Abstract

A technique was developed for assaying axonal transport in retinal ganglion cells using 2 µl injections of 1% cholera toxin b-subunit conjugated to AlexaFluor488 (CTB). In vivo retinal and post-mortem brain imaging by confocal scanning laser ophthalmoscopy and post-mortem microscopy were performed. The transport of CTB was sensitive to colchicine, which disrupts axonal microtubules. The bulk rates of transport were determined to be approximately 80–90 mm/day (anterograde) and 160 mm/day (retrograde). Results demonstrate that axonal transport of CTB can be monitored in vivo in the rodent anterior visual pathway, is dependent on intact microtubules, and occurs by active transport mechanisms.

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  103. M. K. Walsh and H. A. Quigley, “In vivo time-lapse fluorescence imaging of individual retinal ganglion cells in mice,” J. Neurosci. Methods169(1), 214–221 (2008).
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  104. A. Kanamori, M. M. Catrinescu, M. Traistaru, R. Beaubien, and L. A. Levin, “In vivo imaging of retinal ganglion cell axons within the nerve fiber layer,” Invest. Ophthalmol. Vis. Sci.51(4), 2011–2018 (2010).
    [CrossRef] [PubMed]
  105. H. Murata, M. Aihara, Y. N. Chen, T. Ota, J. Numaga, and M. Araie, “Imaging mouse retinal ganglion cells and their loss in vivo by a fundus camera in the normal and ischemia-reperfusion model,” Invest. Ophthalmol. Vis. Sci.49(12), 5546–5552 (2008).
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  106. J. J. Gallagher, X. Zhang, G. J. Ziomek, R. E. Jacobs, and E. L. Bearer, “Deficits in axonal transport in hippocampal-based circuitry and the visual pathway in APP knock-out animals witnessed by manganese enhanced MRI,” Neuroimage60(3), 1856–1866 (2012).
    [CrossRef] [PubMed]
  107. E. L. Bearer, T. L. Falzone, X. W. Zhang, O. Biris, A. Rasin, and R. E. Jacobs, “Role of neuronal activity and kinesin on tract tracing by manganese-enhanced MRI (MEMRI),” Neuroimage37(Suppl 1), S37–S46 (2007).
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  108. Y. Geng, A. Dubra, L. Yin, W. H. Merigan, R. Sharma, R. T. Libby, and D. R. Williams, “Adaptive optics retinal imaging in the living mouse eye,” Biomed. Opt. Express3(4), 715–734 (2012).
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2012

G. R. Howell, I. Soto, X. Zhu, M. Ryan, D. G. Macalinao, G. L. Sousa, L. B. Caddle, K. H. MacNicoll, J. M. Barbay, V. Porciatti, M. G. Anderson, R. S. Smith, A. F. Clark, R. T. Libby, and S. W. John, “Radiation treatment inhibits monocyte entry into the optic nerve head and prevents neuronal damage in a mouse model of glaucoma,” J. Clin. Invest.122(4), 1246–1261 (2012).
[CrossRef] [PubMed]

B. Fortune, C. F. Burgoyne, G. A. Cull, J. Reynaud, and L. Wang, “Structural and functional abnormalities of retinal ganglion cells measured in vivo at the onset of optic nerve head surface change in experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.53(7), 3939–3950 (2012).
[CrossRef] [PubMed]

J. J. Gallagher, X. Zhang, G. J. Ziomek, R. E. Jacobs, and E. L. Bearer, “Deficits in axonal transport in hippocampal-based circuitry and the visual pathway in APP knock-out animals witnessed by manganese enhanced MRI,” Neuroimage60(3), 1856–1866 (2012).
[CrossRef] [PubMed]

Y. Geng, A. Dubra, L. Yin, W. H. Merigan, R. Sharma, R. T. Libby, and D. R. Williams, “Adaptive optics retinal imaging in the living mouse eye,” Biomed. Opt. Express3(4), 715–734 (2012).
[CrossRef] [PubMed]

2011

C. K. Leung, R. N. Weinreb, Z. W. Li, S. Liu, J. D. Lindsey, N. Choi, L. Liu, C. Y. Cheung, C. Ye, K. Qiu, L. J. Chen, W. H. Yung, J. G. Crowston, M. Pu, K. F. So, C. P. Pang, and D. S. Lam, “Long-term in vivo imaging and measurement of dendritic shrinkage of retinal ganglion cells,” Invest. Ophthalmol. Vis. Sci.52(3), 1539–1547 (2011).
[CrossRef] [PubMed]

G. Chidlow, A. Ebneter, J. P. M. Wood, and R. J. Casson, “The optic nerve head is the site of axonal transport disruption, axonal cytoskeleton damage and putative axonal regeneration failure in a rat model of glaucoma,” Acta Neuropathol.121(6), 737–751 (2011).
[CrossRef] [PubMed]

Y. Takihara, M. Inatani, H. Hayashi, N. Adachi, K. Iwao, T. Inoue, M. Iwao, and H. Tanihara, “Dynamic imaging of axonal transport in living retinal ganglion cells in vitro,” Invest. Ophthalmol. Vis. Sci.52(6), 3039–3045 (2011).
[CrossRef] [PubMed]

2010

S. D. Crish, R. M. Sappington, D. M. Inman, P. J. Horner, and D. J. Calkins, “Distal axonopathy with structural persistence in glaucomatous neurodegeneration,” Proc. Natl. Acad. Sci. U.S.A.107(11), 5196–5201 (2010).
[CrossRef] [PubMed]

