Evaluation of the retina and optic nerve in a rat model of chronic glaucoma using in vivo manganese-enhanced magnetic resonance imaging

NeuroImage

Volumn 40, Issue 3, 2008, Pages 1166-1174

  Chan, Kevin C ^a   Fu, Qing ling ^a   Hui, Edward S ^a   So, Kwok fai ^a   Wu, Ed X ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Chronic glaucoma; Fast axonal transport; Intraocular pressure; Manganese enhanced magnetic resonance imaging; Optic nerve; Rat

Indexed keywords

MANGANESE CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARGON LASER; ARTICLE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; FEMALE; GLAUCOMA; IN VIVO STUDY; LASER COAGULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTIC NERVE; PRIORITY JOURNAL; RAT; RETINA; VITREOUS BODY;

ANIMALS; CHRONIC DISEASE; DATA INTERPRETATION, STATISTICAL; DISEASE MODELS, ANIMAL; FEMALE; FUNCTIONAL LATERALITY; GLAUCOMA; MAGNETIC RESONANCE IMAGING; MANGANESE; OPTIC NERVE; RATS; RATS, SPRAGUE-DAWLEY; RETINA; VITREOUS BODY;

EID: 40849095785     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2008.01.002     Document Type: Article

References (77)

1. Anderson D.R., and Hendrickson A. Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Invest. Ophthalmol. 13 (1974) 771-783
2. Aoki I., Wu Y.J., Silva A.C., Lynch R.M., and Koretsky A.P. In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. Neuroimage 22 (2004) 1046-1059
3. Aoki I., Naruse S., and Tanaka C. Manganese-enhanced magnetic resonance imaging (MEMRI) of brain activity and applications to early detection of brain ischemia. NMR Biomed. 17 (2004) 569-580
4. Banerjee D., Hegedus B., Gutmann D.H., and Garbow J.R. Detection and measurement of neurofibromatosis-1 mouse optic glioma in vivo. Neuroimage 35 (2007) 1434-1437
5. Bearer E.L., Falzone T.L., Zhang X., Biris O., Rasin A., and Jacobs R.E. Role of neuronal activity and kinesin on tract tracing by manganese-enhanced MRI (MEMRI). NeuroImage (2007)
6. Berkowitz B.A., Roberts R., Goebel D.J., and Luan H. Noninvasive and simultaneous imaging of layer-specific retinal functional adaptation by manganese-enhanced MRI. Invest Ophthalmol Vis. Sci. 47 (2006) 2668-2674
7. Berkowitz B.A., Roberts R., Luan H., Bissig D., Bui B.V., Gradianu M., Calkins D.J., and Vingrys A.J. Manganese-enhanced MRI studies of alterations of intraretinal ion demand in models of ocular injury. Invest. Ophthalmol. Vis. Sci. 48 (2007) 3796-3804
8. Braun R.D., Gradianu M., Vistisen K.S., Roberts R.L., and Berkowitz B.A. Manganese-enhanced MRI of human choroidal melanoma xenografts. Invest. Ophthalmol. Vis. Sci. 48 (2007) 963-967
9. Chan H.C., Chang R.C., Koon-Ching Ip A., Chiu K., Yuen W.H., Zee S.Y., and So K.F. Neuroprotective effects of Lycium barbarum Lynn on protecting retinal ganglion cells in an ocular hypertension model of glaucoma. Exp. Neurol. 203 (2007) 269-273
10. Chauhan B.C., Levatte T.L., Garnier K.L., Tremblay F., Pang I.H., Clark A.F., and Archibald M.L. Semiquantitative optic nerve grading scheme for determining axonal loss in experimental optic neuropathy. Invest Ophthalmol. Vis. Sci. 47 (2006) 634-640
11. Cheng H., Nair G., Walker T.A., Kim M.K., Pardue M.T., Thule P.M., Olson D.E., and Duong T.Q. Structural and functional MRI reveals multiple retinal layers. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 17525-17530
12. Dandona L., Hendrickson A., and Quigley H.A. Selective effects of experimental glaucoma on axonal transport by retinal ganglion cells to the dorsal lateral geniculate nucleus. Invest Ophthalmol. Vis. Sci. 32 (1991) 1593-1599
13. Duncan R.O., Sample P.A., Weinreb R.N., Bowd C., and Zangwill L.M. Retinotopic organization of primary visual cortex in glaucoma: a method for comparing cortical function with damage to the optic disk. Invest Ophthalmol Vis Sci 48 (2007) 733-744
14. Duncan R.O., Sample P.A., Weinreb R.N., Bowd C., and Zangwill L.M. Retinotopic organization of primary visual cortex in glaucoma: comparing fMRI measurements of cortical function with visual field loss. Prog. Retin Eye Res. 26 (2007) 38-56
