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Magnetic resonance imaging of the retina

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Abstract

This paper reviews recent developments in high-resolution magnetic resonance imaging (MRI) and its application to image anatomy, physiology, and function in the retina of animals. It describes technical issues and solutions in performing retinal MRI, anatomical MRI, blood oxygenation level-dependent functional MRI (fMRI), and blood-flow MRI both of normal retinas and of retinal degeneration. MRI offers unique advantages over existing retinal imaging techniques, including the ability to image multiple layers without depth limitation and to provide multiple clinically relevant data in a single setting. Retinal MRI has the potential to complement existing retinal imaging techniques.

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References

  1. Kaufman PL, Alm A, editors. Adler’s physiology of the eye. St Louis: Mosby; 1992.

    Google Scholar 

  2. Bron AJ, Tripathi RC, Tripathi BJ. Wolff’s anatomy of the eye and orbit. London: Chapman & Hall Medical; 1997.

    Google Scholar 

  3. Buttery RG, Hinrichsen CFL, Weller WL, Haight JR. How thick should a retina be? A comparative study of mammalian species with and without intraretinal vasculature. Vis Res 1991;31:169–187.

    Article  PubMed  CAS  Google Scholar 

  4. Harris A, Kagemann L, Cioffi GA. Assessment of human ocular hemodynamics. Surv Ophthalmol 1998;42:509–533.

    Article  PubMed  CAS  Google Scholar 

  5. Bill A. Circulation in the eye. In: Renkin EM, Michel CC, editors. Handbook of physiology, part 2, in microcirculation. Bethesda, MD: American Physiological Society; 1984. p. 1001–1035.

    Google Scholar 

  6. Cheng H, Nair G, Walker TA, et al. Structural and functional MRI reveals multiple retinal layers. Proc Natl Acad Sci U S A 2006;103:17525–17530.

    Article  PubMed  CAS  Google Scholar 

  7. 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.

    Article  PubMed  CAS  Google Scholar 

  8. Friedman E, Kopald HH, Smith TR. Retinal and choroidal blood flow determined with krypton 85 in anesthetized animals. Invest Ophthalmol 1964;3:539–547.

    PubMed  CAS  Google Scholar 

  9. Fujimoto JG, Brezinski ME, Tearney GJ, et al. Optical biopsy and imaging using optical coherence tomography. Nat Med 1995;1:970–972.

    Article  PubMed  CAS  Google Scholar 

  10. Zawadzki RJ, Jones SM, Olivier SS, et al. Adaptive-optics optical coherence tomography for high-resolution and high-speed 3D retinal in vivo imaging. Opt Exp 2005;13:8532–8546.

    Article  Google Scholar 

  11. Preussner PR, Richard G, Darrelmann O, Weber J, Kreissig I. Quantitative measurement of retinal blood flow in human beings by application of digital image-processing methods to television fluorescein angiograms. Graefes Arch Clin Exp Ophthalmol 1983;221:110–112.

    Article  PubMed  CAS  Google Scholar 

  12. Guyer DR, Yannuzzi LA, Slakter JS, Sorenson JA, Orlock S. The status of indocyanine-green videoangiography. Curr Opin Ophthalmol 1993;4:3–6.

    Article  PubMed  CAS  Google Scholar 

  13. 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.

    PubMed  CAS  Google Scholar 

  14. Riva CE, Logean E, Falsini B. Visually evoked hemodynamical response and assessment of neurovascular coupling in the optic nerve and retina. Prog Retin Eye Res 2005;24:183–215.

    Article  PubMed  Google Scholar 

  15. Cheng H, Duong TQ. Simplified laser-speckle-imaging analysis method and its application to retinal blood flow imaging. Opt Lett 2007;32:2188–2190.

    Article  PubMed  Google Scholar 

  16. Cheng H, Yan Y, Duong TQ. Temporal statistical analysis of laser speckle image and its application to retinal blood-flow imaging. Opt Exp 2008;16:10214–10219.

