Skip to main content
SpringerLink
Log in

Changes in the physiological roles of neurotransmitters during individual development

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Abstract

The classical neurotransmitters (acetylcholine and biogenic monoamines) are multifunctional substances involved in intra- and intercellular signaling at all stages of ontogenesis in multicellular animals. A cyclical scheme is proposed to describe age-related changes in neuro-transmitter functions at different stages of development from oocyte maturation to neuron formation. This may reflect not only the temporospatial organization of neurotransmitter processes, but also the origin of the functions of acetylcholine and biogenic monoamines from the protosynapses of the cleaved embryo to neuronal synapses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. G. A. Buznikov, Low-Molecular Weight Inhibitors of Embryonic Development [in Russian], Nauka, Moscow (1967).

    Google Scholar 

  2. G. A. Buznikov, Neurotransmitters in Embryogenesis [in Russian], Nauka, Moscow (1987).

    Google Scholar 

  3. G. A. Buznikov, L. A. Mal'chenko, L. A. Nikitina, A. Yu. Gananov, and V. S. Emanov, “The action of neurotransmitters and their antagonists on oocyte maturation. I. The effects of serotonin and its antagonists on the sensitivity of starfish oocytes to 1-methyladenine,” Ontogenez,21, No. 5, 530–536 (1990).

    CAS  Google Scholar 

  4. G. A. Buznikov, L. A. Mal'chenko, L. A. Nikitina, A. Yu. Galanov, S. A. Pogosyan, G. L. Papayan, and V. S. Emanov, “The action of neurotransmitters and their antagonists on oocyte maturation. II. The effects of serotonin antagonists on the sensitivity of starfish oocytes to forskolin and ionomycin,” Ontogenez,21, No. 6, 612–619 (1990).

    CAS  Google Scholar 

  5. G. A. Buznikov, L. E. Martynova, T. L. Marshak, A. Yu. Galanov, R. E. Dugnerova, L. A. Nikitina, R. Mileusnich, and L. Rakich, “The actions of protein kinase C activators and inhibitors on early echinoderm embryos,” Ontogenez,24, No. 3, 58–69 (1993).

    CAS  Google Scholar 

  6. Kh. S. Koshtoyants, Protein Bodies, Metabolism, and Nervous Regulation [in Russian], Izdatel'stvo Akademii Nauk SSSR (USSR Academy of Sciences Press), Moscow (1951).

    Google Scholar 

  7. L. E. Martynova, “Gastrulation in the sea urchinStrongylocentrotus drobachiensis in normal conditions and during exposure to various substances,” Ontogenez,12, No. 3, 310–314 (1981).

    CAS  Google Scholar 

  8. L. A. Nikitina, and G. A. Buznikov, “Serotonin inhibits the maturation of green toad oocytes induced by phorbol ester,” Ontogenez,27, No. 2, 122–125 (1996).

    PubMed  CAS  Google Scholar 

  9. L. A. Nikitina, L. A. Mal'chenko, N. A. Teplits, and G. A. Buznikov, “The action of serotonin and its antagonists on thein vitro maturation of amphibian oocytes,” Ontogenez,19, No. 5, 499–507 (1988).

    PubMed  CAS  Google Scholar 

  10. M. A. Rostomyan, K. S. Abramyan, G. A. Buznikov, and É. V. Gusareva, “Electron-cytochemical detection of adenylate cyclase in early sea urchin embryos,” Tsitologiya,27, No. 8, 877–881 (1995).

    Google Scholar 

  11. D. A. Sakharov, “Neurotransmitter multiplicity: functional significance,” Zh. Évol. Biokhim. Fiziol.,26, No. 5, 733–740 (1990).

    PubMed  CAS  Google Scholar 

  12. C. Avila, C. T. Tamse, and A. M. Kuzirian, “Induction of metamorphosis inHemissenda crassicornis larvae (Mollusca, Nudibranchia) by GABA, choline and serotonin,” Invertebr. Reprod. Devel.,29, No. 2, 127–141 (1996).

