Abstract
Summary
The distribution of serotonin-, tyrosine hydroxylase-, and FMRFamide-immunoreactive neuronal elements, as well as the concentrations of serotonin and dopamine in the different parts of the gastrointestinal tract, were studied in the snail Helix pomatia. The sensitivity of the spontaneous contractions of the alimentary tract to serotonin, dopamine, and FMRFamide was also tested. Serotonin-, tyrosine hydroxylase-, and FMRFamide-immunoreactive elements could be demonstrated in each part of the gastrointestinal tract, but they showed different innervation patterns. Serotonin- and tyrosine hydroxylase-immunoreactive elements were dominant in the submucosal layer, whereas FMRFamide-immunoreactive elements were dominant in both the mucosal and submucosal layers. Tyrosine hydroxylase-immunoreactive elements were confined to the longitudinal muscle trabeculae of submucosa, whereas serotonin-immunoreactive elements were distributed throughout the submucosal layer. No serotonin-immunoreactive cell bodies, but only fibers, could be detected in the gastrointestinal tract, and therefore they represent extrinsic elements. Tyrosine hydroxylase- and FMRFamide-immunoreactive cell bodies represent intrinsic elements of the tract. The occurrence and density of the serotonin- and tyrosine hydroxylase-immunoreactive elements showed significant differences in the different parts of the alimentary tract, in accordance with HPLC assays, which revealed a significant frontocaudal decrease in both the serotonin (from 2.11 to 1.21 pM/mg) and dopamine (from 3.28 to 0.52 pM/mg) contents of the different parts of the alimentary tract. Dopamine at 10-5 M concentration proved to be effective only on the longitudinal muscles by increasing the tone and frequency of contractions, but was ineffective on the circular muscles. Serotonin affected both the longitudinal and circular muscles. Serotonin at 10-5 M concentration decreased the tone and increased the frequency of low-amplitude contractions of the longitudinal muscles of the esophagus and the gizzard but increased both the tone and frequency of the crop. Serotonin at 10-9 M concentration slightly decreased the tone and blocked the contractions of the circular muscles in the crop but at 10-5 M concentration induced contractions of the circular muscles in the gizzard. FMRFamide at 10-6 M concentration decreased the tone and was shown to block the contractions of both the longitudinal and circular muscles.
Similar content being viewed by others
Reference
Ajimal, G.S. & Ram, J. L. (1981) Aplysia gastrointestinal tract motility: spontaneous activity and pharmacological sensitivity. Comparative Biochemistry and Physiology 68C, 133-44.
Austin, T., Weiss, S. & Lukowiak, K. (1983) FMRFamide effects on spontaneous and induced contractions of the anterior gizzard of Aplysia. Canadian Journal of Physiology and Pharmacology 61, 949-53.
Brezina, V., Evans, C.G. & Weiss, K.R. (1994a) Enhancement of Ca current in the accessory radula closer muscle of Aplysia californica by neuromodulators that potentiate its contractions. Journal of Neuroscience 14, 4393-411.
Brezina, V., Evans, C.G. & Weiss, K.R. (1994b) Activation of K current in the accessory radula closer muscle of Aplysia californica by neuromodulators that depress its contractions. Journal of Neuroscience 14, 4412-32.
Bulloch, A.G.M., Price, D.A., Murphy, A.D., Lee, T.D. & Bowes, H. (1988) FMRFamide peptides in Helisoma: identification and physiological actions at a peripheral synapse. Journal of Neuroscience 8, 3459-69.
Bullock, T.H., & Horridge, G.A. (1965) Structure and Function in the Nervous Systems of Invertebrates. San Francisco Freeman and Co.
Cardot, J. & Fellman, D. (1983) Immunofluorescent evidence of an FMRFamide-like peptide in the peripheral nervous system of the gastropod mollusc Helix aspersa. Neuroscience Letters 43, 167-72.
Carpenter, D.O., Breese, G., Schanberg, S. & Kopin, I. (1971) Serotonin and dopamine: distribution and accumulation in Aplysia nervous and non-nervous tissues. International Journal of Neuroscience 2, 49-56.
Cottrell, G.A., Greenberg, M.J. & Price, D.A. (1983) Differential effects of the molluscan neuropeptide FMRFamide and the related met-enkephalin derivative YGGFMRFamide on the Helix tentacle retractor muscle. omparative Biochemistry and Physiology 75C, 373-5.
Cottrell, G.A., Schot, L.P. & Dockray, G.J. (1983) Identification and probable role of a single neurone containing the neuropeptide Helix FMRFamide. Nature (London) 304, 638-40.
Elekes, K., S-RÓzsa, K., Vehovszky, A., HernÁdi, L. & SalÁnki, J. (1985) Nerve cells and synaptic connections in the intestinal nerve of the snail, Helix pomatia. Cell and Tissue Research 239, 611-20.
