Abstract

Two-photon excited fluorescence (TPEF) imaging of the retina is a developing technique that provides non-invasive compound-specific measurements from the retina. In this report, we demonstrate high-resolution TPEF imaging of the mouse retina using sensorless adaptive optics (SAO) and optical coherence tomography (OCT). A single near-infrared light source was used for simultaneous multi-modal imaging with OCT and TPEF. The image-based SAO could be performed using the en face OCT or the TPEF for aberration correction. Our results demonstrate OCT and TPEF for angiography. Also, we demonstrate non-invasive cellular-resolution imaging of fluorescently labelled cells and the Retinal Pigment Epithelium (RPE) mosaic.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2019 (2)

2018 (7)

P. Zhang, J. Mocci, D. J. Wahl, R. K. Meleppat, S. K. Manna, M. Quintavalla, R. Muradore, M. V. Sarunic, S. Bonora, E. N. Pugh, and R. J. Zawadzki, “Effect of a contact lens on mouse retinal in vivo imaging: Effective focal length changes and monochromatic aberrations,” Exp. Eye Res. 172, 86–93 (2018).
[Crossref]

M. T. Bernucci, C. W. Merkle, and V. J. Srinivasan, “Investigation of artifacts in retinal and choroidal OCT angiography with a contrast agent,” Biomed. Opt. Express 9(3), 1020–1040 (2018).
[Crossref]

T. Kamali, J. Fischer, S. Farrell, W. H. Baldridge, G. Zinser, and B. C. Chauhan, “Simultaneous in vivo confocal reflectance and two-photon retinal ganglion cell imaging based on a hollow core fiber platform,” J. Biomed. Opt. 23(09), 1 (2018).
[Crossref]

L. L. Molday, D. Wahl, M. V. Sarunic, and R. S. Molday, “Localization and functional characterization of the p.Asn965Ser (N965S) ABCA4 variant in mice reveal pathogenic mechanisms underlying Stargardt macular degeneration,” Hum. Mol. Genet. 27(2), 295–306 (2018).
[Crossref]

G. Palczewska, P. Stremplewski, S. Suh, N. Alexander, D. Salom, Z. Dong, D. Ruminski, E. H. Choi, A. E. Sears, T. S. Kern, M. Wojtkowski, and K. Palczewski, “Two-photon imaging of the mammalian retina with ultrafast pulsing laser,” JCI insight 3(17), 121555 (2018).
[Crossref]

C. Schwarz, R. Sharma, S. K. Cheong, M. Keller, D. R. Williams, and J. J. Hunter, “Selective S Cone Damage and Retinal Remodeling Following Intense Ultrashort Pulse Laser Exposures in the Near-Infrared,” Invest. Ophthalmol. Visual Sci. 59(15), 5973–5984 (2018).
[Crossref]

Z. Liu, J. Tam, O. Saeedi, and D. X. Hammer, “Trans-retinal cellular imaging with multimodal adaptive optics,” Biomed. Opt. Express 9(9), 4246–4262 (2018).
[Crossref]

2017 (4)

Z. Liu, K. Kurokawa, F. Zhang, J. J. Lee, and D. T. Miller, “Imaging and quantifying ganglion cells and other transparent neurons in the living human retina,” Proc. Natl. Acad. Sci. U. S. A. 114(48), 12803–12808 (2017).
[Crossref]

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref]

M. Heisler, S. Lee, Z. Mammo, Y. Jian, M. Ju, A. Merkur, E. Navajas, C. Balaratnasingam, M. F. Beg, and M. V. Sarunic, “Strip-based registration of serially acquired optical coherence tomography angiography,” J. Biomed. Opt. 22(3), 036007 (2017).
[Crossref]

M. Salas, M. Augustin, L. Ginner, A. Kumar, B. Baumann, R. Leitgeb, W. Drexler, S. Prager, J. Hafner, U. Schmidt-Erfurth, and M. Pircher, “Visualization of micro-capillaries using optical coherence tomography angiography with and without adaptive optics,” Biomed. Opt. Express 8(1), 207–222 (2017).
[Crossref]

2016 (6)

2015 (3)

2014 (2)

Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
[Crossref]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref]

2013 (4)

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref]

J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Visual Sci. 54(13), 8237–8250 (2013).
[Crossref]

