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A three-dimensional analysis of the development of the horizontal cell mosaic in the rat retina: Implications for the mechanisms controlling pattern formation

Published online by Cambridge University Press:  12 April 2007

ELENA NOVELLI ,
PAOLA LEONE ,
VALENTINA RESTA  and
LUCIA GALLI-RESTA
ELENA NOVELLI
Affiliation:
Istituto di Neuroscienze CNR, Pisa, Italy
PAOLA LEONE
Affiliation:
Fondazione G.B. Bietti I.R.C.C.S., Roma, Italy
VALENTINA RESTA
Affiliation:
Istituto di Neuroscienze CNR, Pisa, Italy
LUCIA GALLI-RESTA
Affiliation:
Istituto di Neuroscienze CNR, Pisa, Italy
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Abstract

The horizontal cells are known to form a mono-layered mosaic in the adult retina, but are scattered at different retinal depths in early development. To help clarifying when and which spatial constraints appear in the relative positioning of these cells, we have performed a quantitative analysis of the three-dimensional (3D) organization of the horizontal cell mosaic at different developmental stages in the postnatal rat retina. We first analyzed the two-dimensional (2D) distribution of the horizontal cell projections onto a plane parallel to the upper retinal surface in retinal flat-mounts, and thus to the future mature horizontal cell mosaic. We found that this 2D distribution was non random since postnatal day 1 (P1), and had a subsequent stepwise improvement in regularity. This preceded the alignment of cells in a single monolayer, which was observed on P6. We then computed true horizontal cell spacing in 3D, finding non-random 3D positioning already on P1. Simulation studies showed that this order might simply derive from the 2D order observed in the projections of the cells in flat-mount, combined with their limited spread in retinal depth. Throughout the period analyzed, the relative positions of horizontal cells are in good agreement with a minimal spacing rule in which the exclusion zone corresponds to the average size of the inner core of the cell dendritic tree estimated from P1 samples. These data indicate the existence of different phases in the process of horizontal cell 3D spatial ordering, supporting the view that multiple mechanisms are involved in the development of the horizontal cell mosaic.

Keywords

Horizontal cellsMinimal spacingRetinal mosaicsDelaunay triangulation3D analysis
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 1 , January 2007 , pp. 91 - 98
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

