Abstract

Graded refractive index lenses are inherent to advanced visual systems in animals. By understanding their formation and local optical properties, significant potential for improved ocular healthcare may be realized. We report a novel technique measuring the developing optical power of the eye lens, in a living animal, by exploiting the orthogonal imaging modality of a selective plane illumination microscope (SPIM). We have quantified the maturation of the lenticular refractive index at three different visible wavelengths using a combined imaging and ray tracing approach. We demonstrate that the method can be used with transgenic and vital dye labeling as well as with both fixed and living animals. Using a key eye lens morphogen and its inhibitor, we have measured their effects both on lens size and on refractive index. Our technique provides insights into the mechanisms involved in the development of this natural graded index micro-lens and its associated optical properties.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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Corrections

29 May 2018: A correction was made to the copyright.


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References

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  6. C. Slingsby, G. J. Wistow, and A. R. Clark, “Evolution of crystallins for a role in the vertebrate eye lens,” Protein Sci. 22(4), 367–380 (2013).
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    [Crossref] [PubMed]
  9. B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
    [Crossref] [PubMed]
  10. D. Upadhya, M. Ogata, and L. W. Reneker, “Mapk1 is required for establishing the pattern of cell proliferation and for cell survival during lens development,” Development 140(7), 1573–1582 (2013).
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  11. Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
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    [Crossref]
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  17. L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref]
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    [Crossref] [PubMed]
  26. C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, “Stages of embryonic development of the zebrafish,” Dev. Dyn.,  203(3), 253–310 (1995).
    [Crossref] [PubMed]
  27. G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, “Production of clones of homozygous diploid zebra fish (Brachydanio rerio),” Nature 291(5813), 293–296 (1981).
    [Crossref] [PubMed]
  28. S. van der Walt, S. C. Colbert, and G. Varoquaux, “The numpy array: A structure for efficient numerical computation,” Comput. Sci. Eng. 13(2), 22–30 (2011).
    [Crossref]
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  32. V. Fleisch and S. C. F. Neuhauss, “Visual behavior in zebrafish,” Zebrafish 3(2), 1–11 (2006).
    [Crossref]
  33. S. Barnes and R. A. Quinlan, “Small molecules, both dietary and endogenous, influence the onset of lens cataracts,” Exp. Eye. Res. 156, 87–94 (2016).
    [Crossref] [PubMed]

2016 (3)

Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
[Crossref] [PubMed]

M. Jarrin, L. Young, W. Wu, J. M. Girkin, and R. A. Quinlan, “In vivo, ex vivo and in vitro approaches to study intermediate filaments in the eye lens,” Methods Enzymol. 568, 581–611 (2016).
[Crossref]

S. Barnes and R. A. Quinlan, “Small molecules, both dietary and endogenous, influence the onset of lens cataracts,” Exp. Eye. Res. 156, 87–94 (2016).
[Crossref] [PubMed]

2015 (1)

J. Birkenfeld, A. de Castro, and S. Marcos, “Astigmatism of the ex vivo human lens: Surface and gradient refractive index age-dependent contributions,” Invest. Ophthalmol. Vis. Sci. 56(9), 5067–5073 (2015).
[Crossref] [PubMed]

2014 (1)

M. Bahrami, M. Hoshino, B. Pierscionek, N. Yagi, J. Regini, and K. Uesugi, “Optical properties of the lens: an explanation for the zones of discontinuity,” Exp. Eye Res. 124, 93–99 (2014).
[Crossref] [PubMed]

2013 (3)

D. Upadhya, M. Ogata, and L. W. Reneker, “Mapk1 is required for establishing the pattern of cell proliferation and for cell survival during lens development,” Development 140(7), 1573–1582 (2013).
[Crossref] [PubMed]

C. Slingsby, G. J. Wistow, and A. R. Clark, “Evolution of crystallins for a role in the vertebrate eye lens,” Protein Sci. 22(4), 367–380 (2013).
[Crossref] [PubMed]

J. Birkenfeld, A. de Castro, S. Ortiz, D. Pascual, and S. Marcos, “Contribution of the gradient refractive index and shape to the crystalline lens spherical aberration and astigmatism,” Vis. Res. 86, 4 (2013).
[Crossref] [PubMed]

2012 (2)

C. Bourgenot, C. D. Saunter, J. M. Taylor, J. M. Girkin, and G. D. Love, “3D adaptive optics in a light sheet microscope,” Opt. Express 20(12), 13252–13261 (2012).
[Crossref] [PubMed]

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

2011 (6)

L. Gunhaga, “The lens: a classical model of embryonic induction providing new insights into cell determination in early development,” Philos Trans R Soc Lond B Biol Sci. 366(1568), 1193–1203 (2011).
[Crossref] [PubMed]

F. J. Lovicu, J. W. McAvoy, and R. U. de Longh, “Understanding the role of growth factors in embryonic development: insights from the lens,” Philos Trans R Soc Lond B Biol Sci. 366(1568), 1204–1218 (2011).
[Crossref] [PubMed]

H. Zhao, P. H. Brown, M. T. Magone, and P. Schuck, “The molecular refractive function of lens γ- crystallins,” J. Mol. Biol. 411(3), 680–699 (2011).
[Crossref] [PubMed]

