OSA's Digital Library

Biomedical Optics Express

Biomedical Optics Express

  • Editor: Joseph A. Izatt
  • Vol. 4, Iss. 2 — Feb. 1, 2013
  • pp: 364–386

Imaging axonal transport in the rat visual pathway

Carla J. Abbott, Tiffany E. Choe, Theresa A. Lusardi, Claude F. Burgoyne, Lin Wang, and Brad Fortune  »View Author Affiliations


Biomedical Optics Express, Vol. 4, Issue 2, pp. 364-386 (2013)
http://dx.doi.org/10.1364/BOE.4.000364


View Full Text Article

Enhanced HTML    Acrobat PDF (5269 KB)





Browse Journals / Lookup Meetings

Browse by Journal and Year


   


Lookup Conference Papers

Close Browse Journals / Lookup Meetings

Article Tools

Share
Citations

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.

© 2013 OSA

OCIS Codes
(170.3880) Medical optics and biotechnology : Medical and biological imaging
(170.2655) Medical optics and biotechnology : Functional monitoring and imaging

ToC Category:
Functional Imaging

History
Original Manuscript: November 19, 2012
Revised Manuscript: January 10, 2013
Manuscript Accepted: January 28, 2013
Published: January 30, 2013

Citation
Carla J. Abbott, Tiffany E. Choe, Theresa A. Lusardi, Claude F. Burgoyne, Lin Wang, and Brad Fortune, "Imaging axonal transport in the rat visual pathway," Biomed. Opt. Express 4, 364-386 (2013)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-4-2-364


