Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-18T18:39:03.514Z Has data issue: false hasContentIssue false
  • English
  • Français

Assembly and disassembly of a retinal cholinergic network

Published online by Cambridge University Press:  26 July 2011

KEVIN J. FORD  and
MARLA B. FELLER
KEVIN J. FORD
Affiliation:
Department of Molecular and Cellular Biology, University of California, Berkeley, California
MARLA B. FELLER*
Affiliation:
Department of Molecular and Cellular Biology, University of California, Berkeley, California
Get access Rights & Permissions [Opens in a new window]

Abstract

In the few weeks prior to the onset of vision, the retina undergoes a dramatic transformation. Neurons migrate into position and target appropriate synaptic partners to assemble the circuits that mediate vision. During this period of development, the retina is not silent but rather assembles and disassembles a series of transient circuits that use distinct mechanisms to generate spontaneous correlated activity called retinal waves. During the first postnatal week, this transient circuit is comprised of reciprocal cholinergic connections between starburst amacrine cells. A few days before the eyes open, these cholinergic connections are eliminated as the glutamatergic circuits involved in processing visual information are formed. Here, we discuss the assembly and disassembly of this transient cholinergic network and the role it plays in various aspects of retinal development.

Keywords

Acetylcholinestarburst amacrineretinal waves
Type
Review Article
Information
Visual Neuroscience , Volume 29 , Issue 1 , January 2012 , pp. 61 - 71
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acosta, M.L., Chua, J. & Kalloniatis, M. (2007). Functional activation of glutamate ionotropic receptors in the developing mouse retina. The Journal of Comparative Neurology 500, 923–941.CrossRefGoogle ScholarPubMed
Alger, B.E. & Nicoll, R.A. (1980). Epileptiform burst afterhyperolarization: Calcium-dependent potassium potential in hippocampal CA1 pyramidal cells. Science 210, 1122–1124.CrossRefGoogle ScholarPubMed
Baldridge, W.H. (1996). Optical recordings of the effects of cholinergic ligands on neurons in the ganglion cell layer of mammalian retina. The Journal of Neuroscience 16, 5060–5072.CrossRefGoogle ScholarPubMed
Bansal, A., Singer, J.H., Hwang, B.J., Xu, W., Beaudet, A. & Feller, M.B. (2000). Mice lacking specific nicotinic acetylcholine receptor subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON and OFF circuits in the inner retina. The Journal of Neuroscience 20, 7672–7681.CrossRefGoogle ScholarPubMed
Barkis, W.B., Ford, K.J. & Feller, M.B. (2010). Non-cell-autonomous factor induces the transition from excitatory to inhibitory GABA signaling in retina independent of activity. Proceedings of the National Academy of Sciences of the United States of America 107, 22302–22307.CrossRefGoogle ScholarPubMed
Ben-Ari, Y. & Spitzer, N.C. (2010). Phenotypic checkpoints regulate neuronal development. Trends in Neurosciences 33, 485–492.CrossRefGoogle ScholarPubMed
Blankenship, A.G. & Feller, M.B. (2010). Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nature Reviews. Neuroscience 11, 18–29.CrossRefGoogle ScholarPubMed
Blankenship, A.G., Ford, K.J., Johnson, J., Seal, R.P., Edwards, R.H., Copenhagen, D.R. & Feller, M.B. (2009). Synaptic and extrasynaptic factors governing glutamatergic retinal waves. Neuron 62, 230–241.CrossRefGoogle ScholarPubMed
Blazynski, C. (1989). Displaced cholinergic, GABAergic amacrine cells in the rabbit retina also contain adenosine. Visual Neuroscience 3, 425–431.CrossRefGoogle ScholarPubMed
Bodnarenko, S.R. & Chalupa, L.M. (1993). Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature 364, 144–146.CrossRefGoogle Scholar