M. Hoshino, K. Uesugi, N. Yagi, S. Mohri, J. Regini, and B. Pierscionek, “Optical properties of in situ eye lenses measured with x-ray talbot interferometry: a novel measure of growth processes,” PLoS ONE 6(9), e25140 (2011).
[Crossref] [PubMed]

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 1–8 (2011).
[Crossref]

S. van der Walt, S. C. Colbert, and G. Varoquaux, “The numpy array: A structure for efficient numerical computation,” Comput. Sci. Eng. 13(2), 22–30 (2011).
[Crossref]

2010 (1)

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

2009 (2)

D. M. Parichy, M. R. Elizondo, M. G. Mills, T. N. Gordon, and R. E. Engeszer, “Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish,” Dev. Dyn.,  238, 2975–3015 (2009).
[Crossref] [PubMed]

T. M. Greiling and J. I. Clark, “Early lens development in the zebrafish: a three-dimensional time-lapse analysis,” Dev. Dynam. 238(9), 2254–2265 (2009).
[Crossref]

2007 (1)

Y. Verma, K. D. Rao, M. K. Suresh, H. S. Patel, and P. K. Gupta, “Measurement of gradient refractive index profile of crystalline lens of fisheye in vivo using optical coherence tomography,” Appli. Phys. B,  87, 607–610 (2007).
[Crossref]

2006 (2)

K. D. Rao, Y. Verma, H. S. Patel, and P. K. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” Curr. Sci. India 90(11), 1506–1510 (2006).

V. Fleisch and S. C. F. Neuhauss, “Visual behavior in zebrafish,” Zebrafish 3(2), 1–11 (2006).
[Crossref]

2005 (1)

L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
[Crossref] [PubMed]

2004 (2)

C. E. Jones and J. M. Pope, “Measuring optical properties of an eye lens using magnetic resonance imaging,” Magn. Reson. Imaging 22(2), 211–220 (2004).
[Crossref] [PubMed]

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

1997 (1)

S. R. J. Easter and G. N. Nicola, “The development of eye movements in the zebrafish (danio rerio),” Dev. Psychobiol. 31(4), 267–276 (1997).
[Crossref] [PubMed]

1995 (1)

C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, “Stages of embryonic development of the zebrafish,” Dev. Dyn.,  203(3), 253–310 (1995).
[Crossref] [PubMed]

1981 (2)

G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, “Production of clones of homozygous diploid zebra fish (Brachydanio rerio),” Nature 291(5813), 293–296 (1981).
[Crossref] [PubMed]

J. Piatigorsky, “Lens differentiation in vertebrates. a review of cellular and molecular features,” Differentiation 19(3), 134–153 (1981).
[Crossref] [PubMed]

Arneman, E. C.

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

Bahrami, M.

M. Bahrami, M. Hoshino, B. Pierscionek, N. Yagi, J. Regini, and K. Uesugi, “Optical properties of the lens: an explanation for the zones of discontinuity,” Exp. Eye Res. 124, 93–99 (2014).
[Crossref] [PubMed]

Ballard, W. W.

C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, “Stages of embryonic development of the zebrafish,” Dev. Dyn.,  203(3), 253–310 (1995).
[Crossref] [PubMed]

Barnes, S.

S. Barnes and R. A. Quinlan, “Small molecules, both dietary and endogenous, influence the onset of lens cataracts,” Exp. Eye. Res. 156, 87–94 (2016).
[Crossref] [PubMed]

Birkenfeld, J.

J. Birkenfeld, A. de Castro, and S. Marcos, “Astigmatism of the ex vivo human lens: Surface and gradient refractive index age-dependent contributions,” Invest. Ophthalmol. Vis. Sci. 56(9), 5067–5073 (2015).
[Crossref] [PubMed]

J. Birkenfeld, A. de Castro, S. Ortiz, D. Pascual, and S. Marcos, “Contribution of the gradient refractive index and shape to the crystalline lens spherical aberration and astigmatism,” Vis. Res. 86, 4 (2013).
[Crossref] [PubMed]

Bourgenot, C.

Brown, P. H.

H. Zhao, P. H. Brown, M. T. Magone, and P. Schuck, “The molecular refractive function of lens γ- crystallins,” J. Mol. Biol. 411(3), 680–699 (2011).
[Crossref] [PubMed]

Chaudry, B.

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 1–8 (2011).
[Crossref]

Clark, A. R.

C. Slingsby, G. J. Wistow, and A. R. Clark, “Evolution of crystallins for a role in the vertebrate eye lens,” Protein Sci. 22(4), 367–380 (2013).
[Crossref] [PubMed]

Clark, D. T.

D. T. Clark, “Visual responses in developing zebrafish,” Ph.D. thesis, University of Oregon (1981).

Clark, J. I.

T. M. Greiling and J. I. Clark, “Early lens development in the zebrafish: a three-dimensional time-lapse analysis,” Dev. Dynam. 238(9), 2254–2265 (2009).
[Crossref]

Colbert, S. C.

S. van der Walt, S. C. Colbert, and G. Varoquaux, “The numpy array: A structure for efficient numerical computation,” Comput. Sci. Eng. 13(2), 22–30 (2011).
[Crossref]

Cover, T. M.