Sort:  Author  |  Year  |  Journal  |  Reset  

References

  1. A. Brown, “Axonal transport of membranous and nonmembranous cargoes: a unified perspective,” J. Cell Biol.160(6), 817–821 (2003). [CrossRef] [PubMed]
  2. R. D. Vale and R. A. Milligan, “The way things move: looking under the hood of molecular motor proteins,” Science288(5463), 88–95 (2000). [CrossRef] [PubMed]
  3. 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]
  4. P. J. Hollenbeck and W. M. Saxton, “The axonal transport of mitochondria,” J. Cell Sci.118(23), 5411–5419 (2005). [CrossRef] [PubMed]
  5. 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]
  6. 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]
  7. 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). [CrossRef] [PubMed]
  8. 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). [CrossRef] [PubMed]
  9. 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]
  10. 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]
  11. D. R. Anderson and A. Hendrickson, “Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve,” Invest. Ophthalmol.13(10), 771–783 (1974). [PubMed]
  12. 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]
  13. 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). [CrossRef] [PubMed]
  14. 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]
  15. 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]
  16. 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]
  17. 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]
  18. 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]
  19. 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]
  20. P. W. Lampert, M. H. Vogel, and L. E. Zimmerman, “Pathology of the optic nerve in experimental acute glaucoma. Electron microscopic studies,” Invest. Ophthalmol.7(2), 199–213 (1968). [PubMed]
  21. 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). [CrossRef] [PubMed]
  22. 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]
  23. 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]
  24. 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]
  25. 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). [CrossRef] [PubMed]
  26. 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]
  27. 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]
  28. 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]
  29. 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]
  30. 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). [CrossRef] [PubMed]
  31. 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]
  32. 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]
  33. 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). [CrossRef] [PubMed]
  34. 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). [CrossRef] [PubMed]
  35. 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). [CrossRef] [PubMed]
  36. 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]
  37. 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]
  38. S. Reuss and K. Decker, “Anterograde tracing of retinohypothalamic afferents with Fluoro-Gold,” Brain Res.745(1-2), 197–204 (1997). [CrossRef] [PubMed]
  39. 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]
  40. 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]
  41. M. E. Schwab and H. Thoenen, “Retrograde axonal and transsynaptic transport of macromolecules: physiological and pathophysiological importance,” Agents Actions7(3), 361–368 (1977). [CrossRef] [PubMed]
  42. J. D. Mikkelsen, “Visualization of efferent retinal projections by immunohistochemical identification of cholera toxin subunit B,” Brain Res. Bull.28(4), 619–623 (1992). [CrossRef] [PubMed]
  43. 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). [CrossRef] [PubMed]
  44. 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]
  45. 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). [CrossRef] [PubMed]
  46. 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). [CrossRef] [PubMed]
  47. S. Ochs, “Fast transport of materials in mammalian nerve fibers,” Science176(4032), 252–260 (1972). [CrossRef] [PubMed]
  48. S. Inoue, “The effect of colchicine on the microscopic and submicroscopic structure of the mitotic spindle,” Exp. Cell Res. Suppl.2, 305–318 (1952).
  49. O. J. Eigsti, “A cytological study of colchicine effects in the induction of polyploidy in plants,” Proc. Natl. Acad. Sci. U.S.A.24(2), 56–63 (1938). [CrossRef] [PubMed]
  50. O. J. Eigsti and P. D. Dustin, Jr., Colchicine— in Agriculture, Medicine, Biology and Chemistry (Iowa State College Press, Ames, IA, 1955)
  51. A. Dahlström, “Effect of colchicine on transport of amine storage granules in sympathetic nerves of rat,” Eur. J. Pharmacol.5(1), 111–113 (1968). [CrossRef] [PubMed]
  52. G. W. Kreutzberg, “Neuronal dynamics and axonal flow. IV. Blockage of intra-axonal enzyme transport by colchicine,” Proc. Natl. Acad. Sci. U.S.A.62(3), 722–728 (1969). [CrossRef] [PubMed]
  53. J. O. Karlsson and J. Sjöstrand, “The effect of colchicine on the axonal transport of protein in the optic nerve and tract of the rabbit,” Brain Res.13(3), 617–619 (1969). [CrossRef] [PubMed]
  54. 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). [PubMed]
  55. 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]
  56. J. O. Karlsson, H. A. Hansson, and J. Sjöstrand, “Effect of colchicine on axonal transport and morphology of retinal ganglion cells,” Z. Zellforsch. Mikrosk. Anat.115(2), 265–283 (1971). [CrossRef] [PubMed]
  57. I. G. Morgan, “Intraocular colchicine selectively destroys immature ganglion cells in chicken retina,” Neurosci. Lett.24(3), 255–260 (1981). [CrossRef] [PubMed]
  58. 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]
  59. 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). [CrossRef] [PubMed]
  60. R. D. Lund and S. D. Hauschka, “Transplanted neural tissue develops connections with host rat brain,” Science193(4253), 582–584 (1976). [CrossRef] [PubMed]
  61. 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). [CrossRef] [PubMed]
  62. 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). [CrossRef] [PubMed]
  63. U. C. Dräger and D. H. Hubel, “Topography of visual and somatosensory projections to mouse superior colliculus,” J. Neurophysiol.39(1), 91–101 (1976). [PubMed]
  64. 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]
  65. 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). [CrossRef] [PubMed]
  66. 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). [CrossRef] [PubMed]
  67. 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]
  68. 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]
  69. 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]
  70. 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). [CrossRef] [PubMed]
  71. 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]
  72. 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]
  73. 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]
  74. M. M. Black and R. J. Lasek, “Slow components of axonal transport: two cytoskeletal networks,” J. Cell Biol.86(2), 616–623 (1980). [CrossRef] [PubMed]
  75. J. E. Morgan, “Circulation and axonal transport in the optic nerve,” Eye (Lond.)18(11), 1089–1095 (2004). [CrossRef] [PubMed]
  76. 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]
  77. 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). [CrossRef] [PubMed]
  78. B. Grafstein and D. S. Forman, “Intracellular transport in neurons,” Physiol. Rev.60(4), 1167–1283 (1980). [PubMed]
  79. 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). [CrossRef] [PubMed]
  80. 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]
  81. 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). [CrossRef] [PubMed]
  82. 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]
  83. 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]
  84. 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]
  85. 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). [CrossRef] [PubMed]
  86. 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]
  87. 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]
  88. 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]
  89. 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]
  90. 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]
  91. 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]
  92. 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]
  93. 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]
  94. 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]
  95. 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]
  96. 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]
  97. 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]
  98. 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]
  99. 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]
  100. 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]
  101. 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]
  102. 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]
  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). [CrossRef] [PubMed]
  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). [CrossRef] [PubMed]
  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). [CrossRef] [PubMed]
  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). [CrossRef] [PubMed]

Cited By

Alert me when this paper is cited

OSA is able to provide readers links to articles that cite this paper by participating in CrossRef's Cited-By Linking service. CrossRef includes content from more than 3000 publishers and societies. In addition to listing OSA journal articles that cite this paper, citing articles from other participating publishers will also be listed.


« Previous Article

OSA is a member of CrossRef.

CrossCheck Deposited