15. Duong T.Q., Silva A.C., Lee S.P., and Kim S.G. Functional MRI of calcium-dependent synaptic activity: cross correlation with CBF and BOLD measurements. Magn. Reson Med. 43 (2000) 383-392
16. Elluru R.G., Bloom G.S., and Brady S.T. Fast axonal transport of kinesin in the rat visual system: functionality of kinesin heavy chain isoforms. Mol. Biol. Cell 6 (1995) 21-40
17. Fu Q.L., Wu W., Wang H., Li X., Lee V.W., and So K.F. Up-regulated endogenous erythropoietin/erythropoietin receptor system and exogenous erythropoietin rescue retinal ganglion cells after chronic ocular hypertension. Cell Mol. Neurobiol. (2007)
18. Gross R.L., Ji J., Chang P., Pennesi M.E., Yang Z., Zhang J., and Wu S.M. A mouse model of elevated intraocular pressure: retina and optic nerve findings. Trans. Am. Ophthalmol. Soc. 101 (2003) 163-169 discussion 169-171
19. Grozdanic S.D., Betts D.M., Sakaguchi D.S., Allbaugh R.A., Kwon Y.H., and Kardon R.H. Laser-induced mouse model of chronic ocular hypertension. Invest Ophthalmol. Vis. Sci. 44 (2003) 4337-4346
20. Gupta N., and Yucel Y.H. Glaucoma as a neurodegenerative disease. Curr. Opin. Ophthalmol. 18 (2007) 110-114
21. Haapanen A., Ramadan U.A., Autti T., Joensuu R., and Tyynela J. In vivo MRI reveals the dynamics of pathological changes in the brains of cathepsin D-deficient mice and correlates changes in manganese-enhanced MRI with microglial activation. Magn. Reson. Imaging (2007)
22. Hetling J.R., Baig-Silva M.S., Comer C.M., Pardue M.T., Samaan D.Y., Qtaishat N.M., Pepperberg D.R., and Park T.J. Features of visual function in the naked mole-rat Heterocephalus glaber. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 191 (2005) 317-330
23. Hernandez C., Blackburn E., and Alvarez J. Calibre and microtubule content of the non-medullated and myelinated domains of optic nerve axons of rats. Eur. J. Neurosci 1 (1989) 654-658
24. Hiruma H., Katakura T., Takahashi S., Ichikawa T., and Kawakami T. Glutamate and amyloid beta-protein rapidly inhibit fast axonal transport in cultured rat hippocampal neurons by different mechanisms. J. Neurosci. 23 (2003) 8967-8977
25. Johnson E.C., Deppmeier L.M., Wentzien S.K., Hsu I., and Morrison J.C. Chronology of optic nerve head and retinal responses to elevated intraocular pressure. Invest. Ophthalmol. Vis. Sci. 41 (2000) 431-442
26. Kaufman P.L. Nitric-oxide synthase and neurodegeneration/neuroprotection. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 9455-9456
27. Kawai Y., Aoki I., Matsumoto N., Umeda M., Higuchi T., Kershaw J., Silva A.C., and Tanaka C. Detection of reactive giosis using manganese-enhanced MRI (MEMRI). Proc. Intl. Soc. Mag. Reson. Med. 15 (2007) 2463
28. Khosla P.K., Patra S., Prakash P., and Ratnakar K.S. Axoplasmic transport in optic nerve (an experimental study in rabbits). Indian J. Ophthalmol. 30 (1982) 23-28
29. Lau J., Dang M., Hockmann K., and Ball A.K. Effects of acute delivery of endothelin-1 on retinal ganglion cell loss in the rat. Exp. Eye Res. 82 (2006) 132-145
30. Leergaard T.B., Bjaalie J.G., Devor A., Wald L.L., and Dale A.M. In vivo tracing of major rat brain pathways using manganese-enhanced magnetic resonance imaging and three-dimensional digital atlasing. NeuroImage 20 (2003) 1591-1600
31. Li S.K., Jeong E.K., and Hastings M.S. Magnetic resonance imaging study of current and ion delivery into the eye during transscleral and transcorneal iontophoresis. Invest. Ophthalmol. Vis. Sci. 45 (2004) 1224-1231
32. Li R.S., Tay D.K., Chan H.H., and So K.F. Changes of retinal functions following the induction of ocular hypertension in rats using argon laser photocoagulation. Clin. Experiment Ophthalmol. 34 (2006) 575-583
33. Li R.S., Chen B.Y., Tay D.K., Chan H.H., Pu M.L., and So K.F. Melanopsin-expressing retinal ganglion cells are more injury-resistant in a chronic ocular hypertension model. Invest Ophthalmol. Vis. Sci. 47 (2006) 2951-2958