T. M. Cover and J. A. Thomas, Elements of Information Theory (John Wiley & Sons, New York, 1991).
[Crossref]

Cvekl, A.

Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
[Crossref] [PubMed]

de Castro, A.

J. Birkenfeld, A. de Castro, and S. Marcos, “Astigmatism of the ex vivo human lens: Surface and gradient refractive index age-dependent contributions,” Invest. Ophthalmol. Vis. Sci. 56(9), 5067–5073 (2015).
[Crossref] [PubMed]

J. Birkenfeld, A. de Castro, S. Ortiz, D. Pascual, and S. Marcos, “Contribution of the gradient refractive index and shape to the crystalline lens spherical aberration and astigmatism,” Vis. Res. 86, 4 (2013).
[Crossref] [PubMed]

de Longh, R. U.

F. J. Lovicu, J. W. McAvoy, and R. U. de Longh, “Understanding the role of growth factors in embryonic development: insights from the lens,” Philos Trans R Soc Lond B Biol Sci. 366(1568), 1204–1218 (2011).
[Crossref] [PubMed]

Del Bene, F.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Dower, N.

G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, “Production of clones of homozygous diploid zebra fish (Brachydanio rerio),” Nature 291(5813), 293–296 (1981).
[Crossref] [PubMed]

Easter, S. R. J.

S. R. J. Easter and G. N. Nicola, “The development of eye movements in the zebrafish (danio rerio),” Dev. Psychobiol. 31(4), 267–276 (1997).
[Crossref] [PubMed]

Elizondo, M. R.

D. M. Parichy, M. R. Elizondo, M. G. Mills, T. N. Gordon, and R. E. Engeszer, “Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish,” Dev. Dyn.,  238, 2975–3015 (2009).
[Crossref] [PubMed]

Engeszer, R. E.

D. M. Parichy, M. R. Elizondo, M. G. Mills, T. N. Gordon, and R. E. Engeszer, “Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish,” Dev. Dyn.,  238, 2975–3015 (2009).
[Crossref] [PubMed]

Fernald, R. D.

R. D. Fernald, “The optical system of fishes,” in The Visual System of FishR. H. Douglas and M. B. A. Djamgouz, eds. (Chapman and Hall, (1990), pp. 45–61.

Fleisch, V.

V. Fleisch and S. C. F. Neuhauss, “Visual behavior in zebrafish,” Zebrafish 3(2), 1–11 (2006).
[Crossref]

Gao, C. Y

Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
[Crossref] [PubMed]

Girkin, J. M.

M. Jarrin, L. Young, W. Wu, J. M. Girkin, and R. A. Quinlan, “In vivo, ex vivo and in vitro approaches to study intermediate filaments in the eye lens,” Methods Enzymol. 568, 581–611 (2016).
[Crossref]

C. Bourgenot, C. D. Saunter, J. M. Taylor, J. M. Girkin, and G. D. Love, “3D adaptive optics in a light sheet microscope,” Opt. Express 20(12), 13252–13261 (2012).
[Crossref] [PubMed]

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 1–8 (2011).
[Crossref]

Godinho, L.

L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
[Crossref] [PubMed]

Gordon, T. N.

D. M. Parichy, M. R. Elizondo, M. G. Mills, T. N. Gordon, and R. E. Engeszer, “Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish,” Dev. Dyn.,  238, 2975–3015 (2009).
[Crossref] [PubMed]

Greiling, T. M.

T. M. Greiling and J. I. Clark, “Early lens development in the zebrafish: a three-dimensional time-lapse analysis,” Dev. Dynam. 238(9), 2254–2265 (2009).
[Crossref]

Gunhaga, L.

L. Gunhaga, “The lens: a classical model of embryonic induction providing new insights into cell determination in early development,” Philos Trans R Soc Lond B Biol Sci. 366(1568), 1193–1203 (2011).
[Crossref] [PubMed]

Gupta, P. K.

Y. Verma, K. D. Rao, M. K. Suresh, H. S. Patel, and P. K. Gupta, “Measurement of gradient refractive index profile of crystalline lens of fisheye in vivo using optical coherence tomography,” Appli. Phys. B,  87, 607–610 (2007).
[Crossref]

K. D. Rao, Y. Verma, H. S. Patel, and P. K. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” Curr. Sci. India 90(11), 1506–1510 (2006).

Hancher, A.

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

Harris, R.

Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
[Crossref] [PubMed]

Henderson, D. J.

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 1–8 (2011).
[Crossref]

Hirano, M.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

Hoshino, M.

M. Bahrami, M. Hoshino, B. Pierscionek, N. Yagi, J. Regini, and K. Uesugi, “Optical properties of the lens: an explanation for the zones of discontinuity,” Exp. Eye Res. 124, 93–99 (2014).
[Crossref] [PubMed]

M. Hoshino, K. Uesugi, N. Yagi, S. Mohri, J. Regini, and B. Pierscionek, “Optical properties of in situ eye lenses measured with x-ray talbot interferometry: a novel measure of growth processes,” PLoS ONE 6(9), e25140 (2011).
[Crossref] [PubMed]

Huisken, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Imamura, T.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

Jarrin, M.