    CAS  Google Scholar 

  13. B. Baccetti, A. G. Burrini, G. Collodei, C. Falugi, E. Moretti, and P. Piombone, “Receptor-like molecules in sperms of different animal species,” Zygote,3, No. 3, 207–217 (1995).

    PubMed  CAS  Google Scholar 

  14. M. W. Baker, M. M. Vohra, and R. P. Croll, “Serotonin depletors, 5,7-dihydroxytryptamine andp-chlorophenylalanine, cause sprouting in the CNS of the adult snail,” Brain Res.,623, No. 2, 311–315 (1993).

    Article  PubMed  CAS  Google Scholar 

  15. J. Bodis, G. Hartmann, A. Torik, Z. Bognar, H. R. Tinneberg, P. Cledon, and V. Hanf, “Relationship between the monoamine and gonadotrophic contents in follicular fluid of preovulatory graafian follicles after supervulation treatment,” Exp. Clin. Endocrinol.101, No. 2, 178–182 (1993).

    Article  PubMed  CAS  Google Scholar 

  16. J. Bodis, H. R. Tinneberg, A. Torok, P. Cledon, V. Hanf, and F. Pappenfuss, “Effect of noradrenaline and dopamine on progesterone and estradiol secretion of human granulosa cells,” Acta Endocrinol.,129, No. 1, 65–168 (1993).

    Google Scholar 

  17. J. Bodis, A. Torok, H. R. Tinneberg, V. Hanf, M. Hamori, and P. Cledon, “Influence of serotonin on progesterone and estradiol secretion of cultured human granulosa cells,” Fertil. Steril.,57, No. 5, 1008–1011 (1992).

    PubMed  CAS  Google Scholar 

  18. K. M. Brown, and K. G. Anitole, “Serotonin in early embryogenesis,” Trends Comp. Biochem. Physiol.,1, No. 2, 281–288 (1993).

    Google Scholar 

  19. W. J. Burke, C. A. Schmitt, K. N. Gillespie, and S. W. Li, “Norepinephrine transmitter metabolite is a selective cell death messenger,” Brain Res.,722, No. 1-2, 232–235 (1993).

    Google Scholar 

  20. G. A. Buznikov, Neurotransmitters in Embryogenesis, Harwood Academic Press, Chur. (1990).

    Google Scholar 

  21. G. A. Buznikov, “The biogenic monoamines as regulators of early (pre-nervous) embryogenesis: new data,” in: Plasticity and Regeneration of the Nervous System, P. S. Timiras, A. Privat, E. Giacobini, and I. Lauder (eds.), Plenum Press, New York-London (1991).

    Google Scholar 

  22. G. A. Buznikov, L. N. Koikov, Yu. B. Shmukler, and M. J. Whitaker, “Nicotinic antagonists (piperidines and quinuclidines) reduce the susceptibility of early sea urchin embryos to agents evoking calcium shock,” Gen. Pharmacol.,29, No. 1, 49–53 (1997).

    PubMed  CAS  Google Scholar 

  23. G. A. Buznikov, T. L. Marshak, L. A. Malchenko, L. A. Nikitina, Yu. B. Shmukler, A. G. Buznikov, Lj. Rakic, and M. J. Whitaker, “Serotonin and acetylcholine modulate the sensitivity of early sea urchin embryos to protein kinase C activators,” Comp. Biochem. Physiol. (1997), in press.

  24. G. A. Buznikov, L. A. Nikitina, A. Yu. Galanov, L. A. Malchenko, and O. B. Trubnikova, “The control of oocyte maturation in the starfish and amphibians by serotonin and its antagonists,” J. Devel. Biol.,37, No. 2, 363–364 (1993).