34. Lin C.P., Tseng W.Y., Cheng H.C., and Chen J.H. Validation of diffusion tensor magnetic resonance axonal fiber imaging with registered manganese-enhanced optic tracts. Neuroimage 14 (2001) 1035-1047
35. Lin C.P., Wedeen V.J., Chen J.H., Yao C., and Tseng W.Y. Validation of diffusion spectrum magnetic resonance imaging with manganese-enhanced rat optic tracts and ex vivo phantoms. NeuroImage 19 (2003) 482-495
36. Lindsey J.D., Scadeng M., Dubowitz D.J., Crowston J.G., and Weinreb R.N. Magnetic resonance imaging of the visual system in vivo: transsynaptic illumination of V1 and V2 visual cortex. NeuroImage 34 (2007) 1619-1626
37. Mabuchi F., Aihara M., Mackey M.R., Lindsey J.D., and Weinreb R.N. Optic nerve damage in experimental mouse ocular hypertension. Invest Ophthalmol Vis Sci 44 (2003) 4321-4330
38. Mabuchi F., Aihara M., Mackey M.R., Lindsey J.D., and Weinreb R.N. Regional optic nerve damage in experimental mouse glaucoma. Invest. Ophthalmol. Vis. Sci. 45 (2004) 4352-4358
39. Massaad. The role of mitochondrial superoxide in Alzheimer's pathology. Proc. Intl. Soc. Mag. Reson. Med. 15 (2007) 3088
40. Molokhia S.A., Jeong E.K., Higuchi W.I., and Li S.K. Examination of penetration routes and distribution of ionic permeants during and after transscleral iontophoresis with magnetic resonance imaging. Int. J. Pharm. 335 (2007) 46-53
41. Morrison J.C., Fraunfelder F.W., Milne S.T., and Moore C.G. Limbal microvasculature of the rat eye. Invest. Ophthalmol. Vis. Sci. 36 (1995) 751-756
42. Morrison J.C., Moore C.G., Deppmeier L.M., Gold B.G., Meshul C.K., and Johnson E.C. A rat model of chronic pressure-induced optic nerve damage. Exp. Eye Res. 64 (1997) 85-96
43. Morrison J.C. Elevated intraocular pressure and optic nerve injury models in the rat. J. Glaucoma 14 (2005) 315-317
44. Morrison J.C., Johnson E.C., Cepurna W., and Jia L. Understanding mechanisms of pressure-induced optic nerve damage. Prog Retin Eye Res 24 (2005) 217-240
45. Naskar R., Wissing M., and Thanos S. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest Ophthalmol. Vis. Sci. 43 (2002) 2962-2968
46. Neufeld A.H. Nitric oxide: a potential mediator of retinal ganglion cell damage in glaucoma. Surv. Ophthalmol. 43 Suppl 1 (1999) S129-S135
47. Pautler R.G. In vivo, trans-synaptic tract-tracing utilizing manganese-enhanced magnetic resonance imaging (MEMRI). NMR Biomed. 17 (2004) 595-601
48. Pautler R.G. Biological applications of manganese-enhanced magnetic resonance imaging. Methods. Mol. Med. 124 (2006) 365-386
49. Pautler R.G., Silva A.C., and Koretsky A.P. In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging. Magn. Reson. Med. 40 (1998) 740-748
50. Pease M.E., McKinnon S.J., Quigley H.A., Kerrigan-Baumrind L.A., and Zack D.J. Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 41 (2000) 764-774
51. Quigley H.A. Neuronal death in glaucoma. Prog. Retin Eye Res. 18 (1999) 39-57
52. Quigley H.A., and Addicks E.M. Chronic experimental glaucoma in primates. II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport. Invest Ophthalmol. Vis. Sci. 19 (1980) 137-152.
53. Quigley H.A., and Broman A.T. The number of people with glaucoma worldwide in 2010 and 2020. Br. J. Ophthalmol. 90 (2006) 262-267
54. Quigley H.A., Guy J., and Anderson D.R. Blockade of rapid axonal transport. Effect of intraocular pressure elevation in primate optic nerve. Arch. Ophthalmol. 97 (1979) 525-531
55. Quigley H.A., Sanchez R.M., Dunkelberger G.R., L'Hernault N.L., and Baginski T.A. Chronic glaucoma selectively damages large optic nerve fibers. Invest. Ophthalmol. Vis. Sci. 28 (1987) 913-920
56. Ryu S., Brown S.L., Kolozsvary A., Ewing J.R., and Kim J.H. Noninvasive detection of radiation-induced optic neuropathy by manganese-enhanced MRI. Radiat Res. 157 (2002) 500-505
