Skip to main content
NCBI home page
Cellular and Molecular Neurobiology logoLink to Cellular and Molecular Neurobiology
. 1996 Sep;16(5):561–576. doi: 10.1007/BF02152057

Modulation ofin vivo neuronal sprouting by serotonin in the adult CNS of the snail

Michael W Baker 1, Roger P Croll 1,✉
PMCID: PMC11563136  PMID: 8956009

Abstract

  1. Duringin situ recovery from a lesion to the cerebrobuccal connective (CBC) in the snailAchatina fulica, neurons of the buccal ganglia undergo extensive regeneration and sprouting as assessed by axonal dye-fillings of the CBC.

  2. These changes are preceded by the distal degeneration of severed fibres from the serotonergic metacerebral giant neuron (MCG), which results in the depletion of serotonin (5-HT) in the ipsilateral buccal ganglion. We have investigated the potential role of this depletion in causing some of the ensuing neuroplastic events.

  3. Pharmacological depletion of 5-HT using either 5,7-dihydroxtryptamine or p-chlorophenylalanine in normal, unlesioned animals was found to produce supernumerary neuronal labelling similar to that seen following a lesion.

  4. Systemic daily injections of 5-HT were found to partly suppress the sprouting response following the CBC lesion. For example, the contralateral uninjured MCG which is normally induced by the lesion to sprout novel projections into the denervated ganglion, is suppressed from doing so by the 5-HT treatment.

  5. These growth inhibiting effects of 5-HT upon the contralateral MCG could be antagonized by the prior administration of the 5-HT receptor blocker cyproheptadine, suggesting a specific receptor mediated action.

  6. We suggest that 5-HT may play a role in governing the state of neuronal outgrowthin vivo in the CNS of the adult snail, as has been suggested by early developmental and neuronal cultural studies.

Key Words: buccal ganglia, neurite outgrowth, supernumerary fibres, cyproheptadine, molluscs

