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Abstract

Binocular vision depends on retinal ganglion cell (RGC) axon projection either to the same side or to the opposite side of the brain. In this article, we review the molecular mechanisms for decussation of RGC axons, with a focus on axon guidance signaling at the optic chiasm and ipsi- and contralateral axon organization in the optic tract prior to and during targeting. The spatial and temporal features of RGC neurogenesis that give rise to ipsilateral and contralateral identity are described. The albino visual system is highlighted as an apt comparative model for understanding RGC decussation, as albinos have a reduced ipsilateral projection and altered RGC neurogenesis associated with perturbed melanogenesis in the retinal pigment epithelium. Understanding the steps for RGC specification into ipsi- and contralateral subtypes will facilitate differentiation of stem cells into RGCs with proper navigational abilities for effective axon regeneration and correct targeting of higher-order visual centers.

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2020-09-15
2024-06-22
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Literature Cited

  1. Ahmadi K, Herbik A, Wagner M, Kanowski M, Thieme H, Hoffmann MB 2019. Population receptive field and connectivity properties of the early visual cortex in human albinism. NeuroImage 202:116105
    [Google Scholar]
  2. Antinucci P, Suleyman O, Monfries C, Hindges R 2016. Neural mechanisms generating orientation selectivity in the retina. Curr. Biol. 26:1802–15
    [Google Scholar]
  3. Balasubramanian R, Tao C, Polanco K, Zhong J, Wang F et al. 2018. Deficient FGF signaling in the developing peripheral retina disrupts ciliary margin development and causes aniridia. bioRxiv 443416. https://doi.org/10.1101/443416
    [Crossref]
  4. Beermann F, Ruppert S, Hummler E, Bosch FX, Muller G et al. 1990. Rescue of the albino phenotype by introduction of a functional tyrosinase gene into mice. EMBO J 9:2819–26
    [Google Scholar]
  5. Belanger MC, Robert B, Cayouette M 2017. Msx1-positive progenitors in the retinal ciliary margin give rise to both neural and non-neural progenies in mammals. Dev. Cell 40:137–50
    [Google Scholar]
  6. Bhansali P, Rayport I, Rebsam A, Mason C 2014. Delayed neurogenesis leads to altered specification of ventrotemporal retinal ganglion cells in albino mice. Neural Dev 9:11
    [Google Scholar]
  7. Bourguignon C, Li J, Papalopulu N 1998. XBF-1, a winged helix transcription factor with dual activity, has a role in positioning neurogenesis in Xenopus competent ectoderm. Development 125:4889–900
    [Google Scholar]
  8. Bovolenta P, Mason CA. 1987. Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets. J. Neurosci. 7:1447–60
    [Google Scholar]
  9. Bruce FM, Brown S, Smith JN, Fuerst PG, Erskine L 2017. DSCAM promotes axon fasciculation and growth in the developing optic pathway. PNAS 114:1702–7
    [Google Scholar]
  10. Cardozo MJ, Almuedo-Castillo M, Bovolenta P 2019. Patterning the vertebrate retina with morphogenetic signaling pathways. Neuroscientist 11:1073858419874016
    [Google Scholar]
  11. Carreres MI, Escalante A, Murillo B, Chauvin G, Gaspar P et al. 2011. Transcription factor Foxd1 is required for the specification of the temporal retina in mammals. J. Neurosci. 31:5673–81
    [Google Scholar]
  12. Cayouette M, Whitmore AV, Jeffery G, Raff M 2001. Asymmetric segregation of Numb in retinal development and the influence of the pigmented epithelium. J. Neurosci. 21:5643–51
    [Google Scholar]
  13. Centanin L, Hoeckendorf B, Wittbrodt J 2011. Fate restriction and multipotency in retinal stem cells. Cell Stem Cell 9:553–62
