Design principles and developmental mechanisms underlying retinal mosaics

Biological Reviews

Volumn 90, Issue 3, 2015, Pages 854-876

  Reese, Benjamin E ^a   Keeley, Patrick W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autocorrelation; Coverage; Dendritic field; Effective radius; Nearest neighbour; Packing factor; Patterning; Regularity; Tiling; Voronoi domain

Indexed keywords

INVERTEBRATA; MAMMALIA; VERTEBRATA;

ANATOMY AND HISTOLOGY; ANIMAL; CENTRAL NERVOUS SYSTEM; GENETICS; GROWTH, DEVELOPMENT AND AGING; INVERTEBRATE; MUTATION; PHYSIOLOGY; RETINA; VERTEBRATE;

ANIMALS; CENTRAL NERVOUS SYSTEM; INVERTEBRATES; MUTATION; RETINA; VERTEBRATES;

EID: 84937119320     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/brv.12139     Document Type: Article

References (108)

1. Allison, W. T., Barthel, L. K., Skebo, K. M., Takechi, M., Kawamura, S. & Raymond, P. A. (2010). Ontogeny of cone photoreceptor mosaics in zebrafish. Journal of Comparative Neurology 518, 4182-4195.
2. de Andrade, G. B., Long, S. S., Fleming, H., Li, W. & Fuerst, P. G. (2014). DSCAM localization and function at the mouse cone synapse. Journal of Comparative Neurology 522, 2609-2633.
3. Bleckert, A., Schwartz, G. W., Turner, M. H., Rieke, F. & Wong, R. O. (2014). Visual space is represented by nonmatching topographies of distinct mouse retinal ganglion cell types. Current Biology 24, 310-315.
4. Chen, S.-K., Chew, K. S., McNeill, D. S., Keeley, P. W., Ecker, J. L., Mao, B., Pahlberg, J., Kim, B., Lee, S. C. S., Fox, M., et al. (2013). Apoptosis regulates ipRGC spacing necessary for rods and cones to drive circadian photoentrainment. Neuron 77, 503-515.
5. Cheng, P. L. & Poo, M. M. (2012). Early events in axon/dendrite polarization. Annual Review of Neuroscience 35, 181-201.
6. Chung, K., Wallace, J., Kim, S. Y., Kalyanasundaram, S., Andalman, A. S., Davidson, T. J., Mirzabekov, J. J., Zalocusky, K. A., Mattis, J., Denisin, A. K., et al. (2013). Structural and molecular interrogation of intact biological systems. Nature Genetics 497, 332-337.
7. Cook, J. E. (1996). Spatial properties of retinal mosaics: an empirical evaluation of some existing measures. Visual Neuroscience 13, 15-30.
8. Dacey, D. M. (1993). The mosaic of midget ganglion cells in the human retina. Journal of Neuroscience 13, 5334-5355.
9. Dacey, D. M. & Petersen, M. R. (1992). Dendritic field size and morphology of midget and parasol ganglion cells of the human retina. Proceedings of the National Academy of Sciences of the United States of America 89, 9666-9670.
10. Davenport, C. M., Detwiler, P. B. & Dacey, D. M. (2007). Functional polarity of dendrites and axons of primate A1 amacrine cells. Visual Neuroscience 24, 449-457.
11. Dekkers, M. P. & Barde, Y. A. (2013). Developmental biology. Programmed cell death in neuronal development. Science 340, 39-41.
12. Diggle, P. J. (2002). Statistical Analysis of Spatial Point Patterns. Second Edition (). Edward Arnold, London.
13. Ding, Q., Chen, H., Xie, X., Libby, R. T., Tian, N. & Gan, L. (2009). BARHL2 differentially regulates the development of retinal amacrine and ganglion neurons. Journal of Neuroscience 29, 3992-4003.
14. 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 Methods 32, 10306-10317.
15. Eglen, S. J. & Galli-Resta, L. (2006). Retinal mosaics. In Retinal Development (eds E. Sernagor, S. Eglen, B. Harris and R. Wong ), pp. 193-207. Cambridge University Press, Cambridge.
16. Eglen, S. J., Lofgreen, D. D., Raven, M. A. & Reese, B. E. (2008). Analysis of spatial relationships in three dimensions: tools for the study of nerve cell patterning. BMC Neuroscience 9, 68.
17. Eglen, S. J., Raven, M. A., Tamrazian, E. & Reese, B. E. (2003). Dopaminergic amacrine cells in the inner nuclear layer and ganglion cell layer comprise a single functional retinal mosaic. Journal of Comparative Neurology 466, 343-355.
18. Eglen, S. J. & Willshaw, D. J. (2002). Influence of cell fate mechanisms upon retinal mosaic formation: a modelling study. Development 129, 5399-5408.
19. Emoto, K. (2012). Signaling mechanisms that coordinate the development and maintenance of dendritic fields. Current Opinion in Neurobiology 22, 805-811.
20. Euler, T., Detwiler, P. B. & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845-852.