    Article  Google Scholar 

  17. Grinvald A, Bonhoeffer T, Vanzetta I, et al. High-resolution functional optical imaging: from the neocortex to the eye. Ophthalmol Clin North Am 2004;17:53–67.

    Article  PubMed  Google Scholar 

  18. Tsunoda K, Oguchi Y, Hanazona G, Tanifuji M. Mapping coneand rod- induced retinal responsiveness in macaque retina by optical imaging. Invest Ophthalmol Vis Sci 2004;45:3820–3826.

    Article  PubMed  Google Scholar 

  19. Hanazono G, Tsunoda K, Shinoda K, Tsubota K, Miyake Y, Tanifuji M. Intrinsic signal imaging in macaque retina reveals different types of flash-induced light reflectance changes of different origins. Invest Ophthalmol Vis Sci 2007;48:2903–2912.

    Article  PubMed  Google Scholar 

  20. Hanazono G, Tsunoda K, Kazato Y, Tsubota K, Tanifuji M. Evaluating neural activity of retinal ganglion cells by flash-evoked intrinsic signal imaging in macaque retina. Invest Ophthalmol Vis Sci 2008;49:4655–4663.

    Article  PubMed  Google Scholar 

  21. Tsunoda K, Oguchi Y, Hanazono G, Tanifuji M. Mapping coneand rod-induced retinal responsiveness in macaque retina by optical imaging. Invest Ophthalmol Vis Sci 2004;45:3820–3826.

    Article  PubMed  Google Scholar 

  22. 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.

    Article  PubMed  CAS  Google Scholar 

  23. 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.

    Article  PubMed  CAS  Google Scholar 

  24. Wong EC, Buxton RB, Frank LR. Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSSII). Magn Reson Med 1998;39:702–708.

    Article  PubMed  CAS  Google Scholar 

  25. 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.

    Article  PubMed  CAS  Google Scholar 

  26. Detre JA, Zhang W, Roberts DA, et al. Tissue specific perfusion imaging using arterial spin labeling. NMR Biomed 1994;7:75–82.

    Article  PubMed  CAS  Google Scholar 

  27. Williams DS, Detre JA, Leigh JS, Koretsky AP. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci U S A 1992;89:212–216.

    Article  PubMed  CAS  Google Scholar 

  28. 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.

    Article  PubMed  CAS  Google Scholar 

  29. 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.

    Article  PubMed  CAS  Google Scholar 

  30. Zaini MR, Strother SC, Andersen JR, et al. Matching spatial resolution of coregistered PET and 4.0T fMRI brain volumes. Med Phys 1999;26:1559–1567.

    Article  PubMed  CAS  Google Scholar 

  31. Liu HL, Kochunov P, Hou J, et al. 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.

    Article  PubMed  CAS  Google Scholar 

  32. Ogawa S, Lee T-M, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A 1990;87:9868–9872.

    Article  PubMed  CAS  Google Scholar 

  33. Ogawa S, Tank DW, Menon R, et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci U S A 1992;89:5951–5955.

    Article  PubMed  CAS  Google Scholar 

  34. Kwong K, Hoppel B, Weisskoff R, et al. Regional cerebral tissue oxygenation studied with EPI at clinical field strengths. J Magn Reson Imaging 1992;2:44.

    Google Scholar 

  35. 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.

    Article  PubMed  CAS  Google Scholar 

  36. Duong TQ, Kim DS, Ugurbil K, Kim SG. Localized cerebral blood flow response at submillimeter columnar resolution. Proc Natl Acad Sci U S A 2001;98:10904–10909.

    Article  PubMed  CAS  Google Scholar 

  37. Posse S, Elghahwagi B, Wiese S, Kiselev VG. Effect of graded hypo- and hypercapnia on fMRI contrast in visual cortex: quantification of T2* changes by multiecho EPI. Magn Reson Med 2001;46:264–271.