Y. Jian, K. Wong, and M. V. Sarunic, “Graphics processing unit accelerated optical coherence tomography processing at megahertz axial scan rate and high resolution video rate volumetric rendering,” J. Biomed. Opt. 18(2), 026002 (2013).
[Crossref]

L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
[Crossref]

2012 (1)

2011 (1)

2010 (2)

G. Palczewska, T. Maeda, Y. Imanishi, W. Sun, Y. Chen, D. R. Williams, D. W. Piston, A. Maeda, and K. Palczewski, “Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes,” Nat. Med. 16(12), 1444–1449 (2010).
[Crossref]

A. Myronenko and X. Song, “Intensity-based image registration by minimizing residual complexity,” IEEE Trans. Med. Imaging 29(11), 1882–1891 (2010).
[Crossref]

2008 (1)

J. I. W. Morgan, J. J. Hunter, B. Masella, R. Wolfe, D. C. Gray, W. H. Merigan, F. C. Delori, and D. R. Williams, “Light-Induced Retinal Changes Observed with High-Resolution Autofluorescence Imaging of the Retinal Pigment Epithelium,” Invest. Ophthalmol. Visual Sci. 49(8), 3715–3729 (2008).
[Crossref]

2005 (1)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref]

2004 (2)

Y. Imanishi, M. L. Batten, D. W. Piston, W. Baehr, and K. Palczewski, “Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye,” J. Cell Biol. 164(3), 373–383 (2004).
[Crossref]

D. C. Adler, T. H. Ko, and J. G. Fujimoto, “Speckle reduction in optical coherence tomography images by use of a spatially adaptive wavelet filter,” Opt. Lett. 29(24), 2878–2880 (2004).
[Crossref]

1996 (1)

R. H. Webb, “Confocal optical microscopy,” Rep. Prog. Phys. 59(3), 427–471 (1996).
[Crossref]

1990 (1)

W. Denk, J. Strickler, and W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref]

1979 (1)

W. T. Ham, H. A. Mueller, J. J. Ruffolo, and A. M. Clarke, “Sensitivity of the retina to radiation damage as a function of wavelength,” Photochem. Photobiol. 29(4), 735–743 (1979).
[Crossref]

Adler, D. C.

Ahmad, K.

Alexander, N.

G. Palczewska, P. Stremplewski, S. Suh, N. Alexander, D. Salom, Z. Dong, D. Ruminski, E. H. Choi, A. E. Sears, T. S. Kern, M. Wojtkowski, and K. Palczewski, “Two-photon imaging of the mammalian retina with ultrafast pulsing laser,” JCI insight 3(17), 121555 (2018).
[Crossref]

Alexander, N. S.

N. S. Alexander, G. Palczewska, P. Stremplewski, M. Wojtkowski, T. S. Kern, and K. Palczewski, “Image registration and averaging of low laser power two-photon fluorescence images of mouse retina,” Biomed. Opt. Express 7(7), 2671–2691 (2016).
[Crossref]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref]

Artal, P.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref]

Atchison, D. A.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref]

Augustin, M.

Awwal, A.

J. Porter, H. Queener, J. Lin, K. Thorn, and A. Awwal, Adaptive Optics for Vision Science: Principles, Practices, Design and Applications (Wiley, 2006).

Baehr, W.

Y. Imanishi, M. L. Batten, D. W. Piston, W. Baehr, and K. Palczewski, “Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye,” J. Cell Biol. 164(3), 373–383 (2004).
[Crossref]

Balaratnasingam, C.

M. Heisler, S. Lee, Z. Mammo, Y. Jian, M. Ju, A. Merkur, E. Navajas, C. Balaratnasingam, M. F. Beg, and M. V. Sarunic, “Strip-based registration of serially acquired optical coherence tomography angiography,” J. Biomed. Opt. 22(3), 036007 (2017).
[Crossref]

Baldridge, W. H.

T. Kamali, J. Fischer, S. Farrell, W. H. Baldridge, G. Zinser, and B. C. Chauhan, “Simultaneous in vivo confocal reflectance and two-photon retinal ganglion cell imaging based on a hollow core fiber platform,” J. Biomed. Opt. 23(09), 1 (2018).
[Crossref]

Bar-Noam, A. S.

A. S. Bar-Noam, N. Farah, and S. Shoham, “Correction-free remotely scanned two-photon in vivo mouse retinal imaging,” Light: Sci. Appl. 5(1), e16007 (2016).
[Crossref]

Batten, M. L.

