1932

Abstract

High-resolution retinal imaging is revolutionizing how scientists and clinicians study the retina on the cellular scale. Its exquisite sensitivity enables time-lapse optical biopsies that capture minute changes in the structure and physiological processes of cells in the living eye. This information is increasingly used to detect disease onset and monitor disease progression during early stages, raising the possibility of personalized eye care. Powerful high-resolution imaging tools have been in development for more than two decades; one that has garnered considerable interest in recent years is optical coherence tomography enhanced with adaptive optics. State-of-the-art adaptive optics optical coherence tomography (AO-OCT) makes it possible to visualize even highly transparent cells and measure some of their internal processes at all depths within the retina, permitting reconstruction of a 3D view of the living microscopic retina. In this review, we report current AO-OCT performance and its success in visualizing and quantifying these once-invisible cells in human eyes.

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2020-09-15
2024-04-23
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Literature Cited

  1. Anderson DH, Fisher SK, Steinberg RH 1978. Mammalian cones: disc shedding, phagocytosis, and renewal. Investig. Ophthalmol. Vis. Sci. 17:2117–33
    [Google Scholar]
  2. Archibald NK, Clarke MP, Mosimann UP, Burn DJ 2009. The retina in Parkinson's disease. Brain 132:51128–45
    [Google Scholar]
  3. Azimipour M, Jonnal RS, Werner JS, Zawadzki RJ 2019a. Coextensive synchronized SLO-OCT with adaptive optics for human retinal imaging. Opt. Lett. 44:174219–22
    [Google Scholar]
  4. Azimipour M, Migacz JV, Zawadzki RJ, Werner JS, Jonnal RS 2019b. Functional retinal imaging using adaptive optics swept-source OCT at 1.6 MHz. Optica 6:3300–3
    [Google Scholar]
  5. Azimipour M, Valente D, Vienola KV, Werner JS, Zawadzki RJ, Jonnal RS 2020. Investigating the functional response of human cones and rods with a combined adaptive optics SLO-OCT system. Proc. SPIE 11218:1121813
    [Google Scholar]
  6. Azimipour M, Zawadzki RJ, Gorczynska I, Migacz J, Werner JS, Jonnal RS 2018. Intraframe motion correction for raster-scanned adaptive optics images using strip-based cross-correlation lag biases. PLOS ONE 13:10e0206052
    [Google Scholar]
  7. Barral DC, Seabra MC. 2004. The melanosome as a model to study organelle motility in mammals. Pigment Cell Res 17:2111–18
    [Google Scholar]
  8. Baumann B, Baumann SO, Konegger T, Pircher M, Götzinger E et al. 2012. Polarization sensitive optical coherence tomography of melanin provides intrinsic contrast based on depolarization. Biomed. Opt. Express 3:71670–83
    [Google Scholar]
  9. Berisha F, Feke GT, Trempe CL, McMeel JW, Schepens CL 2007. Retinal abnormalities in early Alzheimer's disease. Investig. Ophthalmol. Vis. Sci. 48:52285–89
    [Google Scholar]
  10. Blanks JC, Torigoe Y, Hinton DR, Blanks RH 1996. Retinal pathology in Alzheimer's disease. I. Ganglion cell loss in foveal/parafoveal retina. Neurobiol. Aging 17:3377–84
    [Google Scholar]
  11. Boycott BB, Dowling JE, Kolb H 1969. Organization of the primate retina: light microscopy, with an appendix: a second type of midget bipolar cell in the primate retina. Philos. Trans. R. Soc. Lond. B 255:799109–84
