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Developmental improvement in the regularity and packing of mouse horizontal cells: Implications for mechanisms underlying mosaic pattern formation

Published online by Cambridge University Press:  06 December 2005

MARY A. RAVEN ,
STEPHANIE B. STAGG ,
HADI NASSAR  and
BENJAMIN E. REESE
MARY A. RAVEN
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara, Santa Barbara
STEPHANIE B. STAGG
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara, Santa Barbara
HADI NASSAR
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara, Santa Barbara
BENJAMIN E. REESE
Affiliation:
Neuroscience Research Institute and Department of Psychology, University of California at Santa Barbara, Santa Barbara
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Abstract

The present investigation has sought to determine whether the population of retinal horizontal cells undergoes an increase in the precision of its mosaic patterning during postnatal development, and if so, whether this increase is compatible with three different mechanistic accounts of retinal mosaic formation. Horizontal cells were labeled with antibodies to neurofilaments or calbindin at different developmental stages, and then visualized in retinal wholemounts. Multiple fields were sampled from each retina to determine horizontal cell density, while the X–Y coordinates of each cell in a field were determined. An estimate of total horizontal cell number was calculated for each retina, while the Voronoi domain regularity index and the packing factor were computed for each field. Two strains of mice showing a two-fold difference in the size of their horizontal cell population in maturity were sampled, C57BL/6J and A/J. Horizontal cell number in C57BL/6J was approximately twice that observed in A/J at all postnatal stages, with neither strain showing an effect of age on horizontal cell number. In both strains, however, the Voronoi domain regularity index and the packing factor were significantly lower at P-1 relative to later developmental stages. These results show that accounts of mosaic formation proposing the selective death of irregularly positioned cells, or the periodic occurrence of fate-determining events, are insufficient to establish the final patterning achieved by horizontal cells. Rather, they support the hypothesis that tangential dispersion enhances mosaic patterning during postnatal development.

Keywords

DifferentiationCell deathFate determinationTangential dispersionVoronoi domainRegularity indexPacking factor
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 5 , September 2005 , pp. 569 - 573
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Blanks, J.C. & Bok, D. (1977). An autoradiographic analysis of postnatal cell proliferation in the normal and degenerative mouse retina. Journal of Comparative Neurology 174, 317–328.CrossRefGoogle 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.CrossRefGoogle Scholar
Chalupa, L.M. & Jeyarasasingam, G. (1997). Development of ON and OFF ganglion cell mosaics in cat retina. In Development and Organization of the Retina: From Molecules to Function, ed. Chalupa, L.M. & Finlay, B.L., pp. 77–89. New York: Plenum Press.
Cook, J.E. (1996). Spatial properties of retinal mosaics: An empirical evaluation of some existing measures. Visual Neuroscience 13, 15–30.CrossRefGoogle Scholar
Cook, J.E. (2003). Spatial regularity among retinal neurons. In The Visual Neurosciences, ed. Chalupa, L.M. & Werner, J.S., pp. 463–477. Massachusetts: MIT Press.
Cook, J.E. & Chalupa, L.M. (2000). Retinal mosaics: New insights into an old concept. Trends in Neurosciences 23, 26–34.CrossRefGoogle Scholar
Eglen, S.J. & Willshaw, D.J. (2002). Influence of cell fate mechanisms upon retinal mosaic formation: A modelling study. Development 129, 5399–5408.CrossRefGoogle Scholar
Eglen, S.J., van Ooyen, A., & Willshaw, D.J. (2000). Lateral cell movement driven by dendritic interactions is sufficient to form retinal mosaics. Network: Computation in Neural Systems 11, 103–118.CrossRefGoogle Scholar
Farah, M.H. & Easter, S.S. (2005). Cell birth and death in the mouse retinal ganglion cell layer. Journal of Comparative Neurology 489, 120–134.CrossRefGoogle 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, 1509–1516.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
Hinds, J.W. & Hinds, P.L. (1979). Differentiation of photoreceptors and horizontal cells in the embryonic mouse retina: An electron microscopic, serial section analysis. Journal of Comparative Neurology 187, 495–512.CrossRefGoogle Scholar
Péquignot, M.O., Provost, A.C., Sallé, S., Taupin, P., Sainton, K.M., Marchant, D., Martinou, J.C., Ameisen, J.C., Jais, J.-P., & Abitbol, M. (2003). Major role of BAX in apoptosis during retinal development and in establishment of a functional postnatal retina. Developmental Dynamics 228, 231–238.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Raven, M.A. & Reese, B.E. (2002). Horizontal cell density and mosaic regularity in pigmented and albino mouse retina. Journal of Comparative Neurology 454, 168–176.CrossRefGoogle Scholar
Raven, M.A., Stagg, S.B., & Reese, B.E. (2005). Regularity and packing of the horizontal cell mosaic in different strains of mice. Visual Neuroscience 22, 461–468.CrossRefGoogle Scholar
Reese, B.E. & Galli-Resta, L. (2002). The role of tangential dispersion in retinal mosaic formation. Progress in Retinal and Eye Research 21, 153–168.CrossRefGoogle 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 of the National Academy of Sciences of the U.S.A. 92, 2494–2498.CrossRefGoogle Scholar
Reese, B.E., Necessary, B.D., Tam, P.P.L., Faulkner-Jones, B., & Tan, S.-S. (1999). Clonal expansion and cell dispersion in the developing mouse retina. European Journal of Neuroscience 11, 2965–2978.CrossRefGoogle 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
Rodieck, R.W. (1991). The density recovery profile: A method for the analysis of points in the plane applicable to retinal studies. Visual Neuroscience 6, 95–111.CrossRefGoogle Scholar
Sidman, R.L. (1961). Histogenesis of mouse retina studied with thymidine-H3. In The Structure of the Eye, ed. Smelser, G., pp. 487–505. New York: Academic Press.
Strettoi, E. & Volpini, M. (2002). Retinal organization in the bcl-2-overexpressing transgenic mouse. Journal of Comparative Neurology 446, 1–10.Google Scholar
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.CrossRefGoogle Scholar
Williams, R.W., Strom, R.C., Zhou, G., & Yan, Z. (1998). Genetic dissection of retinal development. Seminars in Cell and Developmental Biology 9, 249–255.CrossRefGoogle Scholar
Young, R.W. (1984). Cell death during differentiation of the retina in the mouse. Journal of Comparative Neurology 229, 362–373.CrossRefGoogle Scholar