Y. Imanishi, M. L. Batten, D. W. Piston, W. Baehr, and K. Palczewski, “Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye,” J. Cell Biol. 164(3), 373–383 (2004).
[Crossref]

Baumann, B.

Beg, M. F.

M. Heisler, S. Lee, Z. Mammo, Y. Jian, M. Ju, A. Merkur, E. Navajas, C. Balaratnasingam, M. F. Beg, and M. V. Sarunic, “Strip-based registration of serially acquired optical coherence tomography angiography,” J. Biomed. Opt. 22(3), 036007 (2017).
[Crossref]

Bernucci, M. T.

Bonora, S.

D. J. Wahl, P. Zhang, J. Mocci, M. Quintavalla, R. Muradore, Y. Jian, S. Bonora, M. V. Sarunic, and R. J. Zawadzki, “Adaptive optics in the mouse eye: wavefront sensing based vs. image-guided aberration correction,” Biomed. Opt. Express 10(9), 4757–4774 (2019).
[Crossref]

P. Zhang, J. Mocci, D. J. Wahl, R. K. Meleppat, S. K. Manna, M. Quintavalla, R. Muradore, M. V. Sarunic, S. Bonora, E. N. Pugh, and R. J. Zawadzki, “Effect of a contact lens on mouse retinal in vivo imaging: Effective focal length changes and monochromatic aberrations,” Exp. Eye Res. 172, 86–93 (2018).
[Crossref]

D. J. Wahl, Y. Jian, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics fluorescence biomicroscope for in vivo retinal imaging in mice,” Biomed. Opt. Express 7(1), 1–12 (2016).
[Crossref]

M. Cua, D. J. Wahl, Y. Zhao, S. Lee, S. Bonora, R. J. Zawadzki, Y. Jian, and M. V. Sarunic, “Coherence-Gated Sensorless Adaptive Optics Multiphoton Retinal Imaging,” Sci. Rep. 6(1), 32223 (2016).
[Crossref]

Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
[Crossref]

Burns, S. A.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref]

Callaway, E. M.