Bodnarenko, S.R., Jeyarasasingam, G. & Chalupa, L.M. (1995). Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity. The Journal of Neuroscience 15, 7037–7045.CrossRefGoogle ScholarPubMed
Bodnarenko, S.R., Yeung, G., Thomas, L. & McCarthy, M. (1999). The development of retinal ganglion cell dendritic stratification in ferrets. Neuroreport 10, 2955–2959.CrossRefGoogle ScholarPubMed
Brandon, C. & Criswell, M.H. (1995). Displaced starburst amacrine cells of the rabbit retina contain the 67-kDa isoform, but not the 65-kDa isoform, of glutamate decarboxylase. Visual Neuroscience 12, 1053–1061.CrossRefGoogle Scholar
Briggman, K.L., Helmstaedter, M. & Denk, W. (2011). Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183–188.CrossRefGoogle ScholarPubMed
Catsicas, M., Bonness, V., Becker, D. & Mobbs, P. (1998). Spontaneous Ca2+ transients and their transmission in the developing chick retina. Current Biology 8, 283–286.CrossRefGoogle ScholarPubMed
Chen, D., Opavsky, R., Pacal, M., Tanimoto, N., Wenzel, P., Seeliger, M.W., Leone, G. & Bremner, R. (2007). Rb-mediated neuronal differentiation through cell-cycle-independent regulation of E2f3a. PLoS Biology 5, e179.CrossRefGoogle ScholarPubMed
Cohen, E.D. (2001). Voltage-gated calcium and sodium currents of starburst amacrine cells in the rabbit retina. Visual Neuroscience 18, 799–809.CrossRefGoogle ScholarPubMed
Cook, J.E. & Chalupa, L.M. (2000). Retinal mosaics: New insights into an old concept. Trends in Neurosciences 23, 26–34.CrossRefGoogle ScholarPubMed
Coombs, J.L., Van Der List, D. & Chalupa, L.M. (2007). Morphological properties of mouse retinal ganglion cells during postnatal development. The Journal of Comparative Neurology 503, 803–814.CrossRefGoogle ScholarPubMed
Demas, J., Eglen, S.J. & Wong, R.O.L. (2003). Developmental loss of synchronous spontaneous activity in the mouse retina is independent of visual experience. The Journal of Neuroscience 23, 2851–2860.CrossRefGoogle ScholarPubMed
Dhingra, N.K., Ramamohan, Y. & Raju, T.R. (1997). Developmental expression of synaptophysin, synapsin I and syntaxin in the rat retina. Brain Research. Developmental Brain Research 102, 267–273.CrossRefGoogle ScholarPubMed
Dmitrieva, N.A., Strang, C.E. & Keyser, K.T. (2007). Expression of alpha 7 nicotinic acetylcholine receptors by bipolar, amacrine, and ganglion cells of the rabbit retina. The Journal of Histochemistry & Cytochemistry 55, 461–476.CrossRefGoogle ScholarPubMed
Drenhaus, U., Morino, P. & Veh, R.W. (2003). On the development of the stratification of the inner plexiform layer in the chick retina. The Journal of Comparative Neurology 460, 1–12.CrossRefGoogle ScholarPubMed
Elshatory, Y., Everhart, D., Deng, M., Xie, X., Barlow, R.B. & Gan, L. (2007). Islet-1 controls the differentiation of retinal bipolar and cholinergic amacrine cells. The Journal of Neuroscience 27, 12707–12720.CrossRefGoogle ScholarPubMed
Elstrott, J., Anishchenko, A., Greschner, M., Sher, A., Litke, A.M., Chichilnisky, E.J. & Feller, M.B. (2008). Direction selectivity in the retina is established independent of visual experience and cholinergic retinal waves. Neuron 58, 499–506.CrossRefGoogle ScholarPubMed
Elstrott, J. & Feller, M.B. (2010). Direction-selective ganglion cells show symmetric participation in retinal waves during development. The Journal of Neuroscience 30, 11197–11201.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr. (1983). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138–144.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Sundquist, S.J. (2010). Development of excitatory and inhibitory neurotransmitters in transitory cholinergic neurons, starburst amacrine cells, and GABAergic amacrine cells of rabbit retina, with implications for previsual and visual development of retinal ganglion cells. Visual Neuroscience 27, 19–42.CrossRefGoogle ScholarPubMed
