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Axon Growth and Guidance pp 104–114Cite as

Neurotransmitters and the Development of Neuronal Circuits

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 621))

Abstract

In the mature brain, neurotransmitters are used for synaptic communication between neurons. But during nervous system development, neurons often express and release transmitters before their axons establish contacts with their target cells. While much is known about the synaptic effects of neurotransmitters, their extrasynaptic effects are less understood. There is increasing evidence that neurotransmitters in the immature nervous system can act as trophic factors that influence different developmental events such as cell proliferation and differentiation. However, more recent work demonstrates that neurotransmitters can also influence the targeting of migrating neurons and growing axons during the formation of neuronal circuits. This chapter will focus on such guidance effects of neurotransmitters during the development of the nervous system. Elucidating extrasynaptic functions during the nervous system development might also provide insights in their potential roles for plasticity and regeneration in the adult nervous system.

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References

  1. Nguyen L, Rigo JM, Rocher V et al. Neurotransmitters as early signals for central nervous system development. Cell Tissue Res 2001; 305(2):187–202.

    Article  PubMed  CAS  Google Scholar 

  2. Mattson MP. Neurotransmitters in the regulation of neuronal cytoarchitecture. Brain Res 1988; 472(2):179–212.

    PubMed  CAS  Google Scholar 

  3. Lauder JM. Neurotransmitters as growth regulatory signals: Role of receptors and second messengers. Trends Neurosci 1993; 16(6):233–240.

    Article  PubMed  CAS  Google Scholar 

  4. Lipton SA, Kater SB. Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci 1989; 12(7):265–270.

    Article  PubMed  CAS  Google Scholar 

  5. Tessier-Lavigne M, Goodman CS. The molecular biology of axon guidance. Science 1996; 274(5290):1123–1133.

    Article  PubMed  CAS  Google Scholar 

  6. Dickson BJ. Molecular mechanisms of axon guidance. Science 2002; 298(5600):1959–1964.

    Article  PubMed  CAS  Google Scholar 

  7. McCobb DP, Cohan CS, Connor JA et al. Interactive effects of serotonin and acetylcholine on neurite elongation. Neuron 1988; 1(5):377–385.

    Article  PubMed  CAS  Google Scholar 

  8. Haydon PG, McCobb DP, Kater SB. Serotonin selectively inhibits growth cone motility and synaptogenesis of specific identified neurons. Science 1984; 226(4674):561–564.

    Article  PubMed  CAS  Google Scholar 

  9. Spencer GE, Klumperman J, Syed NI. Neurotransmitters and neurodevelopment. Role of dopamine in neurite outgrowth, target selection and specific synapse formation. Perspect Dev Neurobiol 1998; 5(4):451–467.

    PubMed  CAS  Google Scholar 

  10. McCobb DP, Haydon PG, Kater SB. Dopamine and serotonin inhibition of neurite elongation of different identified neurons. J Neurosci Res 1988; 19(1):19–26.

    Article  PubMed  CAS  Google Scholar 

  11. Lankford KI, DeMello FG, Klein WL. D1-type dopamine receptors inhibit growth cone motility in cultured retina neurons: Evidence that neurotransmitters act as morphogenic growth regulators in the developing central nervous system. Proc Natl Acad Sci USA 1988; 85(8):2839–2843.

    Article  PubMed  CAS  Google Scholar 

  12. Simeone TA, Sanchez RM, Rho JM. Molecular biology and ontogeny of glutamate receptors in the mammalian central nervous system. J Child Neurol 2004; 19(5):343–360, (discussion 361).

    Article  PubMed  Google Scholar 

  13. Ruthazer ES, Akerman CJ, Cline HT. Control of axon branch dynamics by correlated activity in vivo. Science 2003; 301(5629):66–70.

    Article  PubMed  CAS  Google Scholar 

  14. Fischer M, Kaech S, Wagner U et al. Clutamate receptors regulate actin-based plasticity in dendritic spines. Nat Neurosci 2000; 3(9):887–894.