    Article  PubMed  CAS  Google Scholar 

  38. Cohen ER, Ugurbil K, Kim S-G. Effect of basal conditions on the magnitude and dynamics of the blood oxygenation leveldependent fMRI response. J Cereb Blood Flow Metab 2002;22:1042–1053.

    Article  PubMed  CAS  Google Scholar 

  39. Sicard KM, Duong TQ. Effects of hypoxia, hyperoxia and hypercapnia on baseline and stimulus-evoked BOLD, CBF and CMRO2 in spontaneously breathing animals. Neuroimage 2005;25:850–858.

    Article  PubMed  Google Scholar 

  40. Duong TQ, Iadacola C, Kim S-G. Effect of hyperoxia, hypercapnia and hypoxia on cerebral interstitial oxygen tension and cerebral blood flow in the rat brain: an 19F/1H study. Magn Reson Med 2001;45:61–70.

    Article  PubMed  CAS  Google Scholar 

  41. Silva AC, Koretsky AP. Laminar specificity of functional MRI onset times during somatosensory stimulation in rat. Proc Natl Acad Sci U S A 2002;99:15182–15187.

    Article  PubMed  CAS  Google Scholar 

  42. Goense JB, Logothetis NK. Laminar specificity in monkey V1 using high-resolution SE-fMRI. Magn Reson Imaging 2006;24:381–392.

    Article  PubMed  Google Scholar 

  43. Kim D-S, Duong TQ, Kim S-G. High-resolution mapping of isoorientation columns by fMRI. Nat Neurosci 2000;3:164–169.

    Article  PubMed  CAS  Google Scholar 

  44. Duong TQ, Kim D-S, Ugurbil K, Kim S-G. Localized blood flow response at sub-millimeter columnar resolution. Proc Natl Acad Sci U S A 2001;98:10904–10909.

    Article  PubMed  CAS  Google Scholar 

  45. Cheng K, Waggoner RA, Tanaka K. Human ocular dominance columns as revealed by high-field functional magnetic resonance imaging. Neuron 2001;32:359–397.

    Article  PubMed  CAS  Google Scholar 

  46. 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.

    Article  PubMed  CAS  Google Scholar 

  47. 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.

    PubMed  Google Scholar 

  48. Shen Q, Cheng H, Pardue MT, et al. Magnetic resonance imaging of tissue and vascular layers in the cat retina. J Magn Reson Imaging 2006;23:465–472.

    Article  PubMed  Google Scholar 

  49. Li Y, Cheng H, Duong TQ. Blood-flow magnetic resonance imaging of the retina. Neuroimage 2008;39:1744–1751.

    Article  PubMed  Google Scholar 

  50. Li Y, Cheng H, Shen Q, et al. Blood-flow magnetic resonance imaging of retinal degeneration. Invest Ophthalmol Vis Sci 2009;50:1824–1830.

    Article  PubMed  Google Scholar 

  51. 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.

    Article  PubMed  Google Scholar 

  52. Duong TQ, Pardue MT, Thule PM, et al. Layer-specific anatomical, physiological and functional MRI of the retina. NMR Biomed 2008;21:978–996.

    Article  PubMed  Google Scholar 

  53. Duong TQ, Zhang X, Li Y. Systematic evaluation of hardware and animal stability for high-resolution layer-specific MRI of the retina. J Magn Reson Imaging 2009 (in press).

  54. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn Reson Med 1993;29:804–811.

    Article  PubMed  CAS  Google Scholar 

  55. Kochunov PV, Liu HL, Andrews T, Gao JH, Fox PT, Lancaster JL. A B(0) shift correction method based on edge RMS reduction for EPI fMRI. J Magn Reson Imaging 2000;12:956–959.

    Article  PubMed  CAS  Google Scholar 

  56. Chen J, Wang Q, Zhang H, et al. 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.

    Article  PubMed  Google Scholar 

  57. Nair G, Shen Q, Duong TQ. T1, T2, and ADC of the rat retina at 7T. In: Proceedings of the 16th Annual Meeting of the ISMRM; 3–9 May 2008; Toronto, Canada. Abstract 2224.