    [Google Scholar]
  14. Cheadle L, Tzeng CP, Kalish BT, Harmin DA, Rivera S et al. 2018. Visual experience-dependent expression of Fn14 is required for retinogeniculate refinement. Neuron 99:525–39.e10
    [Google Scholar]
  15. Chen T, Hu Y, Lin X, Huang X, Liu B et al. 2015. Dopamine signaling regulates the projection patterns in the mouse chiasm. Brain Res 1625:324–36
    [Google Scholar]
  16. Cioni JM, Wong HH, Bressan D, Kodama L, Harris WA, Holt CE 2018. Axon-axon interactions regulate topographic optic tract sorting via CYFIP2-dependent WAVE complex function. Neuron 97:1078–93.e6
    [Google Scholar]
  17. Clements R, Wright KM. 2018. Retinal ganglion cell axon sorting at the optic chiasm requires dystroglycan. Dev. Biol. 442:210–19
    [Google Scholar]
  18. Colello RJ, Guillery RW. 1990. The early development of retinal ganglion cells with uncrossed axons in the mouse: retinal position and axonal course. Development 108:515–23
    [Google Scholar]
  19. Colello SJ, Guillery RW. 1998. The changing pattern of fibre bundles that pass through the optic chiasm of mice. Eur. J. Neurosci. 10:3653–63
    [Google Scholar]
  20. Cronin CA, Ryan AB, Talley EM, Scrable H 2003. Tyrosinase expression during neuroblast divisions affects later pathfinding by retinal ganglion cells. J. Neurosci. 23:11692–97
    [Google Scholar]
  21. Drager UC. 1985a. Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse. Proc. R. Soc. Lond. B 224:57–77
    [Google Scholar]
  22. Drager UC. 1985b. Calcium binding in pigmented and albino eyes. PNAS 82:6716–20
    [Google Scholar]
  23. Duan X, Qiao M, Bei F, Kim IJ, He Z, Sanes JR 2015. Subtype-specific regeneration of retinal ganglion cells following axotomy: effects of osteopontin and mTOR signaling. Neuron 85:1244–56
    [Google Scholar]
  24. Dyer MA, Cepko CL. 2001. Regulating proliferation during retinal development. Nat. Rev. Neurosci. 2:333–42
    [Google Scholar]
  25. Elliott J, Jolicoeur C, Ramamurthy V, Cayouette M 2008. Ikaros confers early temporal competence to mouse retinal progenitor cells. Neuron 60:26–39
    [Google Scholar]
  26. Erskine L, Francois U, Denti L, Joyce A, Tillo M et al. 2017. VEGF-A and neuropilin 1 (NRP1) shape axon projections in the developing CNS via dual roles in neurons and blood vessels. Development 144:2504–16
    [Google Scholar]
  27. Fabre PJ, Shimogori T, Charron F 2010. Segregation of ipsilateral retinal ganglion cell axons at the optic chiasm requires the Shh receptor Boc. J. Neurosci. 30:266–75
    [Google Scholar]
  28. Feldheim DA, Vanderhaeghen P, Hansen MJ, Frisen J, Lu Q et al. 1998. Topographic guidance labels in a sensory projection to the forebrain. Neuron 21:1303–13
    [Google Scholar]
  29. Fiederling F, Weschenfelder M, Fritz M, von Philipsborn A, Bastmeyer M, Weth F 2017. Ephrin-A/EphA specific co-adaptation as a novel mechanism in topographic axon guidance. eLife 6:e25533
    [Google Scholar]
  30. Fotaki V, Smith R, Pratt T, Price DJ 2013. Foxg1 is required to limit the formation of ciliary margin tissue and Wnt/beta-catenin signalling in the developing nasal retina of the mouse. Dev. Biol. 380:299–313
    [Google Scholar]
  31. Galvao J, Iwao K, Apara A, Wang Y, Ashouri M et al. 2018. The Kruppel-like factor gene target Dusp14 regulates axon growth and regeneration. Investig. Ophthalmol. Vis. Sci. 59:2736–47
    [Google Scholar]
  32. Garcia-Frigola C, Carreres MI, Vegar C, Mason C, Herrera E 2008. Zic2 promotes axonal divergence at the optic chiasm midline by EphB1-dependent and -independent mechanisms. Development 135:1833–41
    [Google Scholar]
  33. Garcia-Frigola C, Herrera E. 2010. Zic2 regulates the expression of Sert to modulate eye-specific refinement at the visual targets. EMBO J 29:3170–83