    [Google Scholar]
  12. Braaf B, Vienola KV, Sheehy CK, Yang Q, Vermeer KA et al. 2013. Real-time eye motion correction in phase-resolved OCT angiography with tracking SLO. Biomed. Opt. Express 4:151–65
    [Google Scholar]
  13. Bunt AH, Minckler DS. 1977. Displaced ganglion cells in the retina of the monkey. Investig. Ophthalmol. Vis. Sci. 16:195–98
    [Google Scholar]
  14. Burns SA, Elsner AE, Sapoznik KA, Warner RL, Gast TJ 2018. Adaptive optics imaging of the human retina. Prog. Retin. Eye Res. 62:160–65
    [Google Scholar]
  15. Cense AJ, Koperda E, Brown JM, Kocaoglu OP, Gao W et al. 2009. Volumetric retinal imaging with ultrahigh-resolution spectral-domain optical coherence tomography and adaptive optics using two broadband light sources. Opt. Express 17:54095–111
    [Google Scholar]
  16. Chen X, Hou P, Jin C, Zhu W, Luo X et al. 2013. Quantitative analysis of retinal layer optical intensities on three-dimensional optical coherence tomography. Investig. Ophthalmol. Vis. Sci. 54:106846–51
    [Google Scholar]
  17. Choi SS, Zawadzki RJ, Lim MC, Brandt JD, Keltner JL et al. 2011. Evidence of outer retinal changes in glaucoma patients as revealed by ultrahigh-resolution in vivo retinal imaging. Br. J. Ophthalmol. 95:1131–41
    [Google Scholar]
  18. Choi W, Mohler KJ, Potsaid B, Lu CD, Liu JJ et al. 2013. Choriocapillaris and choroidal microvasculature imaging with ultrahigh speed OCT angiography. PLOS ONE 8:12e81499
    [Google Scholar]
  19. Chui TYP, VanNasdale DA, Burns SA 2012. The use of forward scatter to improve retinal vascular imaging with an adaptive optics scanning laser ophthalmoscope. Biomed. Opt. Express 3:102537–49
    [Google Scholar]
  20. Cole ED, Novais EA, Louzada RN, Waheed NK 2016. Contemporary retinal imaging techniques in diabetic retinopathy: a review. Clin. Exp. Ophthalmol. 44:4289–99
    [Google Scholar]
  21. Crooks J, Kolb H. 1992. Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. J. Comp. Neurol. 315:3287–302
    [Google Scholar]
  22. Cuenca N, Ortuño-Lizarán I, Sánchez-Sáez X, Kutsyr O, Albertos-Arranz H et al. 2020. Interpretation of OCT and OCTA images from a histological approach: clinical and experimental implications. Prog. Retin. Eye Res. press
    [Google Scholar]
  23. Curcio CA, Allen KA. 1990. Topography of ganglion cells in human retina. J. Comp. Neurol. 300:15–25
    [Google Scholar]
  24. Curcio CA, Allen KA, Sloan KR, Lerea CL, Hurley JB et al. 1991. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J. Comp. Neurol. 312:4610–24
    [Google Scholar]
  25. Curcio CA, Drucker DN. 1993. Retinal ganglion cells in Alzheimer's disease and aging. Ann. Neurol. 33:3248–57
    [Google Scholar]
  26. Delori FC, Pflibsen KP. 1989. Spectral reflectance of the human ocular fundus. Appl. Opt. 28:61061–77
    [Google Scholar]
  27. Do N. 2016. Parallel processing for adaptive optics optical coherence tomography (AO-OCT) image registration using GPU MS thesis, Indiana Univ./Purdue Univ., Indianapolis:
  28. Dong ZM, Wollstein G, Wang B, Schuman JS 2017. Adaptive optics optical coherence tomography in glaucoma. Prog. Retin. Eye Res. 57:76–88
    [Google Scholar]
  29. Drasdo N, Millican CL, Katholi CR, Curcio CA 2007. The length of Henle fibers in the human retina and a model of ganglion receptive field density in the visual field. Vis. Res. 47:222901–11
    [Google Scholar]
