Cell birth and death in the mouse retinal ganglion cell layer
Open accessAbstract
Here we describe quantitatively the birth and death of the two separate populations of neurons, ganglion cells and displaced amacrine cells, in the mouse retinal ganglion cell layer (GCL). The two cell types, which are roughly equally numerous, were distinguished pre- and postnatally by labeling the ganglion cells retrogradely with fluorescent dye. Embryos were labeled cumulatively with bromodeoxyuridine (BrdU) delivered by an osmotic minipump implanted in the mother; cell birth dates were established as having occurred before or after pump implantation. Early cohorts (GCL cells born before embryonic day [E] 11.8 and E12.8) were 98+/-1.1% and 99+/-0.2% ganglion cells (mean+/-SEM), respectively, and a late cohort (born after E15.8) was 97+/-1.2% displaced amacrines. Thus birth date was a strong predictor of a GCL cell's ultimate identity. Cell death in each cohort was estimated by counting cells at different time points (soon after the cohort was produced and later) and subtracting the later from the earlier number. This method avoids the problem of simultaneous birth and death that has plagued many of the earlier attempts to assess cell death. Negligible numbers died during the first week after a cell's birthday. The amount of cell death differed in the two cohorts; 48.5+/-15% and 29.0+/-12.4% in early and late, respectively, and most of it was postnatal. These findings disagree sharply with an earlier conclusion that ganglion cells die within 5 days of their birthdays or not at all.
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RGC normal programmed cell death is essentially complete by P4/P5.
“previous work has demonstrated that RGC normal programmed cell death is essentially complete by P4/P5 (Farah and Easter, 2005).”
From Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner (2012) · cites this paper as Farah and Easter, 2005
The Postnatal cell death section compares the predominantly ganglion-cell early cohort at P0 and P30, establishing postnatal loss but not when that loss ended. The Developmental cell death section reports dying older GCL cells during P0–P5, but does not establish that RGC death was essentially complete by P4/P5. Searches for P4/P5 and the timing of ganglion-cell death found no passage resolving that endpoint. (LLM, conf=0.72)
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Cites
Estimation of nuclear population from microtome sections
Abercrombie, M. (1946) · The Anatomical Record · doi:10.1002/ar.1090940210 · Cited by 4,363 · see citing works
A common progenitor for neurons and glia persists in rat retina late in development
Turner, D. L., & Cepko, C. L. (1987) · Nature · doi:10.1038/328131a0 · Cited by 1,430 · see citing works
The Major Cell Populations of the Mouse Retina
Jeon, C.-J., Strettoi, E., & Masland, R. H. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08936.1998 · Cited by 1,429 · see citing works
Cell differentiation in the retina of the mouse
Young, R. W. (1985) · The Anatomical Record · doi:10.1002/ar.1092120215 · Cited by 1,079 · see citing works
Cell fate determination in the vertebrate retina.
