Neurotransmitters and neurotrophins

doi:10.1017/CBO9780511541629.008

6 - Neurotransmitters and neurotrophins

Published online by Cambridge University Press: 22 August 2009

Edited by

Bill Harris and

Rachael A. Pearson: Affiliation:
Developmental Biology Unit, Institute of Child Health, University College London, 30 Guilford Street, London WC1N 1EH, UK
Evelyne Sernagor: Affiliation:
University of Newcastle upon Tyne
Stephen Eglen: Affiliation:
University of Cambridge
Bill Harris: Affiliation:
University of Cambridge
Rachel Wong: Affiliation:
Washington University, St Louis

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Summary

Introduction

In addition to intrinsic control mechanisms (see Chapter 5 and Cepko et al., 1996), the production of neurons by progenitor cells and the determination of their fate are regulated via an array of diffusible factors, two families of which are considered in this chapter: neurotransmitters and neurotrophins. Neurotrophins are now known to play an essential role in both the formation and the maintenance of the nervous system throughout development and adult life. There is growing evidence that besides their role as molecules mediating communication between nerve cells in the mature nervous system, a variety of both slow and fast neurotransmitters also play important roles during neuronal development. This chapter reviews recent evidence that demonstrates that a number of non-synaptic neurotransmitter release mechanisms, together with many neurotransmitters and their receptors, are present in the developing retina prior to the onset of synapse formation and that these early neurotransmitters act to modulate a range of events in neural development. Their precise mechanisms of action are still being elucidated but, as described here, the ability to modulate [Ca2+]i is one feature common to these early neurotransmitter systems, and is thought to underlie a number of their developmental actions. It is becoming clear that both neurotransmitters and neurotrophins play important regulatory roles in the early stages of retinal development, including the modulation of proliferation, differentiation, cell survival and circuit formation.

Type: Chapter
Information: Retinal Development , pp. 99 - 125

DOI: https://doi.org/10.1017/CBO9780511541629.008 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2006

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References

Abe, T., Sugihara, H., Nawa, H.et al. (1992). Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca2+ signal transduction. J. Biol. Chem., 267, 13361–8Google Scholar PubMed

Allcorn, S., Catsicas, M. and Mobbs, P. (1996). Developmental expression and self-regulation of Ca2+ entry via AMPA/KA receptors in the embryonic chick retina. Eur. J. Neurosci., 8, 2499–510CrossRef Google Scholar PubMed

Angelini, C., Costa, M., Morescalchi, F.et al. (1998). Muscarinic drugs affect cholinesterase activity and development of eye structures during early chick development. Eur. J. Histochem., 42(4), 309–20Google Scholar PubMed

Aramori, I. and Nakanishi, S. (1992). Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron, 8, 757–65CrossRef Google Scholar PubMed

Attwell, D., Barbour, B. and Szatkowski, M. (1993). Nonvesicular release of neurotransmitter. Neuron, 11, 401–7CrossRef Google Scholar PubMed

Barbacid, M. (1994). The Trk family of neurotrophin receptors. J. Neurobiol., 25, 1386–403CrossRef Google Scholar PubMed

Barde, Y. A. (1989). Trophic factors and neuronal survival. Neuron, 2, 1525–34CrossRef Google Scholar PubMed

Barker, J. L., Behar, T., Li, Y. X.et al. (1998). GABAergic cells and signals in CNS development. Perspect. Dev. Neurobiol., 5, 305–22Google Scholar PubMed

Baughman, R. W. and Bader, C. R. (1977). Biochemical characterization and cellular localization of the cholinergic system in the chicken retina. Brain Res., 138, 469–85CrossRef Google Scholar PubMed

Bennett, M. V., Contreras, J. E., Bukauskas, F. F. and Saez, J. C. (2003). New roles for astrocytes: gap junction hemichannels have something to communicate. Trends Neurosci., 26, 610–17CrossRef Google Scholar PubMed

Bergmann, M., Grabs, D. and Rager, G. (1999). Developmental expression of dynamin in the chick retinotectal system. J. Histochem. Cytochem., 47, 1297–306CrossRef Google Scholar PubMed

Bergmann, M., Grabs, D. and Rager, G. (2000). Expression of pre-synaptic proteins is closely correlated with the chronotopic pattern of axons in the retinotectal system of the chick. J. Comp. Neurol., 418, 361–3723.0.CO;2-U>CrossRef Google Scholar