  30. Drexler W, Fujimoto JG 2015. Optical Coherence Tomography: Technology and Applications Berlin: Springer. , 2nd ed..
  31. Dunn AK, Smithpeter CL, Welch AJ, Richards-Kortum RR 1997. Finite-difference time-domain simulation of light scattering from single cells. J. Biomed. Opt. 2:3262–66
    [Google Scholar]
  32. Feeney-Burns L, Hilderbrand ES, Eldridge S 1984. Aging human RPE: morphometric analysis of macular, equatorial, and peripheral cells. Investig. Ophthalmol. Vis. Sci. 25:2195–200
    [Google Scholar]
  33. Felberer F, Kroisamer J-S, Baumann B, Zotter S, Schmidt-Erfurth U et al. 2014. Adaptive optics SLO/OCT for 3D imaging of human photoreceptors in vivo. Biomed. Opt. Express 5:2439–56
    [Google Scholar]
  34. Fortune B. 2015. In vivo imaging methods to assess glaucomatous optic neuropathy. Exp. Eye Res. 141:139–53
    [Google Scholar]
  35. Franze K, Grosche J, Skatchkov SN, Schinkinger S, Foja C et al. 2007. Muller cells are living optical fibers in the vertebrate retina. PNAS 104:208287–92
    [Google Scholar]
  36. Futter CE. 2006. The molecular regulation of organelle transport in mammalian retinal pigment epithelial cells. Pigment Cell Res 19:2104–11
    [Google Scholar]
  37. Gao H, Hollyfield JG. 1992. Aging of the human retina. Differential loss of neurons and retinal pigment epithelial cells. Investig. Ophthalmol. Vis. Sci. 33:11–17
    [Google Scholar]
  38. Gao W, Cense AJ, Zhang Y, Jonnal RS, Miller DT 2008. Measuring retinal contributions to the optical Stiles-Crawford effect with optical coherence tomography. Opt. Express 16:96486–501
    [Google Scholar]
  39. Georgiou M, Kalitzeos A, Patterson EJ, Dubra A, Carroll J, Michaelides M 2018. Adaptive optics imaging of inherited retinal diseases. Br. J. Ophthalmol. 102:81028–35
    [Google Scholar]
  40. Gibbs D, Azarian SM, Lillo C, Kitamoto J, Klomp AE et al. 2004. Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes. J. Cell Sci. 117:266473–83
    [Google Scholar]
  41. Gibbs D, Kitamoto J, Williams DS 2003. Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein. PNAS 100:116481–86
    [Google Scholar]
  42. Gill JS, Moosajee M, Dubis AM 2019. Cellular imaging of inherited retinal diseases using adaptive optics. Eye 33:1683–98
    [Google Scholar]
  43. Ginner L, Kumar A, Fechtig D, Wurster LM, Salas M et al. 2017. Noniterative digital aberration correction for cellular resolution retinal optical coherence tomography in vivo. Optica 4:8924–31
    [Google Scholar]
  44. Godara P, Dubis AM, Roorda AJ, Duncan JL, Carroll J 2010. Adaptive optics retinal imaging: emerging clinical applications. Optom. Vis. Sci. 87:12930–41
    [Google Scholar]
  45. Gorczynska I, Migacz JV, Zawadzki RJ, Capps AG, Werner JS 2016. Comparison of amplitude-decorrelation, speckle-variance and phase-variance OCT angiography methods for imaging the human retina and choroid. Biomed. Opt. Express 7:3911–42
    [Google Scholar]
  46. Harman A, Abrahams B, Moore S, Hoskins R 2000. Neuronal density in the human retinal ganglion cell layer from 16–77 years. Anat. Rec. 260:2124–31
    [Google Scholar]
  47. Haverkamp S, Haeseleer F, Hendrickson A 2003. A comparison of immunocytochemical markers to identify bipolar cell types in human and monkey retina. Vis. Neurosci. 20:6589–600
    [Google Scholar]
  48. Hermann B, Fernández EJ, Unterhuber A, Sattmann H, Fercher AF et al. 2004. Adaptive-optics ultrahigh-resolution optical coherence tomography. Opt. Lett. 29:182142–44
    [Google Scholar]
  49. Hillmann D, Spahr H, Hain C, Sudkamp H, Franke G et al. 2016a. Aberration-free volumetric high-speed imaging of in vivo retina. Sci. Rep. 6:735209
    [Google Scholar]
  50. Hillmann D, Spahr H, Pfäffle C, Sudkamp H, Franke G, Hüttmann G 2016b. In vivo optical imaging of physiological responses to photostimulation in human photoreceptors. PNAS 113:4613138–43
    [Google Scholar]
  51. Hirooka K, Izumibata S, Ukegawa K, Nitta E, Tsujikawa A 2016. Estimating the rate of retinal ganglion cell loss to detect glaucoma progression: an observational cohort study. Medicine 95:30e4209
    [Google Scholar]
  52. Hogan MJ, Alvarado JA, Weddell JE 1971. Histology of the Human Eye Philadelphia: W.B. Saunders
  53. Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG et al. 1991. Optical coherence tomography. Science 254:50351178–81
    [Google Scholar]
  54. Hunter JJ, Merigan WH, Schallek JB 2019. Imaging retinal activity in the living eye. Annu. Rev. Vis. Sci. 5:15–45
    [Google Scholar]
  55. Izatt JA, Choma MA, Dhalla A-H 2015. Theory of optical coherence tomography. Optical Coherence Tomography: Technology and Applications W Drexler, JG Fujimoto 65–94 Berlin: Springer. , 2nd ed..