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R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
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L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
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J. I. W. Morgan, J. J. Hunter, B. Masella, R. Wolfe, D. C. Gray, W. H. Merigan, F. C. Delori, and D. R. Williams, “Light-Induced Retinal Changes Observed with High-Resolution Autofluorescence Imaging of the Retinal Pigment Epithelium,” Invest. Ophthalmol. Visual Sci. 49(8), 3715–3729 (2008).
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P. Zhang, J. Mocci, D. J. Wahl, R. K. Meleppat, S. K. Manna, M. Quintavalla, R. Muradore, M. V. Sarunic, S. Bonora, E. N. Pugh, and R. J. Zawadzki, “Effect of a contact lens on mouse retinal in vivo imaging: Effective focal length changes and monochromatic aberrations,” Exp. Eye Res. 172, 86–93 (2018).
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L. L. Molday, D. Wahl, M. V. Sarunic, and R. S. Molday, “Localization and functional characterization of the p.Asn965Ser (N965S) ABCA4 variant in mice reveal pathogenic mechanisms underlying Stargardt macular degeneration,” Hum. Mol. Genet. 27(2), 295–306 (2018).
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L. L. Molday, D. Wahl, M. V. Sarunic, and R. S. Molday, “Localization and functional characterization of the p.Asn965Ser (N965S) ABCA4 variant in mice reveal pathogenic mechanisms underlying Stargardt macular degeneration,” Hum. Mol. Genet. 27(2), 295–306 (2018).
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J. I. W. Morgan, J. J. Hunter, B. Masella, R. Wolfe, D. C. Gray, W. H. Merigan, F. C. Delori, and D. R. Williams, “Light-Induced Retinal Changes Observed with High-Resolution Autofluorescence Imaging of the Retinal Pigment Epithelium,” Invest. Ophthalmol. Visual Sci. 49(8), 3715–3729 (2008).
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P. Stremplewski, K. Komar, K. Palczewski, M. Wojtkowski, and G. Palczewska, “Periscope for noninvasive two-photon imaging of murine retina in vivo,” Biomed. Opt. Express 6(9), 3352–3361 (2015).
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G. Palczewska, T. Maeda, Y. Imanishi, W. Sun, Y. Chen, D. R. Williams, D. W. Piston, A. Maeda, and K. Palczewski, “Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes,” Nat. Med. 16(12), 1444–1449 (2010).
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Y. Imanishi, M. L. Batten, D. W. Piston, W. Baehr, and K. Palczewski, “Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye,” J. Cell Biol. 164(3), 373–383 (2004).
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P. Zhang, J. Mocci, D. J. Wahl, R. K. Meleppat, S. K. Manna, M. Quintavalla, R. Muradore, M. V. Sarunic, S. Bonora, E. N. Pugh, and R. J. Zawadzki, “Effect of a contact lens on mouse retinal in vivo imaging: Effective focal length changes and monochromatic aberrations,” Exp. Eye Res. 172, 86–93 (2018).
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D. J. Wahl, P. Zhang, J. Mocci, M. Quintavalla, R. Muradore, Y. Jian, S. Bonora, M. V. Sarunic, and R. J. Zawadzki, “Adaptive optics in the mouse eye: wavefront sensing based vs. image-guided aberration correction,” Biomed. Opt. Express 10(9), 4757–4774 (2019).
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W. T. Ham, H. A. Mueller, J. J. Ruffolo, and A. M. Clarke, “Sensitivity of the retina to radiation damage as a function of wavelength,” Photochem. Photobiol. 29(4), 735–743 (1979).
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D. J. Wahl, Y. Jian, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics fluorescence biomicroscope for in vivo retinal imaging in mice,” Biomed. Opt. Express 7(1), 1–12 (2016).
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J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Visual Sci. 54(13), 8237–8250 (2013).
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C. Schwarz, R. Sharma, W. S. Fischer, M. Chung, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “Safety assessment in macaques of light exposures for functional two-photon ophthalmoscopy in humans,” Biomed. Opt. Express 7(12), 5148–5169 (2016).
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G. Palczewska, P. Stremplewski, S. Suh, N. Alexander, D. Salom, Z. Dong, D. Ruminski, E. H. Choi, A. E. Sears, T. S. Kern, M. Wojtkowski, and K. Palczewski, “Two-photon imaging of the mammalian retina with ultrafast pulsing laser,” JCI insight 3(17), 121555 (2018).
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Thorn, K.

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L. L. Molday, D. Wahl, M. V. Sarunic, and R. S. Molday, “Localization and functional characterization of the p.Asn965Ser (N965S) ABCA4 variant in mice reveal pathogenic mechanisms underlying Stargardt macular degeneration,” Hum. Mol. Genet. 27(2), 295–306 (2018).
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D. J. Wahl, R. Ng, M. J. Ju, Y. Jian, and M. V. Sarunic, “Sensorless adaptive optics multimodal en-face small animal retinal imaging,” Biomed. Opt. Express 10(1), 252–267 (2019).
[Crossref]

D. J. Wahl, P. Zhang, J. Mocci, M. Quintavalla, R. Muradore, Y. Jian, S. Bonora, M. V. Sarunic, and R. J. Zawadzki, “Adaptive optics in the mouse eye: wavefront sensing based vs. image-guided aberration correction,” Biomed. Opt. Express 10(9), 4757–4774 (2019).
[Crossref]

P. Zhang, J. Mocci, D. J. Wahl, R. K. Meleppat, S. K. Manna, M. Quintavalla, R. Muradore, M. V. Sarunic, S. Bonora, E. N. Pugh, and R. J. Zawadzki, “Effect of a contact lens on mouse retinal in vivo imaging: Effective focal length changes and monochromatic aberrations,” Exp. Eye Res. 172, 86–93 (2018).
[Crossref]

M. Cua, D. J. Wahl, Y. Zhao, S. Lee, S. Bonora, R. J. Zawadzki, Y. Jian, and M. V. Sarunic, “Coherence-Gated Sensorless Adaptive Optics Multiphoton Retinal Imaging,” Sci. Rep. 6(1), 32223 (2016).
[Crossref]

D. J. Wahl, Y. Jian, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics fluorescence biomicroscope for in vivo retinal imaging in mice,” Biomed. Opt. Express 7(1), 1–12 (2016).
[Crossref]

Webb, R. H.

R. H. Webb, “Confocal optical microscopy,” Rep. Prog. Phys. 59(3), 427–471 (1996).
[Crossref]

Webb, W.