Berridge, M. J. (1995). Calcium signaling and cell proliferation. BioEssays, 17, 491–500CrossRef Google Scholar

Bliss, T. V. and Collingridge, G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31–9CrossRef Google Scholar PubMed

Bovolenta, P., Frade, J. M., Marti, E.et al. (1996). Neurotrophin-3 antibodies disrupt the normal development of the chick retina. J. Neurosci., 16, 4402–10CrossRef Google Scholar PubMed

Brändle, U., Guenther, E., Irrle, C. and Wheeler-Schilling, T. H. (1998). Gene expression of the P2x receptors in the rat retina. Brain Res. Mol. Brain Res., 59(2), 269–72CrossRef Google Scholar PubMed

Burnashev, N., Monyer, H., Seeburg, P. H. and Sakmann, B. (1992). Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron, 8, 189–98CrossRef Google Scholar PubMed

Burnstock, G. (2004). Cotransmisson. Curr. Opin. Pharmacol., 4(1), 47–52CrossRef Google Scholar

Cai, L., Hayes, N. L. and Nowakowski, R. S. (1997). Synchrony of clonal cell proliferation and contiguity of clonally related cells: production of mosaicism in the ventricular zone of developing mouse neocortex. J. Neurosci., 17, 2088–100CrossRef Google Scholar PubMed

Catsicas, M. and Mobbs, P. (2001). GABAb receptors regulate chick retinal calcium waves. J. Neurosci., 21, 897–910CrossRef Google Scholar PubMed

Catsicas, M., Bonness, V., Becker, D. and Mobbs, P. (1998). Spontaneous Ca2+ transients and their transmission in the developing chick retina. Curr. Biol., 8, 283–6CrossRef Google Scholar PubMed

Catsicas, M., Allcorn, S. and Mobbs, P. (2001). Early activation of Ca2+-permeable AMPA receptors reduces neurite outgrowth in embryonic chick retinal neurons. J. Neurobiol., 49, 200–11CrossRef Google Scholar

Cauley, K., Agranoff, B. W. and Goldman, D. (1990). Multiple nicotinic acetylcholine receptor genes are expressed in goldfish retina and tectum. J. Neurosci., 10, 670–83CrossRef Google Scholar PubMed

Caviness, V. S. Jr.Takahashi, T. and Nowakowski, R. S. (1995). Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci., 18, 379–383CrossRef Google Scholar PubMed

Cepko, C. L., Austin, C. P., Yang, X., Alexiades, M. and Ezzeddine, D. (1996). Cell fate determination in the vertebrate retina. Proc. Natl. Acad. Sci. U. S. A., 93, 589–95CrossRef Google Scholar PubMed

Chalazonitis, A., Rothman, T. P., Chen, J.et al. (1994). Neurotrophin-3 induces neural crest-derived cells from fetal rat gut to develop in vitro as neurons or glia. J. Neurosci., 14 (11 Pt 1), 6571–84CrossRef Google Scholar PubMed

Chalazonitis, A., Rothman, T. P., Chen, J. and Gershon, M. D. (1998). Age-dependent differences in the effects of GDNF and NT-3 on the development of neurons and glia from neural crest-derived precursors immunoselected from the fetal rat gut: expression of GFRalpha-1 in vitro and in vivo. Dev. Biol., 204(2), 385–406CrossRef Google Scholar PubMed

Cherubini, E., Gaiarsa, J. L. and Ari, Ben Y. (1991). GABA: an excitatory transmitter in early postnatal life. Trends Neurosci., 14, 515–19CrossRef Google Scholar PubMed

Cotrina, M. L., Kang, J., Lin, J. H.et al. (1998). Astrocytic gap junctions remain open during ischemic conditions. J. Neurosci., 18(7), 2520–37CrossRef Google Scholar PubMed

Cotrina, M. L., Lin, J. H., Lopez-Garcia, J. C., Naus, C. C. and Nedergaard, M. (2000). ATP-mediated glia signaling. J. Neurosci., 20(8), 2835–44CrossRef Google Scholar PubMed

Cristovao, A. J., Oliveira, C. R. and Carvalho, C. M. (2002a). Expression of AMPA/kainate receptors during development of chick embryo retina cells: in vitro versus in vivo studies. Int. J. Dev. Neurosci., 20(1), 1–9CrossRef Google Scholar