M. Jarrin, L. Young, W. Wu, J. M. Girkin, and R. A. Quinlan, “In vivo, ex vivo and in vitro approaches to study intermediate filaments in the eye lens,” Methods Enzymol. 568, 581–611 (2016).
[Crossref]

Jones, C. E.

C. E. Jones and J. M. Pope, “Measuring optical properties of an eye lens using magnetic resonance imaging,” Magn. Reson. Imaging 22(2), 211–220 (2004).
[Crossref] [PubMed]

Kimmel, C. B.

C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, “Stages of embryonic development of the zebrafish,” Dev. Dyn.,  203(3), 253–310 (1995).
[Crossref] [PubMed]

Kimmel, S. R.

C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, “Stages of embryonic development of the zebrafish,” Dev. Dyn.,  203(3), 253–310 (1995).
[Crossref] [PubMed]

Knauber, D.

G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, “Production of clones of homozygous diploid zebra fish (Brachydanio rerio),” Nature 291(5813), 293–296 (1981).
[Crossref] [PubMed]

Kobrinski, D. A.

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

Koerber, A.

L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
[Crossref] [PubMed]

Kon, T.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

Kuroyanagi, J.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

Leach, S. D.

L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
[Crossref] [PubMed]

Liu, W.

Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
[Crossref] [PubMed]

Love, G. D.

C. Bourgenot, C. D. Saunter, J. M. Taylor, J. M. Girkin, and G. D. Love, “3D adaptive optics in a light sheet microscope,” Opt. Express 20(12), 13252–13261 (2012).
[Crossref] [PubMed]

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 1–8 (2011).
[Crossref]

Lovicu, F. J.

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

F. J. Lovicu, J. W. McAvoy, and R. U. de Longh, “Understanding the role of growth factors in embryonic development: insights from the lens,” Philos Trans R Soc Lond B Biol Sci. 366(1568), 1204–1218 (2011).
[Crossref] [PubMed]

Madakashira, B. P.

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

Magone, M. T.

H. Zhao, P. H. Brown, M. T. Magone, and P. Schuck, “The molecular refractive function of lens γ- crystallins,” J. Mol. Biol. 411(3), 680–699 (2011).
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Marcos, S.

J. Birkenfeld, A. de Castro, and S. Marcos, “Astigmatism of the ex vivo human lens: Surface and gradient refractive index age-dependent contributions,” Invest. Ophthalmol. Vis. Sci. 56(9), 5067–5073 (2015).
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J. Birkenfeld, A. de Castro, S. Ortiz, D. Pascual, and S. Marcos, “Contribution of the gradient refractive index and shape to the crystalline lens spherical aberration and astigmatism,” Vis. Res. 86, 4 (2013).
[Crossref] [PubMed]

McAvoy, J. W.

F. J. Lovicu, J. W. McAvoy, and R. U. de Longh, “Understanding the role of growth factors in embryonic development: insights from the lens,” Philos Trans R Soc Lond B Biol Sci. 366(1568), 1204–1218 (2011).
[Crossref] [PubMed]

MCGreal, R.

Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
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D. M. Parichy, M. R. Elizondo, M. G. Mills, T. N. Gordon, and R. E. Engeszer, “Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish,” Dev. Dyn.,  238, 2975–3015 (2009).
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K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

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M. Hoshino, K. Uesugi, N. Yagi, S. Mohri, J. Regini, and B. Pierscionek, “Optical properties of in situ eye lenses measured with x-ray talbot interferometry: a novel measure of growth processes,” PLoS ONE 6(9), e25140 (2011).
[Crossref] [PubMed]

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L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
[Crossref] [PubMed]

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Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
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V. Fleisch and S. C. F. Neuhauss, “Visual behavior in zebrafish,” Zebrafish 3(2), 1–11 (2006).
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S. R. J. Easter and G. N. Nicola, “The development of eye movements in the zebrafish (danio rerio),” Dev. Psychobiol. 31(4), 267–276 (1997).
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K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
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Nishimura, Y.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
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K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
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D. Upadhya, M. Ogata, and L. W. Reneker, “Mapk1 is required for establishing the pattern of cell proliferation and for cell survival during lens development,” Development 140(7), 1573–1582 (2013).
[Crossref] [PubMed]

Oka, T.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

Ortiz, S.

J. Birkenfeld, A. de Castro, S. Ortiz, D. Pascual, and S. Marcos, “Contribution of the gradient refractive index and shape to the crystalline lens spherical aberration and astigmatism,” Vis. Res. 86, 4 (2013).
[Crossref] [PubMed]

Parichy, D. M.

D. M. Parichy, M. R. Elizondo, M. G. Mills, T. N. Gordon, and R. E. Engeszer, “Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish,” Dev. Dyn.,  238, 2975–3015 (2009).
[Crossref] [PubMed]

Park, S. W.

L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
[Crossref] [PubMed]

Pascual, D.

