Layer-specific anatomical, physiological and functional MRI of the retina

NMR in Biomedicine

Volumn 21, Issue 9, 2008, Pages 978-996

  Duong, Timothy Q ^a,c   Pardue, Machelle T ^b,c   Thulé, Peter M ^b,c   Olson, Darin E ^b,c   Cheng, Haiying ^a   Nair, Govind ^a   Li, Yingxia ^a   Kim, Moon ^c   Zhang, Xiaodong ^a   Shen, Qiang ^a  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

BOLD; Choroid; Diffusion weighted MRI; Functional MRI; High resolution imaging; Manganese enhanced MRI (MEMRI); Retinal blood flow; Retinal diseases

Indexed keywords

BLOOD; DATA STRUCTURES; EYE PROTECTION; HEMODYNAMICS; IMAGING SYSTEMS; IMAGING TECHNIQUES; MANGANESE; MEDICAL IMAGING; OXYGENATION; PHYSIOLOGY; SUGAR (SUCROSE);

BOLD; CHOROID; FUNCTIONAL MRI; HIGH RESOLUTION IMAGING; RETINAL BLOOD FLOW; RETINAL DISEASES;

PHYSIOLOGICAL MODELS;

GADOLINIUM PENTETATE; GROWTH FACTOR; MANGANESE; NEUROPROTECTIVE AGENT; NUCLEAR MAGNETIC RESONANCE IMAGING AGENT; OXYGEN; RETINOL;

CONTRAST ENHANCEMENT; DIABETIC RETINOPATHY; DIFFUSION WEIGHTED IMAGING; EARLY DIAGNOSIS; FLUORESCENCE ANGIOGRAPHY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HYPERCAPNIA; HYPEROXIA; INDOCYANINE GREEN ANGIOGRAPHY; LASER COAGULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTICAL COHERENCE TOMOGRAPHY; OPTICAL RESOLUTION; OXYGEN BLOOD LEVEL; PATHOGENESIS; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA; RETINA BIPOLAR GANGLION CELL; RETINA BLOOD FLOW; RETINA DEGENERATION; RETINA DISEASE; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; RETINITIS PIGMENTOSA; REVIEW; SCANNING LASER OPHTHALMOSCOPY; TISSUE OXYGENATION; VISUAL PROSTHESIS; VISUAL STIMULATION;

ANIMALS; CARBON DIOXIDE; DIABETIC RETINOPATHY; MAGNETIC RESONANCE IMAGING; OXYGEN; PHOTIC STIMULATION; REGIONAL BLOOD FLOW; RETINA; RETINAL DISEASES;

ANIMALIA;

EID: 57149146879     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.1311     Document Type: Review

References (132)