    CAS  Google Scholar 

  25. G. A. Buznikov, and Yu. B. Shmukler, “The possible role of prenervous neurotransmitters in cellular interactions of early embryogenesis: a hypothesis,” Neurochem. Res.,6, No. 1, 55–69 (1981).

    Article  PubMed  CAS  Google Scholar 

  26. G. A. Buznikov, Yu. B. Shmukler, and J. M. Lauder, “From oocyte to neuron: do neurotransmitters function in the same way throughout development?,” Cell. Molec. Neurobiol.,16, No. 5, 532–559 (1996).

    Google Scholar 

  27. A. Capasso, P. Creti, B. De Petrocellis, P. De Prisco, and E. Parisi, “Role of dopamine and indolamine derivatives in the regulation of sea urchin adenylate cyclase,” Biochem. Biophys. Res. Comm.,154, No. 2, 758–764 (1988).

    Article  PubMed  CAS  Google Scholar 

  28. A. Capasso, E. Parisi, P. De Prisco, and B. De Petrocellis, “Catecholamine secretion and adenylate cyclase activation in sea urchin eggs,” Cell. Biol. Int. Rep.,11, No. 6, 457–463 (1987).

    Article  PubMed  CAS  Google Scholar 

  29. V. Carginale, L. Borrelli, A. Capasso, and E. Parisi, “Changes in dopamine uptake and developmental effects of dopamine receptor inactivation in the sea urchin,” Molec. Reprod. Devel.,40, No. 3, 379–385 (1995).

    Article  CAS  Google Scholar 

  30. M. D. C. Carnevali, F. Bonasoro, B. Invernizzi, E. Lucca, U. Welsch, and M. C. Thorndyke, “Tissue distribution of monoamine neurotransmitters in normal and regenerating arms of the feather starAntedon mediterranea,” Cell Tissue Res.,285, No. 2, 341–352 (1996).

    Article  CAS  Google Scholar 

  31. J. Cerda, T. R. Petrino, Y. W. P. Lin, and R. A. Wallace, “Inhibition ofFundulus heteroclitus oocyte maturationin vitro by serotonin (5-hydroxytryptamine),” J. Exp. Zool.,273, No. 3, 224–233 (1995).

    Article  CAS  Google Scholar 

  32. K. J. Christopher, J. P. Chang, and J. I. Goldberg, “Stimulation of ciliary beat frequency by serotonin is mediated by a Ca2+ influx in ciliated cells ofHelisoma trivolvis,” J. Exp. Biol.,199, No. 5, 1105–1113 (1996).

    PubMed  CAS  Google Scholar 

  33. N. Dascal, E. Landau, and Y. Lass, “Xenopus oocyte resting potential, muscarinic responses and the role of calcium and guanosine-3′,5′-cyclic monophosphate,” J. Physiol. (L.),352, 551–574 (1984).

    CAS  Google Scholar 

  34. S. S. Dautov, and L. P. Nezlin, “Nervous system of theTonaria larva (Hemichordata: Enteropneusta). A histochemical and ultrastructural study,” Biol. Bull.,183, No. 3, 463–475 (1992).

    Google Scholar 

  35. R. Deguchi, and K. Osanai, “Serotonin-induced meiosis reinitiation from the first prophase and from the first metaphase in oocytes of the marine bivalveHiatella flaccida: Respective changes in intracellular Ca2+ and pH,” Develop. Biol.,171, No. 2, 483–496 (1995).

    Article  PubMed  CAS  Google Scholar 

  36. Y. Durocher, and P. Guerrier, “Activation of an 85-kDa ribosomal S6 kinase during serotonin-induced oocyte maturation,” Int. J. Devel. Biol.,40, No. 3, 557–566 (1996).

    CAS  Google Scholar 

  37. H. Emanuelsson, “Autoradiographic localization in polychaete embryos of ritiated mesulergine, a selective antagonist of serotonin receptors that inhibits early polychaete development,” Int. J. Devel. Biol.,36, No. 2, 293–302 (1992).