    Article  PubMed  CAS  Google Scholar 

  15. Rossi DJ, Slater NT. The developmental onset of NMDA receptor-channel activity during neuronal migration. Neuropharmacology 1993; 32(11):1239–1248.

    Article  PubMed  CAS  Google Scholar 

  16. Farrant M, Feldmeyer D, Takahashi T et al. NMDA-receptor channel diversity in the developing cerebellum. Nature 1994; 368(6469):335–339.

    Article  PubMed  CAS  Google Scholar 

  17. Komuro H, Rakic P. Modulation of neuronal migration by NMDA receptors. Science 1993; 260(5104):95–97.

    Article  PubMed  CAS  Google Scholar 

  18. Komuro H, Rakic P. Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron 1996; 17(2):275–285.

    Article  PubMed  CAS  Google Scholar 

  19. Komuro H, Rakic P. Selective role of N-type calcium channels in neuronal migration. Science 1992; 257(5071):806–809.

    Article  PubMed  CAS  Google Scholar 

  20. Komuro H, Rakic P. Orchestration of neuronal migration by activity of ion channels, neurotransmitter receptors, and intracellular Ca2+ fluctuations. J Neurobiol 1998; 37(1):110–130.

    Article  PubMed  CAS  Google Scholar 

  21. Zheng JQ, Wan JJ, Poo MM. Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 1996; 16(3):1140–1149.

    PubMed  CAS  Google Scholar 

  22. Guirland C, Suzuki S, Kojima M et al. Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron 2004; 42(1):51–62.

    Article  PubMed  CAS  Google Scholar 

  23. Nowak L, Bregestovski P, Ascher P et al. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 1984; 307(5950):462–465.

    Article  PubMed  CAS  Google Scholar 

  24. Jahr CE, Stevens CF. Glutamate activates multiple single channel conductances in hippocampal neurons. Nature 1987; 325(6104):522–525.

    Article  PubMed  CAS  Google Scholar 

  25. Henley J, Poo MM. Guiding neuronal growth cones using Ca2+ signals. Trends Cell Biol 2004; 14(6):320–330.

    Article  PubMed  CAS  Google Scholar 

  26. Deller T, Haas CA, Frotscher M. Sprouting in the hippocampus after entorhinal cortex lesion is layer-specific but not translaminar: Which molecules may be involved? Restor Neurol Neurosci 2001; 19(3–4):159–167.

    PubMed  CAS  Google Scholar 

  27. Koyama R, Yamada MK, Nishiyama N et al. Group II metabotropic glutamate receptor activation is required for normal hippocampal mossy fibre development in the rat. J Physiol 2002; 539(Pt 1): 157–162.

    Article  PubMed  CAS  Google Scholar 

  28. Ohishi H, Shigemoto R, Nakanishi S et al. Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: An in situ hybridization study. J Comp Neurol 1993; 335(2):252–266.

    Article  PubMed  CAS  Google Scholar 

  29. Shigemoto R, Kinoshita A, Wada E et al. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 1997; 17(19):7503–7522.

    PubMed  CAS  Google Scholar 

  30. Kreibich TA, Chalasani SH, Raper JA. The neurotransmitter glutamate reduces axonal responsiveness to multiple repellents through the activation of metabotropic glutamate receptor 1. J Neurosci 2004; 24(32):7085–7095.

    Article  PubMed  CAS  Google Scholar 

  31. Kapfhammer JP, Raper JA. Collapse of growth cone structure on contact with specific neurites in culture. J Neurosci 1987; 7(1):201–212.

    PubMed  CAS  Google Scholar 

  32. Mattson MP, Dou P, Kater SB. Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. J Neurosci 1988; 8(6):2087–2100.

    PubMed  CAS  Google Scholar 

  33. Metzger F, Wiese S, Sendtner M. Effect of glutamate on dendritic growth in embryonic rat motoneurons. J Neurosci 1998; 18(5):1735–1742.