M. Salinas-Navarro, L. Alarcón-Martínez, F. J. Valiente-Soriano, M. Jiménez-López, S. Mayor-Torroglosa, M. Avilés-Trigueros, M. P. Villegas-Pérez, and M. Vidal-Sanz, “Ocular hypertension impairs optic nerve axonal transport leading to progressive retinal ganglion cell degeneration,” Exp. Eye Res.90(1), 168–183 (2010).
[CrossRef] [PubMed]

Y. Munemasa, Y. Kitaoka, J. Kuribayashi, and S. Ueno, “Modulation of mitochondria in the axon and soma of retinal ganglion cells in a rat glaucoma model,” J. Neurochem.115(6), 1508–1519 (2010).
[CrossRef] [PubMed]

A. Kanamori, M. M. Catrinescu, M. Traistaru, R. Beaubien, and L. A. Levin, “In vivo imaging of retinal ganglion cell axons within the nerve fiber layer,” Invest. Ophthalmol. Vis. Sci.51(4), 2011–2018 (2010).
[CrossRef] [PubMed]

M. F. Cordeiro, L. Guo, K. M. Coxon, J. Duggan, S. Nizari, E. M. Normando, S. L. Sensi, A. M. Sillito, F. W. Fitzke, T. E. Salt, and S. E. Moss, “Imaging multiple phases of neurodegeneration: a novel approach to assessing cell death in vivo,” Cell Death Dis1(1), e3 (2010).
[CrossRef] [PubMed]

2009

C. K. S. Leung and R. N. Weinreb, “Experimental detection of retinal ganglion cell damage in vivo,” Exp. Eye Res.88(4), 831–836 (2009).
[CrossRef] [PubMed]

C. K. S. Leung, J. D. Lindsey, L. Chen, Q. Liu, and R. N. Weinreb, “Longitudinal profile of retinal ganglion cell damage assessed with blue-light confocal scanning laser ophthalmoscopy after ischaemic reperfusion injury,” Br. J. Ophthalmol.93(7), 964–968 (2009).
[CrossRef] [PubMed]

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci.50(12), 5872–5879 (2009).
[CrossRef] [PubMed]

G. C. Walter, R. J. Phillips, E. A. Baronowsky, and T. L. Powley, “Versatile, high-resolution anterograde labeling of vagal efferent projections with dextran amines,” J. Neurosci. Methods178(1), 1–9 (2009).
[CrossRef] [PubMed]

2008

F. Mazzoni, E. Novelli, and E. Strettoi, “Retinal ganglion cells survive and maintain normal dendritic morphology in a mouse model of inherited photoreceptor degeneration,” J. Neurosci.28(52), 14282–14292 (2008).
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B. Fortune, L. Wang, G. Cull, and G. A. Cioffi, “Intravitreal colchicine causes decreased RNFL birefringence without altering RNFL thickness,” Invest. Ophthalmol. Vis. Sci.49(1), 255–261 (2008).
[CrossRef] [PubMed]

I. Soto, E. Oglesby, B. P. Buckingham, J. L. Son, E. D. O. Roberson, M. R. Steele, D. M. Inman, M. L. Vetter, P. J. Horner, and N. Marsh-Armstrong, “Retinal ganglion cells downregulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model,” J. Neurosci.28(2), 548–561 (2008).
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C. Balaratnasingam, W. H. Morgan, L. Bass, L. Ye, C. McKnight, S. J. Cringle, and D. Y. Yu, “Elevated pressure induced astrocyte damage in the optic nerve,” Brain Res.1244, 142–154 (2008).
[CrossRef] [PubMed]

C. K. S. Leung, J. D. Lindsey, J. G. Crowston, W. K. Ju, Q. Liu, D. U. Bartsch, and R. N. Weinreb, “In vivo imaging of murine retinal ganglion cells,” J. Neurosci. Methods168(2), 475–478 (2008).
[CrossRef] [PubMed]

C. K. Leung, J. D. Lindsey, J. G. Crowston, C. Lijia, S. Chiang, and R. N. Weinreb, “Longitudinal profile of retinal ganglion cell damage after optic nerve crush with blue-light confocal scanning laser ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci.49(11), 4898–4902 (2008).
[CrossRef] [PubMed]

D. C. Gray, R. Wolfe, B. P. Gee, D. Scoles, Y. Geng, B. D. Masella, A. Dubra, S. Luque, D. R. Williams, and W. H. Merigan, “In vivo imaging of the fine structure of rhodamine-labeled macaque retinal ganglion cells,” Invest. Ophthalmol. Vis. Sci.49(1), 467–473 (2008).
[CrossRef] [PubMed]

H. Murata, M. Aihara, Y. N. Chen, T. Ota, J. Numaga, and M. Araie, “Imaging mouse retinal ganglion cells and their loss in vivo by a fundus camera in the normal and ischemia-reperfusion model,” Invest. Ophthalmol. Vis. Sci.49(12), 5546–5552 (2008).
[CrossRef] [PubMed]

M. K. Walsh and H. A. Quigley, “In vivo time-lapse fluorescence imaging of individual retinal ganglion cells in mice,” J. Neurosci. Methods169(1), 214–221 (2008).
[CrossRef] [PubMed]

B. Fortune, G. A. Cull, and C. F. Burgoyne, “Relative course of retinal nerve fiber layer birefringence and thickness and retinal function changes after optic nerve transection,” Invest. Ophthalmol. Vis. Sci.49(10), 4444–4452 (2008).
[CrossRef] [PubMed]

2007

E. L. Bearer, T. L. Falzone, X. W. Zhang, O. Biris, A. Rasin, and R. E. Jacobs, “Role of neuronal activity and kinesin on tract tracing by manganese-enhanced MRI (MEMRI),” Neuroimage37(Suppl 1), S37–S46 (2007).
[CrossRef] [PubMed]