    CAS  Google Scholar 

  38. H. Emanuelsson, M. Carlberg, and B. Lowkvist, “Presence of serotonin in early chick embryos,” Cell. Diff.,24, No. 1, 191–200 (1988).

    Article  CAS  Google Scholar 

  39. C. J. Epstein, “Aneuploidy and morphogenesis,” in: The Morphogenesis of Down Syndrome, C. J. Epstein (ed.), Wiley-Liss, New York (1991).

    Google Scholar 

  40. U. Ernsberger and H. Rohrer, “The development of the noradrenergic transmitter phenotype in postganglionic sympathetic neurons,” Neurochem. Res.,21, No. 7, 823–829 (1996).

    PubMed  CAS  Google Scholar 

  41. C. Falugi, “Localization and possible role of molecules associated with the cholinergic system during ‘non-nervous’ developmental events,” Eur. J. Histochem.,37, No. 4,287–294 (1993).

    PubMed  CAS  Google Scholar 

  42. C. Falugi and G. Prestipino, “Localization of putative nicotinic cholinoceptors in the early development ofParacentrotus lividus,” Cell Molec. Biol.,35, No. 2, 147–161 (1989).

    CAS  Google Scholar 

  43. P. P. Fong, K. Kyozuka, H. Abdelghani, J. D. Hardege and J. L. Ram, “In vivo andin vitro induction of germinal vesicle breakdown in a freshwater bivalve, the zebra musselDreissena polymorpha (Pallas),” J. Exp. Zool.,269, No. 5, 467–474 (1994).

    Article  PubMed  CAS  Google Scholar 

  44. P. P. Fong, S. Wade, and M. Rostafin, “Characterization of serotonin receptor mediating parturition in fingernail clamsSphaerium (Musculium) Spp. from eastern North America,” J. Exp. Zool.,275, No. 4, 326–330 (1996).

    Article  CAS  Google Scholar 

  45. S. F. Gilbert, Developmental Biology, Sinauer Assoc. Inc. Publ., Sunderland, USA (1994).

    Google Scholar 

  46. I. Godin and J. D. Gipouloux, “Notochordal catecholamines in exogastrulatedXenopus embryos,” Devel. Growth Diff.,28, No. 2, 137–142 (1986).

    Article  CAS  Google Scholar 

  47. J. I. Goldberg, N. K. Koehncke, K. J. Christopher, C. Neumann, and T. J. Diefenbach, “Pharmacological characterization of a serotonin receptor involved in an early embryonic behaviour ofHelisoma trivolvis,” J. Neurobiol.,25, No. 12, 1545–1557 (1994).

    Article  PubMed  CAS  Google Scholar 

  48. P. Guerrier, C. Leclerc-David, and M. Moreau, “Evidence for the involvement of internal calcium stores during serotonin-induced meiosis reinitiation in oocytes of the bivalve molluscRuditapes philippinarum,” Devel. Biol.,159, No. 2, 474–484 (1993).

    Article  CAS  Google Scholar 

  49. J. B. Gurdon, A. Mitchell, and K. Ryan, “An experimental system for analyzing response to a morphogen gradient,” Proc. Natl. Acad. Sci. USA,93, No. 18, 9334–9338 (1996).

    Article  PubMed  CAS  Google Scholar 

  50. T. Gustafson, “Pharmacological control of muscular activity of the sea urchin larva. IV. Effects of monoamines and adenosine,” Comp. Biochem. Physiol.,98C, No. 2, 307–315 (1991).

    CAS  Google Scholar 

  51. T. Gustafson and M. Toneby, “On the role of serotonin and acetylcholine in sea urchin morphogenesis,” Exp. Cell. Res.,62, No. 1, 102–117 (1970).

    Article  PubMed  CAS  Google Scholar 

  52. R. P. Hellendall, U. Shambra, J. Liu, and J. M. Lauder, “Prenatal expression of 5-HT1c and 5-HT2 receptors in the developing nervous system,” Exp. Neurol.,120, No. 2, 186–201 (1993).