    [Google Scholar]
  56. Jiang M, Esteve-Rudd J, Lopes VS, Diemer T, Lillo C et al. 2015. Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis. J. Cell Biol. 210:4595–611
    [Google Scholar]
  57. Jonnal RS, Besecker JR, Derby JC, Kocaoglu OP, Cense AJ et al. 2010. Imaging outer segment renewal in living human cone photoreceptors. Opt. Express 18:55257–70
    [Google Scholar]
  58. Jonnal RS, Gorczynska I, Migacz JV, Azimipour M, Zawadzki RJ, Werner JS 2017. The properties of outer retinal band three investigated with adaptive-optics optical coherence tomography. Investig. Ophthalmol. Vis. Sci. 58:114559–68
    [Google Scholar]
  59. Jonnal RS, Kocaoglu OP, Wang Q, Lee S, Miller DT 2012. Phase-sensitive imaging of the outer retina using optical coherence tomography and adaptive optics. Biomed. Opt. Express 3:1104–24
    [Google Scholar]
  60. Jonnal RS, Kocaoglu OP, Zawadzki RJ, Lee S-H, Werner JS, Miller DT 2014. The cellular origins of the outer retinal bands in optical coherence tomography images. Investig. Ophthalmol. Vis. Sci. 55:127904–18
    [Google Scholar]
  61. Jonnal RS, Kocaoglu OP, Zawadzki RJ, Lee S-H, Werner JS, Miller DT 2015. Author response: outer retinal bands. Investig. Ophthalmol. Vis. Sci. 56:42507–10
    [Google Scholar]
  62. Jonnal RS, Kocaoglu OP, Zawadzki RJ, Liu Z, Miller DT, Werner JS 2016. A review of adaptive optics optical coherence tomography: technical advances, scientific applications, and the future. Investig. Ophthalmol. Vis. Sci. 57:9OCT51–68
    [Google Scholar]
  63. Jonnal RS, Rha J, Zhang Y, Cense AJ, Gao W, Miller DT 2007. In vivo functional imaging of human cone photoreceptors. Opt. Express 15:2416141–60
    [Google Scholar]
  64. Joo HR, Peterson BB, Haun TJ, Dacey DM 2011. Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections. Vis. Neurosci. 28:129–37
    [Google Scholar]
  65. Ju MJ, Heisler M, Wahl D, Jian Y, Sarunic MV 2017. Multiscale sensorless adaptive optics OCT angiography system for in vivo human retinal imaging. J. Biomed. Opt. 22:121–10
    [Google Scholar]
  66. Jung HW, Kurokawa K, Hinely JC, Crowell JA, Zhang F et al. 2020. Method to evaluate spatial dynamics of inner retinal neurons near arcuate scotomas in glaucomatous patients. Proc. SPIE 11218:1121844
    [Google Scholar]
  67. Jung HW, Liu J, Liu T, George A, Smelkinson MG et al. 2019. Longitudinal adaptive optics fluorescence microscopy reveals cellular mosaicism in patients. JCI Insight 4:6124904
    [Google Scholar]
  68. Kevany BM, Palczewski K. 2010. Phagocytosis of retinal rod and cone photoreceptors. Physiology 25:18–15
    [Google Scholar]
  69. Kocaoglu OP, Cense AJ, Jonnal RS, Wang Q, Lee S et al. 2011a. Imaging retinal nerve fiber bundles using optical coherence tomography with adaptive optics. Vision Res 51:161835–44
    [Google Scholar]
  70. Kocaoglu OP, Ferguson RD, Jonnal RS, Liu Z, Wang Q et al. 2014a. Adaptive optics optical coherence tomography with dynamic retinal tracking. Biomed. Opt. Express 5:72262–84
    [Google Scholar]
  71. Kocaoglu OP, Lee S, Jonnal RS, Wang Q, Herde AE et al. 2011b. Imaging cone photoreceptors in three dimensions and in time using ultrahigh resolution optical coherence tomography with adaptive optics. Biomed. Opt. Express 2:4748–63
    [Google Scholar]
  72. Kocaoglu OP, Liu Z, Zhang F, Kurokawa K, Jonnal RS, Miller DT 2016. Photoreceptor disc shedding in the living human eye. Biomed. Opt. Express 7:114554–68
    [Google Scholar]
  73. Kocaoglu OP, Turner TL, Liu Z, Miller DT 2014b. Adaptive optics optical coherence tomography at 1 MHz. Biomed. Opt. Express 5:124186–200
    [Google Scholar]