    PubMed  CAS  Google Scholar 

  34. Baird DH, Trenkner E, Mason CA. Arrest of afferent axon extension by target neurons in vitro is regulated by the NMDA receptor. J Neurosci 1996; 16(8):2642–2648.

    PubMed  CAS  Google Scholar 

  35. Chang S, De Camilli P. Glutamate regulates actin-based motility, in axonal filopodia. Nat Neurosci 2001; 4(8):787–793.

    Article  PubMed  CAS  Google Scholar 

  36. Vanderklish PW, Edelman GM. Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc Natl Acad Sci USA 2002; 99(3):1639–1644.

    Article  PubMed  CAS  Google Scholar 

  37. McKinney RA, Capogna M, Durr R et al. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 1999; 2(1):44–49.

    Article  PubMed  CAS  Google Scholar 

  38. Hebb. The organization of behavior: A neuropsychological theory. 1949.

    Google Scholar 

  39. Ruthazer ES, Cline HT. Insights into activity-dependent map formation from the retinotectal system: A middle-of-the-brain perspective. J Neurobiol 2004; 59(1):134–146.

    Article  PubMed  CAS  Google Scholar 

  40. Caulfield MP, Birdsall NJ. International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 1998; 50(2):279–290.

    PubMed  CAS  Google Scholar 

  41. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 2002; 111(4):815–835.

    Article  PubMed  CAS  Google Scholar 

  42. Lukas RJ, Changeux JP, Le Novere N et al. International Union of Pharmacology. XX. Current status of the nomenclature for nicotinic acetylcholine receptors and their subunits. Pharmacol Rev 1999; 51(2):397–401.

    PubMed  CAS  Google Scholar 

  43. Zoli M, Le Novere N, Hill Jr JA et al. Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems. J Neurosci 1995; 15(3 Pt 1): 1912–1939.

    PubMed  CAS  Google Scholar 

  44. Dori I, Parnavelas JG. The cholinergic innervation of the rat cerebral cortex shows two distinct phases in development. Exp Brain Res 1989; 76(2):417–423.

    Article  PubMed  CAS  Google Scholar 

  45. Small DH, Reed G, Whitefield B et al. Cholinergic regulation of neurite outgrowth from isolated chick sympathetic neurons in culture. J Neurosci 1995; 15(1 Pt 1):144–151.

    PubMed  CAS  Google Scholar 

  46. Lipton SA, Frosch MP, Phillips MD et al. Nicotinic antagonists enhance process outgrowth by rat retinal ganglion cells in culture. Science 1988; 239(4845):1293–1296.

    Article  PubMed  CAS  Google Scholar 

  47. Owen A, Bird M. Acetylcholine as a regulator of neurite outgrowth and motility in cultured embryonic mouse spinal cord. Neuroreport 1995; 6(17):2269–2272.

    Article  PubMed  CAS  Google Scholar 

  48. Pugh PC, Berg DK. Neuronal acetylcholine receptors that bind alpha-bungarotoxin mediate neurite retraction in a calcium-dependent manner. J Neurosci 1994; 14(2):889–896.

    PubMed  CAS  Google Scholar 

  49. Elsas SM, Kwak EM, Stent GS. Acetylcholine-induced retraction of an identified axon in the developing leech embryo. J Neurosci 1995; 15(2):1419–1436.

    PubMed  CAS  Google Scholar 

  50. Coronas V, Durand M, Chabot JG et al. Acetylcholine induces neuritic outgrowth in rat primary olfactory bulb cultures. Neuroscience 2000; 98(2):213–219.

    Article  PubMed  CAS  Google Scholar 

  51. Rosner H, Fischer H. In growth cones of rat cerebral neurons and human neuroblastoma cells, activation of protein kinase C causes a shift from filopodial to lamellipodial actin dynamics. Neurosci Lett 1996; 219(3):175–178.