J. Birkenfeld, A. de Castro, S. Ortiz, D. Pascual, and S. Marcos, “Contribution of the gradient refractive index and shape to the crystalline lens spherical aberration and astigmatism,” Vis. Res. 86, 4 (2013).
[Crossref] [PubMed]

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Y. Verma, K. D. Rao, M. K. Suresh, H. S. Patel, and P. K. Gupta, “Measurement of gradient refractive index profile of crystalline lens of fisheye in vivo using optical coherence tomography,” Appli. Phys. B,  87, 607–610 (2007).
[Crossref]

K. D. Rao, Y. Verma, H. S. Patel, and P. K. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” Curr. Sci. India 90(11), 1506–1510 (2006).

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M. Bahrami, M. Hoshino, B. Pierscionek, N. Yagi, J. Regini, and K. Uesugi, “Optical properties of the lens: an explanation for the zones of discontinuity,” Exp. Eye Res. 124, 93–99 (2014).
[Crossref] [PubMed]

M. Hoshino, K. Uesugi, N. Yagi, S. Mohri, J. Regini, and B. Pierscionek, “Optical properties of in situ eye lenses measured with x-ray talbot interferometry: a novel measure of growth processes,” PLoS ONE 6(9), e25140 (2011).
[Crossref] [PubMed]

Pope, J. M.

C. E. Jones and J. M. Pope, “Measuring optical properties of an eye lens using magnetic resonance imaging,” Magn. Reson. Imaging 22(2), 211–220 (2004).
[Crossref] [PubMed]

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S. Barnes and R. A. Quinlan, “Small molecules, both dietary and endogenous, influence the onset of lens cataracts,” Exp. Eye. Res. 156, 87–94 (2016).
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M. Jarrin, L. Young, W. Wu, J. M. Girkin, and R. A. Quinlan, “In vivo, ex vivo and in vitro approaches to study intermediate filaments in the eye lens,” Methods Enzymol. 568, 581–611 (2016).
[Crossref]

Rao, K. D.

Y. Verma, K. D. Rao, M. K. Suresh, H. S. Patel, and P. K. Gupta, “Measurement of gradient refractive index profile of crystalline lens of fisheye in vivo using optical coherence tomography,” Appli. Phys. B,  87, 607–610 (2007).
[Crossref]

K. D. Rao, Y. Verma, H. S. Patel, and P. K. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” Curr. Sci. India 90(11), 1506–1510 (2006).

Regini, J.

M. Bahrami, M. Hoshino, B. Pierscionek, N. Yagi, J. Regini, and K. Uesugi, “Optical properties of the lens: an explanation for the zones of discontinuity,” Exp. Eye Res. 124, 93–99 (2014).
[Crossref] [PubMed]

M. Hoshino, K. Uesugi, N. Yagi, S. Mohri, J. Regini, and B. Pierscionek, “Optical properties of in situ eye lenses measured with x-ray talbot interferometry: a novel measure of growth processes,” PLoS ONE 6(9), e25140 (2011).
[Crossref] [PubMed]

Reneker, L. W.

Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
[Crossref] [PubMed]

D. Upadhya, M. Ogata, and L. W. Reneker, “Mapk1 is required for establishing the pattern of cell proliferation and for cell survival during lens development,” Development 140(7), 1573–1582 (2013).
[Crossref] [PubMed]

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

Robinson, M.

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

Saunter, C. D.

C. Bourgenot, C. D. Saunter, J. M. Taylor, J. M. Girkin, and G. D. Love, “3D adaptive optics in a light sheet microscope,” Opt. Express 20(12), 13252–13261 (2012).
[Crossref] [PubMed]

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 1–8 (2011).
[Crossref]

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C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, “Stages of embryonic development of the zebrafish,” Dev. Dyn.,  203(3), 253–310 (1995).
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L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
[Crossref] [PubMed]

Schuck, P.

H. Zhao, P. H. Brown, M. T. Magone, and P. Schuck, “The molecular refractive function of lens γ- crystallins,” J. Mol. Biol. 411(3), 680–699 (2011).
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K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

Shin, H.

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

Shintou, T.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
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Stelzer, E. H. K.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Streisinger, G.

G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, “Production of clones of homozygous diploid zebra fish (Brachydanio rerio),” Nature 291(5813), 293–296 (1981).
[Crossref] [PubMed]

Suresh, M. K.

Y. Verma, K. D. Rao, M. K. Suresh, H. S. Patel, and P. K. Gupta, “Measurement of gradient refractive index profile of crystalline lens of fisheye in vivo using optical coherence tomography,” Appli. Phys. B,  87, 607–610 (2007).
[Crossref]

Swoger, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Tanaka, T.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

Taylor, J. M.

C. Bourgenot, C. D. Saunter, J. M. Taylor, J. M. Girkin, and G. D. Love, “3D adaptive optics in a light sheet microscope,” Opt. Express 20(12), 13252–13261 (2012).
[Crossref] [PubMed]

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 1–8 (2011).
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M. Bahrami, M. Hoshino, B. Pierscionek, N. Yagi, J. Regini, and K. Uesugi, “Optical properties of the lens: an explanation for the zones of discontinuity,” Exp. Eye Res. 124, 93–99 (2014).
[Crossref] [PubMed]

M. Hoshino, K. Uesugi, N. Yagi, S. Mohri, J. Regini, and B. Pierscionek, “Optical properties of in situ eye lenses measured with x-ray talbot interferometry: a novel measure of growth processes,” PLoS ONE 6(9), e25140 (2011).
[Crossref] [PubMed]

Ullmann, B.