    Article  PubMed  CAS  Google Scholar 

  53. N. Ivgy-May, H. Tamir, and M. D. Gershon, “Synaptic properties of serotonergic growth cones in developing rat brain,” J. Neurosci.,14, No. 3, part 1, 1011–1029 (1994).

    PubMed  CAS  Google Scholar 

  54. L. Jaffe, “First messengers at fertilization,” J. Reprod. Fert. Suppl.,42, 107–116 (1990).

    CAS  Google Scholar 

  55. E. Josefsson, J. Bergquist, R. Ekman, and A. Tarkowski, “Catecholamines are synthesized in mouse lymphocytes and regulate function of apoptosis,” Immunology,88, No. 1, 140–146 (1996).

    Article  PubMed  CAS  Google Scholar 

  56. R. Juneja, E. Ito, and S. S. Koide, “Effect of serotonin and tricyclic antidepressants on intracellular calcium concentrations inSpisula oocytes,” Cell Calcium,15, No. 1, 1–6 (1994).

    Article  PubMed  CAS  Google Scholar 

  57. S. Krantic, P. Guerrier, and F. Dube, “Meiosis reinitiation in surf clam oocytes is mediated via a 5-hydroxytryptamine membrane receptor and a vitelline envelope-associated high-affinity binding site,” J. Biol. Chem.,268, No. 1, 7983–7989 (1993).

    PubMed  CAS  Google Scholar 

  58. T. Laasberg, “Ca2+-mobilizing receptors of gastrulating chick embryo,” Comp. Biochem. Physiol.,97C, No. 1, 9–12 (1990).

    CAS  Google Scholar 

  59. J. M. Lauder, “Neurotransmitters as morphogens,” Progr. Brain Res.,73, 365–387 (1988).

    CAS  Google Scholar 

  60. J. M. Lauder, “Ontogeny of the serotonergic system in the rat. Serotonin as a developmental signal,” Ann. N.Y. Acad. Sci.,600, 297–314 (1990).

    PubMed  CAS  Google Scholar 

  61. J. M. Lauder, “Neurotransmitters as growth regulatory signals: role of receptors and second messengers,” Trends Neurosci.,16, No. 6, 233–240 (1993).

    Article  PubMed  CAS  Google Scholar 

  62. J. M. Lauder and J. Liu, “Glial heterogeneity and developing neurotransmitter systems,” Persp. Devel. Neurobiol.,2, No. 3, 239–250 (1994).

    CAS  Google Scholar 

  63. J. M. Lauder, J. Moiseiwitsch, J. Liu, and M. B. Wilkie, “Serotonin in development and pathophysiology,” in: Brain Lesions in the Newborn, H. C. Lou, G. Grisen, and J. Larsen (eds.), Munksgaard, Copenhagen (1994), pp. 60–72.

    Google Scholar 

  64. J. M. Lauder, H. Tamir, and T. W. Sadler, “Serotonin and morphogenesis. I. Sites of serotonin uptake and binding protein immunoreactivity in the mid-gestation mouse embryo,” Development,102, No. 4, 709–720 (1988).

    PubMed  CAS  Google Scholar 

  65. Y. M. Lawrence and K. S. R. Cuthbertson, “Thapsigargin induces cytoplasmic free Ca2+ oscillations in mouse oocytes,” Cell Calcium,17, No. 2, 154–164 (1995).

    Article  PubMed  CAS  Google Scholar 

  66. D. Lipinsky, D. R. Nussenzveig, M. C. Gershengorn, and Y. Oron, “Desensitization of the response to thyrotropin-releasing hormone inXenopus oocytes is an amplified process that precedes calcium mobilization,” Pflüger's Archiv./Eur. J. Physiol.,429, No. 3, 419–425 (1995).