    [Google Scholar]
  34. Gebhardt C, Auer TO, Henriques PM, Rajan G, Duroure K et al. 2019. An interhemispheric neural circuit allowing binocular integration in the optic tectum. Nat. Commun. 10:5471
    [Google Scholar]
  35. Glickstein SB, Monaghan JA, Koeller HB, Jones TK, Ross ME 2009. Cyclin D2 is critical for intermediate progenitor cell proliferation in the embryonic cortex. J. Neurosci. 29:9614–24
    [Google Scholar]
  36. Godement P, Salaün J, Mason CA 1990. Retinal axon pathfinding in the optic chiasm: divergence of crossed and uncrossed fibers. Neuron 5:173–96
    [Google Scholar]
  37. Godement P, Wang L-C, Mason CA 1994. Retinal axon divergence in the optic chiasm: dynamics of growth cone behavior at the midline. J. Neurosci. 14:7024–39
    [Google Scholar]
  38. Gu Z, Ueno M, Klinefelter K, Mamidi M, Yagi T, Yoshida Y 2019. Skilled movements in mice require inhibition of corticospinal axon collateral formation in the spinal cord by semaphorin signaling. J. Neurosci. 39:8885–99
    [Google Scholar]
  39. Ha T, Moon KH, Dai L, Hatakeyama J, Yoon K et al. 2017. The retinal pigment epithelium is a Notch signaling niche in the mouse retina. Cell Rep 19:351–63
    [Google Scholar]
  40. Hatini V, Tao W, Lai E 1994. Expression of winged helix genes, BF-1 and BF-2, define adjacent domains within the developing forebrain and retina. J. Neurobiol. 25:1293–309
    [Google Scholar]
  41. Hernandez-Bejarano M, Gestri G, Spawls L, Nieto-Lopez F, Picker A et al. 2015. Opposing Shh and Fgf signals initiate nasotemporal patterning of the zebrafish retina. Development 142:3933–42
    [Google Scholar]
  42. Herrera E, Brown L, Aruga J, Rachel RA, Dolen G et al. 2003. Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 114:545–57
    [Google Scholar]
  43. Herrera E, Erskine L, Morenilla-Palao C 2019. Guidance of retinal axons in mammals. Semin. Cell Dev. Biol. 85:48–59
    [Google Scholar]
  44. Herrera E, Marcus R, Li S, Williams SE, Erskine L et al. 2004. Foxd1 is required for proper formation of the optic chiasm. Development 131:5727–39
    [Google Scholar]
  45. Herrera E, Mason CA. 2007. The evolution of crossed and uncrossed retinal pathways in mammals. Evolution of Nervous Systems JH Kaas, GF Striedter, TH Bullock, TM Preuss, J Rubenstein, LA Krubitzer 307–17 Cambridge, MA: Academic
    [Google Scholar]
  46. Hornberg H, Cioni JM, Harris WA, Holt CE 2016. Hermes regulates axon sorting in the optic tract by post-trancriptional regulation of neuropilin 1. J. Neurosci. 36:12697–706
    [Google Scholar]
  47. Hoy JL, Bishop HI, Niell CM 2019. Defined cell types in superior colliculus make distinct contributions to prey capture behavior in the mouse. Curr. Biol. 29:4130–38.e5
    [Google Scholar]
  48. Hu Z, Wang K, Bertsch M, Dunn T, Kehoe T et al. 2019. Correlation between electroretinography, foveal anatomy and visual acuity in albinism. Doc. Ophthalmol. 139:21–32
    [Google Scholar]
  49. Huberman AD, Feller MB, Chapman B 2008. Mechanisms underlying development of visual maps and receptive fields. Annu. Rev. Neurosci. 31:479–509
    [Google Scholar]
  50. Huberman AD, Niell CM. 2011. What can mice tell us about how vision works. Trends Neurosci 34:464–73
    [Google Scholar]
  51. Ilia M, Jeffery G. 1996. Delayed neurogenesis in the albino retina: evidence of a role for melanin in regulating the pace of cell generation. Brain Res. Dev. Brain Res. 95:176–83
    [Google Scholar]
  52. Iwai-Takekoshi L, Balasubramanian R, Sitko A, Khan R, Weinreb S et al. 2018. Activation of Wnt signaling reduces ipsilaterally projecting retinal ganglion cells in pigmented retina. Development 145:dev163212
    [Google Scholar]