C. Balaratnasingam, W. H. Morgan, L. Bass, G. Matich, S. J. Cringle, and D. Y. Yu, “Axonal transport and cytoskeletal changes in the laminar regions after elevated intraocular pressure,” Invest. Ophthalmol. Vis. Sci.48(8), 3632–3644 (2007).
[CrossRef] [PubMed]

T. Misgeld, M. Kerschensteiner, F. M. Bareyre, R. W. Burgess, and J. W. Lichtman, “Imaging axonal transport of mitochondria in vivo,” Nat. Methods4(7), 559–561 (2007).
[CrossRef] [PubMed]

2006

K. R. G. Martin, H. A. Quigley, D. Valenta, J. Kielczewski, and M. E. Pease, “Optic nerve dynein motor protein distribution changes with intraocular pressure elevation in a rat model of glaucoma,” Exp. Eye Res.83(2), 255–262 (2006).
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M. D. Fleming, R. M. Benca, and M. Behan, “Retinal projections to the subcortical visual system in congenic albino and pigmented rats,” Neuroscience143(3), 895–904 (2006).
[CrossRef] [PubMed]

D. C. Gray, W. Merigan, J. I. Wolfing, B. P. Gee, J. Porter, A. Dubra, T. H. Twietmeyer, K. Ahamd, R. Tumbar, F. Reinholz, and D. R. Williams, “In vivo fluorescence imaging of primate retinal ganglion cells and retinal pigment epithelial cells,” Opt. Express14(16), 7144–7158 (2006).
[CrossRef] [PubMed]

T. Higashide, I. Kawaguchi, S. Ohkubo, H. Takeda, and K. Sugiyama, “In vivo imaging and counting of rat retinal ganglion cells using a scanning laser ophthalmoscope,” Invest. Ophthalmol. Vis. Sci.47(7), 2943–2950 (2006).
[CrossRef] [PubMed]

L. Guo, T. E. Salt, A. Maass, V. Luong, S. E. Moss, F. W. Fitzke, and M. F. Cordeiro, “Assessment of neuroprotective effects of glutamate modulation on glaucoma-related retinal ganglion cell apoptosis in vivo,” Invest. Ophthalmol. Vis. Sci.47(2), 626–633 (2006).
[CrossRef] [PubMed]

2005

X. R. Huang and R. W. Knighton, “Microtubules contribute to the birefringence of the retinal nerve fiber layer,” Invest. Ophthalmol. Vis. Sci.46(12), 4588–4593 (2005).
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S. Roy, B. Zhang, V. M. Lee, and J. Q. Trojanowski, “Axonal transport defects: a common theme in neurodegenerative diseases,” Acta Neuropathol.109(1), 5–13 (2005).
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P. J. Hollenbeck and W. M. Saxton, “The axonal transport of mitochondria,” J. Cell Sci.118(23), 5411–5419 (2005).
[CrossRef] [PubMed]

2004

J. E. Morgan, “Circulation and axonal transport in the optic nerve,” Eye (Lond.)18(11), 1089–1095 (2004).
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M. F. Cordeiro, L. Guo, V. Luong, G. Harding, W. Wang, H. E. Jones, S. E. Moss, A. M. Sillito, and F. W. Fitzke, “Real-time imaging of single nerve cell apoptosis in retinal neurodegeneration,” Proc. Natl. Acad. Sci. U.S.A.101(36), 13352–13356 (2004).
[CrossRef] [PubMed]

2003

A. Brown, “Axonal transport of membranous and nonmembranous cargoes: a unified perspective,” J. Cell Biol.160(6), 817–821 (2003).
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C. C. Wu, R. M. Russell, R. T. Nguyen, and H. J. Karten, “Tracing developing pathways in the brain: a comparison of carbocyanine dyes and cholera toxin b subunit,” Neuroscience117(4), 831–845 (2003).
[CrossRef] [PubMed]

2002

X. R. Huang and R. W. Knighton, “Linear birefringence of the retinal nerve fiber layer measured in vitro with a multispectral imaging micropolarimeter,” J. Biomed. Opt.7(2), 199–204 (2002).
[CrossRef] [PubMed]

S. Thanos, L. Indorf, and R. Naskar, “In vivo FM: using conventional fluorescence microscopy to monitor retinal neuronal death in vivo,” Trends Neurosci.25(9), 441–444 (2002).
[CrossRef] [PubMed]

2000

C. Kaether, P. Skehel, and C. G. Dotti, “Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons,” Mol. Biol. Cell11(4), 1213–1224 (2000).
[PubMed]

R. D. Vale and R. A. Milligan, “The way things move: looking under the hood of molecular motor proteins,” Science288(5463), 88–95 (2000).
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A. J. Reynolds, S. E. Bartlett, and I. A. Hendry, “Molecular mechanisms regulating the retrograde axonal transport of neurotrophins,” Brain Res. Brain Res. Rev.33(2-3), 169–178 (2000).
[CrossRef] [PubMed]

H. A. Quigley, S. J. McKinnon, D. J. Zack, M. E. Pease, L. A. Kerrigan-Baumrind, D. F. Kerrigan, and R. S. Mitchell, “Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats,” Invest. Ophthalmol. Vis. Sci.41(11), 3460–3466 (2000).
[PubMed]

M. E. Pease, S. J. McKinnon, H. A. Quigley, L. A. Kerrigan-Baumrind, and D. J. Zack, “Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.41(3), 764–774 (2000).
[PubMed]