21. Eysel, U. T., Peichl, L. & Wässle, H. (1985). Dendritic plasticity in the early postnatal feline retina: quantitative characteristics and sensitive period. Journal of Comparative Neurology 242, 134-145.
22. 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.
23. Fuerst, P. G., Bruce, F., Tian, M., Wei, W., Elstrott, J., Feller, M. B., Erskine, L., Singer, J. H. & Burgess, R. W. (2009). DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina. Neuron 64, 484-497.
24. Fuerst, P. G. & Burgess, R. W. (2009). Adhesion molecules in establishing retinal circuitry. Current Opinion in Neurobiology 19, 389-394.
25. Fuerst, P. G., Koizumi, A., Masland, R. H. & Burgess, R. W. (2008). Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451, 470-474.
26. Galli-Resta, L. & Novelli, E. (2000). The effects of natural cell loss on the regularity of the retinal cholinergic arrays. Journal of Neuroscience 20, RC60 (61-65).
27. Galli-Resta, L., Novelli, E., Kryger, Z., Jacobs, G. H. & Reese, B. E. (1999). Modelling the mosaic organization of rod and cone photoreceptors with a minimal-spacing rule. European Journal of Neuroscience 11, 1461-1469.
28. 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.
29. 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.
30. Garrett, A. M. & Burgess, R. W. (2011). Candidate molecular mechanisms for establishing cell identity in the developing retina. Developmental Neurobiology 71, 1258-1272.
31. Garrett, A. M., Tadenev, A. L. & Burgess, R. W. (2012). DSCAMs: restoring balance to developmental forces. Frontiers in Molecular Neuroscience 5, 86.
32. Grimes, W. N., Zhang, J., Graydon, C. W., Kachar, B. & Diamond, J. S. (2010). Retinal parallel processors: more than 100 independent microcircuits operate within a single interneuron. Neuron 65, 873-885.
33. Grueber, W. B. & Sagasti, A. (2010). Self-avoidance and tiling: mechanisms of dendrite and axon spacing. Cold Spring Harbor Perspectives in Biology 2, a001750.
34. Guillemot, F. (2007). Cell fate specification in the mammalian telencephalon. Progress in Neurobiology 83, 37-52.
35. 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.
36. Hore, V. R., Troy, J. B. & Eglen, S. J. (2012). Parasol cell mosaics are unlikely to drive the formation of structured orientation maps in primary visual cortex. Visual Neuroscience 29, 283-299.
37. Huberman, A. D., Manu, M., Koch, S. M., Susman, M. W., Lutz, A. B., Ullian, E. M., Baccus, S. A. & Barres, B. A. (2008). Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59, 425-438.
38. 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.
39. Hughes, M. E., Bortnick, R., Tsubouchi, A., Bäumer, P., Kondo, M., Uemura, T. & Schmucker, D. (2007). Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54, 417-427.
40. Jan, Y. N. & Jan, L. Y. (2010). Branching out: mechanisms of dendritic arborization. Nature Reviews Neuroscience 11, 316-328.
41. Janssen-Bienhold, U., Trümpler, J., Hilgen, G., Schultz, K., Müller, L. P., Sonntag, S., Dedek, K., Dirks, P., Willecke, K. & Weiler, R. (2009). Connexin57 is expressed in dendro-dendritic and axo-axonal gap junctions of mouse horizontal cells and its distribution is modulated by light. Journal of Comparative Neurology 513, 363-374.
42. Kanamori, T., Kanai, M. I., Dairyo, Y., Yasunaga, K., Morikawa, R. K. & Emoto, K. (2013). Compartmentalized calcium transients trigger dendrite pruning in Drosophila sensory neurons. Science 340, 1475-1478.
43. 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.
44. Keeley, P. W., Luna, G., Fariss, R. N., Skyles, K. A., Madsen, N. R., Raven, M. A., Poché, R. A., Swindell, E. C., Jamrich, M., Oh, E. C., et al. (2013). Development and plasticity of outer retinal circuitry following genetic removal of horizontal cells. Journal of Neuroscience 33, 17847-17862.
45. Keeley, P. W. & Reese, B. E. (2010a). Morphology of dopaminergic amacrine cells in the mouse retina: independence from homotypic interactions. Journal of Comparative Neurology 518, 1220-1231.
46. 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.
47. Keeley, P. W., Sliff, B. J., Lee, S. C., Fuerst, P. G., Burgess, R. W., Eglen, S. J. & Reese, B. E. (2012). Neuronal clustering and fasciculation phenotype in Dscam- and Bax-deficient mouse retinas. Journal of Comparative Neurology 520, 1349-1364.
48. 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.
