Abstract

We demonstrate a simple method for mapping optical aberrations with 3D resolution within thick samples. The method relies on the local measurement of the variation in image quality with externally applied aberrations. We discuss the accuracy of the method as a function of the signal strength and of the aberration amplitude and we derive the achievable resolution for the resulting measurements. We then report on measured 3D aberration maps in human skin biopsies and mouse brain slices. From these data, we analyse the consequences of tissue structure and refractive index distribution on aberrations and imaging depth in normal and cleared tissue samples. The aberration maps allow the estimation of the typical aplanetism region size over which aberrations can be uniformly corrected. This method and data pave the way towards efficient correction strategies for tissue imaging applications.

© 2012 OSA

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  1. M. J. Booth, M. A. A. Neil, R. Juškaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Nat. Acad. Sci.99, 5788–5792 (2002).
    [CrossRef] [PubMed]
  2. P. N. Marsh, D. Burns, and J. M. Girkin, “Practical implementation of adaptive optics in multiphoton microscopy,” Opt. Express11, 1123–1130 (2003).
    [CrossRef] [PubMed]
  3. M. Rueckel, J. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Nat. Acad. Sci.103, 17137–17142 (2006).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  6. R. Aviles-Espinosa, J. Andilla, R. Porcar-Guezenec, O. E. Olarte, M. Nieto, X. Levecq, D. Artigas, and P. Loza-Alvarez, “Measurement and correction of in vivo sample aberrations employing a nonlinear guide-star in two-photon excited fluorescence microscopy,” Biomed. Opt. Express2, 3135–3149 (2011).
    [CrossRef] [PubMed]
  7. A. Facomprez, E. Beaurepaire, and D. Débarre, “Accuracy of correction in modal sensorless adaptive optics”, Opt. Express20, 2598–2612 (2012).
    [CrossRef] [PubMed]
  8. N. Olivier, D. Débarre, and E. Beaurepaire, “Dynamic aberration correction for multiharmonic microscopy,” Opt. Lett.34, 3145–3147 (2009).
    [CrossRef] [PubMed]
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    [CrossRef]
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    [CrossRef]
  11. K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt.8, 432–439 (2003).
    [CrossRef] [PubMed]
  12. D. Débarre, E. J. Botcherby, M. J. Booth, and T. Wilson, “Adaptive optics for structured illumination microscopy,” Opt. Express16, 9290–9305 (2008).
    [CrossRef] [PubMed]
  13. M. Kaatz, A. Sturm, P. Elsner, K. König, R. Buckle, and M. J. Koehler, “Depth-resolved measurement of the dermal matrix composition by multiphoton laser tomography,” Skin Res. Technol.16, 131–136 (2010).
    [CrossRef] [PubMed]
  14. J. Livet, T. A. Weissman, H. Kang, R. W. Draft, J. Lu, R. A. Bennis, J. R. Sanes, and J. W. Lichtman, “Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system,” Nature450, 56–62 (2007).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  17. Z. Kam, B. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Computational adaptive optics for live three-dimensional biological imaging,” Proc. Nat. Acad. Sci.98, 3790–3795 (2001).
    [CrossRef] [PubMed]
  18. N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Nat. Acad. Sci.109, 22–27 (2012).
    [CrossRef]
  19. H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14, 1481–1488 (2011).
    [CrossRef] [PubMed]
  20. M. Hart, “Recent advances in astronomical adaptive optics,” Appl. Opt.49, D17–D29 (2010).
    [CrossRef] [PubMed]
  21. N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
    [CrossRef]

2012

A. Facomprez, E. Beaurepaire, and D. Débarre, “Accuracy of correction in modal sensorless adaptive optics”, Opt. Express20, 2598–2612 (2012).
[CrossRef] [PubMed]

D. Débarre, A. Facomprez, and E. Beaurepaire, “Assessing correction accuracy in image-based adaptive optics,” Proc. SPIE8253, 82530F (2012).
[CrossRef]

H. Ait El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A. -M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt.17, 026009 (2012).
[CrossRef]