References

  1. Allison, P., and Benjamin, P. R. (1985). Anatomical studies of central regeneration of an identified interneurone.Proc. R. Soc. Lond. B226:135–157. [Google Scholar]
  2. Baker, M. W., and Croll, R. P. (1992). Serotonin inhibits lesion induced sprouting in the snail CNS: Anin vivo study.Soc. Neurosci. Abstr.18:1470. [Google Scholar]
  3. Baker, M. W., and Croll, R. P. (1993). Cyproheptadine blocks 5-HT inhibition of lesion-induced sprouting in the snail CNS.Soc. Neurosci. Abstr.19:1085. [Google Scholar]
  4. Baker, M. W., and Croll, R. P. (1995). Contralateral sprouting and compensatory innervation following the permanent lesion of a ganglionic connective in the snail (submitted for publication). [DOI] [PubMed]
  5. Baker, M. W., Vohra, M. M., and Croll, R. P. (1993). Serotonin depletors, 5,7-dihydroxytryptamine and p-chlorophenylalanine, cause sprouting in the CNS of the adult snail.Brain Res.623:311–315. [DOI] [PubMed] [Google Scholar]
  6. Bailey, C. H., and Chen, B. (1988). Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons.Proc. Natl. Acad. Sci. USA85:2373–2377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Budnik, V., Morris, L. M., and White, K. (1986). Perturbed patterns of catacholamine-containing neurons in mutantDrosophila deficient in the enzyme DOPA decarboxylase.J. Neurosci.6:3682–3691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bulloch, A. G. M., and Hauser, G. C. (1990). Sprouting by isolated Helisoma neurons: Enhancement by glutamate.Int. J. Dev. Neurosci.8:391–398. [DOI] [PubMed] [Google Scholar]
  9. Bulloch, A. G. M., and Kater, S. B. (1982). Neurite outgrowth and selection of new electrical connections by the adultHelisoma neurons.J. Neurophysiol.48:569–583. [DOI] [PubMed] [Google Scholar]
  10. Buznikov, G. A., Chudakova, I. V., Berysheva L. V., and Vyazmina, N. M. (1968). The role of neurohumours in early embryogenesis. II. Acetylcholine and catecholamine content in developing embryos of sea urchin.J. Embryol. Exp. Morphol.20:119–128. [PubMed] [Google Scholar]
  11. Castellucci, V. F., Carew, T. J., and Kandel, E. R. (1978). Cellular analysis of long-term habituation of the gill-withdrawl reflx inAplysia.Science202:1306–1308. [DOI] [PubMed] [Google Scholar]
  12. Chase, R., and Kamil, R. (1983). Morphology and odor sensitivity of regenerated snailAchatina fulica tentacles.J. Neurobiol.14; 34–50. [DOI] [PubMed] [Google Scholar]
  13. Chiasson, B. J., Baker, M. W., and Croll, R. P. (1994). Morphological changes and functional recovery following axotomy of a serotonergic, cerebrobuccal neuron in the land snail,Achatina fulica.J. Exp. Biol.192:147. [DOI] [PubMed] [Google Scholar]
  14. Cline, H. T., and Constantine-Paton, M. (1990). NMDA receptor agonists and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection.J. Neurosci.10:1197–1216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cohan, C. S., Haydon, P. G., Mercier, A. J., and Kater, S. B. (1987). Formation, maintenance, and functional uncoupling of connections between identifiedHelisoma neuronsin situ.J. Neurobiol.18:329–341. [DOI] [PubMed] [Google Scholar]
  16. Croll, R. P. (1987). Identified neurons and cellular homologies. InNervous Systems in Invertebrates (M. A. Ali, Ed.), NATO-ASI Series, Plenum Press, New York, pp. 41–59. [Google Scholar]
  17. Croll, R. P. (1988). Distribution of monoamines within the central nervous system of the juvenile pulmonate snail,Achatina fulica.Brain Res.460:29–49. [DOI] [PubMed] [Google Scholar]
  18. Croll, R. P., and Baker, M. W. (1990) Axonal regeneration and sprouting following injury to the cerebral-buccal connective in the snail,Achatina fulica.J. Comp. Neurol.300:273–286. [DOI] [PubMed] [Google Scholar]
  19. Croll, R. P., and Baker, M. W. (1990). Serotonergic regulation ofin vivo neuritogenesis in the adult snail.Netherlands J. Zool.44:301–316. [Google Scholar]
  20. Davenport R. W. and Kater, S. B. (1992). Local increases in intracellular calcium elicit local filopodial responses inHelisoma neuronal growth cones.Neuron9:405–416. [DOI] [PubMed] [Google Scholar]
  21. Easter, S. S., and Stuermer, C. A. A. (1984). An evaluation of the hypothesis of shifting terminals in goldfish optic tectum.J. Neuorsci.1:793–811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Forscher, P. (1989). Calcium and polyphosphoinositide control of cytoskeletal dynamics.Trends Neurosci.12:468–474. [DOI] [PubMed] [Google Scholar]
  23. Gerschenfeld, H. M., and Paupardin-Tritsch, D. (1974). On the transmitter function of 5-hydroxytryptamine at excitatory and inhibitory monosynaptic junctions.J. Physiol.243:457–481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Goldberg, J. I., and Kater, S. B. (1989). Expression and function of the neurotransmitter serotonin during development of theHelisoma nervous system.Dev. Biol.131:483–495. [DOI] [PubMed] [Google Scholar]
  25. Haydon, P. G., McCobb, D. P., and Kater, S. B. (1984). Serotonin selectively inhibits growth cone motility and synaptogenesis of specific identified neurons.Science226:561–564. [DOI] [PubMed] [Google Scholar]