Fujiwara-Sakata, M., Muneoka, Y. & Kobayashi, M. (1991) Action and immunoreactivity of neuropeptides in the buccal neuromuscular system of a prosobranch mollusc, Rapana thomasiana. Cell and Tissue Research 264, 57-62.
Gerschenfeld, H.M. (1973) Chemical transmission in invertebrates central nervous system and neuromuscular junctions. Physiological Review 53, 1-119.
Halasy, K., Benedeczky, I., Fekete, E. & GÁbriel, R. (1988) Enteric neuromuscular junctions: comparison of ultrastructural features in different phylogenetic groups. Neuroscience 25, 147-62.
HernÁdi, L. & Elekes, K. (1995) Neurons with different immunoreactivity form clusters in the CNS of Helix pomatia. Acta Biologica Hungarica 46, 271-80.
HernÁdi, L., Elekes, K. & S-RÓzsa, K. (1989) Distribution of serotonin-containing neurons in the central nervous system of the snail Helix pomatia. Comparison of immunocytochemical and 5, 6-dihydroxytryptamine labelling. Cell and Tissue Research 257, 313-23.
HernÁdi, L., Hiripi, L, Vehovszky, A., Kemenes, G. & S-RÓzsa, K. (1992) Ultrastructural biochemical and electrophysiological changes induced by 5,6-dihydroxytryptamine in the CNS of the snail Helix pomatia. Brain Research 578, 221-34.
HernÁdi, L., Juhos, S. & Elekes, K. (1993) Distribution of tyrosinehydroxylase-immunoreactive and dopamine-immunoreactive neurons in the central nervous system of the snail Helix pomatia. Cell and Tissue Research 274, 503-13.
Kabotyansky, E.A. & Sakharov, D.A. (1988) Monoamine-dependent behavioral states in the pteropod mollusc Clione limacina. Symposia Biologica Hungarica 36, 463-77.
Kemenes, G., Hiripi, L. & Benjamin, P.R. (1990) Behavioral and biochemical changes in the feeding system of Lymnaea induced by dopamine and serotonin neurotoxins 6-hydroxydopamine and 5,6-dihydroxytriptamine. Philosophical Transactions of the Royal Society of London B 329, 243-55.
Kobayashi, M., & Muneoka, Y. (1990) Structure and action of molluscan neuropeptides. Zoological Sciences 7, 801-14.
Krajniak, K.G., Greenberg, M.J., Price, D.A., Doble, K.E. & Lee T.D. (1989) The identification and pharmacology of FMRFamide-related peptides and SCPB in the penis and crop of the terrestrial slug, Limax maximus. Comparative Biochemistry and Physiology 94C, 485-92.
Kyriakides, M.A. & McCrohan, C.R. (1989) Effect of putative neuromodulators on rhythmic buccal motor output in Lymnaea stagnalis. Journal of Neurobiology 20, 635-50.
Lehman, H.K. & Greenberg, M.J. (1987) The actions of FMRFamide-like peptides on visceral and somatic muscles of the snail Helix aspersa. Journal of Experimental Biology 131, 55-68.
Lloyd, P.E. (1980) Mechanisms of action of 5-hydroxytryptamine and endogenous peptides on a neuromuscular preparation in the snail, Helix aspersa. Journal of Comparative Physiology 139, 341-47.
Lloyd, P.E. (1980) Modulation of neuromuscular activity by 5-hydroxytryptamine and endogenous peptides in the snail, Helix aspersa. Journal of Comparative Physiology 139, 333-9.
Magoski, N.S. & Bulloch, A.G.M. (1997) Localization, physiology, and modulation of a molluscan dopaminergic synapse. Journal of Neurobiology 33, 247-64.
Murphy, A.D. (1990) An identified pleural ganglion interneuron inhibits patterned motor activity in the buccal ganglia of the snail, Helisoma. Brain Research 525, 300-3.
Murphy, A.D., Lukowiak, K. & Stell, W.K. (1985) Peptidergic modulation of patterned motor output activity in identified neurons of Helisoma. Proceedings of the National Academy of Sciences USA 82, 7140-4.
Price, D.A. (1986) Evolution of a molluscan cardioregulatory peptide. American Zoologist 26, 1007-15.
Price, D.A. & Greenberg, M.J. (1977) Structure of a molluscan cardioexcitatory peptide. Science 197, 670-1.
Rosen, S.C., Weiss, K.R., Goldstein, R.S. & Kupfermann, I. (1989) The role of a modulatory neuron in feeding and satiation in Aplysia: effects of lesioning of the serotonergic metacerebral cells. Journal of Neuroscience 9, 1562-78.