    Article  PubMed  CAS  Google Scholar 

  52. Kozma R, Sarner S, Ahmed S et al. Rho family GTPases and neuronal growth cone remodelling: Relationship between increased complexity induced by Cdc42Hs, Racl, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol Cell Biol 1997; 17(3):1201–1211.

    PubMed  CAS  Google Scholar 

  53. Zheng JQ, Felder M, Connor JA et al. Turning of nerve growth cones induced by neurotransmitters. Nature 1994; 368(6467):140–144.

    Article  PubMed  CAS  Google Scholar 

  54. Kolb B, Tees R, Ables M. The cerebral cortex of the rat. 1990.

    Google Scholar 

  55. Ha DH, Robertson RT, Weiss JH. Distinctive morphological features of a subset of cortical neurons grown in the presence of basal forebrain neurons in vitro. J Neurosci 1998; 18(11):4201–4215.

    PubMed  CAS  Google Scholar 

  56. Lauder JM, Schambra UB. Morphogenetic roles of acetylcholine. Environ Health Perspect 1999; 107(Suppl 1):65–69.

    Article  PubMed  CAS  Google Scholar 

  57. Hohmann CF. A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci Biobehav Rev 2003; 27(4):351–363.

    Article  PubMed  CAS  Google Scholar 

  58. Hohmann CF, Brooks AR, Coyle JT. Neonatal lesions of the basal forebrain cholinergic neurons result in abnormal cortical development. Brain Res 1988; 470(2):253–264.

    PubMed  CAS  Google Scholar 

  59. Hohmann CF, Berger-Sweeney J. Cholinergic regulation of cortical development and plasticity. New twists to an old story. Perspect Dev Neurobiol 1998; 5(4):401–425.

    PubMed  CAS  Google Scholar 

  60. Allendoerfer KL, Shatz CJ. The subplate, a transient neocortical structure: Its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 1994; 17:185–218.

    Article  PubMed  CAS  Google Scholar 

  61. Skaliora I, Adams R, Blakemore C. Morphology and growth patterns of developing thalamocortical axons. J Neurosci 2000; 20(10):3650–3662.

    PubMed  CAS  Google Scholar 

  62. Franek M. History and the present of metabotropic GABAB receptor. Cesk Fysiol 2004; 53(3):117–124.

    PubMed  CAS  Google Scholar 

  63. Marshall FH, Jones KA, Kaupmann K et al. GABAB receptors — The first 7TM heterodimers. Trends Pharmacol Sci 1999; 20(10):396–399.

    Article  PubMed  CAS  Google Scholar 

  64. Wolff JR, Joo F, Dames W. Plasticity in dendrites shown by continuous GABA administration in superior cervical ganglion of adult rat. Nature 1978; 274(5666):72–74.

    Article  PubMed  CAS  Google Scholar 

  65. Matsutani S, Yamamoto N. GABAergic neuron-to-astrocyte signaling regulates dendritic branching in coculture. J Neurobiol 1998; 37(2):251–264.

    Article  PubMed  CAS  Google Scholar 

  66. Michler A. Involvement of GABA receptors in the regulation of neurite growth in cultured embryonic chick tectum. Int J Dev Neurosci 1990; 8(4):463–472.

    Article  PubMed  CAS  Google Scholar 

  67. Obrietan K, van den Pol AN. Growth cone calcium elevation by GABA. J Comp Neurol 1996; 372(2):167–175.

    Article  PubMed  CAS  Google Scholar 

  68. Garbin G, Pollard H, Gaiarsa JL et al. Involvement of GABAA receptors in the outgrowth of cultured hippocampal neurons. Neurosci Lett 1993; 152(1–2):150–154.