Cepko, C. L., Austin, C. P., Yang, X.-J., Alexiades, M. R., & Ezzeddine, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.2.589 · Cited by 989 · see citing works
Vertebrate neural cell-fate determination: Lessons from the retina
Livesey, F. J., & Cepko, C. L. (2001) · Nature reviews. Neuroscience · doi:10.1038/35053522 · Cited by 948 · see citing works
Pax6 Is Required for the Multipotent State of Retinal Progenitor Cells
Marquardt, T., Ashery‐Padan, R., Andrejewski, N., Scardigli, R., Guillemot, F., & Gruß, P. (2001) · Cell · doi:10.1016/s0092-8674(01)00295-1 · Cited by 926 · see citing works
Methods for the Counting of Neurons
Konigsmark, B. W. (1970) · Springer eBooks · doi:10.1007/978-3-642-85986-1_14 · Cited by 768 · see citing works
Jacobson, M. (1991) · Springer eBooks · doi:10.1007/978-1-4757-4954-0 · Cited by 669 · see citing works
Lineage-independent determination of cell type in the embryonic mouse retina
Turner, D. L., Snyder, E. Y., & Cepko, C. L. (1990) · Neuron · doi:10.1016/0896-6273(90)90136-4 · Cited by 662 · see citing works
Multipotent Precursors Can Give Rise to All Major Cell Types of the Frog Retina
Wetts, R., & Fraser, S. E. (1988) · Science · doi:10.1126/science.2449732 · Cited by 661 · see citing works
Cellular determination in the xenopus retina is independent of lineage and birth date
Holt, C. E., Bertsch, T. W., Ellis, H. M., & Harris, W. A. (1988) · Neuron · doi:10.1016/0896-6273(88)90205-x · Cited by 648 · see citing works
Cell death during differentiation of the retina in the mouse
Young, R. W. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902290307 · Cited by 532 · see citing works
Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat
Perry, V. H., Henderson, Z., & Linden, R. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902190309 · Cited by 438 · see citing works
Retinal Ganglion Cell Genesis Requires lakritz, a Zebrafish atonal Homolog
Kay, J. N., Finger‐Baier, K., Roeser, T., Staub, W., & Baier, H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00312-9 · Cited by 417 · see citing works
Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch
Austin, C. P., Feldman, D. E., Ida, J. A., & Cepko, C. L. (1995) · Development · doi:10.1242/dev.121.11.3637 · Cited by 407 · see citing works
Carter‐Dawson, L. D., & LaVail, M. M. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901880205 · Cited by 404 · see citing works
Initial tract formation in the mouse brain
Easter, S., Ross, L., & Frankfurter, A. J. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-01-00285.1993 · Cited by 394 · see citing works
Self-citationTiming and topography of cell genesis in the rat retina
Rapaport, D. H., Wong, L., Wood, E. D., Yasumura, D., & LaVail, M. M. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20134 · Cited by 376 · see citing works
The growth of the retina in Xenopus laevis: an autoradiographic study
Straznicky, K., & Gaze, R. M. (1971) · Development · doi:10.1242/dev.26.1.67 · Cited by 366 · see citing works
Retinal Neurogenesis: The Formation of the Initial Central Patch of Postmitotic Cells
Hu, M., & Easter, S. S. (1999) · Developmental Biology · doi:10.1006/dbio.1998.9031 · Cited by 364 · see citing works
Self-citationGenerating neuronal diversity in the retina: one for nearly all
Marquardt, T., & Gruß, P. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)02028-2 · Cited by 361 · see citing works
Cytogenesis in the monkey retina
Vail, M. M. L., Rapaport, D. H., & RAKIC, P. T. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903090107 · Cited by 292 · see citing works
Ganglion cell distribution in the retina of the mouse.
Dräger, U. C., & Olsen, J. F. (1981) · PubMed · Cited by 262 · see citing works
Dräger, U. C. (1985) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1985.0021 · Cited by 255 · see citing works
Overproduction and Elimination of Retinal Axons in the Fetal Rhesus Monkey