  53. Iwai-Takekoshi L, Ramos A, Schaler A, Weinreb S, Blazeski R, Mason C 2016. Retinal pigment epithelial integrity is compromised in the developing albino mouse retina. J. Comp. Neurol. 524:3696–716
    [Google Scholar]
  54. Jeffery G. 1998. The retinal pigment epithelium as a developmental regulator of the neural retina. Eye 12:Pt. 3b499–503
    [Google Scholar]
  55. Jessell TM. 2000. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1:20–29
    [Google Scholar]
  56. Kalish BT, Cheadle L, Hrvatin S, Nagy MA, Rivera S et al. 2018. Single-cell transcriptomics of the developing lateral geniculate nucleus reveals insights into circuit assembly and refinement. PNAS 115:E1051–60
    [Google Scholar]
  57. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133–38
    [Google Scholar]
  58. Koch SM, Dela Cruz CG, Hnasko TS, Edwards RH, Huberman AD, Ullian EM 2011. Pathway-specific genetic attenuation of glutamate release alters select features of competition-based visual circuit refinement. Neuron 71:235–42
    [Google Scholar]
  59. Kozar K, Sicinski P. 2005. Cell cycle progression without cyclin D-CDK4 and cyclin D-CDK6 complexes. Cell Cycle 4:388–91
    [Google Scholar]
  60. Kralj-Hans I, Tibber M, Jeffery G, Mobbs P 2006. Differential effect of dopamine on mitosis in early postnatal albino and pigmented rat retinae. J. Neurobiol. 66:47–55
    [Google Scholar]
  61. Kruijt CC, de Wit GC, Bergen AA, Florijn RJ, Schalij-Delfos NE, van Genderen MM 2018. The phenotypic spectrum of albinism. Ophthalmology 125:1953–60
    [Google Scholar]
  62. Kubota R, Hokoc JN, Moshiri A, McGuire C, Reh TA 2002. A comparative study of neurogenesis in the retinal ciliary marginal zone of homeothermic vertebrates. Brain Res. Dev. Brain Res. 134:31–41
    [Google Scholar]
  63. Kurimoto T, Yin Y, Habboub G, Gilbert HY, Li Y et al. 2013. Neutrophils express oncomodulin and promote optic nerve regeneration. J. Neurosci. 33:14816–24
    [Google Scholar]
  64. Kuwajima T, Soares CA, Sitko AA, Lefebvre V, Mason C 2017. SoxC transcription factors promote contralateral retinal ganglion cell differentiation and axon guidance in the mouse visual system. Neuron 93:1110–25.e5
    [Google Scholar]
  65. Kuwajima T, Yoshida Y, Takegahara N, Petros TJ, Kumanogoh A et al. 2012. Optic chiasm presentation of Semaphorin6D in the context of Plexin-A1 and Nr-CAM promotes retinal axon midline crossing. Neuron 74:676–90
    [Google Scholar]
  66. Larsson M. 2013. The optic chiasm: a turning point in the evolution of eye/hand coordination. Front. Zool. 10:41
    [Google Scholar]
  67. Lavado A, Jeffery G, Tovar V, de la Villa P, Montoliu L 2006. Ectopic expression of tyrosine hydroxylase in the pigmented epithelium rescues the retinal abnormalities and visual function common in albinos in the absence of melanin. J. Neurochem. 96:1201–11
    [Google Scholar]
  68. LaVail JH, Nixon RA, Sidman RL 1978. Genetic control of retinal ganglion cell projections. J. Comp. Neurol. 182:399–421
    [Google Scholar]
  69. Leamey CA, Merlin S, Lattouf P, Sawatari A, Zhou X et al. 2007. Ten_m3 regulates eye-specific patterning in the mammalian visual pathway and is required for binocular vision. PLOS Biol 5:e241
    [Google Scholar]
  70. Lee H, Brott BK, Kirkby LA, Adelson JD, Cheng S et al. 2014. Synapse elimination and learning rules co-regulated by MHC class I H2-Db. Nature 509:195–200
    [Google Scholar]
  71. Lee MA, Sitko AA, Khalid S, Shirasu-Hiza M, Mason CA 2019. Spatiotemporal distribution of glia in and around the developing mouse optic tract. J. Comp. Neurol. 527:508–21
    [Google Scholar]
  72. Lee R, Petros TJ, Mason CA 2008. Zic2 regulates retinal ganglion cell axon avoidance of ephrinB2 through inducing expression of the guidance receptor EphB1. J. Neurosci. 28:5910–19