1. Kaufman PL, Alm A (eds). Adler's Physiology of the Eye. Mosby: St Louis, 1992.
2. Bron AJ, Tripathi RC, Tripathi BJ. Wolff's Anatomy of the Eye and Orbit. Chapman & Hall Medical: London, 1997.
3. Buttery RG, Hinrichsen CFL, Weller WL. J. R. H. How thick should a retina be? A comparative study of mammalian species with and without intraretinal vasculature. Vision Res 1991; 31: 169-187.
4. Harris A, Kagemann L, Cioffi GA. Assessment of human ocular hemodynamics. Surv Ophthalmol 1998; 42: 509-533.
5. Bill A. Circulation in the eye. In Handbook of Physiology, Part 2, Microcirculation, Renkin EM, Michel CC (eds). American Physiological Society: Bethesda, MD,1984; 1001-1035.
6. Linsenmeier RA, Braun RD. Oxygen distribution and consumption in the cat retina during normoxia and hypoxemia. J. Gen Physiol 1992: 99: 177-197.
7. Linsenmeier RA. Effects of light and darkness on oxygen distribution and consumption in the cat retina. J. Gen Physiol 1986; 88: 521-542.
8. Yu D-I, Cringle SJ, Alder V, Su E-N. Intraretinal oxygen distribution in the rat with graded syetemic hyperoxia and hypercapnia. Invest Ophthalmol Vis Sci 1999; 40: 2082-2087.
9. Cheng H, Nair G, Walker TA, Kim MK, Pardue MT, Thule PM, Olson DE, Duong TQ. Structural and functional MRI reveals multiple retinal layers. Proc Natl Acad Sci USA 2006; 103: 17525-17530.
10. Alm A, Bill A. Blood flow and oxygen extraction in the cat uvea at normal and high intraocular pressures. Acta Physiol Scand 1970; 80: 19-28.
11. Friedman E, Kopald HH, Smith TR. Retinal and choroidal blood flow determined with krypton 85 in anesthetized animals. Invest Ophthalmol 1964; 3: 539-547.
12. Linsenmeier RA, Padnick-Silver L. Metabolic dependence of photoreceptors on the choroid in the normal and detached retina. Invest Ophthalmol Vis Sci 2000; 41: 3117-3123.
13. Parver LM. Choroidal blood flow as a heat dissipating mechanism in the macula. Am J Ophthalmol 1980; 89: 641-646.
14. Parver LM, Auker CR, Carpenter DO, Doyle T. Choroidal blood flow. Arch Ophthalmol 1982; 100: 1327-1330.
15. Fujimoto JG, Brezinski ME, Tearney GJ, Boppart SA, Bouma B, Hee MR, Southern JF, Swanson EA. Optical biopsy and imaging using optical coherence tomography. Nat Med 1995; 1: 970-972.
16. Preussner PR, Richard G, Darrelmann O, Weber J, Kreissig I. Quantitative measurement of retinal blood flow in human beings by application of digital image-processsing methods to television fluorescein angiograms. Graefes Arch Clin Exp Ophthalmol 1983; 221: 110-112.
17. Guyer DR, Yannuzzi LA, Slakter JS, Sorenson JA, Orlock S. The status of indocyanine-green videoangiography. Cur Opin Ophthalmol 1993; 4: 3-6.
18. Chauhan BC, Yu PK, Cringle SJ, Yu DY. Confocal scanning laser Doppler flowmetry in the rat retina: origin of flow signals and dependence on scan depth. Arch Ophthalmol 2006; 124: 397-402.
19. Slakter JS, Yannuzzi LA, Guyer DR, Sorenson JA, Orlock DA. Indocyanine-green angiography. Curr Opin Ophthalmol 1995; 6: 25-32.
20. Riva CE, Grunwald JE, Sinclair SH. Laser Doppler velocimetry study of the effect of pure oxygen breathing on retinal blood flow. Invest Ophthalmol Vis Sci 1983; 24: 47-51.
21. Riva CE, Logean E, Falsini B. Visually evoked hemodynamical response and assessment of neurovascular coupling in the optic nerve and retina. Prog Retinal Eye Res 2005; 24: 183-215.
22. Cheng H, Duong TQ. Simplified laser-speckle-imaging analysis method and its application to retinal blood flow imaging. Opt Lett 2007; 32: 2188-2190.
23. Cheng H, Yan Y, Duong TQ. Temporal statistical analysis of laser speckle image and its application to retinal blood-flow imaging. Optics Express 2008; 16: 10214-10219.