  74. Kolb H, Linberg KA, Fisher SK 1992. Neurons of the human retina: a Golgi study. J. Comp. Neurol. 318:2147–87
    [Google Scholar]
  75. Kurokawa K, Crowell JA, Zhang F, Lassoued A, Miller DT 2019. Measuring neuron loss in the retinal ganglion cell layer in healthy subjects. Investig. Ophthalmol. Vis. Sci. 60:91781
    [Google Scholar]
  76. Kurokawa K, Crowell JA, Zhang F, Miller DT 2020. Suite of methods for assessing inner retinal temporal dynamics across spatial and temporal scales in the living human eye. Neurophotonics 7:1015013
    [Google Scholar]
  77. Kurokawa K, Liu Z, Miller DT 2017. Adaptive optics optical coherence tomography angiography for morphometric analysis of choriocapillaris [invited]. Biomed. Opt. Express 8:31803–22
    [Google Scholar]
  78. Kurokawa K, Sasaki K, Makita S, Hong Y-J, Yasuno Y 2012. Three-dimensional retinal and choroidal capillary imaging by power Doppler optical coherence angiography with adaptive optics. Opt. Express 20:2022796–812
    [Google Scholar]
  79. Laforest T, Künzi M, Kowalczuk L, Carpentras D, Behar-Cohen F, Moser C 2020. Transscleral optical phase imaging of the human retina. Nat. Photon. 14:7439–45
    [Google Scholar]
  80. LaRocca F, Nankivil D, DuBose T, Toth CA, Farsiu S, Izatt JA 2016. In vivo cellular-resolution retinal imaging in infants and children using an ultracompact handheld probe. Nat. Photon. 10:92–11
    [Google Scholar]
  81. Lassoued A, Zhang F, Kurokawa K, Liu Y, Crowell JA, Miller DT 2020. Measuring dysfunction of cone photoreceptors in retinitis pigmentosa with phase-sensitive AO-OCT. Ophthalmic Technol XXX:1121815
    [Google Scholar]
  82. Lazarus HS, Hageman GS. 1994. In situ characterization of the human hyalocyte. Arch. Ophthalmol. 112:101356–62
    [Google Scholar]
  83. Lee S-H, Werner JS, Zawadzki RJ 2013. Improved visualization of outer retinal morphology with aberration cancelling reflective optical design for adaptive optics-optical coherence tomography. Biomed. Opt. Express 4:112508–17
    [Google Scholar]
  84. Lei Y, Garrahan N, Hermann B, Fautsch MP, Johnson DH et al. 2011. Transretinal degeneration in ageing human retina: a multiphoton microscopy analysis. Br. J. Ophthalmol. 95:5727–30
    [Google Scholar]
  85. Liang J, Williams DR, Miller DT 1997. Supernormal vision and high-resolution retinal imaging through adaptive optics. J. Opt. Soc. Am. A 14:112884–92
    [Google Scholar]
  86. Litts K, Zhang Y, Freund K, Curcio C 2018. Optical coherence tomography and histology of age-related macular degeneration support mitochondria as reflectivity sources. Retina 38:3445–61
    [Google Scholar]
  87. Liu Z, Hammer DX, Saeedi O 2019a. Multimodal adaptive optics imaging of ganglion cells in patients with primary open angle glaucoma. Investig. Ophthalmol. Vis. Sci. 60:94608
    [Google Scholar]
  88. Liu Z, Kocaoglu OP, Miller DT 2016. 3D imaging of retinal pigment epithelial cells in the living human retina. Investig. Ophthalmol. Vis. Sci. 57:9OCT533–43
    [Google Scholar]
  89. Liu Z, Kocaoglu OP, Turner TL, Miller DT 2015. Modal content of living human cone photoreceptors. Biomed. Opt. Express 6:93378–404
    [Google Scholar]
  90. Liu Z, Kurokawa K, Hammer DX, Miller DT 2019b. In vivo measurement of organelle motility in human retinal pigment epithelial cells. Biomed. Opt. Express 10:84142–58
    [Google Scholar]
  91. Liu Z, Kurokawa K, Zhang F, Lee JJ, Miller DT 2017. Imaging and quantifying ganglion cells and other transparent neurons in the living human retina. PNAS 114:4812803–8
    [Google Scholar]