Farajian, R., Raven, M.A., Cusato, K. & Reese, B.E. (2004). Cellular positioning and dendritic field size of cholinergic amacrine cells are impervious to early ablation of neighboring cells in the mouse retina. Visual Neuroscience 21, 13–22.CrossRefGoogle ScholarPubMed
Feldheim, D.A. & O’Leary, D.D. (2010). Visual map development: Bidirectional signaling, bifunctional guidance molecules, and competition. Cold Spring Harbor Perspectives in Biology 2, a001768.CrossRefGoogle ScholarPubMed
Feller, M.B., Butts, D.A., Aaron, H.L., Rokhsar, D.S. & Shatz, C.J. (1997). Dynamic processes shape spatiotemporal properties of retinal waves. Neuron 19, 293–306.CrossRefGoogle ScholarPubMed
Feller, M.B., Wellis, D.P., Stellwagen, D., Werblin, F.S. & Shatz, C.J. (1996). Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272, 1182–1187.CrossRefGoogle ScholarPubMed
Fischer, K.F., Lukasiewicz, P.D. & Wong, R.O. (1998). Age-dependent and cell class-specific modulation of retinal ganglion cell bursting activity by GABA. The Journal of Neuroscience 18, 3767–3778.CrossRefGoogle ScholarPubMed
Fisher, L.J. (1979). Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina. The Journal of Comparative Neurology 187, 359–372.CrossRefGoogle ScholarPubMed
Ford, K.J., Felix, A.L. & Feller, M.B. (2010). The Role of Starburst Amacrine Cells in Initiating Retinal Waves. Program No. 335.6. 2010 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience.Google Scholar
Fried, S.I., Münch, T.A. & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.CrossRefGoogle ScholarPubMed
Galli-Resta, L., Novelli, E. & Viegi, A. (2002). Dynamic microtubule-dependent interactions position homotypic neurones in regular monolayered arrays during retinal development. Development 129, 3803–3814.CrossRefGoogle ScholarPubMed
Galli-Resta, L., Novelli, E., Volpini, M. & Strettoi, E. (2000). The spatial organization of cholinergic mosaics in the adult mouse retina. The European Journal of Neuroscience 12, 3819–3822.CrossRefGoogle ScholarPubMed
Galli-Resta, L., Resta, G., Tan, S.S. & Reese, B.E. (1997). Mosaics of islet-1-expressing amacrine cells assembled by short-range cellular interactions. The Journal of Neuroscience 17, 7831–7838.CrossRefGoogle ScholarPubMed
Gavrikov, K.E., Nilson, J.E., Dmitriev, A.V., Zucker, C.L. & Mangel, S.C. (2006). Dendritic compartmentalization of chloride cotransporters underlies directional responses of starburst amacrine cells in retina. Proceedings of the National Academy of Sciences of the United States of America 103, 18793–18798.CrossRefGoogle ScholarPubMed
Godfrey, K.B. & Swindale, N.V. (2007). Retinal wave behavior through activity-dependent refractory periods. PLoS Computational Biology 3, e245.CrossRefGoogle ScholarPubMed
Godinho, L., Mumm, J.S., Williams, P.R., Schroeter, E.H., Koerber, A., Park, S.W., Leach, S.D. & Wong, R.O. (2005). Targeting of amacrine cell neurites to appropriate synaptic laminae in the developing zebrafish retina. Development 132, 5069–5079.CrossRefGoogle ScholarPubMed
Greiner, J.V. & Weidman, T.A. (1981). Histogenesis of the ferret retina. Experimental Eye Research 33, 315–332.CrossRefGoogle ScholarPubMed
Gunhan, E., Choudary, P.V., Landerholm, T.E. & Chalupa, L.M. (2002). Depletion of cholinergic amacrine cells by a novel immunotoxin does not perturb the formation of segregated on and off cone bipolar cell projections. The Journal of Neuroscience 22, 2265–2273.CrossRefGoogle Scholar