RAKIC, P. T., & Riley, K. P. (1983) · Science · doi:10.1126/science.6828871 · Cited by 249 · see citing works
Development of the visual system
Powers, M. K., & Raymond, P. A. (1990) · Springer eBooks · doi:10.1007/978-94-009-0411-8_12 · Cited by 223 · see citing works
Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina
Belliveau, M. J., & Cepko, C. L. (1999) · Development · doi:10.1242/dev.126.3.555 · Cited by 220 · see citing works
Williams, R. W., Bastiani, M. J., Lia, B., & Chalupa, L. M. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902460104 · Cited by 206 · see citing works
Hughes, W. F., & McLoon, S. C. (1979) · Experimental Neurology · doi:10.1016/0014-4886(79)90204-8 · Cited by 191 · see citing works
Cell death in the mammalian visual system during normal development: I. Retinal ganglion cells
Sengelaub, D. R., & Finlay, B. L. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902040402 · Cited by 174 · see citing works
Alexiades, M. R., & Cepko, C. L. (1997) · Development · doi:10.1242/dev.124.6.1119 · Cited by 174 · see citing works
Fast axonal diffusion of 3000 molecular weight dextran amines
Fritzsch, B. (1993) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(93)90060-5 · Cited by 171 · see citing works
Crespo, D., O’Leary, D. D. M., & Cowan, W. M. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90238-x · Cited by 161 · see citing works
Cellular diversification in the vertebrate retina
Harris, W. A. (1997) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(97)80013-5 · Cited by 156 · see citing works
Migration and synaptogenesis of cone photoreceptors in the developing mouse retina
Rich, K. A., Zhan, Y., & Blanks, J. C. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19971110)388:1 · Cited by 156 · see citing works
Hinds, J. W., & Hinds, P. L. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901790204 · Cited by 149 · see citing works
Neurogenesis in the retinal ganglion cell layer of the rat
Reese, B. E., & Colello, R. J. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90062-7 · Cited by 138 · see citing works
Conti, F., Melone, M., Biasi, S. D., Minelli, A., Brecha, N. C., & Ducati, A. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980622)396:1 · Cited by 130 · see citing works
Schnitzer, J., & Rusoff, A. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-12-02948.1984 · Cited by 122 · see citing works
Belecky‐Adams, T. L., Cook, B. E., & Adler, R. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0220 · Cited by 121 · see citing works
Acetylcholine Synthesis by Displaced Amacrine Cells
Hayden, S., Mills, J. W., & Masland, R. M. (1980) · Science · doi:10.1126/science.7433984 · Cited by 114 · see citing works
Spatiotemporal Features of Early Neuronogenesis Differ in Wild-Type and Albino Mouse Retina
Rachel, R. A., Dölen, G., Hayes, N. L., Lu, A., Erskine, L., Nowakowski, R. S., & Mason, C. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-11-04249.2002 · Cited by 113 · see citing works
Sefton, A. J., & Lam, K. S. (1984) · Experimental Brain Research · doi:10.1007/bf00231137 · Cited by 106 · see citing works
Lysophosphatidyl choline facilitates labeling of CNS projections with horseradish peroxidase
Frank, E., Harris, W. A., & Kennedy, M. B. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90059-x · Cited by 99 · see citing works
Galli‐Resta, L., & Ensini, M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-07-02318.1996 · Cited by 97 · see citing works
Generation of retinal cells in the wallaby, Setonix brachyurus (quokka)
Harman, A. M., & Beazley, L. D. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90246-7 · Cited by 80 · see citing works
Histogenesis of the retina in the killifish, Fundulus heteroclitus
Hollyfield, J. G. (1972) · The Journal of Comparative Neurology · doi:10.1002/cne.901440308 · Cited by 80 · see citing works