    Article  CAS  Google Scholar 

  67. J. Liu and J. M. Lauder, “S-100β and insulin-like growth factor II differentially regulate growth of developing serotonin and dopamine neuronsin vitro,” J. Neurosci. Res.,33, No. 2, 248–256 (1992).

    Article  PubMed  Google Scholar 

  68. G. Malinger, H. Zakut, and H. Soreq, “Cholinoceptive properties of human primordial, preantral and antral oocytes:in situ hybridization and biochemical evidence for expression of cholinesterase genes,” J. Mol. Neurosci.,1, No. 2, 77–84 (1989).

    PubMed  CAS  Google Scholar 

  69. L. N. Markova, G. A. Buznikov, N. Kovacevic, L. Rakic, N. B. Salimova, and E. V. Volina, “Histochemical study of biogenic monoamines in early (prenervous) and late embryos of sea urchins,” Int. J. Devel. Neurosci.,3, No. 5, 493–500 (1985).

    Article  CAS  Google Scholar 

  70. M. Misamore, H. Silverman, and J. W. Lynn, “Analysis of fertilization and polyspermy in serotonin-spawned eggs of the zebra mussel,Dreissena polymorpha,” Molec. Reprod. Devel.,43, No. 2,205–216 (1996).

    Article  CAS  Google Scholar 

  71. J. R. D. Moiseiwitsch and J. M. Lauder, “In vitro effects of serotonergic drugs on expression of S-100β and tenascin,” Teratology,47, No. 5, 383 (1993).

    Google Scholar 

  72. J. R. D. Moiseiwitsch and J. M. Lauder, “Serotonin regulates mouse cranial neural crest migration,” Proc. Natl. Acad. Sci. USA,92, No. 16,7182–7186 (1995).

    Article  PubMed  CAS  Google Scholar 

  73. J. R. D. Moiseiwitsch and J. M. Lauder, “Stimulation of murine tooth development in organotypic culture by the neurotransmitter serotonin,” Arch. Oral Biol.,41, No. 2, 161–165 (1996).

    Article  PubMed  CAS  Google Scholar 

  74. A. Nicotra and G. Schatten, “Propranolol, a beta-adrenergic receptor blocker, affects microfilament organization, but not microtubules, during the first division in sea urchin eggs,” Cell Motil. Cytoskel.,16, No. 1, 182–189 (1990).

    Article  CAS  Google Scholar 

  75. A. Nicotra and G. Schatten, “Propranolol induces polyspermy during sea urchin fertilization,” Molec. Reprod. Devel.,43, No. 3, 387–391 (1996).

    Article  CAS  Google Scholar 

  76. L. A. Nikitina, G. A. Buznikov, and J. M. Lauder, “Putative role of serotonin in the maturation of amphibian oocytes”, Proceedings of the 25th Annual Meeting of the Society of Neurosciences, San Diego, California (1995), Vol. 2, p. 862.

  77. K. Palen, L. Thorneby, and H. Emanuelsson, “Effects of serotonin and serotonin antagonists on chick embryogenesis,” W. Roux's Arch.,187, 89–103 (1979).

    Article  Google Scholar 

  78. P. D. Prasad, B. J. Hoffmans, A. J. Moe, C. H. Smith, F. H. Leibach, and V. Ganapathy, “Functional expression of the plasma membrane serotonin transporter but not the vesicular monoamine transporter in human placental trophoblasts and choriocarcinoma cells,” Placenta,17, No. 4, 201–207 (1996).

    Article  PubMed  CAS  Google Scholar 

  79. B. S. Reinoso, A. S. Undie, and P. Levitt, “Dopamine receptors mediate differential morphological effects in cerebral cortical neuronsin vitro,” J. Neurosci. Res.,43, No. 4, 439–453 (1996).

    Article  PubMed  CAS  Google Scholar 

  80. F. Renaud, E. Parisi, A. Capasso, and P. De Prisco, “On the role of serotonin and 5-methoxytryptamine in the regulation of cell division in sea urchin eggs,” Devel. Biol.,98, No. 1, 37–47 (1983).