Cristovao, A. J., Oliveira, C. R. and Carvalho, C. M. (2002b). Expression of functional N-methyl-D-aspartate receptors during development of chick embryo retina cells: in vitro versus in vivo studies. Brain Res. Mol. Brain Res., 99(2), 125–33CrossRef Google Scholar

da Costa Calaza, K., Hokoc, J. N. and Gardino, P. F. (2000). Neurogenesis of GABAergic cells in the click retina. Int. J. Dev. Neurosci., 18(8), 721–6CrossRef Google Scholar

Das, I., Sparrow, J. R., Lin, M. I.et al. (2000). Trk C signaling is required for retinal progenitor cell proliferation. J. Neurosci., 20(8), 2887–95. Erratum in J. Neurosci. 2000 July 15, 201(14), 5574CrossRef Google Scholar PubMed

Rosa, E. J., Bondy, C. A., Hernandez-Sanchez, C.et al. (1994). Insulin and insulin-like growth factor system components gene expression in the chicken retina from early neurogenesis until late development and their effect on neuroepithelial cells. Eur. J. Neurosci., 6(12), 1801–10CrossRef Google Scholar PubMed

Demarque, M., Represa, A., Becq, H.et al. (2002). Paracrine intercellular communication by a Ca2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron, 36, 1051–61CrossRef Google Scholar PubMed

Dolmetsch, R. E., Lewis, R. S., Goodnow, C. C. and Healy, J. I. (1997). Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature, 386(6627), 855–8. Eratum in Nature 1997 July 17, 388(6639), 308CrossRef Google Scholar PubMed

Dolmetsch, R. E., Xu, K. and Lewis, R. S. (1998). Calcium oscillations increase the efficiency and specificity of gene expression. Nature, 392, 933–6CrossRef Google Scholar PubMed

Duarte, C. B., Santos, P. F., Sanchez-Prieto, J. and Carvalho, A. P. (1996). On-line detection of glutamate release from cultured chick retinospheroids. Vis. Res., 36, 1867–72CrossRef Google Scholar PubMed

Fischer, A. J., McKinnon, L. A., Nathanson, N. M. and Stell, W. K. (1998). Identification and localization of muscarinic acetylcholine receptors in the ocular tissues of the chick. J. Comp. Neurol., 392, 273–843.0.CO;2-Z>CrossRef Google Scholar PubMed

Frade, J. M., Rodriguez-Tebar, A. and Barde, Y. A. (1996). Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature, 383, 166–8CrossRef Google Scholar PubMed

Frade, J. M., Bovolenta, P., Martinez-Morales, J. R.et al. (1997). Control of early cell death by BDNF in the chick retina. Development, 124, 3313–20Google Scholar PubMed

Frade, J. M., Bovolenta, P. and Rodriguez-Tebar, A. (1999). Neurotrophins and other growth factors in the generation of retinal neurons. Microsc. Res. Tech., 45, 243–513.0.CO;2-S>CrossRef Google Scholar PubMed

Frambach, D. A. and Misfeldt, D. S. (1983). Furosemide-sensitive Cl transport in embryonic chicken retinal pigment epithelium. Am. J. Physiol., 244, F679–85Google Scholar PubMed

Frederick, J. M. (1987). The emergence of GABA-accumulating neurons during retinal histogenesis in the embryonic chick. Exp. Eye Res., 45, 933–45CrossRef Google Scholar PubMed

Gonzalez-Hoyuela, M., Barbas, J. A. and Rodriguez-Tebar, A. (2001). The autoregulation of retinal ganglion cell number. Development, 128(1), 117–24Google Scholar PubMed

Grabs, D., Bergmann, M. and Rager, G. (2000). Developmental expression of amphiphysin in the retinotectal system of the chick: from mRNA to protein. Eur. J. Neurosci., 12, 1545–53CrossRef Google Scholar PubMed

Greenwood, D., Yao, W. P. and Housley, G. D. (1997). Expression of the P2X2 receptor subunit of the ATP-gated ion channel in the retina. NeuroReport, 8, 1083–8CrossRef Google Scholar PubMed

Greferath, U., Grunert, U., Muller, F. and Wassle, H. (1994). Localization of GABAA receptors in the rabbit retina. Cell Tissue Res., 276(2), 295–307Google Scholar PubMed