Rosen, S.C., Susswein, E.C., Cropper, E.C., Weiss, K.R. & Kupfermann, I. (1989) Selective modulation of spike duration by serotonin and the neuropeptide FMRFamide, SCPB, buccalin and myomodulin in different classes of mechanoafferent neurons in the cerebral ganglion of Aplysia. Journal of Neuroscience 9, 390-402.
Rosen, S.C., Teyke, T., Miller, M.W, Weiss, K.R. & Kupfermann, I. (1991) Identification and characterization of cerebral-to-buccal interneurons implicated in the control of motor programs associated with feeding in Aplysia. Journal of Neuroscience 11, 3630-55.
Ruben, P., & Lukowaik, K. (1983) Modulation of the Aplysia gill withdrawal reflex by dopamine. Journal of Neurobiology 14, 271-84.
Shi, R. & Belardetti, F. (1991) Serotonin inhibits the peptide FMRFamide response through a cyclic AMP-independent pathway in Aplysia. Journal of Neurophysiology 66, 1847-57.
Sossin, W.S., Kirk, M.D. & Scheller, R.H. (1987) Peptidergic modulation of neuronal circuitry controlling feeding in Aplysia. Neuroscience 7, 671-81.
S-RÓzsa, K. (1984) The pharmacology of molluscan neurons. Progress in Neurobiology 23, 79-150.
S-RÓzsa, K., HernÁdi, L. & Kemenes, G. (1986) Selective in vivo labelling of serotonergic neurons by 5,6-dihydroxytryptamine in the snail Helix pomatia. Comparative Biochemistry and Physiology C85, 419-25.
Sternberger, L.A. (1979) Immunocytochemistry. Chichester: John Wiley.
Susswein, A.J. & Kupfermann, I. (1975) Bulk as a stimulus for satiation in Aplysia. Behavioral Biology 13, 203-209.
Teyke, T., Rosen, S.C., Weiss, K.R. & Kupfermann, I. (1993) Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry of Aplysia. Brain Research 630, 226-37.
Trimble, D.L., & Barker, D.L. (1984) Activation by dopamine of patterned motor output from the buccal ganglia of Helisoma trivolis. Journal of Neurobiology 15, 37-48.
Walker, R.J. (1986) Transmitters and modulators. In: The Mollusca (edited by Willows, A.O.D.) pp. 279-485. NewYork: Academic Press.
Weiss, K.R., Cohen, J.L. & Kupfermann, I. (1978) Modulatory control of buccal musculature by serotonergic neuron (metacerebral cell) in Aplysia. Journal of Neurophysiology 41, 181-203.
Weiss, K.R., Koch, U.T., Koester, J., Mandelbaum, D.E. & Kupfermann, I. (1980) Neural and molecular mechanisms of food induced arousal in Aplysia california. In: Advances in Physiological Sciences, Neurobiology of Invertebrates, Vol. 23 (edited by SalÁnki, J.), pp. 305-44. Oxford: Pergamon.
Weiland, S.J. & Gelperin, A. (1983) Dopamine elicits feeding motor program in Limax maximus. Journal of Neuroscience 3, 1735-45.
Yanagawa, M., Fujiwara, M., Takabatake, I., Muneoka, Y. & Kobayashi, M. (1988) Potentiating effects of some invertebrate neuropeptides on twitch contraction of radula muscles of a mollusc Rapana thomasiana. Comparative Biochemistry and Physiology C90, 73-7.
Yeoman, M.S., Pieneman, A.W., Ferguson, G.P., Maat, A.T. & Benjamin, P.R. (1994) Modulatory role for serotonergic cerebral cells in the feeding system of the snail, Lymnaea. I. Fine wire recording in the intact animal and pharmacology. Journal of Neurophysiology 72, 1357-71.
Yeoman, M.S., Kemenes, G., Elliott, C.J.H. & Benjamin, P.R. (1994b) Modulatory role for serotonergic cerebral cells in the feeding system of the snail, Lymnaea. II. Photoinactivation. Journal of Neurophysiology 72, 1372-82.
Zoran, M.J., Haydon, P.G. & Matthews, P.J. (1989) Aminergic and peptidergic modulation of motor function at an identified neuromuscular junction in Helisoma. Journal of Experimental Biology 142, 225-43.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
HERNÁDI, L., ErdÉLyi, L., Hiripi, L. et al. The organization of serotonin-, dopamine-, and FMRFamide- containing neuronal elements and their possible role in the regulation of spontaneous contraction of the gastrointestinal tract in the snail Helix pomatia. J Neurocytol 27, 761–775 (1998). https://doi.org/10.1023/A:1006955018882
Issue Date:
DOI: https://doi.org/10.1023/A:1006955018882