C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, “Stages of embryonic development of the zebrafish,” Dev. Dyn.,  203(3), 253–310 (1995).
[Crossref] [PubMed]

Umemoto, N.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

Upadhya, D.

D. Upadhya, M. Ogata, and L. W. Reneker, “Mapk1 is required for establishing the pattern of cell proliferation and for cell survival during lens development,” Development 140(7), 1573–1582 (2013).
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Y. Verma, K. D. Rao, M. K. Suresh, H. S. Patel, and P. K. Gupta, “Measurement of gradient refractive index profile of crystalline lens of fisheye in vivo using optical coherence tomography,” Appli. Phys. B,  87, 607–610 (2007).
[Crossref]

K. D. Rao, Y. Verma, H. S. Patel, and P. K. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” Curr. Sci. India 90(11), 1506–1510 (2006).

Wagner, B. D.

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

Walker, C.

G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, “Production of clones of homozygous diploid zebra fish (Brachydanio rerio),” Nature 291(5813), 293–296 (1981).
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Wang, F.

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

Wang, Z.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
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Watanabe, K.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
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Weaver, W.

C. E. Shannon and W. Weaver, The Mathematical Theory of Communication (University of Illinois Press, 1949).

Williams, P. R.

L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
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Wistow, G. J.

C. Slingsby, G. J. Wistow, and A. R. Clark, “Evolution of crystallins for a role in the vertebrate eye lens,” Protein Sci. 22(4), 367–380 (2013).
[Crossref] [PubMed]

Wittbrodt, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Wong, R. O.

L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
[Crossref] [PubMed]

Wu, W.

M. Jarrin, L. Young, W. Wu, J. M. Girkin, and R. A. Quinlan, “In vivo, ex vivo and in vitro approaches to study intermediate filaments in the eye lens,” Methods Enzymol. 568, 581–611 (2016).
[Crossref]

Xie, Q.

Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
[Crossref] [PubMed]

Yagi, N.

M. Bahrami, M. Hoshino, B. Pierscionek, N. Yagi, J. Regini, and K. Uesugi, “Optical properties of the lens: an explanation for the zones of discontinuity,” Exp. Eye Res. 124, 93–99 (2014).
[Crossref] [PubMed]

M. Hoshino, K. Uesugi, N. Yagi, S. Mohri, J. Regini, and B. Pierscionek, “Optical properties of in situ eye lenses measured with x-ray talbot interferometry: a novel measure of growth processes,” PLoS ONE 6(9), e25140 (2011).
[Crossref] [PubMed]

Young, L.

M. Jarrin, L. Young, W. Wu, J. M. Girkin, and R. A. Quinlan, “In vivo, ex vivo and in vitro approaches to study intermediate filaments in the eye lens,” Methods Enzymol. 568, 581–611 (2016).
[Crossref]

Zhang, Z.

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

Zhao, H.

H. Zhao, P. H. Brown, M. T. Magone, and P. Schuck, “The molecular refractive function of lens γ- crystallins,” J. Mol. Biol. 411(3), 680–699 (2011).
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Appli. Phys. B (1)

Y. Verma, K. D. Rao, M. K. Suresh, H. S. Patel, and P. K. Gupta, “Measurement of gradient refractive index profile of crystalline lens of fisheye in vivo using optical coherence tomography,” Appli. Phys. B,  87, 607–610 (2007).
[Crossref]

BMC Neurosci. (1)

K. Watanabe, Y. Nishimura, T. Oka, T. Nomoto, T. Kon, T. Shintou, M. Hirano, Y. Shimada, N. Umemoto, J. Kuroyanagi, Z. Wang, Z. Zhang, N. Nishimura, T. Miyazaki, T. Imamura, and T. Tanaka, “In vivo imaging of zebrafish retinal cells using fluorescent coumarin derivatives,” BMC Neurosci.,  11(116), 1–12 (2010).
[Crossref]

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Curr. Sci. India (1)

K. D. Rao, Y. Verma, H. S. Patel, and P. K. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” Curr. Sci. India 90(11), 1506–1510 (2006).

Dev. Dyn. (2)

D. M. Parichy, M. R. Elizondo, M. G. Mills, T. N. Gordon, and R. E. Engeszer, “Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish,” Dev. Dyn.,  238, 2975–3015 (2009).
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C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, “Stages of embryonic development of the zebrafish,” Dev. Dyn.,  203(3), 253–310 (1995).
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Dev. Dynam. (1)

T. M. Greiling and J. I. Clark, “Early lens development in the zebrafish: a three-dimensional time-lapse analysis,” Dev. Dynam. 238(9), 2254–2265 (2009).
[Crossref]

Dev. Psychobiol. (1)

S. R. J. Easter and G. N. Nicola, “The development of eye movements in the zebrafish (danio rerio),” Dev. Psychobiol. 31(4), 267–276 (1997).
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Development (3)