Neuronal death and the development of the pontine nuclei and inferior olive in the chick
Armstrong, R. C., & Clarke, R. C. (1979) · Neuroscience · doi:10.1016/0306-4522(79)90025-3 · Cited by 67 · see citing works
Generation and degeneration of retinal ganglion cells in the chicken
Rager, G. H., & Rager, U. (1976) · Experimental Brain Research · doi:10.1007/bf00239787 · Cited by 62 · see citing works
Cell Production and Cell Death in the Generation of Variation in Neuron Number
Strom, R. C., & Williams, R. W. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-23-09948.1998 · Cited by 61 · see citing works
Harvey, A. R., & Robertson, D. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903250108 · Cited by 57 · see citing works
Voyvodic, J. T., Burne, J. F., & RAFF, M. C. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb01045.x · Cited by 52 · see citing works
Ma, L., Swalla, B. J., Zhou, J., Dobias, S. L., Bell, J. R., Chen, J., Maxson, R. E., & Jeffery, W. R. (1996) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199603)205:3 · Cited by 50 · see citing works
McKay, S. E., & Oppenheim, R. W. (1991) · Journal of Neurobiology · doi:10.1002/neu.480220707 · Cited by 50 · see citing works
Patterns of cytogenesis in the developing retina of the WallabySetonix brachyurus
Harman, A. M., & Beazley, L. D. (1987) · Anatomy and Embryology · doi:10.1007/bf00572536 · Cited by 41 · see citing works
Differential expression and cellular localization of doublecortin in the developing rat retina
Lee, E.-J., Kim, I., Lee, E. M., Kwon, S., Oh, S.-J., & Chun, M. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02583.x · Cited by 36 · see citing works
Gould, T. W., Burek, M. J., Sosnowski, J. M., Prevette, D. M., & Oppenheim, R. W. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9490 · Cited by 23 · see citing works
Lia, B., WILLIAMS, R., & Chalupa, L. M. (1986) · Brain Research · doi:10.1016/s0006-8993(86)80239-6 · Cited by 19 · see citing works
Farah, M. H. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.11.017 · Cited by 16 · see citing works
Self-citationThe isolated mammalian brain: an in vivo preparation suitable for pathway tracing
von Bohlen, O., & Halbach, U. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00543.x · Cited by 11 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Sidman RL. 1961. Histogenesis of mouse retina studied with thymidine- H 3 . In: Smelser G, editor. Structure of the eye. New York: Academic Press. pp 487-506.
Cited by
Sorted by citations
Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089 · see citing works
“To directly address whether microglia are engulfing RGC presynaptic terminals, immunohistochemistry in P5 dLGN for 696 Neuron 74, 691–705, May 24, 2012 ª2012 Elsevier Inc. presynaptic machinery specific to RGCs (i.e., VGlut2) followed by high resolution imagingwas performed.”
Huberman, A. D., Manu, M., Koch, S. M., Susman, M. W., Lutz, A. B., Ullian, E. M., Baccus, S. A., & Barres, B. A. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.018 · Cited by 271 · see citing works
ISL1 and BRN3B co-regulate the differentiation of murine retinal ganglion cells
Pan, L., Deng, M., Xie, X., & Gan, L. (2008) · Development · doi:10.1242/dev.010751 · Cited by 194 · see citing works
Brzezinski, J. A., Prasov, L., & Glaser, T. M. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.03.006 · Cited by 145 · see citing works
γ-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina
Lefebvre, J. L., Zhang, Y., Meister, M., Wang, X., & Sanes, J. R. (2008) · Development · doi:10.1242/dev.027912 · Cited by 144 · see citing works
Ascl1 expression defines a subpopulation of lineage-restricted progenitors in the mammalian retina
Brzezinski, J. A., Kim, E. J., Johnson, J. E. B., & Reh, T. A. (2011) · Development · doi:10.1242/dev.064006 · Cited by 140 · see citing works
The protein kinase DYRK1A regulates caspase-9-mediated apoptosis during retina development.