Hamassaki-Britto, D.E., Gardino, P.F., Hokoc, J.N., Keyser, K.T., Karten, H.J., Lindstrom, J.M. & Britto, L.R. (1994). Differential development of alpha-bungarotoxin-sensitive and alpha-bungarotoxin-insensitive nicotinic acetylcholine receptors in the chick retina. The Journal of Comparative Neurology 347, 161–170.CrossRefGoogle ScholarPubMed
Hanganu, I.L., Ben-Ari, Y. & Khazipov, R. (2006). Retinal waves trigger spindle bursts in the neonatal rat visual cortex. The Journal of Neuroscience 26, 6728–6736.CrossRefGoogle ScholarPubMed
Hayden, S.A., Mills, J.W. & Masland, R.M. (1980). Acetylcholine synthesis by displaced amacrine cells. Science 210, 435–437.CrossRefGoogle ScholarPubMed
Hennig, M.H., Adams, C., Willshaw, D. & Sernagor, E. (2009). Early-stage waves in the retinal network emerge close to a critical state transition between local and global functional connectivity. The Journal of Neuroscience 29, 1077–1086.CrossRefGoogle ScholarPubMed
Hinds, J.W. & Hinds, P.L. (1983). Development of retinal amacrine cells in the mouse embryo: Evidence for two modes of formation. The Journal of Comparative Neurology 213, 1–23.CrossRefGoogle ScholarPubMed
Hoover, F. & Goldman, D. (1992). Temporally correlated expression of nAChR genes during development of the mammalian retina. Experimental Eye Research 54, 561–571.CrossRefGoogle ScholarPubMed
Huberman, A.D., Feller, M.B. & Chapman, B. (2008 a). Mechanisms underlying development of visual maps and receptive fields. Annual Review of Neuroscience 31, 479–509.CrossRefGoogle ScholarPubMed
Huberman, A.D., Manu, M., Koch, S.M., Susman, M.W., Lutz, A.B., Ullian, E.M., Baccus, S.A. & Barres, B.A. (2008 b). Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59, 425–438.CrossRefGoogle ScholarPubMed
Huberman, A.D., Wei, W., Elstrott, J., Stafford, B.K., Feller, M.B. & Barres, B.A. (2009). Genetic identification of an On-Off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62, 327–334.CrossRefGoogle ScholarPubMed
Hutchins, J.B., Bernanke, J.M. & Jefferson, V.E. (1995). Acetylcholinesterase in the developing ferret retina. Experimental Eye Research 60, 113–125.CrossRefGoogle ScholarPubMed
Johnson, J., Tian, N., Caywood, M.S., Reimer, R.J., Edwards, R.H. & Copenhagen, D.R. (2003). Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. The Journal of Neuroscience 23, 518–529.CrossRefGoogle ScholarPubMed
Kaneda, M., Ito, K., Morishima, Y., Shigematsu, Y. & Shimoda, Y. (2007). Characterization of voltage-gated ionic channels in cholinergic amacrine cells in the mouse retina. Journal of Neurophysiology 97, 4225–4234.CrossRefGoogle ScholarPubMed
Kay, J.N., Roeser, T., Mumm, J.S., Godinho, L., Mrejeru, A., Wong, R.O. & Baier, H. (2004). Transient requirement for ganglion cells during assembly of retinal synaptic layers. Development 131, 1331–1342.CrossRefGoogle ScholarPubMed
Kerschensteiner, D., Morgan, J.L., Parker, E.D., Lewis, R.M. & Wong, R.O. (2009). Neurotransmission selectively regulates synapse formation in parallel circuits in vivo. Nature 460, 1016–1020.CrossRefGoogle ScholarPubMed
Kerschensteiner, D. & Wong, R.O.L. (2008). A precisely timed asynchronous pattern of ON and OFF retinal ganglion cell activity during propagation of retinal waves. Neuron 58, 851–858.CrossRefGoogle Scholar
Keyser, K.T., MacNeil, M.A., Dmitrieva, N., Wang, F., Masland, R.H. & Lindstrom, J.M. (2000). Amacrine, ganglion, and displaced amacrine cells in the rabbit retina express nicotinic acetylcholine receptors. Visual Neuroscience 17, 743–752.CrossRefGoogle ScholarPubMed
Kim, I.B., Lee, E.J., Kim, M.K., Park, D.K. & Chun, M.H. (2000). Choline acetyltransferase-immunoreactive neurons in the developing rat retina. The Journal of Comparative Neurology 427, 604–616.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Kim, I.-J., Zhang, Y., Meister, M. & Sanes, J.R. (2010). Laminar restriction of retinal ganglion cell dendrites and axons: Subtype-specific developmental patterns revealed with transgenic markers. The Journal of Neuroscience 30, 1452–1462.CrossRefGoogle ScholarPubMed