49. Kiecker, C. & Lumsden, A. (2012). The role of organizers in patterning the nervous system. Annual Review of Neuroscience 35, 347-367.
50. 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.
51. Kirby, M. A. & Chalupa, L. M. (1986). Retinal crowding alters the morphology of alpha ganglion cells. Journal of Comparative Neurology 251, 532-541.
52. Kise, Y. & Schmucker, D. (2013). Role of self-avoidance in neuronal wiring. Current Opinion in Neurobiology 23, 983-989.
53. Kram, Y. A., Mantey, S. & Corbo, J. C. (2010). Avian cone photoreceptors tile the retina as five independent, self-organizing mosaics. PLoS ONE 5, e8992.
54. Kryger, Z., Galli-Resta, L., Jacobs, G. H. & Reese, B. E. (1998). The topography of rod and cone photoreceptors in the retina of the ground squirrel. Visual Neuroscience 15, 685-691.
55. 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.
56. Lee, S. & Zhou, Z. J. (2006). The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51, 787-799.
57. Lefebvre, J. L., Kostadinov, D., Chen, W. V., Maniatis, T. & Sanes, J. R. (2012). Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488, 517-521.
58. 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.
59. Linden, R. & Reese, B. E. (2006). Programmed cell death. In Retinal Development (eds E. Sernagor, S. Eglen, B. Harris and R. Wong ), pp. 208-241. Cambridge University Press, Cambridge.
60. Livet, J., Weissman, T. A., Kang, H., Draft, R. W., Lu, J., Bennis, R. A., Sanes, J. R. & Lichtman, J. W. (2007). Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450, 56-62.
61. Matsuoka, R. L., Jiang, Z., Samuels, I. S., Nguyen-Ba-Charvet, K. T., Sun, L. O., Peachey, N. S., Chedotal, A., Yau, K. W. & Kolodkin, A. L. (2012). Guidance-cue control of horizontal cell morphology, lamination, and synapse formation in the mammalian outer retina. Journal of Neuroscience 32, 6859-6868.
62. Matthews, B. J., Kim, M. E., Flanagan, J. J., Hattori, D., Clemens, J. C., Zipursky, S. L. & Grueber, W. B. (2007). Dendrite self-avoidance is controlled by Dscam. Cell 129, 593-604.
63. 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.
64. Millard, S. S. & Zipursky, S. L. (2008). Dscam-mediated repulsion controls tiling and self-avoidance. Current Opinion in Neurobiology 18, 84-89.
65. 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.
66. Novelli, E., Resta, V. & Galli-Resta, L. (2005). Mechanisms controlling the formation of retinal mosaics. Progress in Brain Research 147, 141-153.
67. Parrish, J. Z., Emoto, K., Kim, M. D. & Jan, Y. N. (2007). Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annual Review of Neuroscience 30, 399-423.
68. Perry, V. H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683-685.
69. Poché, R. A., Raven, M. A., Kwan, K. M., Furuta, Y., Behringer, R. R. & Reese, B. E. (2008). Somal positioning and dendritic growth of horizontal cells are regulated by interactions with homotypic neighbors. European Journal of Neuroscience 27, 1607-1614.
70. 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.
71. 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.
72. Raven, M. A., Stagg, S. B., Nassar, H. & Reese, B. E. (2005). Developmental improvement in the regularity and packing of mouse horizontal cells: implications for mechanisms underlying mosaic pattern formation. Visual Neuroscience 22, 569-573.
73. Raymond, P. A. & Barthel, L. K. (2004). A moving wave patterns the cone photoreceptor mosaic array in the zebrafish retina. International Journal of Developmental Biology 48, 935-945.
74. Reese, B. E. (2008). Mosaics, tiling and coverage by retinal neurons. In The Senses: Vision (eds R. H. Masland and T. Albright ), pp. 439-456. Elsevier, Oxford.
75. Reese, B. E. (2012). Retinal mosaics: pattern formation driven by ocal interactions between homotypic neighbors. Frontiers in Neural Circuits 6, 24.
76. 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.
77. 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.
78. 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.
79. 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.
80. 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.
81. Rockhill, R. L., Euler, T. & Masland, R. H. (2000). Spatial order within but not between types of retinal neurons. Proceedings of the National Academy of Sciences of the United States of America 97, 2303-2307.