  92. Liu Z, Tam J, Saeedi O, Hammer DX 2018. Trans-retinal cellular imaging with multimodal adaptive optics. Biomed. Opt. Express 9:94246–62
    [Google Scholar]
  93. Martinez-Conde S, Macknik SL, Hubel DH 2004. The role of fixational eye movements in visual perception. Nat. Rev. Neurosci. 5:3229–40
    [Google Scholar]
  94. Medeiros FA, Zangwill LM, Anderson DR, Liebmann JM, Girkin CA et al. 2012. Estimating the rate of retinal ganglion cell loss in glaucoma. Am. J. Ophthalmol. 154:5814–24.e1
    [Google Scholar]
  95. Merino D, Loza-Alvarez P. 2016. Adaptive optics scanning laser ophthalmoscope imaging: technology update. Clin. Ophthalmol. 10:743–55
    [Google Scholar]
  96. Migacz JV, Gorczynska I, Azimipour M, Jonnal RS, Zawadzki RJ, Werner JS 2019. Megahertz-rate optical coherence tomography angiography improves the contrast of the choriocapillaris and choroid in human retinal imaging. Biomed. Opt. Express 10:150–65
    [Google Scholar]
  97. Miller DT, Qu J, Jonnal RS, Thorn KE 2003. Coherence gating and adaptive optics in the eye. Proceedings of Coherence Domain Optical Methods and Optical Coherence Tomography in Biomedicine VII65–72 Bellingham, WA: SPIE
    [Google Scholar]
  98. Miller DT, Williams DR, Morris GM, Liang J 1996. Images of cone photoreceptors in the living human eye. Vision Res 36:81067–79
    [Google Scholar]
  99. Morgan JIW. 2016. The fundus photo has met its match: optical coherence tomography and adaptive optics ophthalmoscopy are here to stay. Ophthalmic Physiol. Opt. 36:3218–39
    [Google Scholar]
  100. Mourant JR, Freyer JP, Hielscher AH, Eick AA, Shen D, Johnson TM 1998. Mechanisms of light scattering from biological cells relevant to noninvasive optical-tissue diagnostics. Appl. Opt. 37:163586–93
    [Google Scholar]
  101. Ogden TE. 1984. Nerve fiber layer of the primate retina: morphometric analysis. Investig. Ophthalmol. Vis. Sci. 25:119–29
    [Google Scholar]
  102. Paques M, Meimon S, Rossant F, Rosenbaum D, Mrejen S et al. 2018. Adaptive optics ophthalmoscopy: application to age-related macular degeneration and vascular diseases. Prog. Retin. Eye Res. 66:1–16
    [Google Scholar]
  103. Pascolini D, Mariotti SP. 2012. Global estimates of visual impairment: 2010. Br. J. Ophthalmol. 95:614–18
    [Google Scholar]
  104. Pfäffle C, Spahr H, Kutzner L, Burhan S, Hilge F et al. 2019. Simultaneous functional imaging of neuronal and photoreceptor layers in living human retina. Opt. Lett. 44:235671–74
    [Google Scholar]
  105. Pircher M, Kroisamer JS, Felberer F, Sattmann H, Götzinger E, Hitzenberger CK 2011. Temporal changes of human cone photoreceptors observed in vivo with SLO/OCT. Biomed. Opt. Express 2:1100–12
    [Google Scholar]
  106. Pircher M, Zawadzki RJ. 2017. Review of adaptive optics OCT (AO-OCT): principles and applications for retinal imaging [invited]. Biomed. Opt. Express 8:52536–62
    [Google Scholar]
  107. Pollreisz A, Messinger JD, Sloan KR, Mittermueller TJ, Weinhandl AS et al. 2018. Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy. Exp. Eye Res. 166:131–39
    [Google Scholar]
  108. Porter J, Queener HM, Lin J, Thorn KE, Awwal A 2006. Adaptive Optics for Vision Science: Principles, Practices, Design and Applications New York: Wiley
  109. Potsaid B, Gorczynska I, Srinivasan VJ, Chen Y, Jiang J et al. 2008. Ultrahigh speed spectral/Fourier domain OCT ophthalmic imaging at 70,000 to 312,500 axial scans per second. Opt. Express 16:1915149–69
    [Google Scholar]
  110. Quigley HA. 1999. Neuronal death in glaucoma. Prog. Retin. Eye Res. 18:139–57
    [Google Scholar]
  111. Quigley HA. 2011. Glaucoma. Lancet 377:97741367–77
    [Google Scholar]