Laguna, A., Aranda, S., Barallobre, M., Barhoum, R., Fernández, E., Fotaki, V., Delabar, J., de la Luna, S., de la Villa, P., & Arbonés, M. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.10.014 · Cited by 131 · see citing works
Jiang, Y., Ding, Q., Xie, X., Libby, R. T., Lefebvre, V., & Gan, L. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.478503 · Cited by 132 · see citing works
Math5 is required for both early retinal neuron differentiation and cell cycle progression
Le, T. T., Wroblewski, E. E., Patel, S., Riesenberg, A. N., & Brown, N. L. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.03.055 · Cited by 110 · see citing works
Complement Targets Newborn Retinal Ganglion Cells for Phagocytic Elimination by Microglia
Anderson, S., Zhang, J., Steele, M. R., Romero, C. O., Kautzman, A. G., Schafer, D. P., & Vetter, M. L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1854-18.2018 · Cited by 106 · see citing works
Anderson, S., Roberts, J. M., Zhang, J., Steele, M. R., Romero, C. O., Bosco, A., & Vetter, M. L. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.062 · Cited by 95 · see citing works
Development of melanopsin-based irradiance detecting circuitry
McNeill, D. S., Sheely, C. J., Ecker, J. L., Badea, T. C., Morhardt, D. R., Guido, W., & Hattar, S. S. (2011) · Neural Development · doi:10.1186/1749-8104-6-8 · Cited by 92 · see citing works
Farah, M. H., Pan, B., Hoffman, P. N., Ferraris, D. V., Tsukamoto, T., Nguyen, T., Wong, P. C., Price, D. L., Slusher, B. S., & Griffin, J. W. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6810-10.2011 · Cited by 82 · see citing works
Self-citationOsterhout, J. A., El-Danaf, R. N., Nguyen, P. L., & Huberman, A. D. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.06.063 · Cited by 78 · see citing works
Cyclin D1 fine-tunes the neurogenic output of embryonic retinal progenitor cells
Das, G., Choi, Y. J., Siciński, P., & Levine, E. M. (2009) · Neural Development · doi:10.1186/1749-8104-4-15 · Cited by 75 · see citing works
More than meets the eye: The role of microglia in healthy and diseased retina
Murenu, E., Gerhardt, M.-J., Biel, M., & Michalakis, S. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1006897 · Cited by 73 · see citing works
Shekhar, K., Whitney, I. E., Butrus, S., Peng, Y.-R., & Sanes, J. R. (2022) · eLife · doi:10.7554/elife.73809 · Cited by 68 · see citing works
Atoh7-independent specification of retinal ganglion cell identity
Brodie-Kommit, J., Clark, B. S., Shi, Q., Shiau, F., Kim, D. W., Langel, J., Sheely, C. J., Ruzycki, P. A., Fries, M., Javed, A., et al. (2021) · Science Advances · doi:10.1126/sciadv.abe4983 · Cited by 62 · see citing works
Hasegawa, S., Kumagai, M., Hagihara, M., Nishimaru, H., Hirano, K., Kaneko, R., Okayama, A., Hirayama, T., Sanbo, M., Hirabayashi, M., et al. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00155 · Cited by 61 · see citing works
Braunger, B. M., Pielmeier, S. M., Demmer, C., Landstorfer, V., Kawall, D., Abramov, N., Leibinger, M., Kleiter, I., Fischer, D., Jägle, H., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0991-13.2013 · Cited by 58 · see citing works
Neuronal apoptosis drives remodeling states of microglia and shifts in survival pathway dependence
Anderson, S. R., Roberts, J. M., Ghena, N., Irvin, E., Schwakopf, J., Cooperstein, I. B., Bosco, A., & Vetter, M. L. (2022) · eLife · doi:10.7554/elife.76564 · Cited by 57 · see citing works
Triplication of DYRK1A causes retinal structural and functional alterations in Down syndrome
Laguna, A., Barallobre, M. J., Marchena, M., Mateus, C., Ramírez, E., Martínez‐Cué, C., Delabar, J. M., Castelo-Branco, M. S., de la Villa, P., & Arbonés, M. L. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt125 · Cited by 54 · see citing works