J. Sun, S. J. Lee, L. Wu, M. Sarntinoranont, and H. Xie, “Refractive index measurement of acute rat brain tissue slices using optical coherence tomography,” Opt. Express20, 1084–1095 (2012).
[CrossRef] [PubMed]

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Nat. Acad. Sci.109, 22–27 (2012).
[CrossRef]

2011

2010

M. Kaatz, A. Sturm, P. Elsner, K. König, R. Buckle, and M. J. Koehler, “Depth-resolved measurement of the dermal matrix composition by multiphoton laser tomography,” Skin Res. Technol.16, 131–136 (2010).
[CrossRef] [PubMed]

M. Hart, “Recent advances in astronomical adaptive optics,” Appl. Opt.49, D17–D29 (2010).
[CrossRef] [PubMed]

N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
[CrossRef]

2009

2008

2007

J. Livet, T. A. Weissman, H. Kang, R. W. Draft, J. Lu, R. A. Bennis, J. R. Sanes, and J. W. Lichtman, “Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system,” Nature450, 56–62 (2007).
[CrossRef] [PubMed]

2006

M. Rueckel, J. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Nat. Acad. Sci.103, 17137–17142 (2006).
[CrossRef] [PubMed]

2003

P. N. Marsh, D. Burns, and J. M. Girkin, “Practical implementation of adaptive optics in multiphoton microscopy,” Opt. Express11, 1123–1130 (2003).
[CrossRef] [PubMed]

K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt.8, 432–439 (2003).
[CrossRef] [PubMed]

2002

M. J. Booth, M. A. A. Neil, R. Juškaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Nat. Acad. Sci.99, 5788–5792 (2002).
[CrossRef] [PubMed]

2001

Z. Kam, B. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Computational adaptive optics for live three-dimensional biological imaging,” Proc. Nat. Acad. Sci.98, 3790–3795 (2001).
[CrossRef] [PubMed]

Agard, D. A.

Z. Kam, B. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Computational adaptive optics for live three-dimensional biological imaging,” Proc. Nat. Acad. Sci.98, 3790–3795 (2001).
[CrossRef] [PubMed]

Ait El Madani, H.

H. Ait El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A. -M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt.17, 026009 (2012).
[CrossRef]

Andilla, J.

Ando, R.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14, 1481–1488 (2011).
[CrossRef] [PubMed]

Artigas, D.

Aviles-Espinosa, R.

Bagot, M.

H. Ait El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A. -M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt.17, 026009 (2012).
[CrossRef]

Beaurepaire, E.

D. Débarre, A. Facomprez, and E. Beaurepaire, “Assessing correction accuracy in image-based adaptive optics,” Proc. SPIE8253, 82530F (2012).
[CrossRef]

A. Facomprez, E. Beaurepaire, and D. Débarre, “Accuracy of correction in modal sensorless adaptive optics”, Opt. Express20, 2598–2612 (2012).
[CrossRef] [PubMed]

N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
[CrossRef]

N. Olivier, D. Débarre, and E. Beaurepaire, “Dynamic aberration correction for multiharmonic microscopy,” Opt. Lett.34, 3145–3147 (2009).
[CrossRef] [PubMed]

Ben Arous, J.

Bennis, R. A.

J. Livet, T. A. Weissman, H. Kang, R. W. Draft, J. Lu, R. A. Bennis, J. R. Sanes, and J. W. Lichtman, “Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system,” Nature450, 56–62 (2007).
[CrossRef] [PubMed]

Bensussan, A.

H. Ait El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A. -M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt.17, 026009 (2012).
[CrossRef]

Betzig, E.

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Nat. Acad. Sci.109, 22–27 (2012).
[CrossRef]

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods7, 141–147 (2009).
[CrossRef] [PubMed]

Binding, J.

Boccara, C.

Booth, M. J.

Botcherby, E. J.

Bourdieu, L.

Bourgine, P.

N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
[CrossRef]

Buckle, R.

M. Kaatz, A. Sturm, P. Elsner, K. König, R. Buckle, and M. J. Koehler, “Depth-resolved measurement of the dermal matrix composition by multiphoton laser tomography,” Skin Res. Technol.16, 131–136 (2010).
[CrossRef] [PubMed]

Burns, D.