W. Denk, J. Strickler, and W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref]

Werner, J. S.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref]

Williams, D. R.

C. Schwarz, R. Sharma, S. K. Cheong, M. Keller, D. R. Williams, and J. J. Hunter, “Selective S Cone Damage and Retinal Remodeling Following Intense Ultrashort Pulse Laser Exposures in the Near-Infrared,” Invest. Ophthalmol. Visual Sci. 59(15), 5973–5984 (2018).
[Crossref]

C. Schwarz, R. Sharma, W. S. Fischer, M. Chung, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “Safety assessment in macaques of light exposures for functional two-photon ophthalmoscopy in humans,” Biomed. Opt. Express 7(12), 5148–5169 (2016).
[Crossref]

A. Guevara-Torres, D. R. Williams, and J. B. Schallek, “Imaging translucent cell bodies in the living mouse retina without contrast agents,” Biomed. Opt. Express 6(6), 2106–2119 (2015).
[Crossref]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref]

J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Visual Sci. 54(13), 8237–8250 (2013).
[Crossref]

L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
[Crossref]

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. Express 3(4), 715–734 (2012).
[Crossref]

Y. Geng, L. A. Schery, R. Sharma, A. Dubra, K. Ahmad, R. T. Libby, and D. R. Williams, “Optical properties of the mouse eye,” Biomed. Opt. Express 2(4), 717–738 (2011).
[Crossref]

G. Palczewska, T. Maeda, Y. Imanishi, W. Sun, Y. Chen, D. R. Williams, D. W. Piston, A. Maeda, and K. Palczewski, “Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes,” Nat. Med. 16(12), 1444–1449 (2010).
[Crossref]

J. I. W. Morgan, J. J. Hunter, B. Masella, R. Wolfe, D. C. Gray, W. H. Merigan, F. C. Delori, and D. R. Williams, “Light-Induced Retinal Changes Observed with High-Resolution Autofluorescence Imaging of the Retinal Pigment Epithelium,” Invest. Ophthalmol. Visual Sci. 49(8), 3715–3729 (2008).
[Crossref]

Wojtkowski, M.

Wolfe, R.

J. I. W. Morgan, J. J. Hunter, B. Masella, R. Wolfe, D. C. Gray, W. H. Merigan, F. C. Delori, and D. R. Williams, “Light-Induced Retinal Changes Observed with High-Resolution Autofluorescence Imaging of the Retinal Pigment Epithelium,” Invest. Ophthalmol. Visual Sci. 49(8), 3715–3729 (2008).
[Crossref]

Wong, K.

Y. Jian, K. Wong, and M. V. Sarunic, “Graphics processing unit accelerated optical coherence tomography processing at megahertz axial scan rate and high resolution video rate volumetric rendering,” J. Biomed. Opt. 18(2), 026002 (2013).
[Crossref]

Xu, J.

Ye, C.

Yin, L.

Yoon, G.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref]

Young, L. K.

S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref]

Zawadzki, R. J.

D. J. Wahl, P. Zhang, J. Mocci, M. Quintavalla, R. Muradore, Y. Jian, S. Bonora, M. V. Sarunic, and R. J. Zawadzki, “Adaptive optics in the mouse eye: wavefront sensing based vs. image-guided aberration correction,” Biomed. Opt. Express 10(9), 4757–4774 (2019).
[Crossref]

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[Crossref]

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[Crossref]

M. Cua, D. J. Wahl, Y. Zhao, S. Lee, S. Bonora, R. J. Zawadzki, Y. Jian, and M. V. Sarunic, “Coherence-Gated Sensorless Adaptive Optics Multiphoton Retinal Imaging,” Sci. Rep. 6(1), 32223 (2016).
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Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
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Z. Liu, K. Kurokawa, F. Zhang, J. J. Lee, and D. T. Miller, “Imaging and quantifying ganglion cells and other transparent neurons in the living human retina,” Proc. Natl. Acad. Sci. U. S. A. 114(48), 12803–12808 (2017).
[Crossref]

Zhang, P.