24. Silva AC, Koretsky AP. Laminar specificity of functional MRI onset times during somatosensory stimulation in rat. Proc Natl Acad Sci USA 2002; 99: 15182-15187.
25. Goense JB, Logothetis NK. Laminar specificity in monkey V1 using high-resolution SE-fMRI. Magn Reson Imag 2006; 24: 381-392.
26. Kim D-S, Duong TQ, Kim S-G. High-resolution mapping of iso-orientation columns by fMRI. Nat Neurosci 2000; 3: 164-169.
27. Duong TQ, Kim D-S, Ugurbil K, Kim S-G. Localized blood flow response at sub-millimeter columnar resolution. Proc Natl Acad Sci USA 2001; 98: 10904-10909.
28. Cheng K, Waggoner RA, Tanaka K. Human ocular dominance columns as revealed by high-field functional magnetic resonance imaging. Neuron 2001; 32: 359-397.
29. Duong TQ, Kim D-S, Ugurbil K, Kim S-G. Spatio-temporal dynamics of the BOLD fMRI signals in cat visual cortex: toward mapping columnar structures using the early negative response. Magn Reson Med 2000; 44: 231-242.
30. Shen Q, Cheng H, Pardue MT, Chang TF, Nair G, Vo VT, Shonat RD, Duong TQ. Magnetic resonance imaging of tissue and vascular layers in the cat retina. J. Magn Reson Imaging 2006; 23: 465-472.
31. Chen J, Wang Q, Zhang H, Yang X, Wang J, Berkowitz BA, Wickline SA, Song SK. In vivo quantification of T(1), T(2), and apparent diffusion coefficient in the mouse retina at 11.74T. Magn Reson Med 2008; 59: 731-738.
32. Nair G, Cheng H, Duong TQ. Layer-specific manganese-enhanced MRI of retinal degeneration in RCS rats. Society for Neuroscience 2006; Atlanta, GA: p. 489.
33. Nair G, Cheng H, Kim M, Walker TA, Olson DE, Thulé PM, Pardue MT, Duong TQ. Manganese-enhanced MRI reveals multiple cellular and vascular layers in normal and degenerated retinas. Proc Int Soc Magn Reson Med 2007; Berlin, Germany: p. 2452.
34. Li Y, Cheng H, Duong TQ. Blood-flow magnetic resonance imaging of the retina. Neuroimage 2008; 39: 1744-1751.
35. Duong TQ, Ngan SC, Ugurbil K, Kim SG. Functional magnetic resonance imaging of the retina. Invest Ophthalmol Vis Sci 2002; 43: 1176-1181.
36. Berkowitz BA, Wilson CA. Quantitative mapping of ocular oxygenation using magnetic resonance imaging. Magn Reson Med 1995; 33: 579-581.
37. Luan H, Roberts R, Sniegowski M, Goebel DJ, Berkowitz BA. Retinal thickness and subnormal retinal oxygenation response in experimental diabetic retinopathy. Invest Ophthalmo Viz Sci 2006; 47: 320-328.
38. Wilson DF, Pastuszko A, DiGiacomo JE, Pawlowski M, Schneiderman R, Delivoria-Papadopoulos M. Effect of hyperventilation on oxygenation of the brain cortex of newborn piglets. J. Appl Physiol 1991; 70: 2691-2696.
39. 2 mapping. Invest Ophthalmol Vis Sci 1996; 37: 2089-2098.
40. Trick GL, Edwards P, Desai U, Berkowitz BA. Early supernormal retinal oxygenation response in patients with diabetes. Invest Ophthalmol Vis Sci 2006; 47: 1612-1619.
41. Berkowitz BA, Roberts R, Goebel DJ, Luan H. Noninvasive and simultaneous imaging of layer-specific retinal functional adaptation by manganese-enhanced MRI. Invest Ophthalmol Vis Sci 2006; 47: 2668-2674.
42. Berkowitz BA, Roberts R, Stemmler A, Luan H, Gradianu M. Impaired apparent ion demand in experimental diabetic retinopathy: correction by lipoic Acid. Invest Ophthalmol Vis Sci 2007; 48: 4753-4758.
43. Berkowitz BA, Roberts R, Penn JS, Gradianu M. High-resolution manganese-enhanced MRI of experimental retinopathy of prematurity. Invest Ophthalmol Vis Sci 2007; 48: 4733-4740.
44. Berkowitz BA, Kowluru RA, Frank RN, Kern TS, Hohman TC, Prakash M. Subnormal retinal oxygenation response precedes diabetic-like retinopathy. Invest Ophthalmol Vis Sci 1999; 40: 2100-2105.
