JE, Murphy AD, Bulloch AGM, Lukowiak K (1986) Evidence for an excitatory effect of GABA on feeding patterned motor activity (PMA) of Helisoma trivolis. Soc Neurosci Abstr 12:792Google Scholar
  35. Richmond JE, Bulloch AGM, Lukowiak KD (1987) Electrophysiological and biochemical evidence for GABA as neurotransmitter in Helisoma trivolis. Soc Neurosci Abstr 13:1070Google Scholar
  36. Richmond JE, Bulloch AGM, Bauce L, Lukowiak K (1991) Evidence for the presence, synthesis, immunoreactivity, and uptake of GABA in the nervous system of the snail Helisoma trivolis. J Comp Neurol 307:131–143Google Scholar
  37. Roberts E, Chase TN, Tower DB (1976) GABA in nervous system function, vol 5. Raven Press, New YorkGoogle Scholar
  38. Robinson TN, Olsen RW (1988) GABA. In: Lunt GG, Olsen RW (eds) Comparative invertebrate neurochemistry. Croom Helm, London, pp 90–123Google Scholar
  39. Soinila S, Mpitsos GJ (1991) Immunohistochemistry of diverging and converging neurotransmitter system in mollusks. Biol Bull 181:484–499Google Scholar
  40. Somogyi P, Hodgson AJ, Chubb IA, Penke B, Erdei A (1985) Antisera to aminobutyric acid. II. Immunocytochemical application to the central nervous system. J Histochem Cytochem 33:240–248Google Scholar
  41. S-Rózsa K, Kiss T, V-Szôke J (1973) On the role of bioactive substances in the rhythm regulation of heart muscle cells of Gastropoda and Insecta. In: Salánki J (ed) Neurobiology of invertebrates. Akadémiai Kiadó, Budapest, pp 167–182Google Scholar
  42. Sternberger LA (1979) Immunocytochemistry. Wiley, New YorkGoogle Scholar
  43. Takeuchi H (1992) Sensitivities of Achatina giant neurons to putative amino acid neurotransmitters. Comp Biochem Physiol [C] 103:1–12Google Scholar
  44. Usherwood PNR (1977) Neuromuscular transmission in insects. In: Hoyle G (ed) Identified neurons and behavior of arthropods. Plenum Press, New York, pp 31–48Google Scholar
  45. Vehovszky Á, Hernádi L, Elekes K, Balaban P (1993) Serotonergic input onidentified command neurons in Helix. Acta Biol Hung 44:97–101Google Scholar
  46. Vitellaro-Zuccarello L, De Biasi S (1988) GABA-like immunoreactivity in the pedal ganglia of Mytilus galloprovincialis: light and electron microscopic study. J Comp Neurol 267:516–524Google Scholar
  47. Walker RJ (1986) Transmitters and modulators. In: Willows AOD (ed) The Mollusca, vol 9. Neurobiology and behavior part 2. Academic Press, New York, pp 279–485Google Scholar
  48. Walker RJ, Aranza MJ, Kerkut GA, Woodruff GN (1975) The action of gamma-aminobutyric acid (GABA) and related compounds on two identifiable neurones in the brain of the snail Helix aspersa. Comp Biochem Physiol [C] 50:147–154Google Scholar
  49. Walker RJ, Holden-Dye LM, Vehovszky Á, Bokisch AJ, Cox RTL (1988) Some aspects of molluscan neuropharmacology. Symp Biol Hung 36:63–76Google Scholar
  50. Yarowsky PJ, Carpenter DO (1977) GABA-mediated excitatory responses on Aplysia neurones. Life Sci 20:1441–1448Google Scholar
  51. Yarowsky PJ, Carpenter DO (1978) Receptors for gamma-aminobutyric acid (GABA) on Aplysia neurons. Brain Res 144:75–94Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • L. Hernádi
    • 1
  1. 1.Balaton Limnological Research Institute of the Hungarian Academy of SciencesTihanyHungary

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