Pushing the envelope of retinal ganglion cell genesis: Context dependent function of Math5 (Atoh7)
Prasov, L., & Glaser, T. M. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.05.005 · Cited by 52 · see citing works
Blume, Z. I., Lambert, J. M., Lovel, A. G., & Mitchell, D. M. (2020) · Developmental Dynamics · doi:10.1002/dvdy.163 · Cited by 51 · see citing works
Miesfeld, J. B., Ghiasvand, N. M., Marsh-Armstrong, B. P., Marsh‐Armstrong, N., Miller, E. B., Zhang, P., Manna, S. K., Zawadzki, R. J., Brown, N. L., & Glaser, T. M. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2006888117 · Cited by 44 · see citing works
Apoptosis Regulates ipRGC Spacing Necessary for Rods and Cones to Drive Circadian Photoentrainment
Chen, S., Chew, K. S., McNeill, D. S., Keeley, P. W., Ecker, J. L., Mao, B. Q., Pahlberg, J., Kim, B., Lee, S., Fox, M. A., et al. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.028 · Cited by 47 · see citing works
Expression of transcription factors divides retinal ganglion cells into distinct classes
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Retinal ganglion cells: dying to survive
Guerin, M. B., McKernan, D. P., O'Brien, C. J., & Cotter, T. G. (2006) · The International Journal of Developmental Biology · doi:10.1387/ijdb.062159mg · Cited by 43 · see citing works
Imaging retinal ganglion cells: Enabling experimental technology for clinical application
Smith, C. A., & Chauhan, B. C. (2014) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2014.10.003 · Cited by 35 · see citing works
Neurogenesis and cell death in the ganglion cell layer of vertebrate retina
Farah, M. H. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.04.002 · Cited by 35 · see citing works
Self-citationOntogenetic Cell Death and Phagocytosis in the Visual System of Vertebrates
Francisco‐Morcillo, J., Bejarano‐Escobar, R., Rodríguez‐León, J., Navascués, J., & Martín‐Partido, G. (2014) · Developmental Dynamics · doi:10.1002/dvdy.24174 · Cited by 32 · see citing works
Raven, M. A., Stagg, S. B., Nassar, H., & Reese, B. E. (2005) · Visual Neuroscience · doi:10.1017/s095252380522504x · Cited by 31 · see citing works
Math5 (Atoh7) gene dosage limits retinal ganglion cell genesis
Prasov, L., Nagy, M. S., Rudolph, D. D., & Glaser, T. M. (2012) · Neuroreport · doi:10.1097/00001756-201207110-00011 · Cited by 30 · see citing works
Programmed Cell Death During Retinal Development of the Mouse Eye
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Heterochronic misexpression of Ascl1 in the Atoh7 retinal cell lineage blocks cell cycle exit
Hufnagel, R. B., Riesenberg, A. N., Quinn, M. E., Brzezinski, J. A., Glaser, T. M., & Brown, N. L. (2013) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2013.02.004 · Cited by 28 · see citing works
Vision-Dependent and -Independent Molecular Maturation of Mouse Retinal Ganglion Cells
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A role for DNA methylation in regulation of EphA5 receptor expression in the mouse retina
Petkova, T. D., Seigel, G. M., & Otteson, D. C. (2010) · Vision Research · doi:10.1016/j.visres.2010.09.022 · Cited by 26 · see citing works
Mouse Retinal Development: A Dark Horse Model for Systems Biology Research
Zhang, X., Serb, J. M., & Greenlee, M. H. W. (2011) · Bioinformatics and Biology Insights · doi:10.4137/bbi.s6930 · Cited by 25 · see citing works
Microglia: Friends or Foes in Glaucoma? A Developmental Perspective
Ahmad, I., & Subramani, M. (2022) · Stem Cells Translational Medicine · doi:10.1093/stcltm/szac077 · Cited by 22 · see citing works
Pacal, M., & Bremner, R. (2013) · Developmental Dynamics · doi:10.1002/dvdy.24103 · Cited by 22 · see citing works