Kim, I.J., Zhang, Y., Yamagata, M., Meister, M. & Sanes, J.R. (2008). Molecular identification of a retinal cell type that responds to upward motion. Nature 452, 478–482.CrossRefGoogle ScholarPubMed
Komuro, H. & Kumada, T. (2005). Ca2+ transients control CNS neuronal migration. Cell Calcium 37, 387–393.CrossRefGoogle ScholarPubMed
Koschak, A., Reimer, D., Huber, I., Grabner, M., Glossmann, H., Engel, J. & Striessnig, J. (2001). alpha 1D (Cav1.3) subunits can form l-type Ca2+ channels activating at negative voltages. The Journal of Biological Chemistry 276, 22100–22106.CrossRefGoogle ScholarPubMed
Koulen, P., Malitschek, B., Kuhn, R., Wässle, H. & Brandstätter, J.H. (1996). Group II and group III metabotropic glutamate receptors in the rat retina: Distributions and developmental expression patterns. The European Journal of Neuroscience 8, 2177–2187.CrossRefGoogle ScholarPubMed
Lancaster, B. & Adams, P.R. (1986). Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. Journal of Neurophysiology 55, 1268–1282.CrossRefGoogle ScholarPubMed
Lee, S., Kim, K. & Zhou, Z.J. (2010). Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 68, 1159–1172.CrossRefGoogle ScholarPubMed
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E. & Masland, R.H. (1999). The shapes and numbers of amacrine cells: Matching of photofilled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. The Journal of Comparative Neurology 413, 305–326.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Martins, R.A.P. & Pearson, R.A. (2008). Control of cell proliferation by neurotransmitters in the developing vertebrate retina. Brain Research 1192, 37–60.CrossRefGoogle ScholarPubMed
Masland, R.H. (2001). The fundamental plan of the retina. Nature Neuroscience 4, 877–886.CrossRefGoogle ScholarPubMed
Masland, R.H. & Ames, A. III. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.CrossRefGoogle Scholar
Masland, R.H., Mills, J.W. & Cassidy, C. (1984). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society of London. Series B, Containing Papers of a Biological Character 223, 121–139.Google ScholarPubMed
Matsuoka, R.L., Nguyen-Ba-Charvet, K.T., Parray, A., Badea, T.C., Chédotal, A. & Kolodkin, A.L. (2011). Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 470, 259–263.CrossRefGoogle ScholarPubMed
Mehta, V. & Sernagor, E. (2006). Early neural activity and dendritic growth in turtle retinal ganglion cells. The European Journal of Neuroscience 24, 773–786.CrossRefGoogle ScholarPubMed
Meister, M., Wong, R.O., Baylor, D.A. & Shatz, C.J. (1991). Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939–943.CrossRefGoogle ScholarPubMed
Mooney, R., Penn, A.A., Gallego, R. & Shatz, C.J. (1996). Thalamic relay of spontaneous retinal activity prior to vision. Neuron 17, 863–874.CrossRefGoogle ScholarPubMed
Mumm, J.S., Williams, P.R., Godinho, L., Koerber, A., Pittman, A.J., Roeser, T., Chien, C.B., Baier, H. & Wong, R.O. (2006). In vivo imaging reveals dendritic targeting of laminated afferents by zebrafish retinal ganglion cells. Neuron 52, 609–621.CrossRefGoogle ScholarPubMed
Novelli, E., Resta, V. & Galli-Resta, L. (2005). Mechanisms controlling the formation of retinal mosaics. Progress in Brain Research 147, 141–153.CrossRefGoogle ScholarPubMed
O’Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the United States of America 86, 3414–3418.CrossRefGoogle ScholarPubMed
Ozaita, A., Petit-Jacques, J., Völgyi, B., Ho, C.S., Joho, R.H., Bloomfield, S.A. & Rudy, B. (2004). A unique role for Kv3 voltage-gated potassium channels in starburst amacrine cell signaling in mouse retina. The Journal of Neuroscience 24, 7335–7343.CrossRefGoogle ScholarPubMed