    Article  CAS  Google Scholar 

  81. M. Reuter and M. Gustafsson, “Neuronal signal substances in asexual multiplication and development in flatworms,” Cell. Molec. Neurobiol.,16, No. 5, 591–616 (1996).

    Article  PubMed  CAS  Google Scholar 

  82. S. J. Rowe, N. J. Messenger, and A. E. Warner, “The role of noradrenaline in the differentiation of amphibian embryonic neurons,” Development,19, No. 4, 1343–1357 (1993).

    Google Scholar 

  83. I. Ruiz and A. Altaba, “Pattern formation in the vertebrate neural plate,” Trends Neurosci.,17, No. 6, 233–243 (1994).

    Article  Google Scholar 

  84. U. Schmidt, C. Beyer, A. B. Destreicher, I. Reisert, K. Shilling, and C. Pilgrim, “Activation of dopaminergic D-1 receptors promotes morphogenesis of developing striatal neurons,” Neuroscience,74, No. 2, 453–460 (1996).

    Article  PubMed  CAS  Google Scholar 

  85. F. M. Shilling, D. J. Carroll, A. J. Muslin, J. A. Escobedo, L. T. Williams, and L. A. Jaffe, “Evidence for both tyrosine kinase and G-protein-coupled pathways leading to starfish egg activation,” Devel. Biol.,162, No. 2, 590–599 (1994).

    Article  CAS  Google Scholar 

  86. Yu. B. Shmukler, “Possibility of membrane reception of neurotransmitters in sea urchin early embryos,” Comp. Biochem. Physiol.,106C, No. 1, 269–273 (1993).

    CAS  Google Scholar 

  87. Yu. B. Shmukler and G. A. Buznikov, “Functional coupling of neurotransmitters with second messengers during cleavage division: facts and hypotheses,” Persp. Devel. Neurobiol. (1997), in press.

  88. Yu. B. Shmukler, G. A. Buznikov, and M. J. Whitaker, “The effect of serotonergic substances on free calcium ion concentrations in the earlyLytechinus pictus embryos,” in: Proceedings of the Congress of the European Developmental Biology Organization, Toulouse, France (1995).

  89. D. L. Shuey, T. W. Sadler, and J. M. Lauder, “Serotonin as a regulator of craniofacial morphogenesis. Site-specific malformations following exposure to serotonin uptake inhibitors,” Teratology,46, No. 4, 367–378 (1992).

    Article  PubMed  CAS  Google Scholar 

  90. D. L. Shuey, T. W. Sadler, H. Tamir, and J. M. Lauder, “Serotonin and morphogenesis. II. Transient expression of serotonin uptake and binding protein during craniofacial morphogenesis in the mouse,” Anat. Embryol.,187 No. 1, 75–85 (1993).

    Article  PubMed  CAS  Google Scholar 

  91. H. Tamir and M. D. Gershon, “Serotonin-containing vesicles” Ann. N.Y. Acad. Sci.,600, 53–67 (1990).

    PubMed  CAS  Google Scholar 

  92. M. Toth, D. Benjamin, and T. Shenk, “Targeted disruption of the 5-HT2 receptor results in developmental abnormalities in mice,” Abstr. IUPHAR Third Satellite Meeting on Serotonin (1994).

  93. K. Turlejski, “Evolutionary ancient role of serotonin: longlasting regulation of activity and development,” Acta Neurobiol. Exp.,56, No. 2, 619–636 (1996).

    CAS  Google Scholar 

  94. S. Ueda, X. F. Gu, P. M. Whitaker-Azmitia, I. Naruse, and E. C. Azmitia, “Neuro-glial neurotrophic interaction in the S-100β retarded mutant mouse (polydactyly Nagoya). I. Immunocytochemical and neurochemical studies,” Brain Res.,633, No. 1-2, 275–283 (1994).