  58. Vinores SA. Assessment of blood-retinal barrier integrity. Histol Histopathol 1995;10:141–154.

    PubMed  CAS  Google Scholar 

  59. Luan H, Roberts R, Sniegowski M, Goebel DJ, Berkowitz BA. Retinal thickness and subnormal retinal oxygenation response in experimental diabetic retinopathy. Invest Ophthalmol Vis Sci 2006;47:320–328.

    Article  PubMed  Google Scholar 

  60. Trokel S. Effect of respiratory gases upon choroidal hemodynamics. Arch Ophthalmol 1965;73:838–842.

    PubMed  CAS  Google Scholar 

  61. 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.

    Article  CAS  Google Scholar 

  62. 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.

    PubMed  CAS  Google Scholar 

  63. 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.

    PubMed  CAS  Google Scholar 

  64. 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.

    Article  PubMed  Google Scholar 

  65. Herscovitch P, Raichle ME. What is the correct value for the brainblood partition coefficient for water? J Cereb Blood Flow Metab 1985;5:65–69.

    PubMed  CAS  Google Scholar 

  66. 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.

    Article  PubMed  Google Scholar 

  67. 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.

    Article  PubMed  CAS  Google Scholar 

  68. 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.

    Article  PubMed  CAS  Google Scholar 

  69. Matta BF, Heath KJ, Tipping K, Summors AC. Direct cerebral vasodilatory effects of sevoflurane and isoflurane. Anesthesiology 1999;91:677–680.

    Article  PubMed  CAS  Google Scholar 

  70. Sicard K, Shen Q, Brevard M, et al. 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.

    Article  PubMed  CAS  Google Scholar 

  71. 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.

    Google Scholar 

  72. Berson EL. Retinitis pigmentosa: unfolding its mystery. Proc Natl Acad Sci U S A 1996;93:4526–4528.

    Article  PubMed  CAS  Google Scholar 

  73. Jones BW, Watt CB, Marc RE. Retinal remodeling. Clin Exp Optom 2005;88:282–291.

    Article  PubMed  Google Scholar 

  74. Gal A, Li Y, Thompson DA, et al. Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet 2000;26:270–271.

    Article  PubMed  CAS  Google Scholar 

  75. D’Cruz PM, Yasumura D, Weir J, et al. Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum Mol Genet 2000;9:645–651.

    Article  PubMed  Google Scholar 

  76. Mullen RJ, LaVail MM. Inherited retinal dystrophy: primary defect in pigment epithelium determined with experimental rat chimeras. Science 1976;192:799–801.

    Article  PubMed  CAS  Google Scholar 

  77. 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.

    PubMed  Google Scholar 

  78. Milam AH, Li ZY, Fariss RN. Histopathology of the human retina in retinitis pigmentosa. Prog Retin Eye Res 1998;17:175–205.

    Article  PubMed  CAS  Google Scholar 

  79. Dowling JE, Sidman RL. Inherited retinal dystrophy in the rat. J Cell Biol 1962;14:73–109.

    Article  PubMed  CAS  Google Scholar 

  80. 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.

    Article  PubMed  Google Scholar 

  81. Rizzo JFr, Wyatt J, Humayun M, et al. Retinal prosthesis: an encouraging first decade with major challenges ahead. Ophthalmology 2001;108:13–14.

    Article  PubMed  Google Scholar 

  82. 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.

    Article  PubMed  Google Scholar 

  83. Zhang X, Li Y, Duong TQ. Image stability evaluation and motion correction for high resolution MRI of the rat retina. Proc Magn Reson Med 2009; Honolulu, Hawaii. p 4600.

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Correspondence to Timothy Q. Duong.

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Duong, T.Q., Muir, E.R. Magnetic resonance imaging of the retina. Jpn J Ophthalmol 53, 352–367 (2009). https://doi.org/10.1007/s10384-009-0688-1

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