Abstract
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.
Similar content being viewed by others
References
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 69:512–521
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 105–150
Bagust J, Fitzsimos JTR, Kerkut GA (1979) Evidence for integrating activity in the isolated intestinal nerve of Helix aspersa. Comp Biochem Physiol [A] 62:397–408
Bailey CH, Castellucci VF, Koester J, Kandel ER (1979) Cellular studies of peripheral neurons in siphon skin of Aplysia californiaca. J Neurophysiol 42:530–557
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]84:231–241
Bullock TH, Horridge GA (1965) Structure and function in the nervous systems of invertebrates. Freeman, San Francisco, London
Cline H, Nushbaum MP, Kristan WB Jr (1985) Identified GABAergic inhibitory motor neurons in the leech nervous system take up GABA. Brain Res 348:359–362
Cooke IRC, Gelperin A (1988) Distribution of GABA-like immunoreactive neurons in the slug Limax maximus. Cell Tissue Res 253:77–81
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 173–191
Cottrell GA (1974) Serotonin and free amino acid analysis of ganglia and isolated neurones of Aplysia dactylomela. J Neurochem 22:557–559
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 5:53–59
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 42:583–591
Elekes K, Florey E (1987) Immunocytochemical evidence for the GABAergic innervation of the stretch receptor neurons in crayfish. Neuroscience 33:1111–1122
Elekes K, Nässel DR (1990) Distribution of FMRFamide-like immunoreactive neurons in the central nervous system of the snail Helix pomatia. Cell Tissue Res 262:177–190
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 239:611–620
Enna SJ (1983) The GABA receptors. Humana Press, Clifton, NJ
Gerschenfeld HM, Lasansky A (1964) Action of glutamic acid and other naturally occurring amino acids on snail central neurons. Int J Neuropharmacol 3:301–314
Gorman ALF, Mirolli M (1969) The input-output organization of a pair of giant neurons in the mollusc, Anisodoris nobilis (McFarland). J Exp Biol 51:615–634
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 147
Hernádi L (1993) Somatotopic representation of the head areas in the cerebral ganglion of the snail Helix pomatia. Acta Biol Hung 43:221–230
Hernádi L, Elkes K (1993) Peptidergic and aminergic centers in the Helix cerebral ganglia: somatotopy and immunocytochemistry. Acta Biol Hung 44:89–92
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 35:49–69
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 257:313–323
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 33:229–239
Johnson CD, Stretton AOW (1987) GABA-immunoreactivity in inhibitory motor neurons of the nematode Ascaris. J Neurosci 7:223–235
Kerkut GA, Walker RJ (1961) The effects of drugs on neurons of the snail Helix aspersa. Comp Biochem Physiol 3:143–160
Leak LD, Walker RJ (1980) Invertebrate neuropharmacology. Blackie, Glasgow
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 436–608
Nässel DR, Elekes K (1984) Ultrastructural demonstration of serotonin-immunoreactivity in the nervous system of an insect (Calliphora erythrocephala). Neurosci Lett 48:203–210
Osborne NN (1971) Occurrence of GABA and taurine in the nervous system of the dogfish and some invertebrates. Comp Gen Pharmacol 2:433–438
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 1:263–272
Osborne NN, Szczpaniak AC, Neuhoff V (1973) Amines and amino acids in identified neurones of Helix pomatia. Int J Neurosci 5:125–131
Peretz B, Jacklet JW, Lukowiak K (1976) Habituation of reflexes in Aplysia: contribution of the peripheral and central nervous system. Science 191:396–399
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 12:792
Richmond JE, Bulloch AGM, Lukowiak KD (1987) Electrophysiological and biochemical evidence for GABA as neurotransmitter in Helisoma trivolis. Soc Neurosci Abstr 13:1070
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 307:131–143
Roberts E, Chase TN, Tower DB (1976) GABA in nervous system function, vol 5. Raven Press, New York
Robinson TN, Olsen RW (1988) GABA. In: Lunt GG, Olsen RW (eds) Comparative invertebrate neurochemistry. Croom Helm, London, pp 90–123
Soinila S, Mpitsos GJ (1991) Immunohistochemistry of diverging and converging neurotransmitter system in mollusks. Biol Bull 181:484–499
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 33:240–248
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 167–182
Sternberger LA (1979) Immunocytochemistry. Wiley, New York
Takeuchi H (1992) Sensitivities of Achatina giant neurons to putative amino acid neurotransmitters. Comp Biochem Physiol [C] 103:1–12
Usherwood PNR (1977) Neuromuscular transmission in insects. In: Hoyle G (ed) Identified neurons and behavior of arthropods. Plenum Press, New York, pp 31–48
Vehovszky Á, Hernádi L, Elekes K, Balaban P (1993) Serotonergic input onidentified command neurons in Helix. Acta Biol Hung 44:97–101
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 267:516–524
Walker RJ (1986) Transmitters and modulators. In: Willows AOD (ed) The Mollusca, vol 9. Neurobiology and behavior part 2. Academic Press, New York, pp 279–485
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] 50:147–154
Walker RJ, Holden-Dye LM, Vehovszky Á, Bokisch AJ, Cox RTL (1988) Some aspects of molluscan neuropharmacology. Symp Biol Hung 36:63–76
Yarowsky PJ, Carpenter DO (1977) GABA-mediated excitatory responses on Aplysia neurones. Life Sci 20:1441–1448
Yarowsky PJ, Carpenter DO (1978) Receptors for gamma-aminobutyric acid (GABA) on Aplysia neurons. Brain Res 144:75–94
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hernádi, L. Distribution and anatomy of GABA-like immunoreactive neurons in the central and peripheral nervous system of the snail Helix pomatia . Cell Tissue Res 277, 189–198 (1994). https://doi.org/10.1007/BF00303096
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00303096