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.Google Scholar
Cameron, D.A. & Carney, L.H. (2004). Cellular patterns in the inner retina of adult zebrafish: Quantitative analyses and a computational model of their formation. Journal of Comparative Neurology 471, 11–25.Google Scholar
Cook, J.E. & Chalupa, L.M. (2000). Retinal mosaics: New insights into an old concept. Trends in Neuroscience 23, 26–34.Google Scholar
Edqvist, P.H. & Hallbook, F. (2004). Newborn horizontal cells migrate bi-directionally across the neuroepithelium during retinal development. Development 131, 1343–1351.Google Scholar
Eglen, S.J. & Galli-Resta, L. (2006). Retinal mosaics. In Retinal development, eds. Sernagor, E., Eglen, S.J., Harris, W. & Wong, R.O.L., pp. 193–207. Cambridge: Cambridge University Press.
Eglen, S.J., Galli-Resta, L. & Reese, B.E. (2003). Theoretical models of retinal mosaic formation. In Modelling Neuronal Development, ed. van Ooyen, A., pp. 133–150. Massachusetts: MIT Press.
Eglen, S.J., van Ooyen, A. & Willshaw, D.J. (2000). Lateral cell movement driven by dendritic interactions is sufficient to form retinal mosaics. Network 11, 103–118.Google Scholar
Eysel, U.T., Peichl, L. & Wassle, H. (1985). Dendritic plasticity in the early postnatal feline retina: Quantitative characteristics and sensitive period. Journal of Comparative Neurology 242, 134–145.Google Scholar
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.Google Scholar
Freeman, M. (1997). Cell determination strategies in the Drosophila eye. Development 124, 261–270.Google Scholar
Galli-Resta, L. (1998). Patterning the vertebrate retina: The early assembly of retinal mosaics. Seminars in Cell Developmental Biology 9, 279–284.Google Scholar
Galli-Resta, L. (2000). Local, possibly contact-mediated signalling restricted to homotypic neurons controls the regular spacing of cells within the cholinergic arrays in the developing rodent retina. Development 127, 1499–1508.Google Scholar
Galli-Resta, L. (2001). Assembling the vertebrate retina: Global patterning from short-range cellular interactions. Neuroreport 12, A103–A106.Google Scholar
Galli-Resta, L. (2002). Putting neurons in the right places: Local interactions in the genesis of retinal architecture. Trends in Neuroscience 25, 638–643.Google Scholar
Galli-Resta, L. & Ensini, M. (1996). An intrinsic limit between genesis and death of individual neurons in the developing retinal ganglion cell layer. Journal of Neuroscience 16, 2318–2324.Google Scholar
Galli-Resta, L., Novelli, E., Kryger, Z., Jacobs, G. & Reese, B. (1999). Modelling the mosaic organization of rod and cone photoreceptors with a minimal spacing rule. European Journal of Neuroscience 11, 1438–1446.Google Scholar
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.Google Scholar
Galli-Resta, L., Resta, G., Tan, S.-S. & Reese, B. (1997). Mosaics of Islet-1 expressing amacrine cells assembled by short range cellular interactions. Journal of Neuroscience 17, 7831–7838.Google Scholar
Grumnbaum, B. & Shephard, G.C. (1989). Tilings and patterns. An introduction. New York: Freeman and Co.
Jeyarasasingam, G., Snider, C.J., Ratto, G.-M. & Chalupa, L.M. (1998). Activity regulated cell death contributes to the formation of ON and OFF α ganglion cell mosaics. Journal of Comparative Neurology 394, 335–343.Google Scholar
Lin, B., Wang, S.W. & Masland, R.H. (2004). Retinal ganglion cell type, size, and spacing can be specified independent of homotypic dendritic contacts. Neuron 43, 475–485.Google Scholar
McCabe, K.L., Gunther, E.C. & Reh, T.A. (1999). The development of the pattern of retinal ganglion cells in the chick retina: Mechanisms that control differentiation. Development 126, 5713–5724.Google Scholar
Pasteels, B., Rogers, J., Blachier, F. & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 1–16.Google Scholar
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683–685.Google Scholar
Rapaport, D.H. (2006). Retinal neurogenesis. In Retinal development, eds. Sernagor, E., Eglen, S.J., Harris, W. & Wong, R.O.L., pp. 30–58. Cambridge: Cambridge University Press.
Raven, M.A., Eglen, S.J., Ohab, J.J. & Reese, B.E. (2003). Determinants of the exclusion zone in dopaminergic amacrine cell mosaics. Journal of Comparative Neurology 461, 123–136.Google Scholar
Raven, M.A., Stagg, S.B., Nassar, H. & Reese, B.E. (2005a). Developmental improvement in the regularity and packing of mouse horizontal cells: implications for mechanisms underlying mosaic pattern formation. Visual Neuroscience 22, 569–573.Google Scholar
Raven, M.A., Stagg, S.B. & Reese, B.E. (2005b). Regularity and packing of the horizontal cell mosaic in different strains of mice. Visual Neuroscience 22, 461–468.Google Scholar
Reese, B., Necessary, B., Tam, P., Faulkner-Jones, B. & Tan, S. (1999). Clonal expansion and cell dispersion in the developing mouse retina. European Journal of Neuroscience 11, 2965–2978.Google Scholar
Reese, B.E. & Colello, R.J. (1992). Neurogenesis in the retinal ganglion cell layer of the rat retina. Neuroscience 46, 419–429.Google 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.Google Scholar
Reese, B.E., Harvey, A.R. & Tan, S.-S. (1995). Radial and tangential dispersion patterns in the mouse retina are cell-class specific. Proceedings National Academy of Science, USA 92, 2494–2498.Google Scholar
Reese, B.E., Raven, M.A. & Stagg, S.B. (2005). Afferents and homotypic neighbors regulate horizontal cell morphology, connectivity, and retinal coverage. Journal of Neuroscience 25, 2167–2175.Google Scholar
Resta, V., Novelli, E., Di Virgilio, F. & Galli-Resta, L. (2005). Neuronal death induced by endogenous extracellular ATP in retinal cholinergic neuron density control. Development 132, 2873–2882.Google Scholar
Scheibe, R., Schnitzer, J., Röhrenbeck, J., Wohlrab, F. & Reichenbach, A. (1995). Development of A-type (axonless) horizontal cells in the rabbit retina. Journal of Comparative Neurology 354, 438–458.Google Scholar
Shaw, G. & Weber, K. (1984). The intermediate filament complement of the retina: A comparison between different mammalian species. European Journal of Cell Biology 33, 95–104.Google Scholar
Tucker, R., Binder, L. & Matus, A. (1989). Differential localization of the high- and low-molecular weight variants of MAP2 in the developing retina. Brain Research 466, 313–318.Google Scholar
Tucker, R.P. & Matus, A.I. (1988). Microtubule-associated proteins characteristic of embryonic brain are found in the adult mammalian retina. Developmental Biology 130, 423–434.Google Scholar
Tyler, M.J., Carney, L.H. & Cameron, D.A. (2005). Control of cellular pattern formation in the vertebrate inner retina by homotypic regulation of cell-fate decisions. Journal of Neuroscience 25, 4565–4576.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.Google Scholar
Wässle, H., Peichl, L. & Boycott, B.B. (1983). A spatial analysis of on- and off-ganglion cells in the cat retina. Vision Research 23, 1151–1160.Google Scholar
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society of London B 200, 441–461.Google Scholar
Wong, R.O. & Godinho, L. (2003). Development of the vertebrate retina. In The Visual Neurosciences, Vol. 1, eds. Chalupa, L.M. & Werner, J.S., pp. 77–93. Massachusetts: MIT Press.