    Article  PubMed  CAS  Google Scholar 

  95. C. Vaillaincourt, A. Petit, and S. Belisle, “D2 dopamine agonists inhibit adenosine-3′,5′-cyclic monophosphate (cAMP) production in human term trophoblastic cells,” Life Sci.,55, No. 20, 1545–1552 (1994).

    Article  Google Scholar 

  96. C. Vaillaincourt, A. Petit, N. Gallo Payet, D. Bellabarba, J. G. Lehoux, and S. Belisle, “Labeling of D2 dopaminergic and 5-HT2 serotonergic binding sites in human trophoblastic cells using [3H]-spiperone,” J. Recept. Res.,14, No. 1, 11–22 (1994).

    Google Scholar 

  97. A. Vernadakis, “Glia-neuron intercommunication and synaptic plasticity,” Progr. Neurobiol.,49, No. 3, 185–214 (1996).

    Article  PubMed  CAS  Google Scholar 

  98. J. A. Wallace, “Monoamines in the early chick embryo: demonstration of serotonin synthesis and the regional distribution of serotonin-concentrating cells during morphogenesis,” Am. J. Anat.,165, No. 3, 261–276 (1982).

    Article  PubMed  CAS  Google Scholar 

  99. M. Walther, R. Ulrich, M. Kroiher, and S. Berking, “Metamorphosis and pattern formation inHydractinia echinata, a colonial hydroid,” Int. J. Devel. Biol.,40, No. 1, 313–322 (1996).

    CAS  Google Scholar 

  100. S. Webb, R. A. Anderson, and N. A. Brown, “Mouse trisomy 16 model of heart defects in Down's syndrome: atrioventricular cushion cells and volumes,” Teratology,49, No. 5, 373 (1994).

    Google Scholar 

  101. P. M. Whitaker-Azmitia, M. Druse, P. Walker, and J. M. Lauder, “Serotonin as a developmental signal,” Behav. Brain Res.,73, No. 1-2, 19–29 (1995).

    Article  CAS  Google Scholar 

  102. P. M. Whitaker-Azmitia, A. V. Shemer, J. Caruso, L. Molino, and E. C. Azmitia, “Role of high-affinity serotonin receptors in neuronal growth,” Ann. N.Y. Acad. Sci.,600, 315–330 (1990).

    PubMed  CAS  Google Scholar 

  103. M. S. Yavarone, D. L. Shuey, T. W. Sadler, and J. M. Lauder, “Serotonin uptake in the ectoplacental cone and placenta of the mouse,” Placenta,14, No. 2, 149–161 (1993).

    PubMed  CAS  Google Scholar 

  104. M. S. Yavarone, D. L. Shuey, H. Tamir, T. W. Sadler, and J. M. Lauder, “Serotonin and cardiac morphogenesis in the mouse embryo,” Teratology,47, No. 6, 573–584 (1993).

    Article  PubMed  CAS  Google Scholar 

  105. I. Yazaki, E. Tosti, and B. Dale, “Cytoskeletal elements link calcium channel activity and the cell cycle in early sea urchin embryos,” Development,121, No. 6, 1827–1831 (1995).

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. N. K. Kol'tsov Institute of Developmental Biology, Russian Academy of Sciences, 26 Vavilov Street, 117808, Moscow, Russia

    G. A. Buznikov & Yu. B. Shmukler

  2. University of Northern Carolina, 27599-7090, Chapel Hill, NC, USA

    J. M. Lauder

Authors
  1. G. A. Buznikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu. B. Shmukler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. M. Lauder
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 83, No. 10, pp. 1–15, October, 1997.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buznikov, G.A., Shmukler, Y.B. & Lauder, J.M. Changes in the physiological roles of neurotransmitters during individual development. Neurosci Behav Physiol 29, 11–21 (1999). https://doi.org/10.1007/BF02461353

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02461353

Key Words

Search

Navigation