Pearson, R., Catsicas, M., Becker, D. & Mobbs, P. (2002). Purinergic and muscarinic modulation of the cell cycle and calcium signaling in the chick retinal ventricular zone. The Journal of Neuroscience 22, 7569–7579.CrossRefGoogle ScholarPubMed
Penn, A.A., Riquelme, P.A., Feller, M.B. & Shatz, C.J. (1998). Competition in retinogeniculate patterning driven by spontaneous activity. Science 279, 2108–2112.CrossRefGoogle ScholarPubMed
Putzier, I., Kullmann, P.H.M., Horn, J.P. & Levitan, E.S. (2009). Cav1.3 channel voltage dependence, not Ca2+ selectivity, drives pacemaker activity and amplifies bursts in nigral dopamine neurons. The Journal of Neuroscience 29, 15414–15419.CrossRefGoogle Scholar
Reese, B.E. & Galli-Resta, L. (2002). The role of tangential dispersion in retinal mosaic formation. Progress in Retinal & Eye Research 21, 153–168.CrossRefGoogle ScholarPubMed
Reese, B.E., Raven, M.A., Giannotti, K.A. & Johnson, P.T. (2001). Development of cholinergic amacrine cell stratification in the ferret retina and the effects of early excitotoxic ablation. Visual Neuroscience 18, 559–570.CrossRefGoogle ScholarPubMed
Roska, B. & Werblin, F. (2001). Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587.CrossRefGoogle ScholarPubMed
Sah, P. & Isaacson, J.S. (1995). Channels underlying the slow afterhyperpolarization in hippocampal pyramidal neurons: Neurotransmitters modulate the open probability. Neuron 15, 435–441.CrossRefGoogle ScholarPubMed
Sarter, M., Parikh, V. & Howe, W.M. (2009). Phasic acetylcholine release and the volume transmission hypothesis: Time to move on. Nature Reviews. Neuroscience 10, 383–390.CrossRefGoogle ScholarPubMed
Schmidt, M., Humphrey, M.F. & Wässle, H. (1987). Action and localization of acetylcholine in the cat retina. Journal of Neurophysiology 58, 997–1015.CrossRefGoogle ScholarPubMed
Sernagor, E., Eglen, S.J. & O’Donovan, M.J. (2000). Differential effects of acetylcholine and glutamate blockade on the spatiotemporal dynamics of retinal waves. The Journal of Neuroscience 20, RC56.CrossRefGoogle ScholarPubMed
Sernagor, E., Eglen, S.J. & Wong, R.O. (2001). Development of retinal ganglion cell structure and function. Progress in Retinal & Eye Research 20, 139–174.CrossRefGoogle ScholarPubMed
Sernagor, E. & Grzywacz, N.M. (1996). Influence of spontaneous activity and visual experience on developing retinal receptive fields. Current Biology 6, 1503–1508.CrossRefGoogle ScholarPubMed
Sernagor, E., Young, C. & Eglen, S.J. (2003). Developmental modulation of retinal wave dynamics: Shedding light on the GABA saga. The Journal of Neuroscience 23, 7621–7629.CrossRefGoogle ScholarPubMed
Sharma, R.K. & Ehinger, B. (1997). Mitosis in developing rabbit retina: An immunohistochemical study. Experimental Eye Research 64, 97–106.CrossRefGoogle ScholarPubMed
Singer, J.H., Mirotznik, R.R. & Feller, M.B. (2001). Potentiation of L-type calcium channels reveals nonsynaptic mechanisms that correlate spontaneous activity in the developing mammalian retina. The Journal of Neuroscience 21, 8514–8522.CrossRefGoogle ScholarPubMed
Spira, A.W., Millar, T.J., Ishimoto, I., Epstein, M.L., Johnson, C.D., Dahl, J.L. & Morgan, I.G. (1987). Localization of choline acetyltransferase-like immunoreactivity in the embryonic chick retina. The Journal of Comparative Neurology 260, 526–538.CrossRefGoogle ScholarPubMed
Spitzer, N.C., Root, C.M. & Borodinsky, L.N. (2004). Orchestrating neuronal differentiation: Patterns of Ca2+ spikes specify transmitter choice. Trends in Neurosciences 27, 415–421.CrossRefGoogle ScholarPubMed
Stacy, R.C., Demas, J., Burgess, R.W., Sanes, J.R. & Wong, R.O.L. (2005). Disruption and recovery of patterned retinal activity in the absence of acetylcholine. The Journal of Neuroscience 25, 9347–9357.CrossRefGoogle ScholarPubMed