B. P. Madakashira, D. A. Kobrinski, A. Hancher, E. C. Arneman, B. D. Wagner, F. Wang, H. Shin, F. J. Lovicu, L. W. Reneker, and M. Robinson, “Frs2α enhances fibroblast growth factor-mediated survival and differentiation in lens development,” Development 139(24), 4601–4612 (2012).
[Crossref] [PubMed]

D. Upadhya, M. Ogata, and L. W. Reneker, “Mapk1 is required for establishing the pattern of cell proliferation and for cell survival during lens development,” Development 140(7), 1573–1582 (2013).
[Crossref] [PubMed]

L. Godinho, J. S. Mumm, P. R. Williams, E. H. Schroeter, A. Koerber, S. W. Park, S. D. Leach, and R. O. Wong, “Targeting of amacrine cell neurites to appopriate synaptic laminae in the developing zebrafish retina,” Development 132(22), 5069–5079 (2005).
[Crossref] [PubMed]

Differentiation (1)

J. Piatigorsky, “Lens differentiation in vertebrates. a review of cellular and molecular features,” Differentiation 19(3), 134–153 (1981).
[Crossref] [PubMed]

Exp. Eye Res. (1)

M. Bahrami, M. Hoshino, B. Pierscionek, N. Yagi, J. Regini, and K. Uesugi, “Optical properties of the lens: an explanation for the zones of discontinuity,” Exp. Eye Res. 124, 93–99 (2014).
[Crossref] [PubMed]

Exp. Eye. Res. (1)

S. Barnes and R. A. Quinlan, “Small molecules, both dietary and endogenous, influence the onset of lens cataracts,” Exp. Eye. Res. 156, 87–94 (2016).
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Invest. Ophthalmol. Vis. Sci. (1)

J. Birkenfeld, A. de Castro, and S. Marcos, “Astigmatism of the ex vivo human lens: Surface and gradient refractive index age-dependent contributions,” Invest. Ophthalmol. Vis. Sci. 56(9), 5067–5073 (2015).
[Crossref] [PubMed]

J. Biol. Chem. (1)

Q. Xie, R. MCGreal, R. Harris, C. Y Gao, W. Liu, L. W. Reneker, L. S Musil, and A. Cvekl, “Regulation of c-maf and α A-crystallin in ocular lens by fibroblast growth factor signalling,” J. Biol. Chem. 291, 3947–3958 (2016).
[Crossref] [PubMed]

J. Biomed. Opt. (1)

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 1–8 (2011).
[Crossref]

J. Mol. Biol. (1)

H. Zhao, P. H. Brown, M. T. Magone, and P. Schuck, “The molecular refractive function of lens γ- crystallins,” J. Mol. Biol. 411(3), 680–699 (2011).
[Crossref] [PubMed]

Magn. Reson. Imaging (1)

C. E. Jones and J. M. Pope, “Measuring optical properties of an eye lens using magnetic resonance imaging,” Magn. Reson. Imaging 22(2), 211–220 (2004).
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Methods Enzymol. (1)

M. Jarrin, L. Young, W. Wu, J. M. Girkin, and R. A. Quinlan, “In vivo, ex vivo and in vitro approaches to study intermediate filaments in the eye lens,” Methods Enzymol. 568, 581–611 (2016).
[Crossref]

Nature (1)

G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, “Production of clones of homozygous diploid zebra fish (Brachydanio rerio),” Nature 291(5813), 293–296 (1981).
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Opt. Express (1)

Philos Trans R Soc Lond B Biol Sci. (2)

L. Gunhaga, “The lens: a classical model of embryonic induction providing new insights into cell determination in early development,” Philos Trans R Soc Lond B Biol Sci. 366(1568), 1193–1203 (2011).
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F. J. Lovicu, J. W. McAvoy, and R. U. de Longh, “Understanding the role of growth factors in embryonic development: insights from the lens,” Philos Trans R Soc Lond B Biol Sci. 366(1568), 1204–1218 (2011).
[Crossref] [PubMed]

PLoS ONE (1)

M. Hoshino, K. Uesugi, N. Yagi, S. Mohri, J. Regini, and B. Pierscionek, “Optical properties of in situ eye lenses measured with x-ray talbot interferometry: a novel measure of growth processes,” PLoS ONE 6(9), e25140 (2011).
[Crossref] [PubMed]

Protein Sci. (1)

C. Slingsby, G. J. Wistow, and A. R. Clark, “Evolution of crystallins for a role in the vertebrate eye lens,” Protein Sci. 22(4), 367–380 (2013).
[Crossref] [PubMed]

Science (1)

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Vis. Res. (1)

J. Birkenfeld, A. de Castro, S. Ortiz, D. Pascual, and S. Marcos, “Contribution of the gradient refractive index and shape to the crystalline lens spherical aberration and astigmatism,” Vis. Res. 86, 4 (2013).
[Crossref] [PubMed]

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V. Fleisch and S. C. F. Neuhauss, “Visual behavior in zebrafish,” Zebrafish 3(2), 1–11 (2006).
[Crossref]

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C. E. Shannon and W. Weaver, The Mathematical Theory of Communication (University of Illinois Press, 1949).

