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. 1992 Aug;12(4):317–326. doi: 10.1007/BF00734932

A topography and ultrastructural characterization ofin vivo 5,7-dihydroxytryptamine-labeled serotonin-containing neurons in the central nervous system ofAplysia californica

L Hernádi 1, K S-Rózsa 1,2, B Jahan-Parwar 2, D O Carpenter 2,✉
PMCID: PMC11567466  PMID: 1394370

Abstract

  1. Several weeks after administration of 5,7-dihydroxytryptamine (5,7-DHT) toAplysia, a dark pigmentation appears in serotonin-containing neurons, and this pigmentation allows visual identification of serotonergic neurons but does not appear to alter their physiology.

  2. We have determined the distribution of labeled nerve cell bodies in the various ganglia ofAplysia and have characterized the pigment containing structures in both control and labeled neurons.

  3. All neurons in this preparation, whether or not they utilize serotonin as a transmitter, contain pigment granules, and three types of pigment granules can be distinguished. After 5,7-DHT a new type of granule appears in serotonergic neurons, probably reflecting lysosomes that have accumulated serotonergic synaptic vesicles that contain the oxidized 5,7-DHT.

  4. It remains unclear why this substance does not cause neurotoxicity in mollusks as it does in mammalian preparations.

Key words: serotonin; neurotoxin; 5,7-dihydroxytryptamine; Aplysia; electron microscopy; pigment; granules