Cheng, T.-W., Liu, X.-B., Faulkner, R. L., Stephan, A. H., Barres, B. A., Huberman, A. D., & Cheng, H.-J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3455-10.2010 · Cited by 22 · see citing works
Integral bHLH factor regulation of cell cycle exit and RGC differentiation
Maurer, K. A., Kowalchuk, A. M., Shoja‐Taheri, F., & Brown, N. L. (2018) · Developmental Dynamics · doi:10.1002/dvdy.24638 · Cited by 19 · see citing works
Gamlin, C. R., Zhang, C., Dyer, M. A., & Wong, R. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.080 · Cited by 21 · see citing works
Fatty acid amide hydrolase expression during retinal postnatal development in rats
Zabouri, N., Ptito, M., Casanova, C., & Bouchard, J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.008 · Cited by 20 · see citing works
Temporal requirement of the alternative-splicing factor Sfrs1 for the survival of retinal neurons
Kanadia, R., Clark, V. E., Punzo, C., Trimarchi, J. M., & Cepko, C. L. (2008) · Development · doi:10.1242/dev.024620 · Cited by 16 · see citing works
CD11c ‐Expressing Microglia Are Transient, Driven by Interactions With Apoptotic Cells
Ghena, N., Anderson, S., Roberts, J. M., Irvin, E., Schwakopf, J., Bosco, A., & Vetter, M. L. (2025) · Glia · doi:10.1002/glia.24674 · Cited by 14 · see citing works
The effect of Rbfox2 modulation on retinal transcriptome and visual function
Gu, L., Kawaguchi, R., Caprioli, J., & Piri, N. (2020) · Scientific Reports · doi:10.1038/s41598-020-76879-5 · Cited by 14 · see citing works
Famiglietti, E. V., & Sundquist, S. J. (2010) · Visual Neuroscience · doi:10.1017/s0952523810000052 · Cited by 14 · see citing works
Ma, G., Ding, J., Kim, T.-H., & Yao, X. (2022) · Applied Sciences · doi:10.3390/app12041860 · Cited by 13 · see citing works
Voyatzis, S., Muzerelle, A., Gaspar, P., & Nicol, X. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031105 · Cited by 11 · see citing works
Photoreceptor degeneration has heterogeneous effects on functional retinal ganglion cell types
Dyszkant, N., Oesterle, J., Qiu, Y., Harrer, M., Schubert, T., Gonschorek, D., & Euler, T. (2025) · The Journal of Physiology · doi:10.1113/jp287643 · Cited by 9 · see citing works
Rohon-beard neurons do not succumb to programmed cell death during zebrafish development
Liu, K. E., & Kucenas, S. (2024) · Developmental Biology · doi:10.1016/j.ydbio.2024.06.020 · Cited by 8 · see citing works
Linden, R., & Reese, B. E. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511541629.013 · Cited by 9 · see citing works
A Novel Reporter Mouse Uncovers Endogenous Brn3b Expression
Miltner, A. M., Mercado-Ayon, Y., Cheema, S. K., Zhang, P., Zawadzki, R. J., & Torre, A. L. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20122903 · Cited by 8 · see citing works
Making of a retinal cell: insights into retinal cell-fate determination.
Goetz, J. J., Farris, C., Chowdhury, R., & Trimarchi, J. (2014) · International Review of Cell and Molecular Biology · doi:10.1016/b978-0-12-800097-7.00007-5 · Cited by 9 · see citing works
The role of Goldilocks protein kinase DYRK1A in embryonic development
Johnson, H. K., Litovchick, L., & DICKINSON, A. J. G. (2025) · Developmental Biology · doi:10.1016/j.ydbio.2025.06.009 · Cited by 5 · see citing works
Innate Immune Pathways Regulating Retinal Cell Development and Regeneration
Ghena, N., López, N. N., Roberts, J. M., Bosco, A., & Vetter, M. L. (2025) · Annual Review of Vision Science · doi:10.1146/annurev-vision-102122-110045 · Cited by 4 · see citing works
Specification of retinal cell types
Bösze, B., Hufnagel, R. B., & Brown, N. L. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814405-3.00021-7 · Cited by 4 · see citing works
Specification of Retinal Cell Types
Hufnagel, R. B., & Brown, N. L. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397265-1.00072-1 · Cited by 4 · see citing works