T. M. Cover and J. A. Thomas, Elements of Information Theory (John Wiley & Sons, New York, 1991).
[Crossref]

D. T. Clark, “Visual responses in developing zebrafish,” Ph.D. thesis, University of Oregon (1981).

R. D. Fernald, “The optical system of fishes,” in The Visual System of FishR. H. Douglas and M. B. A. Djamgouz, eds. (Chapman and Hall, (1990), pp. 45–61.

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Figures (5)

Fig. 1
Fig. 1 Alignment of the zebrafish embryo within the SPIM system. (a) The axes of the zebrafish embryo showing the left-right axis, which we align parallel to the light sheet (purple shading), and the anteroposterior axis, about which we rotate the embryo. The axes of the light sheet are also shown indicating direction of propagation along x and the optical axis of the imaging objective (blue shading), z. (b) A rotated version of (a) showing the propagation of the light sheet through the eye of the zebrafish embryo and its subsequent focusing. The light sheet is refracted by the eye lens as indicated. This is observed via the fluorescence signal in the surrounding tissue. Additional refraction by the second (right-most) eye lens is not considered and our analysis does not include light that has passed through it. (c) The same as (b), but indicating the GRIN measurement procedure, where a pencil beam is selected using a slit aperture.
Fig. 2
Fig. 2 The method used to measure the focal length of the zebrafish eye lens, using a 2 dpf embryo as an example. (a) The fluorescence excitation map derived by rasterizing a geometric ray trace, which modeled the lens as a disk of uniform RI, and then adding Gaussian blur to minimize aliasing artifacts in the bitmap image generation. (b) The density map of fluorophors in the sample simulated by a radial projection of the intensity profile derived from the fluorescence image. (c) the multiplication of (a) and (b) then the addition of (b) multiplied by a background value to simulate out-of-plane and scattered fluorescence. (d) The original fluorescence image that was compared to the simulated image (c) and the difference minimized using the Nelder-Mead simplex algorithm to find the optimal RI to use in the ray trace. (e) An overlay of the simulated image (in green), computed using the optimal RI in the steps shown in (a) – (c), which are the simulated images, on the original fluorescence image. The area of the simulated image has been extended to the focal point, although in practice the area containing the second eye is not used. In this immature lens the focal point is far beyond the corresponding retina, and in this case, outside of the embryo.
Fig. 3
Fig. 3 Zebrafish lens development from day 2 to 4 dpf. (a) The increase in radius of the zebrafish eye lens for three final concentrations of Coumarin 6 (5.7, 17.1 and 34.2) μM and a control condition (no Coumarin 6). (b) The effective RI of the zebrafish lens, which develops most rapidly between 3 and 4 dpf, for the same concentrations of Coumarin 6. (c) The RI of the zebrafish lens measured at three excitation wavelengths using both Coumarin 6 (17.1 μM) and BoDIPY TMRE (100 μM) as fluorescent markers. Chromatic aberration is not detectable in the lenses of these embryos. (d) The ratio of the effective focal length, for three concentrations of Coumarin 6 and control, of the zebrafish lens to the distance between the center of the eye lens and the photoreceptor layer in the retina. This ratio should equal one if the eye were focusing appropriately on to the retina. Error bars represent the standard error of the mean from six measurements and the labels in panels (a), (b) and (d) refer to the concentration of Coumarin 6 used to measure the focal length with 405 nm excitation light. We note that different clutches were used in experiment (i) (panels (a), (b) and (d)) and experiment (ii) (panel (c). Variability arises from small developmental differences within the same clutch [25–27], in particular in panel (b) the increased RI with 17.1 μm Coumarin 6 at 4 dpf is largely driven by a single outlier (RI=1.62).
Fig. 4
Fig. 4 FGF2 mediated effects upon zebrafish lens development. Zebrafish were exposed to either increased FGF2 concentrations or to a small molecule inhibitor of FGF-signaling, SU5402. Animals from the same clutch were used as controls. (a) The change in the radius of the zebrafish lens and (b) the change diameter of the zebrafish eye, measured across its widest part. Both of these measurements show a significant reduction in the dimensions of the eye when the FGF pathway is inhibited and a significant increase in these dimensions when this pathway is further activated. (c) The effective RI of the zebrafish lens and (d) the ratio of the effective focal length of the zebrafish lens to the distance between the center of the lens and the photoreceptor layer in the retina. SU5402 decreased the RI, whilst FGF2 increased the RI relative to controls. A minimum of five independent measurements were made for each data point. Error bars represent the standard error of the mean.
Fig. 5
Fig. 5 Measurement of the GRIN of the zebrafish eye lens. (a) An example (a 2 dpf zebrafish) of the average of six images, each of which was recorded for a different position of the aperture placed approximately 12 μm apart. This was used for the image comparison and parameter optimization. (b) The RI profile measured for a 2, 3, and 4 dpf zebrafish fixed in paraformaldehyde. The coloured bands and the error bars indicate the 95 % confidence limits on the measurement of the RI profile from a single image (i.e. a single zebrafish eye), determined by repeating the optimization algorithm ten times. (c) The development of the RI in the core of the eye lens and of (d) the coefficients A1−3 with age.

Equations (2)

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f = n R 2 ( n 1 ) ,
n ( r ) = i = 0 3 A i r 2 i ,

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