Greka, A., Lipton, S. A. and Zhang, D. (2000). Expression of GABAC receptor rho1 and rho2 subunits during development of the mouse retina. Eur. J. Neurosci., 12(10), 3575–82CrossRef Google Scholar

Gu, X. and Spitzer, N. C. (1993). Low-threshold Ca2+ current and its role in spontaneous elevations of intracellular Ca2+ in developing Xenopus neurons. J. Neurosci., 13, 4936–48CrossRef Google Scholar PubMed

Gu, X. and Spitzer, N. C. (1995). Distinct aspects of neuronal differentiation encoded by frequency of spontaneous Ca2+ transients. Nature, 375, 784–7CrossRef Google Scholar PubMed

Gu, X., Olson, E. C. and Spitzer, N. C. (1994). Spontaneous neuronal calcium spikes and waves during early differentiation. J. Neurosci., 14, 6325–35CrossRef Google Scholar PubMed

Hamassaki-Britto, D. E., Gardino, P. F., Hokoc, J. N.et al. (1994). Differential development of alpha-bungarotoxin-sensitive and alpha-bungarotoxin-insensitive nicotinic acetylcholine receptors in the chick retina. J. Comp. Neurol., 347, 161–70CrossRef Google Scholar PubMed

Hapner, S. J., Boeshore, K. L., Large, T. H. and Lefcort, F. (1998). Neural differentiation promoted by truncated trkC receptors in collaboration with p75(NTR). Dev. Biol., 201, 90–100CrossRef Google Scholar

Harada, C., Harada, T., Nakamura, K.et al. (2006). Effect of p75 (NTR) on the regulation of naturally occurring cell death and retinal ganglion cell number in the mouse eye. Dev. Biol., 290(1), 57–65CrossRef Google Scholar PubMed

Harrison, P. K., Falugi, C., Angelini, C. and Whitaker, M. J. (2002). Muscarinic signaling affects intracellular calcium concentration during the first cell cycle of sea urchin embryos. Cell Calcium, 31(6), 289–97CrossRef Google Scholar PubMed

Haydar, T. F., Wang, F., Schwartz, M. L. and Rakic, P. (2000). Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J. Neurosci., 20, 5764–74CrossRef Google Scholar PubMed

Hayden, S. A., Mills, J. W. and Masland, R. M. (1980). Acetylcholine synthesis by displaced amacrine cells. Science, 210(4468), 435–7CrossRef Google Scholar PubMed

Johnson, J., Tian, N., Caywood, M. S.et al. (2003). Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J. Neurosci., 23, 518–29CrossRef Google Scholar PubMed

Kalcheim, C., Barde, Y. A., Thoenen, H. and Douarin, N. M. (1987). In vivo effect of brain-derived neurotrophic factor on the survival of developing dorsal root ganglion cells. EMBO J. 6(10), 2871–3Google Scholar PubMed

Karne, A., Oakley, D. M. and Wong, G. K. and Wong, R. O. (1997). Immunocytochemical localization of GABA, GABAA receptors, and synapse-associated proteins in the developing and adult ferret retina. Vis. Neurosci., 14(6), 1097–108CrossRef Google Scholar PubMed

Katz, B. and Miledi, R. (1977). Transmitter leakage from motor nerve endings. Proc. R. Soc. London B Biol. Sci., 196(1122), 59–72CrossRef Google Scholar PubMed

Keyser, K. T., Hughes, T. E., Whiting, P. J., Lindstrom, J. M. and Karten, H. J. (1988). Cholinoceptive neurons in the retina of the chick: an immunohistochemical study of the nicotinic acetylcholine receptors. Vis. Neurosci., 1(4), 349–66CrossRef Google Scholar PubMed

Kim, I. B., Park, D. K., Oh, S. J. and Chun, M. H. (1999). Horizontal cells of the rat retina show choline acetyltransferase- and vesicular acetylcholine transporter-like immunoreactivities during early postnatal developmental stages. Neurosci. Lett., 253(2), 83–6CrossRef Google Scholar

Kim, I. B., Lee, E. J., Kim, M. K., Park, D. K. and Chun, M. H. (2000). Choline acetyltransferase-immunoreactive neurons in the developing rat retina. J. Comp. Neurol., 427(4), 604–163.0.CO;2-C>CrossRef Google Scholar PubMed