S. Roy, P. Coffee, G. Smith, R. K. Liem, S. T. Brady, and M. M. Black, “Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport,” J. Neurosci.20(18), 6849–6861 (2000).
[PubMed]

L. Wang, C. L. Ho, D. Sun, R. K. H. Liem, and A. Brown, “Rapid movement of axonal neurofilaments interrupted by prolonged pauses,” Nat. Cell Biol.2(3), 137–141 (2000).
[CrossRef] [PubMed]

1999

J. Lu, P. Shiromani, and C. B. Saper, “Retinal input to the sleep-active ventrolateral preoptic nucleus in the rat,” Neuroscience93(1), 209–214 (1999).
[CrossRef] [PubMed]

C. C. Wu, R. M. Russell, and H. J. Karten, “The transport rate of cholera toxin B subunit in the retinofugal pathways of the chick,” Neuroscience92(2), 665–676 (1999).
[CrossRef] [PubMed]

R. Engelmann and B. A. Sabel, “In vivo imaging of mammalian central nervous system neurons with the in vivo confocal neuroimaging (ICON) method,” Methods Enzymol.307, 563–570 (1999).
[CrossRef] [PubMed]

1998

T. Nakata, S. Terada, and N. Hirokawa, “Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons,” J. Cell Biol.140(3), 659–674 (1998).
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N. Rivera and N. Lugo, “Four retinal ganglion cell types that project to the superior colliculus in the thirteen-lined ground squirrel (Spermophilus tridecemlineatus),” J. Comp. Neurol.396(1), 105–120 (1998).
[CrossRef] [PubMed]

1997

S. Reuss and K. Decker, “Anterograde tracing of retinohypothalamic afferents with Fluoro-Gold,” Brain Res.745(1-2), 197–204 (1997).
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Q. Zhou and R. W. Knighton, “Light scattering and form birefringence of parallel cylindrical arrays that represent cellular organelles of the retinal nerve fiber layer,” Appl. Opt.36(10), 2273–2285 (1997).
[CrossRef] [PubMed]

B. A. Sabel, R. Engelmann, and M. F. Humphrey, “In vivo confocal neuroimaging (ICON) of CNS neurons,” Nat. Med.3(2), 244–247 (1997).
[CrossRef] [PubMed]

1996

A. Angelucci, F. Clascá, and M. Sur, “Anterograde axonal tracing with the subunit B of cholera toxin: a highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains,” J. Neurosci. Methods65(1), 101–112 (1996).
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1994

S. Thanos, J. Kacza, J. Seeger, and J. Mey, “Old dyes for new scopes: the phagocytosis-dependent long-term fluorescence labelling of microglial cells in vivo,” Trends Neurosci.17(5), 177–182 (1994).
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1993

T. A. Viancour and N. A. Kreiter, “Vesicular fast axonal transport rates in young and old rat axons,” Brain Res.628(1-2), 209–217 (1993).
[CrossRef] [PubMed]

1992

J. D. Mikkelsen, “Visualization of efferent retinal projections by immunohistochemical identification of cholera toxin subunit B,” Brain Res. Bull.28(4), 619–623 (1992).
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M. Hirakawa, J. T. McCabe, and M. Kawata, “Time-related changes in the labeling pattern of motor and sensory neurons innervating the gastrocnemius muscle, as revealed by the retrograde transport of the cholera toxin B subunit,” Cell Tissue Res.267(3), 419–427 (1992).
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1991

L. Dandona, A. Hendrickson, and H. A. Quigley, “Selective effects of experimental glaucoma on axonal transport by retinal ganglion cells to the dorsal lateral geniculate nucleus,” Invest. Ophthalmol. Vis. Sci.32(5), 1593–1599 (1991).
[PubMed]

1990

P. H. Luppi, P. Fort, and M. Jouvet, “Iontophoretic application of unconjugated cholera toxin B subunit (CTb) combined with immunohistochemistry of neurochemical substances: a method for transmitter identification of retrogradely labeled neurons,” Brain Res.534(1-2), 209–224 (1990).
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1989

J. J. Quattrochi, A. N. Mamelak, R. D. Madison, J. D. Macklis, and J. A. Hobson, “Mapping neuronal inputs to REM sleep induction sites with carbachol-fluorescent microspheres,” Science245(4921), 984–986 (1989).
[CrossRef] [PubMed]

1988

J. O. Johansson, “Inhibition and recovery of retrograde axoplasmic transport in rat optic nerve during and after elevated IOP in vivo,” Exp. Eye Res.46(2), 223–227 (1988).
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M. Vidal-Sanz, M. P. Villegas-Pérez, G. M. Bray, and A. J. Aguayo, “Persistent retrograde labeling of adult rat retinal ganglion cells with the carbocyanine dye diI,” Exp. Neurol.102(1), 92–101 (1988).
[CrossRef] [PubMed]

1987

P. H. Luppi, K. Sakai, D. Salvert, P. Fort, and M. Jouvet, “Peptidergic hypothalamic afferents to the cat nucleus raphe pallidus as revealed by a double immunostaining technique using unconjugated cholera toxin as a retrograde tracer,” Brain Res.402(2), 339–345 (1987).
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A. C. Breuer, M. P. Lynn, M. B. Atkinson, S. M. Chou, A. J. Wilbourn, K. E. Marks, J. E. Culver, and E. J. Fleegler, “Fast axonal transport in amyotrophic lateral sclerosis: an intra-axonal organelle traffic analysis,” Neurology37(5), 738–748 (1987).
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1986

M. G. Honig and R. I. Hume, “Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures,” J. Cell Biol.103(1), 171–187 (1986).
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J. O. Johansson, “Retrograde axoplasmic transport in rat optic nerve in vivo. What causes blockage at increased intraocular pressure?” Exp. Eye Res.43(4), 653–660 (1986).
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1984