D. J. Wahl, P. Zhang, J. Mocci, M. Quintavalla, R. Muradore, Y. Jian, S. Bonora, M. V. Sarunic, and R. J. Zawadzki, “Adaptive optics in the mouse eye: wavefront sensing based vs. image-guided aberration correction,” Biomed. Opt. Express 10(9), 4757–4774 (2019).
[Crossref]

P. Zhang, J. Mocci, D. J. Wahl, R. K. Meleppat, S. K. Manna, M. Quintavalla, R. Muradore, M. V. Sarunic, S. Bonora, E. N. Pugh, and R. J. Zawadzki, “Effect of a contact lens on mouse retinal in vivo imaging: Effective focal length changes and monochromatic aberrations,” Exp. Eye Res. 172, 86–93 (2018).
[Crossref]

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S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
[Crossref]

Zhao, Y.

M. Cua, D. J. Wahl, Y. Zhao, S. Lee, S. Bonora, R. J. Zawadzki, Y. Jian, and M. V. Sarunic, “Coherence-Gated Sensorless Adaptive Optics Multiphoton Retinal Imaging,” Sci. Rep. 6(1), 32223 (2016).
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T. Kamali, J. Fischer, S. Farrell, W. H. Baldridge, G. Zinser, and B. C. Chauhan, “Simultaneous in vivo confocal reflectance and two-photon retinal ganglion cell imaging based on a hollow core fiber platform,” J. Biomed. Opt. 23(09), 1 (2018).
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Biomed. Opt. Express (15)

Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
[Crossref]

C. Schwarz, R. Sharma, W. S. Fischer, M. Chung, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “Safety assessment in macaques of light exposures for functional two-photon ophthalmoscopy in humans,” Biomed. Opt. Express 7(12), 5148–5169 (2016).
[Crossref]

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. Express 3(4), 715–734 (2012).
[Crossref]

D. J. Wahl, Y. Jian, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics fluorescence biomicroscope for in vivo retinal imaging in mice,” Biomed. Opt. Express 7(1), 1–12 (2016).
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M. T. Bernucci, C. W. Merkle, and V. J. Srinivasan, “Investigation of artifacts in retinal and choroidal OCT angiography with a contrast agent,” Biomed. Opt. Express 9(3), 1020–1040 (2018).
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D. J. Wahl, R. Ng, M. J. Ju, Y. Jian, and M. V. Sarunic, “Sensorless adaptive optics multimodal en-face small animal retinal imaging,” Biomed. Opt. Express 10(1), 252–267 (2019).
[Crossref]

D. J. Wahl, P. Zhang, J. Mocci, M. Quintavalla, R. Muradore, Y. Jian, S. Bonora, M. V. Sarunic, and R. J. Zawadzki, “Adaptive optics in the mouse eye: wavefront sensing based vs. image-guided aberration correction,” Biomed. Opt. Express 10(9), 4757–4774 (2019).
[Crossref]

Y. Geng, L. A. Schery, R. Sharma, A. Dubra, K. Ahmad, R. T. Libby, and D. R. Williams, “Optical properties of the mouse eye,” Biomed. Opt. Express 2(4), 717–738 (2011).
[Crossref]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref]

P. Stremplewski, K. Komar, K. Palczewski, M. Wojtkowski, and G. Palczewska, “Periscope for noninvasive two-photon imaging of murine retina in vivo,” Biomed. Opt. Express 6(9), 3352–3361 (2015).
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N. S. Alexander, G. Palczewska, P. Stremplewski, M. Wojtkowski, T. S. Kern, and K. Palczewski, “Image registration and averaging of low laser power two-photon fluorescence images of mouse retina,” Biomed. Opt. Express 7(7), 2671–2691 (2016).
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Z. Liu, J. Tam, O. Saeedi, and D. X. Hammer, “Trans-retinal cellular imaging with multimodal adaptive optics,” Biomed. Opt. Express 9(9), 4246–4262 (2018).
[Crossref]

A. Guevara-Torres, D. R. Williams, and J. B. Schallek, “Imaging translucent cell bodies in the living mouse retina without contrast agents,” Biomed. Opt. Express 6(6), 2106–2119 (2015).
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Clin. Ophthalmol. (1)