Komuro, H.Rakic, P. (1993). Modulation of neuronal migration by NMDA receptors. Science, 260(5104), 95–7CrossRef Google Scholar PubMed

Komuro, H. and Rakic, P. (1996). Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron, 17(2), 275–85CrossRef Google Scholar PubMed

Komuro, H. and Rakic, P. (1998). Orchestration of neuronal migration by activity of ion channels, neurotransmitter receptors, and intracellular Ca2+ fluctuations. J. Neurobiol., 37(1), 110–30. Review3.0.CO;2-C>CrossRef Google Scholar PubMed

Laasberg, T. (1990). Ca2+-mobilizing receptors of gastrulating chick embryo. Comp. Biochem. Physiol. C, 97(1), 9–12CrossRef Google Scholar PubMed

Layer, P. G. (1991). Cholinesterases during development of the avian nervous system. Cell. Mol. Neurobiol., 11(1), 7–33. ReviewCrossRef Google Scholar PubMed

Lewin, G. R. and Barde, Y. A. (1996). Physiology of the neurotrophins. Annu. Rev. Neurosci., 19, 289–317CrossRef Google Scholar PubMed

Liets, L. C. and Chalupa, L. M. (2001). Glutamate-mediated responses in developing retinal ganglion cells. Prog. Brain Res., 134, 1–16CrossRef Google Scholar PubMed

Turco, Lo J. J., Owens, D. F., Heath, M. J., Davis, M. B. and Kriegstein, A. R. (1995). GABA and glutamate depolarise cortical progenitor cells and inhibit DNA synthesis. Neuron, 15(6), 1287–98Google Scholar

Maric, D., Liu, Q. Y., Grant, G. M.et al. (2000). Functional ionotropic glutamate receptors emerge during terminal cell division and early neuronal differentiation of rat neuroepithelial cells. J. Neurosci. Res., 61(6), 652–623.0.CO;2-J>CrossRef Google Scholar PubMed

Maric, D., Liu, Q., Maric, I.et al. (2001). GABA expression dominates neuronal lineage progression in the embryonic rat neocortex and facilitates neurite outgrowth via GABAA autoreceptor/Cl− channels. J. Neurosci., 21(7), 2343–60CrossRef Google Scholar

McKinnon, L. A. and Nathanson, N. M. (1995). Tissue-specific regulation of muscarinic acetylcholine receptor expression during embryonic development. J. Biol. Chem., 270(35), 20 636–42CrossRef Google Scholar PubMed

Mitchell, C. H. (2001). Release of ATP by a human retinal pigment epithelial cell line: potential for autocrine stimulation through subretinal space. J. Physiol., 534, 193–202CrossRef Google Scholar PubMed

Moll, V., Weick, M., Milenkovic, I.et al. (2002). P2Y receptor-mediated stimulation of Müller glial DNA synthesis. Invest. Ophthalmol. Vis. Sci., 43(3), 766–73Google Scholar PubMed

Morita, M., Higuchi, C., Moto, T.et al. (2003). Dual regulation of calcium oscillation in astrocytes by growth factors and pro-inflammatory cytokines via the mitogen-activated protein kinase cascade. J. Neurosci., 23(34), 10 944–52CrossRef Google Scholar PubMed

Murphy, S. N. and Miller, R. J. (1989). Two distinct quisqualate receptors regulate Ca2+ homeostasis in hippocampal neurons in vitro. Mol. Pharmacol., 35(5), 671–80Google Scholar PubMed

Nadler, L. S., Rosoff, M. L., Hamilton, S. E.et al. (1999). Molecular analysis of the regulation of muscarinic receptor expression and function. Life Sci., 64(6–7), 375–9. ReviewCrossRef Google Scholar PubMed

Naruoka, H., Kojima, R., Ohasa, M., Layer, P. G. and Saito, T. (2003). Transient muscarinic calcium mobilisation in transdifferentiating as in reaggregating embryonic chick retinae. Brain Res. Dev. Brain Res., 134(2), 233–44CrossRef Google Scholar

Newman, E. A. (2001). Propagation of intercellular calcium waves in retinal astrocytes and Müller cells. J. Neurosci., 21(7), 2215–23CrossRef Google Scholar PubMed

Nishi, S., Minota, S. and Karczmar, A. G. (1974). Primary afferent neurons: the ionic mechanism for GABA-mediated depolarisation. Neuropharmacology, 13, 215–19CrossRef Google Scholar