    [Google Scholar]
  73. Leventhal AG, Schall JD, Ault SJ, Provis JM, Vitek DJ 1988. Class-specific cell death shapes the distribution and pattern of central projection of cat retinal ganglion cells. J. Neurosci. 8:2011–27
    [Google Scholar]
  74. Lim JH, Stafford BK, Nguyen PL, Lien BV, Wang C et al. 2016. Neural activity promotes long-distance, target-specific regeneration of adult retinal axons. Nat. Neurosci. 19:1073–84
    [Google Scholar]
  75. Lin L, Wang J, Chan CK, Chan SO 2007. Effects of exogenous hyaluronan on midline crossing and axon divergence in the optic chiasm of mouse embryos. Eur. J. Neurosci. 26:1–11
    [Google Scholar]
  76. Lo Giudice Q, Leleu M, La Manno G, Fabre PJ 2019. Single-cell transcriptional logic of cell-fate specification and axon guidance in early born retinal neurons. Development 146:dev178103
    [Google Scholar]
  77. Lodato S, Shetty AS, Arlotta P 2015. Cerebral cortex assembly: generating and reprogramming projection neuron diversity. Trends Neurosci 38:117–25
    [Google Scholar]
  78. Marcucci F, Murcia-Belmonte V, Wang Q, Coca Y, Ferreiro-Galve S et al. 2016. The ciliary margin zone of the mammalian retina generates retinal ganglion cells. Cell Rep 17:3153–64
    [Google Scholar]
  79. Marcucci F, Soares CA, Mason C 2019. Distinct timing of neurogenesis of ipsilateral and contralateral retinal ganglion cells. J. Comp. Neurol. 527:212–24
    [Google Scholar]
  80. Marcus RC, Shimamura K, Sretavan D, Lai E, Rubenstein JL, Mason CA 1999. Domains of regulatory gene expression and the developing optic chiasm: correspondence with retinal axon paths and candidate signaling cells. J. Comp. Neurol. 403:346–58
    [Google Scholar]
  81. Marshak S, Nikolakopoulou AM, Dirks R, Martens GJ, Cohen-Cory S 2007. Cell-autonomous TrkB signaling in presynaptic retinal ganglion cells mediates axon arbor growth and synapse maturation during the establishment of retinotectal synaptic connectivity. J. Neurosci. 27:2444–56
    [Google Scholar]
  82. Martinez-Morales JR, Del Bene F, Nica G, Hammerschmidt M, Bovolenta P, Wittbrodt J 2005. Differentiation of the vertebrate retina is coordinated by an FGF signaling center. Dev. Cell 8:565–74
    [Google Scholar]
  83. Mason C, Guillery R. 2019. Conversations with Ray Guillery on albinism: linking Siamese cat visual pathway connectivity to mouse retinal development. Eur. J. Neurosci. 49:913–27
    [Google Scholar]
  84. McKay BS. 2019. Pigmentation and vision: Is GPR143 in control. J. Neurosci. Res. 97:77–87
    [Google Scholar]
  85. Morenilla-Palao C, López-Cascales MT, López-Atalaya JP, Baeza D, Calvo-Diaz L et al. 2019. Zic2 abrogates an alternative Wnt signaling pathway to convert axon attraction into repulsion. bioRxiv 759407. https://doi.org/10.1101/759407
    [Crossref]
  86. Morin LP, Studholme KM. 2014. Retinofugal projections in the mouse. J. Comp. Neurol. 522:3733–53
    [Google Scholar]
  87. Nagai T, Aruga J, Takada S, Gunther T, Sporle R et al. 1997. The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev. Biol. 182:299–313
    [Google Scholar]
  88. Nakamoto C, Durward E, Horie M, Nakamoto M 2019. Nell2 regulates the contralateral-versus-ipsilateral visual projection as a domain-specific positional cue. Development 146:dev170704
    [Google Scholar]
  89. Neumann CJ, Nuesslein-Volhard C. 2000. Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science 289:2137–39
    [Google Scholar]
  90. Norsworthy MW, Bei F, Kawaguchi R, Wang Q, Tran NM et al. 2017. Sox11 expression promotes regeneration of some retinal ganglion cell types but kills others. Neuron 94:1112–20.e4
    [Google Scholar]