  26. Haydon, P. G., McCobb, D. P., and Kater, S. B. (1987). The regulation of neurite outgrowth, growth cone motility, and electrical synaptogenesis by serotonin.J. Neurobiol.18:197–215. [DOI] [PubMed] [Google Scholar]
  27. Kater, S. B., and Mills, L. R. (1991). Regulation of growth cone behavior by calcium.J. Neurosci.11:891–899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Komuro, H., and Raskic, P. (1992). Selective role of N-type calcium channels in neuronal migration.Science257:806–809. [DOI] [PubMed] [Google Scholar]
  29. Komuro, H., and Raskic, P. (1993). Modulation of neuronal migration by NMDA receptors.Science260:95–97. [DOI] [PubMed] [Google Scholar]
  30. Kostenko, M. A., Musienko, V. S., and Smolikhina, T. I. (1983). Ca2+ and pH affect the neurite formation in cultured mollusc isolated neurons.,Brain Res.276:43–50. [DOI] [PubMed] [Google Scholar]
  31. Lankford, K. L., and Letourneau, P. C. (1989). Evidence that calcium may control neurite outgrowth by regulating the stability of actin filamentsJ. Cell Biol.109:1229–1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lauder, J., and Krebs, H. (1978). Serotonin as a differentiation signal in early neurogenesis.Dev. Neurosci.1:15–30. [DOI] [PubMed] [Google Scholar]
  33. Lauder, J. M. (1993). Neurotransmitters as growth regulatory signals: Role of receptor and second messengers.Trends Neurosci.16:233–240. [DOI] [PubMed] [Google Scholar]
  34. Lipton, S. A. and Kater, S. B. (1989). Neurotransmitter regulation of neuronal outgrowth, plasticity and survival.TINS12:265–270. [DOI] [PubMed] [Google Scholar]
  35. Lockerbie, R. O. (1990). Biochemical pharmacology of isolated neuronal growth cones: Implications for synaptogenesis.J. Cell Biol.112:1215–1227. [DOI] [PubMed] [Google Scholar]
  36. Lockerbie, R. O., Miller, V. E., and Pfenninger, K. H. (1991). Regulated plasmalemmal expansion in nerve growth cones.J. Cell Biol.112:1215–1227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Mattson, M. P., and Kater, S. B. (1988). Calcium regulation of neurite elongation and growth cone motility.J. Neurosci.7:4034–4043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mayford, M., Barzilai, A., Keller, F., Schacher, S., and Kandel, E. R. (1992). Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity inAplysia.Science256:638–644. [DOI] [PubMed] [Google Scholar]
  39. McCobb, D. P., Cohen, C. S., Connor, J. A., and Kater, S. B. (1988). Interactive effects of serotonin and acetylcholine on neurite elongation.Neuron1:377–385. [DOI] [PubMed] [Google Scholar]
  40. Murphy, A. D., and Kater, S. B. (1980). Sprouting and functional regeneration of an identified neuron inHelisoma.Brain Res.186:251–272. [DOI] [PubMed] [Google Scholar]
  41. Murphy, A. D., Barker, D. L., Loring, J. E., and Kater, S. B. (1985). Sprouting and functional regeneration of an identified serotonergic neuron following axotonomy.J. Neurobiol.16:137–151. [DOI] [PubMed] [Google Scholar]
  42. Murrain, M., Murphy, A. D., Mills, L. R., and Kater, S. B. (1990). Neuron-specific modulation by serotonin of regenerative outgrowth and intracellular calcium within the CNS ofHelisoma trivolis.J. Neurobiol.21:611–618. [DOI] [PubMed] [Google Scholar]
  43. Purves, D., and Lichtman, J. W. (1985).Principles of Neural Development, Sinauer Associates, Sunderland, MA, pp. 124–127. [Google Scholar]
  44. Rehder, V., Jensen, R. J., and Kater, S. B. (1990). The initial stages of neural regeneration are dependent upon intracellular calcium levels.Neuroscience51:565–574. [DOI] [PubMed] [Google Scholar]
  45. Sakharov, D. A. (1970). Cellular aspects of invertebrate neuropharmacology.Annu. Rev. Pharmacol.10:335–352. [DOI] [PubMed] [Google Scholar]
  46. Sakharov, D. A. (1976). Nerve cell homologies in gastropods. InNeurobiology of Invertebrates: Gastropoda Brain (J. Salankir, Ed.), Akademiai Kiado, Budapest, pp. 27–40. [Google Scholar]
  47. Schwartz, J. H., and Shkolnik, L. J. (1981). The giant serotonergic neuron ofAplysia: A multitargeted nerve cell.J. Neurosci.1:606–618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Siegelbaum, S., Camardo, J. S., and Kandel, E. R. (1982). Serotonin and cyclic AMP close single K+ channels inAplysia sensory neurones.Nature,299:413–416. [DOI] [PubMed] [Google Scholar]
  49. Strittmatter, S. M., Valenzuela, D., Kennedy, T. E., Neer, E. J., and Fishman, M. C. (1990). G0 is a major growth cone protein subject to regulation by GAP-43.Nature,344:836–841. [DOI] [PubMed] [Google Scholar]
  50. Weiss, K. R., and Kupfermann, I. (1976). Homology of the giant seroteonergic neurons (metacerebral cells) inAplysia and pulmonate molluscs.Brian Res.117:33–49. [DOI] [PubMed] [Google Scholar]
  51. Weiss, K. R., Cohen, J. L., and Kupfermann, I. (1978). Modulatory control of buccal musculature by a serotonergic neuron (metacerebral cell) inAplysia.J. Neurophysiol.41, 181203. [DOI] [PubMed] [Google Scholar]
  52. Zheng, J. Q., Felder, M., Connor, J. A. and Poo, M. (1994). Turning of nerve growth cones induced by neurotransmitters.Nature368:140–144. [DOI] [PubMed] [Google Scholar]

Articles from Cellular and Molecular Neurobiology are provided here courtesy of Springer

RESOURCES