Ockel, M., Lewin, G. R. and Barde, Y. A. (1996). In vivo effects of neurotrophin-3 during sensory neurogenesis. Development, 122(1), 301–7Google Scholar PubMed

Ohmasa, M. and Saito, T. (2004). GABAA-receptor-mediated increase in intracellular Ca2+ concentration in the regenerating retina of adult newt. Neurosci. Res., 49, 219–27CrossRef Google Scholar PubMed

Oppenheim, R. W., Prevette, D., Yin, Q. W., Collins, F. and MacDonald, J. (1991). Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science, 251(5001), 1616–18CrossRef Google Scholar PubMed

Owens, D. F. and Kriegstein, A. R. (1998). Patterns of intracellular calcium fluctuation in precursor cells of the neocortical ventricular zone. J. Neurosci., 18(14), 5374–88CrossRef Google Scholar PubMed

Pannicke, T., Fischer, W., Biedermann, B.et al. (2000). P2X7 receptors in Müller glial cells from the human retina. J. Neurosci., 20, 5965–72CrossRef Google Scholar PubMed

Pearson, R., Catsicas, M., Becker, D. and Mobbs, P. (2002). Purinergic and muscarinic modulation of the cell cycle and calcium signaling in the chick retinal ventricular zone. J. Neurosci., 22, 7569–79CrossRef Google Scholar PubMed

Pearson, R. A., Catsicas, M., Becker, D. L. et al. (2004). Ca2+ signaling and gap junction coupling within and between pigment epithelium and neural retina in the developing chick. Eur. J. Neurosci., 19, 2435–45CrossRef Google Scholar

Pearson, R. A., Dale, N., Llaudet, E. and Mobbs, P. (2005a). ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron, 46, 731–44CrossRef Google Scholar

Pearson, R. A., Luneborg, N. L., Becker, D. and Mobbs, P. (2005b). Gap junctions modulate interkinetic nuclear migration in retinal progenitor cells. J. Neurosci., 25(46), 10803–14CrossRef Google Scholar

Pellegrini-Giampietro, D. E., Bennett, M. V. and Zukin, R. S. (1992). Are Ca2+-permeable kainate/AMPA receptors more abundant in immature brain?Neurosci. Lett., 144(1–2), 65–9CrossRef Google Scholar PubMed

Prada, C., Puga, J., Perez-Mendez, L., Lopez, R. and Ramirez, G. (1991). Spatial and temporal patterns of neurogenesis in the chick retina. Eur. J. Neurosci., 3, 559–69CrossRef Google Scholar PubMed

Pruss, R. M., Akeson, R. L., Racke, M. M. and Wilburn, J. L. (1991). Agonist-activated cobalt uptake identifies divalent cation-permeable kainate receptors on neurons and glial cells. Neuron, 7(3), 509–18CrossRef Google Scholar PubMed

Purves, D., Snider, W. D. and Voyvodic, J. T. (1988). Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature, 336(6195), 123–8. ReviewCrossRef Google Scholar PubMed

Rajan, I., Witte, S. and Cline, H. T. (1999). NMDA receptor activity stabilizes pre-synaptic retinotectal axons and post-synaptic optic tectal cell dendrites in vivo. J. Neurobiol., 38(3), 357–683.0.CO;2-#>CrossRef Google Scholar

Rakic, P. and Komuro, H. (1995). The role of receptor/channel activity in neuronal cell migration. J. Neurobiol., 26(3), 299–315CrossRef Google Scholar PubMed

Reichling, D. B., Kyrozis, A., Wang, J. and MacDermott, A. B. (1994). Mechanisms of GABA and glycine depolarisation-induced calcium transients in rat dorsal horn neurons. J. Physiol., 476, 411–21CrossRef Google Scholar

Rodríguez-Tébar, A., Dechant, G. and Barde, Y. A. (1990). Binding of brain-derived neurotrophic factor to the nerve growth factor receptor. Neuron, 4(4), 487–92CrossRef Google Scholar PubMed

Rodríguez-Tébar, A., Dechant, G., Gotz, R. and Barde, Y. A. (1992). Binding of neurotrophin-3 to its neuronal receptors and interactions with nerve growth factor and brain-derived neurotrophic factor. EMBO J. 11(3), 917–22Google Scholar PubMed