L. C. Katz, A. Burkhalter, and W. J. Dreyer, “Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex,” Nature310(5977), 498–500 (1984).
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R. J. Lasek, J. A. Garner, and S. T. Brady, “Axonal transport of the cytoplasmic matrix,” J. Cell Biol.99(1), 212s–221s (1984).
[CrossRef] [PubMed]

1983

N. K. Gonatas, A. Stieber, J. Gonatas, T. Mommoi, and P. H. Fishman, “Endocytosis of exogenous GM1 ganglioside and cholera toxin by neuroblastoma cells,” Mol. Cell. Biol.3(1), 91–101 (1983).
[PubMed]

C. Davidson, W. R. Green, and V. G. Wong, “Retinal atrophy induced by intravitreous colchicine,” Invest. Ophthalmol. Vis. Sci.24(3), 301–311 (1983).
[PubMed]

1982

X. C. Wan, J. Q. Trojanowski, and J. O. Gonatas, “Cholera toxin and wheat germ agglutinin conjugates as neuroanatomical probes: their uptake and clearance, transganglionic and retrograde transport and sensitivity,” Brain Res.243(2), 215–224 (1982).
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J. Q. Trojanowski, J. O. Gonatas, and N. K. Gonatas, “Horseradish peroxidase (HRP) conjugates of cholera toxin and lectins are more sensitive retrogradely transported markers than free HRP,” Brain Res.231(1), 33–50 (1982).
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1981

R. L. Radius and D. R. Anderson, “Reversibility of optic nerve damage in primate eyes subjected to intraocular pressure above systolic blood pressure,” Br. J. Ophthalmol.65(10), 661–672 (1981).
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R. L. Radius and D. R. Anderson, “Rapid axonal transport in primate optic nerve. Distribution of pressure-induced interruption,” Arch. Ophthalmol.99(4), 650–654 (1981).
[CrossRef] [PubMed]

I. G. Morgan, “Intraocular colchicine selectively destroys immature ganglion cells in chicken retina,” Neurosci. Lett.24(3), 255–260 (1981).
[CrossRef] [PubMed]

1980

M. M. Black and R. J. Lasek, “Slow components of axonal transport: two cytoskeletal networks,” J. Cell Biol.86(2), 616–623 (1980).
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H. A. Quigley and E. M. Addicks, “Chronic experimental glaucoma in primates. II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport,” Invest. Ophthalmol. Vis. Sci.19(2), 137–152 (1980).
[PubMed]

R. L. Radius and D. R. Anderson, “Breakdown of the normal optic nerve head blood-brain barrier following acute elevation of intraocular pressure in experimental animals,” Invest. Ophthalmol. Vis. Sci.19(3), 244–255 (1980).
[PubMed]

R. L. Radius, E. L. Schwartz, and D. R. Anderson, “Failure of unilateral carotid artery ligation to affect pressure-induced interruption of rapid axonal transport in primate optic nerves,” Invest. Ophthalmol. Vis. Sci.19(2), 153–157 (1980).
[PubMed]

B. Grafstein and D. S. Forman, “Intracellular transport in neurons,” Physiol. Rev.60(4), 1167–1283 (1980).
[PubMed]

1979

H. A. Quigley, J. Guy, and D. R. Anderson, “Blockade of rapid axonal transport. Effect of intraocular pressure elevation in primate optic nerve,” Arch. Ophthalmol.97(3), 525–531 (1979).
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P. W. Land and R. D. Lund, “Development of the rat’s uncrossed retinotectal pathway and its relation to plasticity studies,” Science205(4407), 698–700 (1979).
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1978

K. C. Joseph, S. U. Kim, A. Stieber, and N. K. Gonatas, “Endocytosis of cholera toxin into neuronal GERL,” Proc. Natl. Acad. Sci. U.S.A.75(6), 2815–2819 (1978).
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D. S. Minckler, A. H. Bunt, and I. B. Klock, “Radioautographic and cytochemical ultrastructural studies of axoplasmic transport in the monkey optic nerve head,” Invest. Ophthalmol. Vis. Sci.17(1), 33–50 (1978).
[PubMed]

D. Gaasterland, T. Tanishima, and T. Kuwabara, “Axoplasmic flow during chronic experimental glaucoma. 1. Light and electron microscopic studies of the monkey optic nervehead during development of glaucomatous cupping,” Invest. Ophthalmol. Vis. Sci.17(9), 838–846 (1978).
[PubMed]

1977

D. S. Minckler, A. H. Bunt, and G. W. Johanson, “Orthograde and retrograde axoplasmic transport during acute ocular hypertension in the monkey,” Invest. Ophthalmol. Vis. Sci.16(5), 426–441 (1977).
[PubMed]

H. A. Quigley and D. R. Anderson, “Distribution of axonal transport blockade by acute intraocular pressure elevation in the primate optic nerve head,” Invest. Ophthalmol. Vis. Sci.16(7), 640–644 (1977).
[PubMed]

M. E. Schwab and H. Thoenen, “Retrograde axonal and transsynaptic transport of macromolecules: physiological and pathophysiological importance,” Agents Actions7(3), 361–368 (1977).
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1976

H. Quigley and D. R. Anderson, “The dynamics and location of axonal transport blockade by acute intraocular pressure elevation in primate optic nerve,” Invest. Ophthalmol.15(8), 606–616 (1976).
[PubMed]