Pacal, M., & Bremner, R. (2014) · Developmental Dynamics · doi:10.1002/dvdy.24047 · Cited by 2 · see citing works
Qu, C., Bian, D., Li, X., Xiao, J., Wu, C., Li, Y., Jiang, T., Zhou, X., Qu, J., & Chen, J.-G. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.689448 · Cited by 2 · see citing works
Microglial mechanisms of viable retinal ganglion cell elimination
López, N. N., Rodríguez, Y. L., & Vetter, M. L. (2025) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2025.1719791 · Cited by 1 · see citing works
Identification of Downstream Targets of the Putative Transcription Factor Prdm8
Allen, K. J. (2009) · TSpace (University of Toronto) · Cited by 1 · see citing works
Hoffman, P., & Wong, P. (2011)
Beros, J. L. (2020) · UWA Profiles and Research Repository (UWA) · doi:10.26182/5f641ba971915
Cell behaviors that pattern developing tissues: the case of the vertebrate nervous system
Rocha-Martins, M. (2023) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2023.11.003
Developmental Synchrony of Retinal Waves, Apoptosis, and Angiogenesis in Postnatal RetinaPreprint
Savage, M. A., Bertram, C., de Montigny, J., Thorne, C. A., Queen, R. A., Lako, M., Hilgen, G., & Sernagor, E. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.19.712402
La coopération entre cellules ganglionnaires de la rétine façonne la connectivité du système visuel
Louail, A. (2019) · theses.fr (ABES) · doi:10.70675/b0db1fc6z9302z4a5ez8e7fzcbcbbf0f67a5
Developmental synchrony of retinal waves, apoptosis, and angiogenesis in postnatal retinaPreprint
Savage, M. A., Bertram, C., de Montigny, J., Thorne, C. A., Queen, R. A., Lako, M., Hilgen, G., & Sernagor, E. (2026) · eLife · doi:10.7554/elife.111419
Developmental Synchrony of Retinal Waves, Apoptosis, and Angiogenesis in Postnatal RetinaPreprint
Savage, M. A., Bertram, C., de Montigny, J., Thorne, C. A., Queen, R. A., Lako, M., Hilgen, G., & Sernagor, E. (2026) · eLife · doi:10.7554/elife.111419.1
Developmental Synchrony of Retinal Waves, Apoptosis, and Angiogenesis in Postnatal RetinaPreprint
Savage, M. A., Bertram, C., de Montigny, J., Thorne, C. A., Queen, R. A., Lako, M., Hilgen, G., & Sernagor, E. (2026) · eLife · doi:10.7554/elife.111419.2
Developmental synchrony of retinal waves, apoptosis, and angiogenesis in postnatal retina
Savage, M. A., Bertram, C., de Montigny, J., Thorne, C. A., Queen, R. A., Lako, M., Hilgen, G., & Sernagor, E. (2026) · eLife · doi:10.7554/elife.111419.3
- Authors
- Farah, M. H., & Easter, S. S.
- Affiliations
- University of Michigan (US)
- Corresponding author
- Farah, Mohamed H.
- ORCID
- Farah, Mohamed H.
- Venue
- The Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2005
- Volume
- 489
- Issue
- 1
- Pages
- 120-134
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W1982237034
- Cited by
- 73
- References
- 61
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 1 · 2023: 1 · 2022: 6 · 2021: 1 · 2020: 6 · 2019: 4 · 2018: 1 · 2017: 1 · 2016: 2 · 2014: 6 · 2013: 8 · 2012: 5
- FWCI
- 1.25
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Deep Blue (University of Michigan) (submittedVersion)
- Funders
- National Institutes of Health (5t32mh014279-33)
- National Institute of Mental Health (MH 14279)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Ophthalmology › Glaucoma and retinal disorders
- Keywords
- retinal ganglion cells, displaced amacrine cells, cell death, cell lineage, embryonic development, BrdU labeling, retrograde tracing, mouse retina
- MeSH terms
- Animals, Antimetabolites, Bromodeoxyuridine, Cell Count, Cell Nucleus, Female, Gestational Age, Immunohistochemistry, Pregnancy, Retina, Retinal Ganglion Cells, Cell Death, In Situ Nick-End Labeling, Mice
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