  91. Osterhout JA, El-Danaf RN, Nguyen PL, Huberman AD 2014. Birthdate and outgrowth timing predict cellular mechanisms of axon target matching in the developing visual pathway. Cell Rep 8:1006–17
    [Google Scholar]
  92. Pak W, Hindges R, Lim YS, Pfaff SL, O'Leary DD 2004. Magnitude of binocular vision controlled by islet-2 repression of a genetic program that specifies laterality of retinal axon pathfinding. Cell 119:567–78
    [Google Scholar]
  93. Pearson RA, Dale N, Llaudet E, Mobbs P 2005. ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46:731–44
    [Google Scholar]
  94. Peng J, Fabre PJ, Dolique T, Swikert SM, Kermasson L et al. 2018. Sonic hedgehog is a remotely produced cue that controls axon guidance trans-axonally at a midline choice point. Neuron 97:326–40.e4
    [Google Scholar]
  95. Petros TJ, Bryson JB, Mason C 2010. Ephrin-B2 elicits differential growth cone collapse and axon retraction in retinal ganglion cells from distinct retinal regions. Dev. Neurobiol. 70:781–94
    [Google Scholar]
  96. Petros TJ, Rebsam A, Mason CA 2008. Retinal axon growth at the optic chiasm: to cross or not to cross. Annu. Rev. Neurosci. 31:295–315
    [Google Scholar]
  97. Picker A, Cavodeassi F, Machate A, Bernauer S, Hans S et al. 2009. Dynamic coupling of pattern formation and morphogenesis in the developing vertebrate retina. PLOS Biol 7:e1000214
    [Google Scholar]
  98. Plas DT, Lopez JE, Crair MC 2005. Pretarget sorting of retinocollicular axons in the mouse. J. Comp. Neurol. 491:305–19
    [Google Scholar]
  99. Plump AS, Erskine L, Sabatier C, Brose K, Epstein CJ et al. 2002. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33:219–32
    [Google Scholar]
  100. Poulter JA, Al-Araimi M, Conte I, van Genderen MM, Sheridan E et al. 2013. Recessive mutations in SLC38A8 cause foveal hypoplasia and optic nerve misrouting without albinism. Am. J. Hum. Genet. 93:1143–50
    [Google Scholar]
  101. Pratt T, Conway CD, Tian NM, Price DJ, Mason JO 2006. Heparan sulphation patterns generated by specific heparan sulfotransferase enzymes direct distinct aspects of retinal axon guidance at the optic chiasm. J. Neurosci. 26:6911–23
    [Google Scholar]
  102. Pratt T, Tian NM, Simpson TI, Mason JO, Price DJ 2004. The winged helix transcription factor Foxg1 facilitates retinal ganglion cell axon crossing of the ventral midline in the mouse. Development 131:3773–84
    [Google Scholar]
  103. Prieur DS, Rebsam A. 2017. Retinal axon guidance at the midline: chiasmatic misrouting and consequences. Dev. Neurobiol. 77:844–60
    [Google Scholar]
  104. Prusky GT, Douglas RM. 2004. Characterization of mouse cortical spatial vision. Vis. Res. 44:3411–18
    [Google Scholar]
  105. Quina LA, Pak W, Lanier J, Banwait P, Gratwick K et al. 2005. Brn3a-expressing retinal ganglion cells project specifically to thalamocortical and collicular visual pathways. J. Neurosci. 25:11595–604
    [Google Scholar]
  106. Rachel RA, Dolen G, Hayes NL, Lu A, Erskine L et al. 2002a. Spatiotemporal features of early neuronogenesis differ in wild-type and albino mouse retina. J. Neurosci. 22:4249–63
    [Google Scholar]
  107. Rachel RA, Mason CA, Beermann F 2002b. Influence of tyrosinase levels on pigment accumulation in the retinal pigment epithelium and on the uncrossed retinal projection. Pigment Cell Res 15:273–81
    [Google Scholar]
  108. Randlett O, Poggi L, Zolessi FR, Harris WA 2011. The oriented emergence of axons from retinal ganglion cells is directed by laminin contact in vivo. Neuron 70:266–80
    [Google Scholar]
  109. Raper J, Mason C. 2010. Cellular strategies of axonal pathfinding. Cold Spring Harb. Perspect. Biol. 2:a001933
    [Google Scholar]