R. D. Lund and S. D. Hauschka, “Transplanted neural tissue develops connections with host rat brain,” Science193(4253), 582–584 (1976).
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U. C. Dräger and D. H. Hubel, “Topography of visual and somatosensory projections to mouse superior colliculus,” J. Neurophysiol.39(1), 91–101 (1976).
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1974

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K. A. James, J. J. Bray, I. G. Morgan, and L. Austin, “The effect of colchicine on the transport of axonal protein in the chicken,” Biochem. J.117(4), 767–771 (1970).
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S. D. Crish, R. M. Sappington, D. M. Inman, P. J. Horner, and D. J. Calkins, “Distal axonopathy with structural persistence in glaucomatous neurodegeneration,” Proc. Natl. Acad. Sci. U.S.A.107(11), 5196–5201 (2010).
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G. Chidlow, A. Ebneter, J. P. M. Wood, and R. J. Casson, “The optic nerve head is the site of axonal transport disruption, axonal cytoskeleton damage and putative axonal regeneration failure in a rat model of glaucoma,” Acta Neuropathol.121(6), 737–751 (2011).
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A. Kanamori, M. M. Catrinescu, M. Traistaru, R. Beaubien, and L. A. Levin, “In vivo imaging of retinal ganglion cell axons within the nerve fiber layer,” Invest. Ophthalmol. Vis. Sci.51(4), 2011–2018 (2010).
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C. K. S. Leung, J. D. Lindsey, L. Chen, Q. Liu, and R. N. Weinreb, “Longitudinal profile of retinal ganglion cell damage assessed with blue-light confocal scanning laser ophthalmoscopy after ischaemic reperfusion injury,” Br. J. Ophthalmol.93(7), 964–968 (2009).
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H. Murata, M. Aihara, Y. N. Chen, T. Ota, J. Numaga, and M. Araie, “Imaging mouse retinal ganglion cells and their loss in vivo by a fundus camera in the normal and ischemia-reperfusion model,” Invest. Ophthalmol. Vis. Sci.49(12), 5546–5552 (2008).
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G. Chidlow, A. Ebneter, J. P. M. Wood, and R. J. Casson, “The optic nerve head is the site of axonal transport disruption, axonal cytoskeleton damage and putative axonal regeneration failure in a rat model of glaucoma,” Acta Neuropathol.121(6), 737–751 (2011).
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B. Fortune, L. Wang, G. Cull, and G. A. Cioffi, “Intravitreal colchicine causes decreased RNFL birefringence without altering RNFL thickness,” Invest. Ophthalmol. Vis. Sci.49(1), 255–261 (2008).
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G. R. Howell, I. Soto, X. Zhu, M. Ryan, D. G. Macalinao, G. L. Sousa, L. B. Caddle, K. H. MacNicoll, J. M. Barbay, V. Porciatti, M. G. Anderson, R. S. Smith, A. F. Clark, R. T. Libby, and S. W. John, “Radiation treatment inhibits monocyte entry into the optic nerve head and prevents neuronal damage in a mouse model of glaucoma,” J. Clin. Invest.122(4), 1246–1261 (2012).
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A. Angelucci, F. Clascá, and M. Sur, “Anterograde axonal tracing with the subunit B of cholera toxin: a highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains,” J. Neurosci. Methods65(1), 101–112 (1996).
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Coffee, P.

S. Roy, P. Coffee, G. Smith, R. K. Liem, S. T. Brady, and M. M. Black, “Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport,” J. Neurosci.20(18), 6849–6861 (2000).
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C. Balaratnasingam, W. H. Morgan, L. Bass, L. Ye, C. McKnight, S. J. Cringle, and D. Y. Yu, “Elevated pressure induced astrocyte damage in the optic nerve,” Brain Res.1244, 142–154 (2008).
[CrossRef] [PubMed]

C. Balaratnasingam, W. H. Morgan, L. Bass, G. Matich, S. J. Cringle, and D. Y. Yu, “Axonal transport and cytoskeletal changes in the laminar regions after elevated intraocular pressure,” Invest. Ophthalmol. Vis. Sci.48(8), 3632–3644 (2007).
[CrossRef] [PubMed]

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S. D. Crish, R. M. Sappington, D. M. Inman, P. J. Horner, and D. J. Calkins, “Distal axonopathy with structural persistence in glaucomatous neurodegeneration,” Proc. Natl. Acad. Sci. U.S.A.107(11), 5196–5201 (2010).
[CrossRef] [PubMed]

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C. K. Leung, R. N. Weinreb, Z. W. Li, S. Liu, J. D. Lindsey, N. Choi, L. Liu, C. Y. Cheung, C. Ye, K. Qiu, L. J. Chen, W. H. Yung, J. G. Crowston, M. Pu, K. F. So, C. P. Pang, and D. S. Lam, “Long-term in vivo imaging and measurement of dendritic shrinkage of retinal ganglion cells,” Invest. Ophthalmol. Vis. Sci.52(3), 1539–1547 (2011).
[CrossRef] [PubMed]

C. K. Leung, J. D. Lindsey, J. G. Crowston, C. Lijia, S. Chiang, and R. N. Weinreb, “Longitudinal profile of retinal ganglion cell damage after optic nerve crush with blue-light confocal scanning laser ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci.49(11), 4898–4902 (2008).
[CrossRef] [PubMed]

C. K. S. Leung, J. D. Lindsey, J. G. Crowston, W. K. Ju, Q. Liu, D. U. Bartsch, and R. N. Weinreb, “In vivo imaging of murine retinal ganglion cells,” J. Neurosci. Methods168(2), 475–478 (2008).
[CrossRef] [PubMed]

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B. Fortune, L. Wang, G. Cull, and G. A. Cioffi, “Intravitreal colchicine causes decreased RNFL birefringence without altering RNFL thickness,” Invest. Ophthalmol. Vis. Sci.49(1), 255–261 (2008).
[CrossRef] [PubMed]

Cull, G. A.