45. Vinores SA. Assessment of blood-retinal barrier integrity. Histol Histopathol 1995; 10: 141-154.
46. Duong TQ, Shen Q, Cheng H, Chang TF, Shonat RD. Magnetic resonance imaging of anatomical layers in the cat retina. In. Invest Ophthalmol Vis Sci 2005; Suppl: 1049.
47. Shen Q, Cheng H, Chang T, Nair G, Shonat RD, Duong TQ. Magnetic resonance imaging of anatomical layers of the cat retina. Proc Int Soc Magn Reson Med, 2005; Miami, FL: p. 1033.
48. Eaton AM, Hatchell DL. Measurement of retinal blood vessel width using computerized image analysis. Invest Ophthalmol Vis Sci 1988; 29: 1258-1264.
49. Newsom RS, Sullivan PM, Rassam SM, Jagoe R, Kohner EM. Retinal vessel measurement: comparison between observer and computer driven methods. Graefes Arch Clin Exp Ophthalmol 1992; 230: 221-225.
50. Roy CS, Sherrington CS. On the regulation of blood supply of the brain. J. Physiol 1890. 1: 85-108.
51. Riva CE, Harino S, Shonat RD, Petrig BL. Flicker evoked increase in optic nerve head blood flow in anesthetized cats. Neurosci Lett 1991; 128: 291-296.
52. Mandecka A, Dawczynski J, Blum M, Muller N, Kloos C, Wolf G, Vilser W, Hoyer H, Muller UA. Influence of flickering light on the retinal vessels in diabetic patients. Diabetes Care 2007; 30: 3048-3052.
53. Yu D-Y, Cringle SJ, Su E-N, Yu PK. Intraretinal oxygen levels before and after photoreceptor loss in the RCS rat. Invest Ophthalmol Vis Sci 2000; 41: 3999-4006.
54. Grinvald A, Bonhoeffer T, Vanzetta I, Pollack A, Aloni E, Ofri R, Nelson D. High-resolution functional optical imaging: from the neocortex to the eye. Ophthalmol Clin North Am 2004; 17: 53-67.
55. Zarella MD, Li H, Kwon Y, Kardon R, Soliz P, Tso DY. The origins and spatio-temporal properties of stimulus dependent intrinsic optical signals of the retina. Society for Neuroscience, 2004; Program No. 934.910.
56. Ogawa S, Lee T-M, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 1990; 87: 9868-9872.
57. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim S-G, Merkle H, Ugurbil K. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 1992; 89: 5951-5955.
58. Kwong K, Hoppel B, Weisskoff R, Kiihne S, Barrere B, Moore J, Poncelet B, Rosen B, Thulborn K. Regional cerebral tissue oxygenation studied with EPI at clinical field strengths. J. Magn Reson Imag 1992; 2: 44.
59. Bandettini PA, Wong EC, Hinks RS, Rikofsky RS, Hyde JS. Time course EPI of human brain function during task activation. Magn Reson Med 1992; 25: 390-397.
60. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001; 412: 150-157.
61. Duong TQ, Kim DS, Ugurbil K, Kim SG. Localized cerebral blood flow response at submillimeter columnar resolution. Proc Natl Acad Sci USA 2001; 98: 10904-10909.
62. * changes by multiecho EPI. Magn Reson Med 2001; 46: 264-271.
63. Cohen ER, Ugurbil K, Kim S-G. Effect of basal conditions on the magnitude and dynamics of the blood oxygenation level-dependent fMRI response. J. Cereb Blood Flow Metab, 2002; 22: 1042-1053.
64. 2 in spontaneously breathing animals. Neuroimage 2005; 25: 850-858.
65. 1H study. Magn Reson Med 2001; 45: 61-70.
66. Trokel S. Effect of respiratory gases upon choroidal hemodynamics. Arch Ophthalmol 1965; 73: 838-842.
67. Kety SS, Schmidt CF. The effects of altered arterial tensions of carbon dioxide and oxygen on cerebral blood flow and cerebral oxygen consumption of normal young men. J. Clin Invest 1948; 27: 484-491.
68. Riva CE, Cranstoun SD, Mann RM, Barnes GE. Local choroidal blood flow in the cat by laser Doppler flowmetry. Invest Ophthalmol Vis Sci 1994; 35: 608-618.
69. Ogawa S, Menon RS, Tank DW, Kim SG, Merkle H, Ellermann JM, Ugurbil K. Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A. comparison of signal characteristics with a biophysical model. Biophys J 1993; 64: 803-812.