  110. Raviv S, Bharti K, Rencus-Lazar S, Cohen-Tayar Y, Schyr R et al. 2014. PAX6 regulates melanogenesis in the retinal pigmented epithelium through feed-forward regulatory interactions with MITF. PLOS Genet 10:e1004360
    [Google Scholar]
  111. Rebsam A, Bhansali P, Mason CA 2012. Eye-specific projections of retinogeniculate axons are altered in albino mice. J. Neurosci. 32:4821–26
    [Google Scholar]
  112. Rebsam A, Petros TJ, Mason CA 2009. Switching retinogeniculate axon laterality leads to normal targeting but abnormal eye-specific segregation that is activity dependent. J. Neurosci. 29:14855–63
    [Google Scholar]
  113. Roffler-Tarlov S, Liu JH, Naumova EN, Bernal-Ayala MM, Mason CA 2013. L-Dopa and the albino riddle: content of L-Dopa in the developing retina of pigmented and albino mice. PLOS ONE 8:e57184
    [Google Scholar]
  114. Rossi AM, Fernandes VM, Desplan C 2017. Timing temporal transitions during brain development. Curr. Opin. Neurobiol. 42:84–92
    [Google Scholar]
  115. Sajgo S, Ghinia MG, Brooks M, Kretschmer F, Chuang K et al. 2017. Molecular codes for cell type specification in Brn3 retinal ganglion cells. PNAS 114:E3974–83
    [Google Scholar]
  116. Sanchez-Arrones L, Nieto-Lopez F, Sanchez-Camacho C, Carreres MI, Herrera E et al. 2013. Shh/Boc signaling is required for sustained generation of ipsilateral projecting ganglion cells in the mouse retina. J. Neurosci. 33:8596–607
    [Google Scholar]
  117. Seth A, Culverwell J, Walkowicz M, Toro S, Rick JM et al. 2006. belladonna/(Ihx2) is required for neural patterning and midline axon guidance in the zebrafish forebrain. Development 133:725–35
    [Google Scholar]
  118. Sitko AA, Kuwajima T, Mason CA 2018. Eye-specific segregation and differential fasciculation of developing retinal ganglion cell axons in the mouse visual pathway. J. Comp. Neurol. 526:1077–96
    [Google Scholar]
  119. Sitko AA, Mason CA. 2016. Organization of axons in their tract. Organization of Axons in Their Tract KS Rockland 267–88 Amsterdam: Elsevier
    [Google Scholar]
  120. Soares CA, Mason CA. 2015. Transient ipsilateral retinal ganglion cell projections to the brain: extent, targeting, and disappearance. Dev. Neurobiol. 75:1385–401
    [Google Scholar]
  121. Su J, Klemm MA, Josephson AM, Fox MA 2013. Contributions of VLDLR and LRP8 in the establishment of retinogeniculate projections. Neural Dev 8:11
    [Google Scholar]
  122. Sun F, Park KK, Belin S, Wang D, Lu T et al. 2011. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 480:372–75
    [Google Scholar]
  123. Takahashi H, Sakuta H, Shintani T, Noda M 2009. Functional mode of FoxD1/CBF2 for the establishment of temporal retinal specificity in the developing chick retina. Dev. Biol. 331:300–10
    [Google Scholar]
  124. Takahashi H, Shintani T, Sakuta H, Noda M 2003. CBF1 controls the retinotectal topographical map along the anteroposterior axis through multiple mechanisms. Development 130:5203–15
    [Google Scholar]
  125. Thaler JP, Koo SJ, Kania A, Lettieri K, Andrews S et al. 2004. A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41:337–50
    [Google Scholar]
  126. Tian NM, Pratt T, Price DJ 2008. Foxg1 regulates retinal axon pathfinding by repressing an ipsilateral program in nasal retina and by causing optic chiasm cells to exert a net axonal growth-promoting activity. Development 135:4081–89
    [Google Scholar]
  127. Tibber MS, Becker D, Jeffery G 2007. Levels of transient gap junctions between the retinal pigment epithelium and the neuroblastic retina are influenced by catecholamines and correlate with patterns of cell production. J. Comp. Neurol. 503:128–34
    [Google Scholar]
  128. Tibber MS, Whitmore AV, Jeffery G 2006. Cell division and cleavage orientation in the developing retina are regulated by L-DOPA. J. Comp. Neurol. 496:369–81