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Figures (10)

Fig. 1
Fig. 1

Anterograde assay showing the time-course of CTB uptake into RGCs and their axons within the eye in vivo by CSLO. (a) CSLO infrared reflectance image (“CSLO-IR”) provides orientation to the ocular fundus. (b)–(c) CSLO fluorescence (“CSLO-FL”) images taken at 0.5 h (b), and 24 h (c) after intravitreal CTB injection demonstrate increasing uptake and transport of CTB in RGC axons over time. RGC uptake of CTB is first seen superiorly near the injection site; axon bundle filling typically progresses toward the optic disc and throughout the rest of the fundus. (d) High magnification CSLO-FL image obtained in a different eye 24 h after CTB injection and (e) flat-mount retinal microscopy (x20) corresponding to inset box in (d) demonstrate fluorescent RGC soma (arrow) and axons. Scale bar in (a) applies (a)–(c).

Fig. 2
Fig. 2

Results of anterograde axonal transport 24 h after unilateral CTB injection. The right eye (a), (b) received an intravitreal injection of CTB, while the left eye (c), (d) was a non-injected control. CSLO images in vivo (a), (c) and post-mortem micrographs (x5) of flat-mount retina (b), (d) show strong CTB fluorescence in RGCs and axons of the right eye only. Post-mortem imaging of the optic nerves and chiasm (ventral view, (e), (f) and superior colliculi (dorsal view, (g), (h)) obtained either by CSLO (e), (g) or by epi-fluorescence microscopy (x5) montages (f), (h) show unilateral fluorescence of the ipsilateral optic nerve and contralateral superior colliculus. This indicates that CSLO and microscopy are both able to clearly detect successfully transported CTB to the optic nerves and superior colliculi. Scale bars: (a) applies (a)–(d); (g) applies (g), (h). Abbreviations: fluorescence (FL), right eye (OD), left eye (OS), right (R), left (L), optic nerves (ON), superior colliculi (SC).

Fig. 3
Fig. 3

Results of retrograde axonal transport 24 h after CTB injection bilaterally into the superior colliculi. (a)–(d) CSLO fundus images in vivo and post-mortem micrographs (x5) of flat-mount retinas from the right and left eyes demonstrate strong CTB fluorescence of RGC somas and optic discs bilaterally, indicating successful axonal transport of CTB. Higher magnification CSLO fundus image in vivo (e) and post-mortem microscopy (x20) of the retina (f) shows the fluorescent RGC somas and dendrites. Box in (e) indicates region shown in (f). Post-mortem imaging of the dorsal midbrain by CSLO (g) reveals bilateral fluorescence of both superior colliculi indicating that CTB diffuses throughout the superior colliculi from the central injection sites. Scale bars: (a) applies (a)–(d). Abbreviations: fluorescence (FL), right eye (OD), left eye (OS), right (R), left (L), optic nerves (ON), superior colliculi (SC).

Fig. 4
Fig. 4

Effect of colchicine on anterograde axonal transport. (a)–(d) Fluorescence mode CSLO fundus images obtained in vivo 24 h after CTB injections from the right and left eyes of a bilateral CTB positive control rat (a), (b) and another bilateral CTB rat that had unilateral (OD) pre-treatment with intravitreal colchicine (c), (d). (e)-(h) High magnification post-mortem fluorescence micrographs of flat-mount retinas from the bilateral positive control (x20; (e), (f)) and the unilateral colchicine animal (x10; (g), (h)). The CSLO images and the micrographs demonstrate strong CTB fluorescence of RGC somas, RNFL and optic discs bilaterally, indicating successful uptake of CTB by RGCs across all retinas. Box in (a)–(d) indicates region shown in (e)–(h). Post-mortem imaging of the ventral and dorsal midbrain by CSLO (i)–(l) reveals bilateral fluorescence of both optic nerves and tracts (i) and both superior colliculi (j) in the bilateral positive control rat, indicating patent axonal transport of CTB in both pathways. However for the unilateral colchicine rat, the ipsilateral optic nerve and contralateral optic tract (k) and contralateral superior colliculus (l) to the colchicine-injected eye exhibit minimal fluorescence, indicating disruption of axonal transport in the colchicine-treated pathway. The fellow control eye (OS) in the unilateral colchicine rat shows patent axonal transport (CTB fluorescence) at its corresponding brain structures (k), (l). Scale bars: (a) applies (a)–(d), (e) applies (e)–(h), (i) applies (i)–(l). Abbreviations: fluorescence (FL), right eye (OD), left eye (OS), right (R), left (L), optic nerves (ON), superior colliculi (SC).

Fig. 5
Fig. 5

Effect of colchicine on anterograde axonal transport. Average fluorescence intensity (±SEM) is shown for the group of rats (n = 7, bars with small checks) in which one eye was pre-treated with an intravitreal injection of either vehicle or colchicine prior to intravitreal injection of CTB; a unilateral control group of rats (n = 3, bars with larger checks) in which the intravitreal injection of CTB was unilateral with the fellow eye serving as a non-injected control (CTB–); a bilateral positive control group of rats (n = 4, open bars) in which CTB was injected into the vitreous bilaterally (CTB+)); and a negative control group of naïve rats (n = 3, solid bars) which were sacrificed without any CTB injection in either eye (CTB–). Colchicine reduced the fluorescence intensity of the contralateral superior colliculus 24 h after CTB injection to the level of non-injected controls (CTB–); contrast between hemispheres was nearly as great as that in the group of unilateral controls. Abbreviations: right superior colliculus (R) and left superior colliculus (L).