References

  1. Balaban, P. M., Zakharov, I. S., and Matz, V. N. (1985). Method of vital selective staining of serotonergic nerve cells by 5,7-dihydroxytryptamine.Dokl. Akad. Nauk USSR283735–738. [Google Scholar]
  2. Baumgarten, H. G., Evetts, K. D., Holman, R. B., Iversen, L. L., Vogt, M., and Wilson, G. (1972a). Effects of 5,6-dihydroxytryptamine on monoaminergic neurones in the central nervous system of the rat.J. Neurochem.191587–1597. [DOI] [PubMed] [Google Scholar]
  3. Baumgarten, H. G., Lachenmayer, L., and Schlossberger, H. G. (1972b). Evidence for degeneration of indolamine containing nerve terminals in rat brain induced by 5,6-dihydroxytryptamine.Z. Zellforsch.125553–569. [DOI] [PubMed] [Google Scholar]
  4. Baumgarten, H. G., Björklund, A., Lachenmayer, L., and Nobin, A. (1973). Evaluation of the effects of 5,7-dihydroxytryptamine on serotonin and catecholamine neurons in the rat CNS.Acta Physiol. Scand. Suppl.3911–19. [PubMed] [Google Scholar]
  5. Baumgarten, H. G., Lachenmayer, L., and Björklund, A. (1977). Chemical lesioning of indolamine pathways. InMethods in Psychobiology (R. D. Myers, Ed.), Academic Press, New York, San Francisco, London, Vol. III, pp. 47–98. [Google Scholar]
  6. Baumgarten, H. G., Klemm, H. P., Lachenmayer, L., Björklund, A., Lovenberg, W., and Schlossberger, H. G. (1978). Mode and mechanism of action of neurotoxic indolamines: A review and progress report.Ann. N.Y. Acad. Sci.3053–24. [DOI] [PubMed] [Google Scholar]
  7. Baumgarten, H. G., Klemm, H. P., Sievers, J., and Schlossberger, H. G. (1982). Dihydroxytryptamines as tools to study the neurobiology of serotonin.Brain Res. Bull.9131–150. [DOI] [PubMed] [Google Scholar]
  8. Björklund, A., Horn, A. S., Baumgarten, H. G., Nobin, A., and Schlossberger, H. G. (1975). Neurotoxicity of hydroxylated tryptamines: Structure-activity relationships. 2.In vitro studies on monoamines uptake which inhibition and uptake impairment.Acta Physiol. Scand.42929–60. [PubMed] [Google Scholar]
  9. Cottrell, G. A., and Osborne, N. N. (1970). Subcellular localization of serotonin in an identified serotonin-containing neuron.Nature225470–472. [DOI] [PubMed] [Google Scholar]
  10. Elekes, K., Hernádi, L., and Kemenes, G. (1988). Serotonin immunoreactive neurons in the CNS ofHelix andLymnaea. InNeurobiology of Invertebrates, Transmitters, Modulators and Receptors (J. Salánki and K. S.-Rózsa, Eds.), Akademiai Kiad, Budapest, pp. 703–711. [Google Scholar]
  11. Goldstein, R., Kistler, H. B., Steinbusch, H. W. M., and Schwartz, J. H. (1984). Distribution of serotonin-immunoreactivity in the juvenileAplysia.Neuroscience11535–547. [DOI] [PubMed] [Google Scholar]
  12. Hernádi, L., Kemenes, G., and S.-Rózsa, K. (1987). Selectivein vivo labelling of serotonergic neurons by 5,6-dihydroxytryptamine in the snailHelix pomatia L. InNeurobiology, Molluscan Models (H. H. Boer, W. P. M. Geraerts, and J. Joosse, Eds.), Mon. Kon. Ned. Acad. Wetensch, North-Holland, Amsterdam, Oxford, New York, pp. 22–25. [Google Scholar]
  13. Hernádi, L., Vehovszky, A., and S.-Rózsa, K. (1988). 5,6-dihydroxytryptamine induced ultrastructural changes as a specific marker of the serotonergic system in the CNS ofHelix pomatia. InNeurobiology of Invertebrates, Transmitters, Modulators and Receptors (J. Salánki, and K. S.-Rózsa, Eds.), Akademiai Kiad, Budapest, pp. 173–183. [Google Scholar]
  14. Hernádi, L., Elekes, K., and S.-Rózsa, K. (1989). Distribution of serotonin-containing neurons in the central nervous system of the snailHelix pomatia: Comparison of immunocytochemical and 5,6-dihydroxytryptamine labeling.Cell Tissue Res.257313–323. [Google Scholar]
  15. Jahan-Parwar, B., and Fredman, S. M. (1976). Cerebral ganglion ofAplysia: Cellular organization and origin of nerves.Comp. Biochem. Physiol.53A347–357. [DOI] [PubMed] [Google Scholar]
  16. Jahan-Parwar, B., S.-Rózsa, K., Salánki, J., Evans, M. L., and Carpenter, D. O. (1987).In vivo labelling of serotonin-containing neurons by 5,7-dihydroxytryptamine inAplysia.Brain Res.426173–178. [DOI] [PubMed] [Google Scholar]
  17. Jonsson, G. (1980). Chemical neurotoxins as denervation tools in neurobiology.Neuroscience3169–187. [DOI] [PubMed] [Google Scholar]
  18. Jonsson, G. (1983). Chemical lesioning techniques: Monoamine neurotoxins. InHandbook of Chemical Neuroanatomy (A. Björklund and T. Hoelt, Eds.), Elsevier, Amsterdam, pp. 463–507. [Google Scholar]
  19. Kandel, E. R., and Schwartz, J. H. (1982). Molecular biology of learning: Modulation of transmitter release.Science218433–443. [DOI] [PubMed] [Google Scholar]
  20. Kemenes, G., Elekes, K., Hiripi, L., and Benjamin, P. R. (1989). A comparison of four techniques for mapping the distribution of serotonin and serotonin-containing neurons in fixed and living ganglia of the snail,Lymnaea.J. Neurocytol.18193–208. [DOI] [PubMed] [Google Scholar]
  21. Kistler, H. B. Jr., Hawkins, R. D., Koester, J., Steinbusch, H. W. M., Kandel, E. R., and Schwartz, J. H. (1985). Distribution of serotonin-immunoreactive cell bodies and processes in the abdominal ganglion of matureAplysia.J. Neurosci.572–80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Klein, M., and Kandel, E. R. (1980). Mechanism of calcium current modulation underlaying presynaptic facilitation and behavioral sensitization inAplysia.Proc. Natl. Acad. Sci. USA776912–6916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Klemm, H. P., Baumgarten, H. G., and Schlossberger, H. G. (1980). Polarographic measurements of spontaneous and mitochondria-promoted oxidation of 5,6- and 5,7-dihydroxytryptamine.J. Neurochem.351400–1408. [DOI] [PubMed] [Google Scholar]
  24. Longley, R. D., and Longley, A. J. (1986). Serotonin immunoreactivity of neurons in the gastropodAplysia californica.J. Neurobiol.17339–358. [DOI] [PubMed] [Google Scholar]
  25. Ono, J. K., and McCaman, R. E. (1984). Immunocytochemical localization and direct assays of serotonin-containing neurons inAplysia.Neuroscience11549–560. [DOI] [PubMed] [Google Scholar]
  26. Salimova, N. B., Sakharov, D. A., Milosevic, I., Turpaev, T. M., and Rakic, L. (1987). Monoamine containing neurons in theAplysia brain.Brain Res.400285–299. [DOI] [PubMed] [Google Scholar]
  27. Schkolnik, L. J., and Schwartz, J. H. (1980). Genesis and maturation of serotonergic vesicles in identified giant cerebral neuron ofAplysia.J. Neurophysiol.43945–967. [DOI] [PubMed] [Google Scholar]
  28. Schwartz, J. H., Schkolnik, L. J., and Goldberg, D. J. (1979). Specific association of neurotransmitter with somatic lysosomes in an identified serotonergic neuron ofAplysia californica.Proc. Natl. Acad. Sci. USA765967–5971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sinhababu, A. K., and Borchardt, R. T. (1988). Molecular mechanism of biological action of the serotonergic neurotoxin 5,7-dihydroxytryptamine.Neurochem. Int.12273–284. [DOI] [PubMed] [Google Scholar]
  30. S.-Rózsa, K., Hernádi, L., and Kemenes, G. (1986). Selectivein vivo labelling of serotonergic neurons by 5,6-dihydroxytryptamine in the snailHelix pomatia L.Comp. Biochem. Physiol.85C419–425. [Google Scholar]
  31. Walters, E. T., and Byrne, J. H. (1983). Associative conditioning of single sensory neurons suggests a cellular mechanism of learning.Science219405–408. [DOI] [PubMed] [Google Scholar]

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