  112. Rodieck RW. 1998. The First Steps in Seeing Sunderland, MA: Sinauer Assoc.
  113. Roorda AJ, Duncan JL. 2015. Adaptive optics ophthalmoscopy. Annu. Rev. Vis. Sci. 1:19–50
    [Google Scholar]
  114. Roorda AJ, Williams DR. 1999. The arrangement of the three cone classes in the living human eye. Nature 397:6719520–22
    [Google Scholar]
  115. Ruggiero L, Finnemann SC. 2014. Rhythmicity of the retinal pigment epithelium. The Retina and Circadian Rhythms G Tosini, PM Iuvone, DG McMahon, SP Collin 95–112 Berlin: Springer
    [Google Scholar]
  116. Sabesan R, Hofer H, Roorda AJ 2015. Characterizing the human cone photoreceptor mosaic via dynamic photopigment densitometry. PLOS ONE 10:12e0144891
    [Google Scholar]
  117. Salas M, Augustin M, Ginner L, Kumar A, Baumann B et al. 2017. Visualization of micro-capillaries using optical coherence tomography angiography with and without adaptive optics. Biomed. Opt. Express 8:1207–22
    [Google Scholar]
  118. Schnapf JL, Nunn BJ, Meister M, Baylor DA 1990. Visual transduction in cones of the monkey Macaca fascicularis.. J. Physiol 427:681–713
    [Google Scholar]
  119. Scoles D, Sulai YN, Langlo CS, Fishman GA, Curcio CA et al. 2014. In vivo imaging of human cone photoreceptor inner segments. Investig. Ophthalmol. Vis. Sci. 55:74244–51
    [Google Scholar]
  120. South FA, Kurokawa K, Liu Z, Liu Y-Z, Miller DT, Boppart SA 2018. Combined hardware and computational optical wavefront correction. Biomed. Opt. Express 9:62562–74
    [Google Scholar]
  121. Spaide RF, Curcio CA. 2011. Anatomical correlates to the bands seen in the outer retina by optical coherence tomography: literature review and model. Retina 31:81609–19
    [Google Scholar]
  122. Staurenghi G, Sadda S, Chakravarthy U, Spaide RF 2014. Proposed lexicon for anatomic landmarks in normal posterior segment spectral-domain optical coherence tomography: the IN·OCT consensus. Ophthalmology 121:81572–78
    [Google Scholar]
  123. Steinberg RH, Wood I, Hogan MJ 1977. Pigment epithelial ensheathment and phagocytosis of extrafoveal cones in human retina. Philos. Trans. R. Soc. Lond. Ser. B 277:958459–71
    [Google Scholar]
  124. Stockman A, Sharpe LT. 2000. The spectral sensitivities of the middle- and long-wavelength-sensitive cones derived from measurements in observers of known genotype. Vis. Res. 40:131711–37
    [Google Scholar]
  125. Tanna H, Dubis AM, Ayub N, Tait DM, Rha J et al. 2010. Retinal imaging using commercial broadband optical coherence tomography. Br. J. Ophthalmol. 94:3372–76
    [Google Scholar]
  126. Torti C, Povazay B, Hofer B, Unterhuber A, Carroll J et al. 2009. Adaptive optics optical coherence tomography at 120,000 depth scans/s for non-invasive cellular phenotyping of the living human retina. Opt. Express 17:2219382–400
    [Google Scholar]
  127. Vagaja NN, Chinnery HR, Binz N, Kezic JM, Rakoczy EP, McMenamin PG 2012. Changes in murine hyalocytes are valuable early indicators of ocular disease. Investig. Ophthalmol. Vis. Sci. 53:31445–51
    [Google Scholar]
  128. Volpe NJ, Simonett J, Fawzi AA, Siddique T 2015. Ophthalmic manifestations of amyotrophic lateral sclerosis (an American Ophthalmological Society Thesis). Trans. Am. Ophthalmol. Soc. 113:T12
    [Google Scholar]
  129. Wang L, Dong J, Cull G, Fortune B, Cioffi GA 2003. Varicosities of intraretinal ganglion cell axons in human and nonhuman primates. Investig. Ophthalmol. Vis. Sci. 44:12–9
    [Google Scholar]
  130. Watanabe M, Rodieck RW. 1989. Parasol and midget ganglion cells of the primate retina. J. Comp. Neurol. 289:3434–54
    [Google Scholar]
  131. Weinreb RN, Aung T, Medeiros FA 2014. The pathophysiology and treatment of glaucoma: a review. JAMA 311:181901–11
    [Google Scholar]
  132. Weiter JJ, Delori FC, Wing GL, Fitch KA 1986. Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes. Investig. Ophthalmol. Vis. Sci. 27:2145–52
    [Google Scholar]
  133. Wells-Gray EM, Choi SS, Ohr M, Cebulla CM, Doble N 2019. Photoreceptor identification and quantitative analysis for the detection of retinal disease in AO-OCT imaging. Ophthalmic Technol XXIX:108580O-1–9
    [Google Scholar]