Rodríguez-Tébar, A., Rosa, E. J. and Arribas, A. (1993). Neurotrophin-3 receptors in the developing chicken retina. Eur. J. Biochem., 211(3), 789–94CrossRef Google Scholar PubMed

Rorig, B. and Grantyn, R. (1994). Ligand- and voltage-gated ion channels are expressed by embryonic mouse retinal neurones. NeuroReport, 5(10), 1197–200CrossRef Google Scholar PubMed

Rudolph, U., Crestani, F. and Mohler, H. (2001). GABA(A) receptor sub-types: dissecting their pharmacological functions. Trends Pharmacol. Sci., 22(4), 188–94. ReviewCrossRef Google Scholar

Sakaki, Y., Fukuda, Y. and Yamashita, M. (1996). Muscarinic and purinergic Ca2+ mobilisations in the neural retina of early embryonic chick. Int. J. Dev. Neurosci., 14, 691–9CrossRef Google Scholar

Sanches, G., Alencar, L. S. and Ventura, A. L. (2002). ATP induces proliferation of retinal cells in culture via activation of PKC and extracellular signal-regulated kinase cascade. Int. J. Dev. Neurosci., 20, 21–7CrossRef Google Scholar PubMed

Santella, L. (1998). The role of calcium in the cell cycle: facts and hypotheses. Biochem. Biophys. Res. Commun., 244(2), 317–24. ReviewCrossRef Google Scholar PubMed

Santella, L., Kyozuka, K., Riso, L. and Carafoli, E. (1998). Calcium, protease action, and the regulation of the cell cycle. Cell Calcium, 23(2–3), 123–30. ReviewCrossRef Google Scholar PubMed

Santos, A. A., Medina, S. V., Sholl-Franco, A. and Araujo, E. G. (2003). PMA decreases the proliferation of retinal cells in vitro: the involvement of acetylcholine and BDNF. Neurochem. Int., 42, 73–80CrossRef Google Scholar PubMed

Bredariol, Santos A. and Hamassaki-Britto, D. (2001). Ionotropic glutamate receptors during the development of the chick retina. J. Comp. Neurol., 441, 58–70CrossRef Google Scholar

Schwartz, E. A. (1987). Depolarisation without calcium can release gamma-aminobutyric acid from a retinal neuron. Science, 238(4825), 350–5CrossRef Google Scholar

Segal, M. and Barker, J. L. (1984). Rat hippocampal neurons in culture: properties of GABA-activated Cl− ion conductance. J. Neurophysiol., 51(3), 500–15CrossRef Google Scholar PubMed

Shatz, C. J. (1996). Emergence of order in visual system development. J. Physiol. Paris, 90(3–4), 141–50. ReviewCrossRef Google Scholar PubMed

Sherry, D. M., Wang, M. M., Bates, J. and Frishman, L. J. (2003). Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J. Comp. Neurol., 465(4), 480–98CrossRef Google Scholar PubMed

Short, A. D., Winston, G. P. and Taylor, C. W. (2000). Different receptors use inositol trisphosphate to mobilize Ca(2+) from different intracellular pools. Biochem. J., 351(Pt 3), 683–6CrossRef Google Scholar PubMed

Somahano, F., Roberts, P. J. and Lopez-Colome, A. M. (1988). Maturational changes in retinal excitatory amino acid receptors. Dev. Brain Res., 42, 59–67CrossRef Google Scholar

Spitzer, N. C., Debaca, R. C., Allen, K. A. and Holliday, J. (1993). Calcium dependence of differentiation of GABA immunoreactivity in spinal neurons. J. Comp. Neurol., 337(1), 168–75CrossRef Google Scholar PubMed

Stout, C. E., Costantin, J. L., Naus, C. C., and Charles, A. C. (2002). Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J. Biol. Chem., 277(12), 10 482–8CrossRef Google Scholar PubMed

Sugioka, M. and Yamashita, M. (2003). Calcium signaling to nucleus via store-operated system during cell cycle in retinal neuroepithelium. Neurosci. Res., 45, 447–58CrossRef Google Scholar PubMed

Sugioka, M., Fukuda, Y. and Yamashita, M. (1996). Ca2+ responses to ATP via purinoceptors in the early embryonic chick retina. J. Physiol., 493(3), 855–63CrossRef Google Scholar PubMed

