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Random spatial patterning of cone bipolar cell mosaics in the mouse retina

Published online by Cambridge University Press:  09 January 2017

PATRICK W. KEELEY ,
JASON J. KIM ,
SAMMY C.S. LEE ,
SILKE HAVERKAMP  and
BENJAMIN E. REESE
PATRICK W. KEELEY
Affiliation:
Neuroscience Research Institute, University of California, Santa Barbara, CA 93106-5060
JASON J. KIM
Affiliation:
Neuroscience Research Institute, University of California, Santa Barbara, CA 93106-5060
SAMMY C.S. LEE
Affiliation:
Department of Ophthalmology and Save Sight Institute, University of Sydney, Sydney, NSW 2000, Australia
SILKE HAVERKAMP
Affiliation:
Institute of Cellular and Molecular Anatomy, Goethe-University, Frankfurt am Main 60590, Germany
BENJAMIN E. REESE*
Affiliation:
Neuroscience Research Institute, University of California, Santa Barbara, CA 93106-5060 Department of Psychological & Brain Sciences, University of California, Santa Barbara, CA 93106-9660
*
*Address correspondence to: B.E. Reese, Neuroscience Research Institute, University of California, Santa Barbara, CA 93106-5060. E-mail: breese@psych.ucsb.edu
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Abstract

Retinal bipolar cells spread their dendritic arbors to tile the retinal surface, extending them to the tips of the dendritic fields of their homotypic neighbors, minimizing dendritic overlap. Such uniform nonredundant dendritic coverage of these populations would suggest a degree of spatial order in the properties of their somal distributions, yet few studies have examined the patterning in retinal bipolar cell mosaics. The present study examined the organization of two types of cone bipolar cells in the mouse retina, the Type 2 cells and the Type 4 cells, and compared their spatial statistical properties with those of the horizontal cells and the cholinergic amacrine cells, as well as to random simulations of cells matched in density and constrained by soma size. The Delauney tessellation of each field was computed, from which nearest neighbor distances and Voronoi domain areas were extracted, permitting a calculation of their respective regularity indexes (RIs). The spatial autocorrelation of the field was also computed, from which the effective radius and packing factor (PF) were determined. Both cone bipolar cell types were found to be less regular and less efficiently packed than either the horizontal cells or cholinergic amacrine cells. Furthermore, while the latter two cell types had RIs and PFs in excess of those for their matched random simulations, the two types of cone bipolar cells had spatial statistical properties comparable to random distributions. An analysis of single labeled cone bipolar cells revealed dendritic arbors frequently skewed to one side of the soma, as would be expected from a randomly distributed population of cells with dendrites that tile. Taken together, these results suggest that, unlike the horizontal cells or cholinergic amacrine cells which minimize proximity to one another, cone bipolar cell types are constrained only by their physical size.

Keywords

Regularity indexPacking factorVoronoi domainNearest neighborEffective radiusExclusion zoneDendritic coverage
Type
Research Article
Information
Visual Neuroscience , Volume 34 , 2017 , E002
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

Supported by NIH grant EY-019968.