D. Merino and P. Loza-Alvarez, “Adaptive optics scanning laser ophthalmoscope imaging: technology update,” Clin. Ophthalmol. 10, 743–755 (2016).
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P. Zhang, J. Mocci, D. J. Wahl, R. K. Meleppat, S. K. Manna, M. Quintavalla, R. Muradore, M. V. Sarunic, S. Bonora, E. N. Pugh, and R. J. Zawadzki, “Effect of a contact lens on mouse retinal in vivo imaging: Effective focal length changes and monochromatic aberrations,” Exp. Eye Res. 172, 86–93 (2018).
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L. L. Molday, D. Wahl, M. V. Sarunic, and R. S. Molday, “Localization and functional characterization of the p.Asn965Ser (N965S) ABCA4 variant in mice reveal pathogenic mechanisms underlying Stargardt macular degeneration,” Hum. Mol. Genet. 27(2), 295–306 (2018).
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J. I. W. Morgan, J. J. Hunter, B. Masella, R. Wolfe, D. C. Gray, W. H. Merigan, F. C. Delori, and D. R. Williams, “Light-Induced Retinal Changes Observed with High-Resolution Autofluorescence Imaging of the Retinal Pigment Epithelium,” Invest. Ophthalmol. Visual Sci. 49(8), 3715–3729 (2008).
[Crossref]

J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Visual Sci. 54(13), 8237–8250 (2013).
[Crossref]

C. Schwarz, R. Sharma, S. K. Cheong, M. Keller, D. R. Williams, and J. J. Hunter, “Selective S Cone Damage and Retinal Remodeling Following Intense Ultrashort Pulse Laser Exposures in the Near-Infrared,” Invest. Ophthalmol. Visual Sci. 59(15), 5973–5984 (2018).
[Crossref]

J. Biomed. Opt. (3)

Y. Jian, K. Wong, and M. V. Sarunic, “Graphics processing unit accelerated optical coherence tomography processing at megahertz axial scan rate and high resolution video rate volumetric rendering,” J. Biomed. Opt. 18(2), 026002 (2013).
[Crossref]

T. Kamali, J. Fischer, S. Farrell, W. H. Baldridge, G. Zinser, and B. C. Chauhan, “Simultaneous in vivo confocal reflectance and two-photon retinal ganglion cell imaging based on a hollow core fiber platform,” J. Biomed. Opt. 23(09), 1 (2018).
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[Crossref]

Rep. Prog. Phys. (1)

R. H. Webb, “Confocal optical microscopy,” Rep. Prog. Phys. 59(3), 427–471 (1996).
[Crossref]

Sci. Rep. (1)

M. Cua, D. J. Wahl, Y. Zhao, S. Lee, S. Bonora, R. J. Zawadzki, Y. Jian, and M. V. Sarunic, “Coherence-Gated Sensorless Adaptive Optics Multiphoton Retinal Imaging,” Sci. Rep. 6(1), 32223 (2016).
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S. Marcos, J. S. Werner, S. A. Burns, W. H. Merigan, P. Artal, D. A. Atchison, K. M. Hampson, R. Legras, L. Lundstrom, G. Yoon, J. Carroll, S. S. Choi, N. Doble, A. M. Dubis, A. Dubra, A. Elsner, R. Jonnal, D. T. Miller, M. Paques, H. E. Smithson, L. K. Young, Y. Zhang, M. Campbell, J. Hunter, A. Metha, G. Palczewska, J. Schallek, and L. C. Sincich, “Vision science and adaptive optics, the state of the field,” Vision Res. 132, 3–33 (2017).
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Figures (10)