Sugioka, M., Fukuda, Y. and Yamashita, M. (1998). Development of glutamate-induced intracellular Ca2+ rise in the embryonic chick retina. J. Neurobiol., 34(2), 113–253.0.CO;2-5>CrossRef Google Scholar PubMed

Sugioka, M., Zhou, W. L., Hofmann, H. D. and Yamashita, M. (1999). Involvement of P2 purinoceptors in the regulation of DNA synthesis in the neural retina of chick embryo. Int. J. Dev. Neurosci., 17, 135–44CrossRef Google Scholar PubMed

Syed, M. M., Lee, S., He, S. and Zhou, Z. J. (2004a). Spontaneous waves in the ventricular zone of developing mammalian retina. J. Neurophysiol., 91(5), 1999–2009CrossRef Google Scholar

Syed, M. M., Lee, S., Zheng, J. and Zhou, Z. J. (2004b). Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J. Physiol., 560(2), 533–49CrossRef Google Scholar

Wada, E., Wada, K., Boulter, J.et al. (1989). Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J. Comp. Neurol., 284(2), 314–35CrossRef Google Scholar PubMed

Warr, O., Takahashi, M. and Attwell, D. (1999). Modulation of extracellular glutamate concentration in rat brain slices by cystine-glutamate exchange. J. Physiol., 514(3), 783–93CrossRef Google Scholar PubMed

Weissman, T. A., Riquelme, P. A., Ivic, L., Flint, A. C., and Kriegstein, A. R. (2004). Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron, 43(5), 647–61CrossRef Google Scholar PubMed

Wheeler-Schilling, T. H., Marquordt, K., Kohler, K., Guenther, E. and Jabs, R. (2001). Identification of purinergic receptors in retinal ganglion cells. Brain Res. Mol. Brain Res., 92(1–2), 177–80CrossRef Google Scholar PubMed

Whitaker, M. and Larman, M. G. (2001). Calcium and mitosis. Semin. Cell Dev. Biol., 12(1), 53–8CrossRef Google Scholar PubMed

Wong, R. O. (1995a). Cholinergic regulation of [Ca2+]ⅰ during cell division and differentiation in the mammalian retina. J. Neurosci., 15(4), 2696–706CrossRef Google Scholar

Wong, R. O. (1995b). Effects of glutamate and its analogs on intracellular calcium levels in the developing retina. Vis. Neurosci., 12(5), 907–17CrossRef Google Scholar

Wong, R. O. (1999). Retinal waves: stirring up a storm. Neuron, 24(3), 493–5CrossRef Google Scholar PubMed

Wong, W. T., Sanes, J. R. and Wong, R. O. (1998). Developmentally regulated spontaneous activity in the embryonic chick retina. J. Neurosci., 18(21), 8839–52CrossRef Google Scholar PubMed

Wong, W. T., Myhr, K. L., Miller, E. D. and Wong, R. O. (2000). Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity. J. Neurosci., 20(1), 351–60CrossRef Google Scholar PubMed

Wu, G. Y. and Cline, H. T. (1998). Stabilisation of dendritic arbor structure in vivo by CaMKII. Science, 279(5348), 222–6CrossRef Google Scholar

Yamashita, M. and Fukuda, Y. (1993). Calcium channels and GABA receptors in the early embryonic chick retina. J. Neurobiol., 24(12), 1600–14CrossRef Google Scholar PubMed

Yamashita, M., Yoshimoto, Y. and Fukuda, Y. (1994). Muscarinic acetylcholine responses in the early embryonic chick retina. J. Neurobiol., 25(9), 1144–53CrossRef Google Scholar PubMed

Yang, H. and Kunes, S. (2004). Nonvesicular release of acetylcholine is required for axon targeting in the Drosophila visual system. Proc. Natl. Acad. Sci. U. S. A., 101(42), 15 213–8CrossRef Google Scholar PubMed

Zhang, L., Spigelman, I. and Carlen, P. L. (1991). Development of GABA-mediated, chloride-dependent inhibition in CA1 pyramidal neurones of immature rat hippocampal slices. J. Physiol., 444, 25–49CrossRef Google Scholar PubMed

Zheng, J. Q. (2000). Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature, 403(6765), 89–93CrossRef Google Scholar PubMed

Zheng, J. Q., Felder, M., Connor, J. A. and Poo, M. M. (1994). Turning of nerve growth cones induced by neurotransmitters. Nature, 368(6467), 140–4CrossRef Google Scholar PubMed