References

Breuninger, T., Puller, C., Haverkamp, S., & Euler, T. (2011). Chromatic bipolar cell pathways in the mouse retina. Journal of Neuroscience 31, 6504–6517.CrossRefGoogle ScholarPubMed
Cook, J.E. (1996). Spatial properties of retinal mosaics: An empirical evaluation of some existing measures. Visual Neuroscience 13, 15–30.Google Scholar
Cook, J.E. (1998). Getting to grips with neuronal diversity: What is a neuronal type? In Development and Organization of the Retina, eds. Chalupa, L., & Finlay, B., pp. 91–120. New York: Plenum Press.Google Scholar
DeVries, S.H., Li, W., & Saszik, S. (2006). Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50, 735–748.Google Scholar
Dunn, F.A. & Wong, R.O. (2012). Diverse strategies engaged in establishing stereotypic wiring patterns among neurons sharing a common input at the visual system’s first synapse. Journal of Neuroscience 32, 10306–10317.Google Scholar
Eglen, S.J. & Willshaw, D.J. (2002). Influence of cell fate mechanisms upon retinal mosaic formation: A modelling study. Development 129, 5399–5408.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
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. Journal of Neuroscience 17, 7831–7838.Google Scholar
Haverkamp, S., Specht, D., Majumdar, S., Zaidi, N.F., Brandstätter, J.H., Wasco, W., Wässle, H., & Tom Dieck, S. (2008). Type 4 OFF cone bipolar cells of the mouse retina express calsenilin and contact cones as well as rods. Journal of Comparative Neurology 507, 1087–1101.Google Scholar
Helmstaedter, M., Briggman, K.L., Turaga, S.C., Jain, V., Seung, H.S., & Denk, W. (2013). Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500, 168–174.Google Scholar
Huang, L., Max, M., Margolskee, R.F., Su, H., Masland, R.H., & Euler, T. (2003). The G protein subunit Gg13 is co-expressed with Gao and Gb3 in retinal on bipolar cells. Journal of Comparative Neurology 455, 1–10.Google Scholar
Huckfeldt, R.M., Schubert, T., Morgan, J.L., Godinho, L., Di Cristo, G., Huang, Z.J., & Wong, R.O.L. (2009). Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nature Neuroscience 12, 35–43.Google Scholar
Kay, J.N., Chu, M.W., & Sanes, J.R. (2012). MEGF10 and MEGF11 mediate homotypic interactions required for mosaic spacing of retinal neurons. Nature 483, 465–469.Google Scholar
Keeley, P.W., Kim, J.J., St. John, A.J., & Reese, B.E. (2016). Variation in cellular density is not predictive of the variation in mosaic regularity for the VGluT3+ amacrine cell population. Association for Research in Vision and Ophthalmology Abstracts, 1780.Google Scholar
Keeley, P.W., Madsen, N.R., St. John, A.J., & Reese, B.E. (2014c). Programmed cell death of retinal cone bipolar cells is independent of afferent or target control. Developmental Biology 394, 191–196.Google Scholar
Keeley, P.W. & Reese, B.E. (2010b). Role of afferents in the differentiation of bipolar cells in the mouse retina. Journal of Neuroscience 30, 1677–1685.Google Scholar
Keeley, P.W. & Reese, B.E. (2014). The patterning of retinal horizontal cells: Normalizing the regularity index enhances the detection of genomic linkage. Frontiers in Neuroanatomy 8, 113.Google Scholar
Keeley, P.W., Whitney, I.E., Madsen, N.R., St. John, A.J., Borhanian, S., Leong, S.A., Williams, R.W., & Reese, B.E. (2014a). Independent genomic control of neuronal number across retinal cell types. Developmental Cell 30, 103–109.Google Scholar
Keeley, P.W., Whitney, I.E., Raven, M.A., & Reese, B.E. (2007). Dendritic spread and functional coverage of starburst amacrine cells. Journal of Comparative Neurology 505, 539–546.Google Scholar
Keeley, P.W., Whitney, I.E., & Reese, B.E. (2017). Genomic control of retinal cell number: Challenges, protocol, and results. Methods in Molecular Biology 1488, 365–390.Google Scholar