70. Calamante F, Gadian DG, Connelly A. Quantification of perfusion using bolus tracking magnetic resonance imaging in stroke: assumptions, limitations, and potential implications for clinical use. Stroke 2002; 33: 1146-1151.
71. Alsop D, Detre J. Reduced transit-time sensitivity in noninvasive magnetic resonance imaging of human cerebral blood flow. J. Cereb Blood Flow Metab 1996; 16: 1236-1249.
72. Wong EC, Buxton RB, Frank LR. Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSSII). Magn Reson Med 1998; 39: 702-708.
73. Wong EC, Buxton RB, Frank LR. A theoretical and experimental comparison of continuous and pulsed arterial spin labeling techniques for quantitative perfusion imaging. Magn Reson Med 1998; 40: 348-355.
74. Detre JA, Zhang W, Roberts DA, Silva AC, Williams DS, Grandis DJ, Koretsky AP, Leigh JS. Tissue specific perfusion imaging using arterial spin labeling. NMR Biomed 1994; 7: 75-82.
75. Williams DS, Detre JA, Leigh JS, Koretsky AP. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci USA 1992; 89: 212-216.
76. Duong TQ, Silva AC, Lee S-P, Kim S-G. Functional MRI of calcium-dependent synaptic activity: cross correlation with CBF and BOLD measurements. Magn Reson Med 2000; 43: 383-392.
77. Tsekos NV, Zhang F, Merkle H, Nagayama M, Iadecola C, Kim S-G. Quantitative measurements of cerebral blood flow in rats using the FAIR technique: correlation with previous iodoantipyrine autoradiographic studies. Magn Reson Med 1998; 39: 564-573.
78. Zaini MR, Strother SC, Andersen JR, Liow J-S, Kjems U, Tegeler C, Kim S-G. Matching spatial resolution of coregistered PET and 4.0T fMRI brain volumes. Med Phys 1999; 26: 1559-1567.
79. Liu HL, Kochunov P, Hou J, Pu Y, Mahankali S, Feng CM, Yee SH, Wan YL, Fox PT, Gao JH. Perfusion-weighted imaging of interictal hypoperfusion in temporal lobe epilepsy using FAIRHASTE: comparison with H(2)(15)O PET measurements. Magn Reson Med 2001; 45: 431-435.
80. Meng X, Fisher M, Shen Q, Sotak CM, Duong TQ. Characterizing the diffusion/perfusion mismatch in experimental focal cerebral ischemia. Ann Neurol 2004; 55: 207-212.
81. Shen Q, Meng X, Fisher M, Sotak CH, Duong TQ. Pixel-by-pixel spatiotemporal progression of focal ischemia derived using quantitative perfusion and diffusion imaging. J. Cereb Blood Flow Metab 2003; 23: 1479-1488.
82. Shen Q, Fisher M, Sotak CH, Duong TQ. Effects of reperfusion on ADC and CBF pixel-by-pixel dynamics in stroke: characterizing tissue fates using quantitative diffusion and perfusion imaging. J. Cereb Blood Flow Metab 2004: 24: 280-290.
83. Shen Q, Ren H, Cheng H, Fisher M, Duong TQ. Functional, perfusion and diffusion MRI of acute focal ischemic brain injury. J. Cereb Blood Flow Metab 2005; 25: 1265-1279.
84. Herscovitch P. Raichle ME. What is the correct value for the brain-blood partition coefficient for water? J Cereb Blood Flow Metab 1985; 5: 65-69.
85. Liu ZM, Schmidt KF, Sicard KM, Duong TQ. Imaging oxygen consumption in forepaw somatosensory stimulation in rats under isoflurane anesthesia. Magn Reson Med 2004; 52: 277-285.
86. Alm A, Bill A. Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): a study with radioactively labeled microspheres including flow determinations in brain and some other tissues. Exp Eye Res 1973; 15: 15-29.
87. Wang L, Fortune B, Cull G, McElwain KM, Cioffi GA. Microspheres method for ocular blood flow measurement in rats: size and dose optimization. Exp Eye Res 2007; 84: 108-117.
88. Matta BF, Heath KJ, Tipping K, Summors AC. Direct cerebral vasodilatory effects of sevoflurane and isoflurane. Anesthesiology 1999; 91: 677-680.