Stacy, R.C. & Wong, R.O.L. (2003). Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina. The Journal of Comparative Neurology 456, 154–166.CrossRefGoogle ScholarPubMed
Stafford, B.K., Sher, A., Litke, A.M. & Feldheim, D.A. (2009). Spatial-temporal patterns of retinal waves underlying activity-dependent refinement of retinofugal projections. Neuron 64, 200–212.CrossRefGoogle ScholarPubMed
Stellwagen, D., Shatz, C.J. & Feller, M.B. (1999). Dynamics of retinal waves are controlled by cyclic AMP. Neuron 24, 673–685.CrossRefGoogle ScholarPubMed
Strang, C.E., Andison, M.E., Amthor, F.R. & Keyser, K.T. (2005). Rabbit retinal ganglion cells express functional alpha7 nicotinic acetylcholine receptors. American Journal of Physiology. Cell Physiology 289, C644–C655.CrossRefGoogle ScholarPubMed
Sun, C., Warland, D.K., Ballesteros, J.M., van der List, D. & Chalupa, L.M. (2008). Retinal waves in mice lacking the β2 subunit of the nicotinic acetylcholine receptor. Proceedings of the National Academy of Sciences of the United States of America 105, 13638–13643.CrossRefGoogle ScholarPubMed
Syed, M.M., Lee, S., He, S. & Zhou, Z.J. (2004 a). Spontaneous waves in the ventricular zone of developing mammalian retina. Journal of Neurophysiology 91, 1999–2009.CrossRefGoogle ScholarPubMed
Syed, M.M., Lee, S., Zheng, J. & Zhou, Z.J. (2004 b). Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. The Journal of Physiology, 560, 533–549.CrossRefGoogle ScholarPubMed
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society of London. Series B, Containing Papers of a Biological Character 223, 101–119.Google ScholarPubMed
Taylor, W.R. & Vaney, D.I. (2003). New directions in retinal research. Trends in Neurosciences 26, 379–385.CrossRefGoogle ScholarPubMed
Torborg, C.L. & Feller, M.B. (2005). Spontaneous patterned retinal activity and the refinement of retinal projections. Progress in Neurobiology 76, 213–235.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society of London. Series B, Containing Papers of a Biological Character 220, 501–508.Google ScholarPubMed
Vaney, D.I. (1990). The Mosaic of Amacrine Cells in the Mammalian Retina. Oxford: Pergamon Press. ROYAUME-UNI.Google Scholar
Vogalis, F., Furness, J.B. & Kunze, W.A. (2001). Afterhyperpolarization current in myenteric neurons of the guinea pig duodenum. Journal of Neurophysiology 85, 1941–1951.CrossRefGoogle ScholarPubMed
Voinescu, P.E., Emanuela, P., Kay, J.N. & Sanes, J.R. (2009). Birthdays of retinal amacrine cell subtypes are systematically related to their molecular identity and soma position. The Journal of Comparative Neurology 517, 737–750.CrossRefGoogle ScholarPubMed
Wang, C.-T., Blankenship, A.G., Anishchenko, A., Elstrott, J., Fikhman, M., Nakanishi, S. & Feller, M.B. (2007). GABA(A) receptor-mediated signaling alters the structure of spontaneous activity in the developing retina. The Journal of Neuroscience 27, 9130–9140.CrossRefGoogle ScholarPubMed
Wang, M.M., Janz, R., Belizaire, R., Frishman, L.J. & Sherry, D.M. (2003). Differential distribution and developmental expression of synaptic vesicle protein 2 isoforms in the mouse retina. The Journal of Comparative Neurology 460, 106–122.CrossRefGoogle ScholarPubMed
Warland, D.K., Huberman, A.D. & Chalupa, L.M. (2006). Dynamics of spontaneous activity in the fetal macaque retina during development of retinogeniculate pathways. The Journal of Neuroscience 26, 5190–5197.CrossRefGoogle ScholarPubMed
Wassle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews. Neuroscience 5, 747–757.CrossRefGoogle ScholarPubMed
Wei, W., Hamby, A.M., Zhou, K. & Feller, M.B. (2011). Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 469, 402–406.CrossRefGoogle ScholarPubMed