57. Sasaoka M., Taniguchi T., Shimazawa M., Ishida N., Shimazaki A., and Hara H. Intravitreal injection of endothelin-1 caused optic nerve damage following to ocular hypoperfusion in rabbits. Exp. Eye Res. 83 (2006) 629-637
58. Serrano F., Terashima T., Chan L.C., and Pautler R.G. In vivo assessment of axonal transport in diabetic mice using manganese-enhanced MRI (MEMRI). Proc. Intl. Soc. Mag. Reson. Med. 15 (2007) 2463
59. Silva A.C., Lee J.H., Aoki I., and Koretsky A.P. Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed 17 (2004) 532-543
60. Smith K.D., Kallhoff V., Zheng H., and Pautler R.G. In vivo axonal transport rates decrease in a mouse model of Alzheimer's disease. NeuroImage 35 (2007) 1401-1408
61. Song S.K., Sun S.W., Ju W.K., Lin S.J., Cross A.H., and Neufeld A.H. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. NeuroImage 20 (2003) 1714-1722
62. Sun S.W., Liang H.F., Le T.Q., Armstrong R.C., Cross A.H., and Song S.K. Differential sensitivity of in vivo and ex vivo diffusion tensor imaging to evolving optic nerve injury in mice with retinal ischemia. NeuroImage 32 (2006) 1195-1204
63. Taylor A.C., and Weiss P. Demonstration of axonal flow by the movement of tritium-labeled protein in mature optic nerve fibers. Proc. Natl. Acad. Sci. U. S. A. 54 (1965) 1521-1527
64. Takeda A. Manganese action in brain function. Brain Res. Brain Res. Rev. 41 (2003) 79-87
65. Thanos S., and Naskar R. Correlation between retinal ganglion cell death and chronically developing inherited glaucoma in a new rat mutant. Exp Eye Res. 79 (2004) 119-129
66. Thuen M., Singstad T.E., Pedersen T.B., Haraldseth O., Berry M., Sandvig A., and Brekken C. Manganese-enhanced MRI of the optic visual pathway and optic nerve injury in adult rats. J. Magn. Reson Imaging 22 (2005) 492-500
67. Van der Linden A., Van Meir V., Tindemans I., Verhoye M., and Balthazart J. Applications of manganese-enhanced magnetic resonance imaging (MEMRI) to image brain plasticity in song birds. NMR Biomed 17 (2004) 602-612
68. Van der Linden A., Van Camp N., Ramos-Cabrer P., and Hoehn M. Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition. NMR Biomed. 20 (2007) 522-545
69. van der Zijden J.P., Wu O., van der Toorn A., Roeling T.P., Bleys R.L., and Dijkhuizen R.M. Changes in neuronal connectivity after stroke in rats as studied by serial manganese-enhanced MRI. NeuroImage 34 (2007) 1650-1657
70. Vickers J.C., Craig J.E., Stankovich J., McCormack G.H., West A.K., Dickinson J.L., McCartney P.J., Coote M.A., Healey D.L., and Mackey D.A. The apolipoprotein epsilon4 gene is associated with elevated risk of normal tension glaucoma. Mol. Vis. 8 (2002) 389-393
71. Wang J., Ge J., Sadun A.A., and Lam T.T. Characteristics of optic nerve damage induced by chronic intraocular hypertension in rat. Yan Ke Xue Bao 20 (2004) 25-29
72. Watanabe T., Michaelis T., and Frahm J. Mapping of retinal projections in the living rat using high-resolution 3D gradient-echo MRI with Mn2+-induced contrast. Magn. Reson. Med. 46 (2001) 424-429
73. Watanabe T., Frahm J., and Michaelis T. Functional mapping of neural pathways in rodent brain in vivo using manganese-enhanced three-dimensional magnetic resonance imaging. NMR Biomed. 17 (2004) 554-568
74. WoldeMussie E., Ruiz G., Wijono M., and Wheeler L.A. Neuroprotection of retinal ganglion cells by brimonidine in rats with laser-induced chronic ocular hypertension. Invest. Ophthalmol. Vis. Sci. 42 (2001) 2849-2855
75. Xu J., Heys J.J., Barocas V.H., and Randolph T.W. Permeability and diffusion in vitreous humour: implications for drug delivery. Pharm Res. 17 (2000) 664-669
76. Yang J., and Wu E.X. Detection of cortical gray matter lesion in the late phase of mild hypoxic-ischemic injury by manganese-enhanced MRI. NeuroImage 39 (2008) 669-679
77. Yucel Y.H., Zhang Q., Weinreb R.N., Kaufman P.L., and Gupta N. Effects of retinal ganglion cell loss on magno-, parvo-, koniocellular pathways in the lateral geniculate nucleus and visual cortex in glaucoma. Prog. Retin. Eye Res. 22 (2003) 465-481