Fig. 1.
Fig. 1. Schematic of the Sensorless Adaptive Optics (SAO) Optical Coherence Tomography (OCT) and Two-Photon Excitation Fluorescence (TPEF) imaging system. The imaging system was constructed with a pellicle beam splitter (PeBS), a variable focus lens (VFL), a deformable mirror (DM), a dichroic mirror (DcM), galvanometer-scanning mirrors (GM), emission filters (EF), a photo-multiplier tube (PMT), dispersion compensation (DC), and the following lenses: L1 = 100 mm, L2 = 300 mm, L3 = 400 mm, L4 = 100 mm, L5 = 2×125 mm, L6 = 2×50 mm. The reference arm denoted as a dashed line.
Fig. 2.
Fig. 2. Optical Coherence Tomography (OCT) and Two-Photon Excited Fluorescence (TPEF) images of the mouse retina before (top row) and after (bottom row) OCT-guided Sensorless Adaptive Optics (SAO). The improvement in the OCT B-scan is shown in the left column, the improvement in the en face OCT is shown in the middle column, and the improvement in the TPEF is shown in the right column. The yellow arrows represent the imaging focal position and the line between the blue arrows represents the cross-sectional location of the OCT B-scans. Scale bars: 50 µm.
Fig. 3.
Fig. 3. (a) OCT B-scans (top row), OCTA en face (middle row), and TPEF (bottom row) with the focal plane at the Outer Plexiform Layer (OPL), Inner Plexiform Layer (IPL), and Nerve Fiber Layer (NFL). In the right column, the images of the vascular layers were composited with a MIP. The red arrows point out connecting vessels in the TPEF. (b) Cross-sectional TPEF images (left) of the inner retinal vasculature before and after Adaptive Optics (SAO) acquired with a 25-step z-stack that was interpolated to 75 image pixels. The axial intensity profile plot between the red and blue arrows of the TPEF cross-sectional images. Scale bars: 50 µm.
Fig. 4.
Fig. 4. TPEF imaging of GFP labelled microglia (B6.129P2(Cg)-Cx3cr1{tm1Litt}/J) in the mouse retina. (a) Single TPEF frame (left) and an average of 100 frames (right) at a ∼0.8 mm FOV. The red square represents a 100 µm FOV to represent the scale of the microglia. Scale bar: 100 µm. (b) TPEF images of a GFP labelled microglia cells before (left) and after (right) Sensorless Adaptive Optics (SAO). (c) TPEF image after SAO. Scale bars: 20 µm.
Fig. 5.
Fig. 5. Comparison of a GFP labelled retinal ganglion cell that was imaged using SAO TPEF (left) and using SAO SPEF with the same 200 µm FOV (middle). A SPEF image is also shown at a ∼1.3 mm FOV (right), where the red square represents the 200 µm FOV that was used for the other images. Left scale bar: 20 µm. Right scale bar: 100 µm.
Fig. 6.
Fig. 6. OCT B-scans (top row) and TPEF (middle row) imaging with the focal plane at the Nerve Fiber Layer (NFL), Inner Plexiform Layer (IPL), and Outer Plexiform Layer (OPL) of a Thy-1 YFP-16 Line (B6.Cg-Tg(Thy1-YFP)16Jrs/J) transgenic mouse. The blue arrow and yellow arrow point at fluorescently labelled cell bodies. The red arrow points at fluorescently labelled axons. In the bottom row, the OCTA en face image (magenta) was composited with the TPEF image (green). Vertical scale bar: 50 µm. Horizontal scale bars: 20 µm.
Fig. 7.
Fig. 7. (a) The SAO-OCT B-scans in linear scale (top row) and the en face OCT (bottom row) with the focal plane at the Nerve Fiber Layer (NFL), Outer Plexiform Layer (OPL), and Retinal Pigment Epithelium (RPE) in the mouse retina. The en face OCT images were extracted between the cyan arrows (NFL), yellow arrows (OPL), and green arrows (RPE). The OCT B-scans were located between the red arrows on the en face OCT image. (b) TPEF images of the RPE of the mouse retina before and after SAO. (c) An intensity line plot between the blue arrows and the red arrows on the TPEF images of the RPE mosaic. Scale bars: 50 µm.
Fig. 8.
Fig. 8. (a) TPEF images of the RPE (left), en face OCT (middle), and OCT B-scans (right). (b) TPEF images of the RPE (left), en face OCT (middle), and OCT B-scans (right) from the same mouse four days later. (c) The digital enlargement of the TPEF images on day 1 (green) and day 4 (magenta), which were combined with a MIP. Scale bars: 50 µm.
Fig. 9.
Fig. 9. TPEF from the RPE layer of the mouse retina in three different mouse strains, including a pigmented B6 mouse (C57BL/6J), an albino B6 mouse (B6(Cg)-Tyr{c-2J}/J), and a pigmented rpe65 mouse (B6(A)-Rpe65{rd12}/J). Scale bar: 100 µm.
Fig. 10.
Fig. 10. TPEF image of a pigmented rpe65 mouse (B6(A)-Rpe65{rd12}/J) with different central wavelengths, including 760 nm, 780 nm, 800 nm, and 820 nm. The red arrow highlights an RPE cell where the fluorescence near the cell membrane is reduced with longer wavelengths. Scale bar: 50 µm.

Tables (2)

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Table 1. Laser specifications used for each fluorescent sample and the calculated resolution.

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Table 2. Summary of mice that were used in this report.

Equations (1)

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S N R = 10 log max ( I ) 2 σ b 2 ,

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