89. Sicard K, Shen Q, Brevard M, Sullivan R, Ferris CF, King JA, Duong TQ. Regional cerebral blood flow and BOLD response in conscious and anesthetized rats under basal and hypercapnic conditions: implications for fMRI studies. J. Cereb Blood Flow Metab 2003; 23: 472-481.
90. Duong TQ, Kim S-G. In vivo MR measurements of regional arterial and venous blood volume fractions in intact rat brain. Magn Reson Med 2000; 43: 392-402.
91. Duong TQ, Ngan S-C, Ugurbil K, Kim S-G. Functional magnetic resonance imaging of the retina. Invest Ophthalmol Vis Sci 2002; 43: 1176-1181.
92. Cotzias G, Horiuchi M, Fuenzalida S, Mena I. Clearance of tissue manganese concentrations with persistence of the neurological picture. Neurology 1968; 18: 376-382.
93. Newland M, Cox C, Hamada R, Oberdoerster G, Weiss R. The clearance of manganese chloride in the primate. Fundam Appl Toxicol 1987; 9: 314-328.
94. Lin Y-J, Koretsky AP. Manganese ion enhances T1-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn Reson Med 1997; 38: 378-398.
95. Pautler RG, Koretsky AP. Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging. Neuroimage 2002; 16: 441-448.
96. Silva AC, Lee JH, Aoki I, Koretsky AP. Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed 2004; 17: 532-543.
97. Pautler RG. Biological applications of manganese-enhanced magnetic resonance imaging. Methods Mol Med 2006; 124: 365-386.
98. 2: dose-dependent and temporal evolution of T1 contrast. Magn Reson Med 2005; 53: 640-648.
99. Aoki I, Wu YJ, Silva AC, Lynch RM, Koretsky AP. In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. Neuroimage 2004; 22: 1046-1059.
100. Chan KC, Fu QL, Hui ES, So KF, Wu EX. Evaluation of the retina and optic nerve in a rat model of chronic glaucoma using in vivo manganese-enhanced magnetic resonance imaging. Neuroimage 2008; 40: 1166-1174.
101. Berson EL. Retinitis pigmentosa: unfolding its mystery. Proc Natl Acad Sci USA 1996; 93: 4526-4528.
102. Sieving PA, Caruso RC, Tao W, Coleman HR, Thompson DJ, Fullmer KR, Bush RA. Ciliary neurotrophic factor (CNTF) for human retinal degeneration: phase I trial of CNTF delivered by encapsulated cell intraocular implants. Proc Natl Acad Sci USA 2006; 103: 3896-3901.
103. Chao HM, Chidlow G, Melena J, Wood JP, Osborne NN. An investigation into the potential mechanisms underlying the neuroprotective effect of clonidine in the retina. Brain Res 2000; 877: 47-57.
104. Acland GM, Aguirre GD, Ray J, Zhang Q, Aleman TS, Cideciyan AV, Pearce-Kelling SE, Anand V, Zeng Y, Magure AM, Jacobson SQ, Hauswirth WW, Bennett J. Gene therapy restores vision in a canine model of childhood blindness. Nat Genet 2001; 28: 92-95.
105. Rizzo JFr, Wyatt J, Humayun M, de Juan E, Liu W, Chow A, Eckmiller R, Zrenner E, Yagi T, Abrams G. Retinal prosthesis: an encouraging first decade with major challenges ahead. Ophthalmology 2001; 108: 13-14.
106. Gal A, Li Y, Thompson DA, Weir J, Orth U, Jacobson SG, Apfelstedt-Sylla E, Vollrath D. Mutations in MERTK, the human orthologue o the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet 2000; 26: 270-271.
107. D'Cruz PM, Yasumura D, Weir J, Matthes MT, Abderrahim H, LaVail MM, Vollrath D. Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum Mol Genet 2000; 9: 645-651.
108. Mullen RJ, LaVail MM. Inherited retinal dystrophy: primary defect in pigment epithelium determined with experimental rat chimeras. Science 1976; 192: 799-801.
109. Dowling JE, Sidman RL. Inherited retinal dystrophy in the rat. J. Cell Biol 1962; 14: 73-109.
110. Ball S, Hanzlicek B, Blum M, Pardue MT. Evaluation of inner retinal structure in the aged RCS rat. Adv Exp Med Biol 2003; 533: 181-188.