Fig. 6
Fig. 6

Effect of colchicine on retrograde axonal transport. (a)–(d) CSLO fluorescence fundus images in vivo of the right (a) and left (c) eyes and post-mortem micrographs (x10) of flat-mount right (b) and left (d) retinas, 24 h after bilateral superior colliculi injections of CTB and unilateral (OD) pre-treatment with intravitreal colchicine. There was substantially less CTB fluorescence in the RGCs of the eye pre-treated with colchicine (a), (b) than the fellow control eye (c), (d), indicating disruption of retrograde axonal transport of CTB in the colchicine eye only. The RGC fluorescence in the fellow control eye (c), (d) is similar to the that in the bilateral positive control shown in Fig. 3, indicating patent axonal transport of CTB. (e) CSLO infrared reflectance image provides orientation to the dorsal midbrain including the superior colliculi. (f) Accompanying CSLO in fluorescence mode shows that both superior colliculi fluoresce equally with near full coverage, indicating that the difference in RGC fluorescence is not due to a failed CTB injection. Scale bars: (a) applies (a), (c), (b) applies (b), (d), (e) applies (e), (f). Abbreviations: fluorescence (FL), right eye (OD), left eye (OS), right (R), left (L), infra-red (IR), superior colliculi (SC).

Fig. 7
Fig. 7

Effect of colchicine on retrograde axonal transport. Average RGC density (±SEM) measured in vivo by CSLO (a) and post-mortem by microscopy of retinal flat-mounts (b) is shown for the group of rats (n = 5, bars with checks) in which one eye was pre-treated with an intravitreal injection of either vehicle or colchicine prior to bilateral injection of CTB into the superior colliculus; a bilateral positive control group of rats (n = 9, open bars) in which CTB was injected into the superior colliculus bilaterally (CTB+)); and a negative control group of naïve rats (n = 3, solid bars) which were sacrificed without any CTB injection (CTB–). Colchicine reduced the density of CTB–positive RGCs nearly completely (i.e., nearly to the level of non-injected controls). Abbreviations: right eye (OD) and left eye (OS).

Fig. 8
Fig. 8

Results of anterograde transport rate experiment. Representative examples from a cross-sectional series demonstrate the time of earliest detected CTB fluorescence at the optic nerves and superior colliculi after unilateral intravitreal CTB injections into the right eye. (a)–(c) Post-mortem imaging (montages) of the ventral midbrain by CSLO at (a) 5h, (b) 6h, and (c) 7h after CTB injection reveals greater fluorescence in the ipsilateral (right) optic nerve than the left, first noticeable at 5h (a) and more obviously noticeable at 6h (b) and 7h (c). (d)–(f) Post-mortem imaging of the corresponding dorsal midbrains by CSLO at (d) 5h, (e) 6h, and (f) 7h shows greater relative fluorescence intensity in the contralateral (left) superior colliculus, first noticeable at 6h (e) and more clearly noticeable by 7h (f). These results show that CTB reaches the optic nerve by 5h after intravitreal injection and the superior colliculus by 6h, indicating that CTB travels by fast active axonal transport when compared to known rates [1]. Scale bars: (a) applies (a)–(c), (d) applies (d)–(f). Abbreviations: fluorescence (FL), right eye (OD), right (R), left (L), optic nerves (ON), superior colliculi (SC).

Fig. 9
Fig. 9

Results of experiment to estimate bulk-rate of anterograde axonal CTB transport. Relative fluorescence intensity (CTB injected side (Exp) relative to non-injected (Ctrl) side) is plotted versus time after unilateral intravitreal CTB injection for the ipsilateral optic nerve (a) and contralateral superior colliculus (b). Solid line through data represents results of fit to the data of the equation: Y = IF(X < X0, Y0,Y0 + (Plateau – Y0)*(1 – exp(–K*(X – X0)))), which was used as a secondary method to determine the first time after injection that fluorescence intensity began to rise above that of the opposite-side structure (i.e., the X0 parameter corresponding to the point that exponential growth began from baseline). For optic nerve, X0 = 1.64 (95% CI −0.07 to 3.35); for superior colliculus, X0 = 5.48 (95% CI 2.78 to 8.19). Error bars = SEM. N ≥ 3 rats per time point. Abbreviations: Exp = Experimental, Ctrl = Control.

Fig. 10
Fig. 10

Examples from a longitudinal series demonstrate the time of earliest detected CTB fluorescence at the optic disc and RGCs after bilateral superior colliculi CTB injections in order to determine the rate of retrograde transport of CTB. CSLO fluorescence fundus images (a)–(f) were taken in vivo at pre-injection baseline (a), (d) then every 30 min from 2 to 5 h after CTB injection. At 3h the first sign of optic disc fluorescence (arrow) was noted in the right (b) and left (e) eyes, clearly brighter than at baseline. At 4h the first sign of RGC fluorescence (asterisk) was noted predominantly superior-nasally in the right (c) and left (f) eyes. Post-mortem micrographs (x10) of flat-mount right (g) and left (h) retinas at 5h after injection confirm CTB fluorescence at the disc and RGCs in all retinal quadrants. Brightness and contrast of images were adjusted to maximize visibility in panels of this figure. Scale bars: (a) applies (a)–(f), (g) applies (g), (h).. Abbreviations: fluorescence (FL), right eye (OD), left eye (OS), superior (S), inferior (I), nasal (N), temporal (T).

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Table 1 Retrograde assay CSLO, microscopy and stereotactic surgery details

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