Keeley, P.W., Zhou, C., Lu, L., Williams, R.W., Melmed, S., & Reese, B.E. (2014b). Pituitary tumor transforming gene 1 regulates the patterning of retinal mosaics. Proceedings of the National Academy of Sciences of the United States of America 111, 9295–9300.Google Scholar
Kouyama, N. & Marshak, D.W. (1997). The topographical relationship between two neuronal mosaics in the short wavelength-sensitive system of the primate retina. Visual Neuroscience 14, 159–167.Google Scholar
Lee, S.C., Cowgill, E.J., Al-Nabulsi, A., Quinn, E.J., Evans, S.M., & Reese, B.E. (2011). Homotypic regulation of neuronal morphology and connectivity in the mouse retina. Journal of Neuroscience 31, 14126–14133.Google Scholar
Lindstrom, S.H., Ryan, D.G., Shi, J., & DeVries, S.H. (2014). Kainate receptor subunit diversity underlying response diversity in retinal off bipolar cells. Journal of Physiology 592, 1457–1477.Google Scholar
Masland, R.H. (2012). The neuronal organization of the retina. Neuron 76, 266–280.Google Scholar
Misgeld, T., Kerschensteiner, M., Bareyre, F.M., Burgess, R.W., & Lichtman, J.W. (2007). Imaging axonal transport of mitochondria in vivo . Nature Methods 4, 559–561.Google Scholar
Morgan, J.L., Dhingra, A., Vardi, N., & Wong, R.O. (2006). Axons and dendrites originate from neuroepithelial-like processes of retinal bipolar cells. Nature Neuroscience 9, 85–92.Google 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.Google 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.Google Scholar
Raven, M.A., Stagg, S.B., Nassar, H., & Reese, B.E. (2005b). 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. (2005a). Regularity and packing of the horizontal cell mosaic in different strains of mice. Visual Neuroscience 22, 461–468.Google Scholar
Reese, B.E. (2008). Mosaics, tiling and coverage by retinal neurons. In Vision, eds. Masland, R.H., & Albright, T., pp. 439–456. Oxford: Elsevier.Google Scholar
Reese, B.E. & Keeley, P.W. (2015). Design principles and developmental mechanisms underlying retinal mosaics. Biological Reviews. 90, 854–876.Google Scholar
Reese, B.E., Keeley, P.W., Lee, S.C., & Whitney, I.E. (2011). Developmental plasticity of dendritic morphology and the establishment of coverage and connectivity in the outer retina. Developmental Neurobiology 71, 1273–1285.Google 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.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
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.Google Scholar
Saszik, S. & DeVries, S.H. (2012). A mammalian retinal bipolar cell uses both graded changes in membrane voltage and all-or-nothing Na+ spikes to encode light. Journal of Neuroscience Methods 32, 297–307.Google Scholar
Seung, H.S. & Sumbul, U. (2014). Neuronal cell types and connectivity: Lessons from the retina. Neuron 83, 1262–1272.Google Scholar
Shekhar, K., Lapan, S.W., Whitney, I.E., Tran, N.M., Macosko, E.Z., Kowalczyk, M., Adiconis, X., Levin, J.Z., Nemesh, J., Goldman, M., McCarroll, S.A., Cepko, C.L., Regev, A., & Sanes, J.R. (2016). Comprehensive classification of retinal bipolar neurons by single-cell transcriptomics. Cell 166, 1308–1323.Google Scholar
Wässle, H., Puller, C., Müller, F., & Haverkamp, S. (2009). Cone contacts, mosaics and territories of bipolar cells in the mouse retina. Journal of Neuroscience 29, 106–117.Google Scholar
Whitney, I.E., Keeley, P.W., St. John, A.J., Kautzman, A.G., Kay, J.N., & Reese, B.E. (2014). Sox2 regulates cholinergic amacrine cell positioning and dendritic stratification in the retina. Journal of Neuroscience 34, 10109–10121.Google Scholar
Whitney, I.E., Raven, M.A., Keeley, P.W., & Reese, B.E. (2008). Spatial patterning of cholinergic amacrine cells in the mouse retina. Journal of Comparative Neurology 508, 1–12.Google Scholar
Wong, G.T., Ruiz-Avila, L., & Margolskee, R.F. (1999). Directing gene expression to gustducin-positive taste receptor cells. Journal of Neuroscience 19, 5802–5809.Google Scholar