West Greenlee, M.H., Finley, S.K., Wilson, M.C., Jacobson, C.D. & Sakaguchi, D.S. (1998). Transient, high levels of SNAP-25 expression in cholinergic amacrine cells during postnatal development of the mammalian retina. The Journal of Comparative Neurology 394, 374–385.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Wong, R.O. (1995). Cholinergic regulation of [Ca2+]i during cell division and differentiation in the mammalian retina. The Journal of Neuroscience 15, 2696–2706.CrossRefGoogle ScholarPubMed
Wong, R.O. & Collin, S.P. (1989). Dendritic maturation of displaced putative cholinergic amacrine cells in the rabbit retina. The Journal of Comparative Neurology 287, 164–178.CrossRefGoogle ScholarPubMed
Wong, R.O., Meister, M. & Shatz, C.J. (1993). Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11, 923–938.CrossRefGoogle ScholarPubMed
Wong, W.T., Myhr, K.L., Miller, E.D. & Wong, R.O. (2000). Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity. The Journal of Neuroscience 20, 351–360.CrossRefGoogle ScholarPubMed
Wong, R.O. & Oakley, D.M. (1996). Changing patterns of spontaneous bursting activity of on and off retinal ganglion cells during development. Neuron 16, 1087–1095.CrossRefGoogle Scholar
Wong, W.T., Sanes, J.R. & Wong, R.O. (1998). Developmentally regulated spontaneous activity in the embryonic chick retina. The Journal of Neuroscience 18, 8839–8852.CrossRefGoogle ScholarPubMed
Wong, W.T. & Wong, R.O. (2001). Changing specificity of neurotransmitter regulation of rapid dendritic remodeling during synaptogenesis. Nature Neuroscience 4, 351–352.CrossRefGoogle ScholarPubMed
Xu, H.P., Chen, H., Ding, Q., Xie, Z.H., Chen, L., Diao, L., Wang, P., Gan, L., Crair, M.C. & Tian, N. (2010). The immune protein CD3zeta is required for normal development of neural circuits in the retina. Neuron 65, 503–515.CrossRefGoogle ScholarPubMed
Xu, H. & Tian, N. (2004). Pathway-specific maturation, visual deprivation, and development of retinal pathway. The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology & Psychiatry 10, 337–346.CrossRefGoogle ScholarPubMed
Yamagata, M. & Sanes, J.R. (2008). Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451, 465–469.CrossRefGoogle ScholarPubMed
Zhang, L.L., Fina, M.E. & Vardi, N. (2006 a). Regulation of KCC2 and NKCC during development: Membrane insertion and differences between cell types. The Journal of Comparative Neurology 499, 132–143.CrossRefGoogle ScholarPubMed
Zhang, L.L., Pathak, H.R., Coulter, D.A., Freed, M.A. & Vardi, N. (2006 b). Shift of intracellular chloride concentration in ganglion and amacrine cells of developing mouse retina. Journal of Neurophysiology 95, 2404–2416.CrossRefGoogle ScholarPubMed
Zheng, J.J., Lee, S. & Zhou, Z.J. (2004). A developmental switch in the excitability and function of the starburst network in the mammalian retina. Neuron 44, 851–864.CrossRefGoogle ScholarPubMed
Zheng, J., Lee, S. & Zhou, Z.J. (2006). A transient network of intrinsically bursting starburst cells underlies the generation of retinal waves. Nature Neuroscience 9, 363–371.CrossRefGoogle ScholarPubMed
Zhou, Z.J. (1998). Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina. The Journal of Neuroscience 18, 4155–4165.CrossRefGoogle ScholarPubMed
Zhou, Z.J. & Fain, G.L. (1996). Starburst amacrine cells change from spiking to nonspiking neurons during retinal development. Proceedings of the National Academy of Sciences of the United States of America 93, 8057–8062.CrossRefGoogle ScholarPubMed
Zhou, Z.J. & Zhao, D. (2000). Coordinated transitions in neurotransmitter systems for the initiation and propagation of spontaneous retinal waves. The Journal of Neuroscience 20, 6570–6577.CrossRefGoogle ScholarPubMed