    [Google Scholar]
  129. Trakhtenberg EF, Li Y, Feng Q, Tso J, Rosenberg PA et al. 2018. Zinc chelation and Klf9 knockdown cooperatively promote axon regeneration after optic nerve injury. Exp. Neurol. 300:22–29
    [Google Scholar]
  130. Tran NM, Shekhar K, Whitney IE, Jacobi A, Benhar I et al. 2019. Single-cell profiles of retinal ganglion cells differing in resilience to injury reveal neuroprotective genes. Neuron 104:1039–55.e12
    [Google Scholar]
  131. Triplett JW, Wei W, Gonzalez C, Sweeney NT, Huberman AD et al. 2014. Dendritic and axonal targeting patterns of a genetically-specified class of retinal ganglion cells that participate in image-forming circuits. Neural Dev 9:2
    [Google Scholar]
  132. Tripodi M, Stepien AE, Arber S 2011. Motor antagonism exposed by spatial segregation and timing of neurogenesis. Nature 479:61–66
    [Google Scholar]
  133. Tropepe V, Coles BL, Chiasson BJ, Horsford DJ, Elia AJ et al. 2000. Retinal stem cells in the adult mammalian eye. Science 287:2032–36
    [Google Scholar]
  134. Trousse F, Marti E, Gruss P, Torres M, Bovolenta P 2001. Control of retinal ganglion cell axon growth: a new role for Sonic hedgehog. Development 128:3927–36
    [Google Scholar]
  135. Umemori H, Linhoff MW, Ornitz DM, Sanes JR 2004. FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118:257–70
    [Google Scholar]
  136. Upton AL, Salichon N, Lebrand C, Ravary A, Blakely R et al. 1999. Excess of serotonin (5-HT) alters the segregation of ispilateral and contralateral retinal projections in monoamine oxidase A knock-out mice: possible role of 5-HT uptake in retinal ganglion cells during development. J. Neurosci. 19:7007–24
    [Google Scholar]
  137. Wang Q, Marcucci F, Cerullo I, Mason C 2016. Ipsilateral and contralateral retinal ganglion cells express distinct genes during decussation at the optic chiasm. eNeuro 3: ENEURO.0169-16.2016
    [Google Scholar]
  138. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR 2004. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43:647–61
    [Google Scholar]
  139. Wetts R, Serbedzija GN, Fraser SE 1989. Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. Dev. Biol. 136:254–63
    [Google Scholar]
  140. Williams SE, Grumet M, Colman DR, Henkemeyer M, Mason CA, Sakurai T 2006. A role for Nr-CAM in the patterning of binocular visual pathways. Neuron 50:535–47
    [Google Scholar]
  141. Williams SE, Mann F, Erskine L, Sakurai T, Wei S et al. 2003. Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 39:919–35
    [Google Scholar]
  142. Wilton DK, Dissing-Olesen L, Stevens B 2019. Neuron-glia signaling in synapse elimination. Annu. Rev. Neurosci. 42:107–27
    [Google Scholar]
  143. Wong GK, Baudet ML, Norden C, Leung L, Harris WA 2012. Slit1b-Robo3 signaling and N-cadherin regulate apical process retraction in developing retinal ganglion cells. J. Neurosci. 32:223–28
    [Google Scholar]
  144. Wu S, Chang KC, Nahmou M, Goldberg JL 2018. Induced pluripotent stem cells promote retinal ganglion cell survival after transplant. Investig. Ophthalmol. Vis. Sci. 59:1571–76
    [Google Scholar]
  145. Xiao T, Staub W, Robles E, Gosse NJ, Cole GJ, Baier H 2011. Assembly of lamina-specific neuronal connections by slit bound to type IV collagen. Cell 146:164–76
    [Google Scholar]
  146. Young RW. 1985. Cell differentiation in the retina of the mouse. Anat. Rec. 212:199–205
    [Google Scholar]
  147. Zeng H, Sanes JR. 2017. Neuronal cell-type classification: challenges, opportunities and the path forward. Nat. Rev. Neurosci. 18:530–46
    [Google Scholar]
/content/journals/10.1146/annurev-vision-091517-034306
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