  134. Wells-Gray EM, Choi SS, Slabaugh M, Weber P, Doble N 2018a. Inner retinal changes in primary open-angle glaucoma revealed through adaptive optics-optical coherence tomography. J. Glaucoma 27:111025–28
    [Google Scholar]
  135. Wells-Gray EM, Choi SS, Zawadzki RJ, Finn SC, Greiner C et al. 2018b. Volumetric imaging of rod and cone photoreceptor structure with a combined adaptive optics-optical coherence tomography-scanning laser ophthalmoscope. J. Biomed. Opt. 23:31–15
    [Google Scholar]
  136. Werner JS, Keltner JL, Zawadzki RJ, Choi SS 2011. Outer retinal abnormalities associated with inner retinal pathology in nonglaucomatous and glaucomatous optic neuropathies. Eye 25:3279–89
    [Google Scholar]
  137. Wilk MA, Huckenpahler AL, Collery RF, Link BA, Carroll J 2017. The effect of retinal melanin on optical coherence tomography images. Transl. Vis. Sci. Technol. 6:28
    [Google Scholar]
  138. Wilson JD, Cottrell WJ, Foster TH 2007. Index-of-refraction-dependent subcellular light scattering observed with organelle-specific dyes. J. Biomed. Opt. 12:1014010
    [Google Scholar]
  139. Wilson JD, Foster TH. 2007. Characterization of lysosomal contribution to whole-cell light scattering by organelle ablation. J. Biomed. Opt. 12:3030503
    [Google Scholar]
  140. Wong KSK, Jian Y, Cua M, Bonora S, Zawadzki RJ, Sarunic MV 2015. In vivo imaging of human photoreceptor mosaic with wavefront sensorless adaptive optics optical coherence tomography. Biomed. Opt. Express 6:2580–90
    [Google Scholar]
  141. Young RW. 1967. The renewal of photoreceptor cell outer segments. J. Cell Biol. 33:161–72
    [Google Scholar]
  142. Young RW, Bok D. 1969. Participation of the retinal pigment epithelium in the rod outer segment renewal process. J. Cell Biol. 42:2392–403
    [Google Scholar]
  143. Zawadzki RJ, Cense AJ, Zhang Y, Choi SS, Miller DT, Werner JS 2008. Ultrahigh-resolution optical coherence tomography with monochromatic and chromatic aberration correction. Opt. Express 16:118126–43
    [Google Scholar]
  144. Zawadzki RJ, Choi SS, Jones SM, Oliver SS, Werner JS 2007. Adaptive optics-optical coherence tomography: optimizing visualization of microscopic retinal structures in three dimensions. J. Opt. Soc. Am. A 24:51373–83
    [Google Scholar]
  145. Zawadzki RJ, Jones SM, Olivier SS, Zhao M, Bower BA et al. 2005. Adaptive-optics optical coherence tomography for high-resolution and high-speed 3D retinal in vivo imaging. Opt. Express 13:218532–46
    [Google Scholar]
  146. Zhang F. 2019. Imaging physiological activities of photoreceptors with adaptive optics optical coherence tomography in the living human eye PhD thesis, Indiana Univ Indianapolis:
  147. Zhang F, Kurokawa K, Lassoued A, Crowell JA, Miller DT 2019. Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics. PNAS 116:7951–56
    [Google Scholar]
  148. Zhang F, Liu Z, Kurokawa K, Miller DT 2017. Tracking dynamics of photoreceptor disc shedding with adaptive optics-optical coherence tomography. Ophthalmic Technol XXVII:1004517
    [Google Scholar]
  149. Zhang P, Zawadzki RJ, Goswami M, Nguyen PT, Yarov-Yarovoy V et al. 2017. In vivo optophysiology reveals that G-protein activation triggers osmotic swelling and increased light scattering of rod photoreceptors. PNAS 114:14E2937–46
    [Google Scholar]
  150. Zhang Q-X, Lu R-W, Messinger JD, Curcio CA, Guarcello V, Yao X-C 2013. In vivo optical coherence tomography of light-driven melanosome translocation in retinal pigment epithelium. Sci. Rep. 3:12644
    [Google Scholar]
  151. Zhang T, Kho AM, Srinivasan VJ 2019. Improving visible light OCT of the human retina with rapid spectral shaping and axial tracking. Biomed. Opt. Express 10:62918–31
    [Google Scholar]
  152. Zhang Y, Cense AJ, Rha J, Jonnal RS, Gao W et al. 2006. High-speed volumetric imaging of cone photoreceptors with adaptive optics spectral-domain optical coherence tomography. Opt. Express 14:104380–94
    [Google Scholar]
  153. Zhang Y, Rha J, Jonnal RS, Miller DT 2005. Adaptive optics parallel spectral domain optical coherence tomography for imaging the living retina. Opt. Express 13:124792–811
    [Google Scholar]
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