    Google Scholar 

  69. LoTurco JJ, Owens DF, Heath MJ et al. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 1995; 15(6):1287–1298.

    Article  PubMed  CAS  Google Scholar 

  70. Marty S, Berninger B, Carroll P et al. GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron 1996; 16(3):565–570.

    Article  PubMed  CAS  Google Scholar 

  71. Haydar TF, Wang F, Schwartz ML et al. Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 2000; 20(15):5764–5774.

    PubMed  CAS  Google Scholar 

  72. Nadarajah B, Parnavelas JG. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 2002; 3(6):423–432.

    Article  PubMed  CAS  Google Scholar 

  73. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 1972; 145(1):61–83.

    Article  PubMed  CAS  Google Scholar 

  74. Anderson SA, Marin O, Horn C et al. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 2001; 128(3):353–363.

    PubMed  CAS  Google Scholar 

  75. Behar TN, Schaffner AE, Tran HT et al. GABA-induced motility of spinal neuroblasts develops along a ventrodorsal gradient and can be mimicked by agonists of GABAA and GABAB receptors. J Neurosci Res 1995; 42(1):97–108.

    Article  PubMed  CAS  Google Scholar 

  76. Behar TN, Schaffner AE, Scott CA et al. Differential response of cortical plate and ventricular zone cells to GABA as a migration stimulus. J Neurosci 1998; 18(16):6378–6387.

    PubMed  CAS  Google Scholar 

  77. Behar TN, Schaffner AE, Scott CA et al. GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb Cortex 2000; 10(9):899–909.

    Article  PubMed  CAS  Google Scholar 

  78. Behar TN, Smith SV, Kennedy RT et al. GABA(B) receptors mediate motility signals for migrating embryonic cortical cells. Cereb Cortex 2001; 11(8):744–753.

    Article  PubMed  CAS  Google Scholar 

  79. Behar TN, Scott CA, Greene CL et al. Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci 1999; 19(11):4449–4461.

    PubMed  CAS  Google Scholar 

  80. Xiang Y, Li Y, Zhang Z et al. Nerve growth cone guidance mediated by G protein-coupled receptors. Nat Neurosci 2002; 5(9):843–848.

    Article  PubMed  CAS  Google Scholar 

  81. Song H, Ming G, He Z et al. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 1998; 281(5382):1515–1518.

    Article  PubMed  CAS  Google Scholar 

  82. Höpker VH, Shewan D, Tessier-Lavigne M et al. Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 1999; 401(6748):69–73.

    Article  PubMed  Google Scholar 

  83. Priest CA, Puche AC. GABAB receptor expression and function in olfactory receptor neuron axon growth. J Neurobiol 2004; 60(2):154–165.

    Article  PubMed  CAS  Google Scholar 

  84. Bird M, Owen A. Neurite outgrowth-regulating properties of GABA and the effect of serum on mouse spinal cord neurons in culture. J Anat 1998; 193 (Pt 4):503–508.

    Article  PubMed  CAS  Google Scholar 

  85. Lieske V, Bennett-Clarke CA, Rhoades RW. Effects of serotonin on neurite outgrowth from thalamic neurons in vitro. Neuroscience 1999; 90(3):967–974.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institut für Allgemeine Zoologie und Tierphysiologie, Universitaet Jena, Erbertstrasse 1, 07743, Jena, Germany

    Tina Ruediger & Juergen Bolz

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  1. Tina Ruediger
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  2. Juergen Bolz
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  1. Laboratoire de Neurobiologie du Developpement et de la Regeneration (LNDR), Centre de Neurochimie de CNRS, Strasbourg, France

    Dominique Bagnard Ph.D.

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Ruediger, T., Bolz, J. (2007). Neurotransmitters and the Development of Neuronal Circuits. In: Bagnard, D. (eds) Axon Growth and Guidance. Advances in Experimental Medicine and Biology, vol 621. Springer, New York, NY. https://doi.org/10.1007/978-0-387-76715-4_8

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