82. 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.
83. Roorda, A., Metha, A. B., Lennie, P. & Williams, D. R. (2001). Packing arrangement of the three cone classes in primate retina. Vision Research 41, 1291-1306.
84. Sanes, J. R. & Zipursky, S. L. (2010). Design principles of insect and vertebrate visual systems. Neuron 66, 15-36.
85. Schmucker, D. & Chen, B. (2009). Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. Genes and Development 23, 147-156.
86. Shelley, J., Dedek, K., Schubert, T., Feigenspan, A., Schultz, K., Hombach, S., Willecke, K. & Weiler, R. (2006). Horizontal cell receptive fields are reduced in connexin57-deficient mice. European Journal of Neuroscience 23, 3176-3186.
87. Soba, P., Zhu, S., Emoto, K., Younger, S., Yang, S.-J., Yu, H.-H., Lee, T., Jan, L. Y. & Jan, Y.-N. (2007). Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization. Neuron 54, 403-416.
88. Solecki, D. J. (2012). Sticky situations: recent advances in control of cell adhesion during neuronal migration. Current Opinion in Neurobiology 22, 791-798.
89. Stacy, R. C. & Wong, R. O. L. (2003). Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina. Journal of Comparative Neurology 456, 154-166.
90. Stenkamp, D. L. & Cameron, D. A. (2002). Cellular pattern formation in the retina: retinal regeneration as a model system. Molecular Vision 8, 280-293.
91. Stenkamp, D. L., Powers, M. K., Carney, L. H. & Cameron, D. A. (2001). Evidence for two distinct mechanisms of neurogenesis and cellular pattern formation in regenerated goldfish retinas. Journal of Comparative Neurology 431, 363-381.
92. Strettoi, E. & Volpini, M. (2002). Retinal organization in the bcl-2-overexpressing transgenic mouse. Journal of Comparative Neurology 446, 1-10.
93. Sugimura, K., Shimono, K., Uemura, T. & Mochizuki, A. (2007). Self-organizing mechanism for development of space-filling neuronal dendrites. PLoS Computational Biology 3, e212.
94. Sun, L. O., Jiang, Z., Rivlin-Etzion, M., Hand, R., Brady, C. M., Matsuoka, R. L., Yau, K.-W., Feller, M. B. & Kolodkin, A. L. (2013). On and off retinal circuit assembly by divergent molecular mechanisms. Science 342, 1241974.
95. Tsukamoto, Y. & Omi, N. (2013). Functional allocation of synaptic contacts in microcircuits from rods via rod bipolar to aii amacrine cells in the mouse retina. Journal of Comparative Neurology 521, 3541-3555.
96. 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.
97. Waites, C. L., Craig, A. M. & Garner, C. C. (2005). Mechanisms of vertebrate synaptogenesis. Annual Review of Neuroscience 28, 251-274.
98. Wässle, H., Peichl, L. & Boycott, B. B. (1978). Topography of horizontal cells in the retina of the domestic cat. Proceedings of the Royal Society of London B 203, 269-291.
99. Wässle, H., Peichl, L. & Boycott, B. B. (1981). Dendritic territories of cat retinal ganglion cells. Nature 292, 344-345.
100. 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.
101. 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.
102. Whitney, I. E., Raven, M. A., Ciobanu, D. C., Poché, R. A., Ding, Q., Elshatory, Y., Gan, L., Williams, R. W. & Reese, B. E. (2011). Genetic modulation of horizontal cell number in the mouse retina. Proceedings of the National Academy of Sciences of the United States of America 108, 9697-9702.
103. Whitney, I. E., Raven, M. A., Ciobanu, D. C., Williams, R. W. & Reese, B. E. (2009). Multiple genes on chromosome 7 regulate dopaminergic amacrine cell number in the mouse retina. Investigative Ophthalmology and Visual Science 50, 1996-2003.
104. 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.
105. Willardsen, M. I. & Link, B. A. (2011). Cell biological regulation of division fate in vertebrate neuroepithelial cells. Developmental Dynamics 240, 1865-1879.
106. Witkovsky, P. (2004). Dopamine and retinal function. Documenta Ophthalmologica 108, 17-40.
107. Zhang, Y., Kim, I. J., Sanes, J. R. & Meister, M. (2012a). The most numerous ganglion cell type of the mouse retina is a selective feature detector. Proceedings of the National Academy of Sciences of the United States of America 109, 2391-2398.
108. Zhang, L., Song, N. N., Chen, J. Y., Huang, Y., Li, H. & Ding, Y. Q. (2012b). Satb2 is required for dendritic arborization and soma spacing in mouse cerebral cortex. Cerebral Cortex 22, 1510-1519.