111. Milam AH, Li ZY, Fariss RN. Histopathology of the human retina in retinitis pigmentosa. Prog Retinal Eye Res 1998; 17: 175-205.
112. Padnick-Silver L, Kang Derwent JJ, Giuliano E, Narfstrom K, Linsenmeier RA. Retinal oxygenation and oxygen metabolism in Abyssinian cats with a hereditary retinal degeneration. Invest Ophthalmol Vis Sci 2006; 47: 3683-3689.
113. Li Y, Cheng H, Shen Q, Kim M, Olson DE, Thule PM, Pardue MT, Duong TQ. Blood-flow MRI of retinal degeneration. Proc Int Soc Magn Reson Med, 2008; Toronto, Canada: p. 1872.
114. Aiello LP, Gardner TW, King GL, Blankenship G, Cavallerano JD, Ferris FL, Klein R. Diabetic retinopathy. Diabetes Care 1998; 21: 143-156.
115. Alder VA, Su EN, Yu DY, Cringle SJ, Yu PK. Diabetic retinopathy: early functional changes. Clin Exp Pharm Physiol 1997; 24: 785-788.
116. No-author. Early worsening of diabetic retinopathy in the Diabetes Control and Complications Trial. Arch Ophthalmol 1998; 116: 874-886.
117. Frank RN. On the pathogenesis of diabetic retinopathy: a 1990 update. Ophthalmology 1991; 98: 586-593.
118. Patz A. Studies on retinal neovascularization: Friedenwald Lecture. Invest Ophthalmol Vis Sci 1980; 19: 1133-1138.
119. Stefansson E. Ocular oxygenation and the treatment of diabetic retinopathy. Surv Ophthalmol 2006; 51: 364-380.
120. Stefansson E. Oxygen and diabetic eye disease. Graefe's Arch Ophthalmol 1990; 228: 120-123.
121. Stefánsson E, Hatchell DL, Fisher BL, Sutherland ES, Machemer R. Panretinal photocoagulation and retinal oxygenation in normal and diabetic cats. Am J Ophthalmol 1986; 101: 657-664.
122. Molnar I, Poitry IS, Tsacopoulos M, Gilodi N, Leuenberger PM. Effect of laser photocoagulation on oxygenation of the retina in miniature pigs. Invest Ophthalmol Vis Sci 1985; 26: 1410-1414.
123. Landers MB III, Stefánsson E, Wolbarsht ML. Panretinal photocoagulation and retinal oxygenation. Retina 1982; 2: 167-175.
124. Grunwald JE, Riva CE, Brucker AJ, Sinclair SH, Petrig BL. Effect of panretinal photocoagulation on retinal blood flow in proliferative diabetic retinopathy. Ophthalmology 1986; 93: 590-595.
125. Alder VA, Cringle SJ, Brown M. The effect of regional retinal photocoagulation on vitreal oxygen tension. Invest Ophthalmol Vis Sci 1987; 28: 1078-1085.
126. Shimada Y, Li Y, Bearse M, Sutter E, Fung W. Assessment of early retinal changes in diabetes using a new multifocal ERG protocol. Br J Ophthalmol 2001; 85: 414-419.
127. Grunwald JE, Riva E, Brucker CEAJ, Sinclair SH, Petrig BL. Altered retinal vascular response to 100% oxygen breathing in diabetes mellitus. Ophthalmology 1984; 91: 1447-1452.
128. Grunwald JE, Riva CE, Baine J, Brucker AJ. Total retinal volumetric blood flow rate in diabetic patients with poor glycemic control. Invest Ophthalmol Vis Sci 1992; 33: 356-363.
129. Linsenmeier RA. The role of the choridal circulation in the retinal oxygenation. XIIIe Int Congress Eye Res Paris, 1998; Paris: p. S13.
130. Cheng H, Olson DE, Liu Y, Thule PM, Pardue MT, Duong TQ. Lamina- specific anatomical and functional imaging of normal and diabetic retina. Proc Int Soc Magn Reson Med, 2006; Seattle, Washington: p. 806.
131. Roberts R, Luan H, Berkowitz BA. Alpha-lipoic acid corrects late-phase supernormal retinal oxygenation response in experimental diabetic retinopathy. Invest Ophthalmol Vis Sci 2006; 47: 4077-4082.
132. Shen Q, Ren H, Bouley J, Fisher M, Duong TQ. Dynamic tracking of acute ischemic tissue fates using improved unsupervised ISODATA analysis of high-resolution quantitative perfusion and diffusion data. J. Cereb Blood Flow Metab 2004; 24: 887-897.