Colonna, A.

H. Ait El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A. -M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt.17, 026009 (2012).
[CrossRef]

Débarre, D.

Denk, W.

M. Rueckel, J. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Nat. Acad. Sci.103, 17137–17142 (2006).
[CrossRef] [PubMed]

Draft, R. W.

J. Livet, T. A. Weissman, H. Kang, R. W. Draft, J. Lu, R. A. Bennis, J. R. Sanes, and J. W. Lichtman, “Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system,” Nature450, 56–62 (2007).
[CrossRef] [PubMed]

Duloquin, L.

N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
[CrossRef]

Dupuy, A.

H. Ait El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A. -M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt.17, 026009 (2012).
[CrossRef]

Elsner, P.

M. Kaatz, A. Sturm, P. Elsner, K. König, R. Buckle, and M. J. Koehler, “Depth-resolved measurement of the dermal matrix composition by multiphoton laser tomography,” Skin Res. Technol.16, 131–136 (2010).
[CrossRef] [PubMed]

Facomprez, A.

A. Facomprez, E. Beaurepaire, and D. Débarre, “Accuracy of correction in modal sensorless adaptive optics”, Opt. Express20, 2598–2612 (2012).
[CrossRef] [PubMed]

D. Débarre, A. Facomprez, and E. Beaurepaire, “Assessing correction accuracy in image-based adaptive optics,” Proc. SPIE8253, 82530F (2012).
[CrossRef]

Faure, E.

N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
[CrossRef]

Fukami, K.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14, 1481–1488 (2011).
[CrossRef] [PubMed]

Gigan, S.

Girkin, J. M.

Gustafsson, M. G. L.

Z. Kam, B. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Computational adaptive optics for live three-dimensional biological imaging,” Proc. Nat. Acad. Sci.98, 3790–3795 (2001).
[CrossRef] [PubMed]

Hama, H.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14, 1481–1488 (2011).
[CrossRef] [PubMed]

Hanser, B.

Z. Kam, B. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Computational adaptive optics for live three-dimensional biological imaging,” Proc. Nat. Acad. Sci.98, 3790–3795 (2001).
[CrossRef] [PubMed]

Hart, M.

Ji, N.

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Nat. Acad. Sci.109, 22–27 (2012).
[CrossRef]

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods7, 141–147 (2009).
[CrossRef] [PubMed]

Juškaitis, R.

M. J. Booth, M. A. A. Neil, R. Juškaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Nat. Acad. Sci.99, 5788–5792 (2002).
[CrossRef] [PubMed]

Kaatz, M.

M. Kaatz, A. Sturm, P. Elsner, K. König, R. Buckle, and M. J. Koehler, “Depth-resolved measurement of the dermal matrix composition by multiphoton laser tomography,” Skin Res. Technol.16, 131–136 (2010).
[CrossRef] [PubMed]

Kam, Z.

Z. Kam, B. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Computational adaptive optics for live three-dimensional biological imaging,” Proc. Nat. Acad. Sci.98, 3790–3795 (2001).
[CrossRef] [PubMed]

Kang, H.

J. Livet, T. A. Weissman, H. Kang, R. W. Draft, J. Lu, R. A. Bennis, J. R. Sanes, and J. W. Lichtman, “Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system,” Nature450, 56–62 (2007).
[CrossRef] [PubMed]

Kawano, H.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14, 1481–1488 (2011).
[CrossRef] [PubMed]

Koehler, M. J.

M. Kaatz, A. Sturm, P. Elsner, K. König, R. Buckle, and M. J. Koehler, “Depth-resolved measurement of the dermal matrix composition by multiphoton laser tomography,” Skin Res. Technol.16, 131–136 (2010).
[CrossRef] [PubMed]

König, K.

M. Kaatz, A. Sturm, P. Elsner, K. König, R. Buckle, and M. J. Koehler, “Depth-resolved measurement of the dermal matrix composition by multiphoton laser tomography,” Skin Res. Technol.16, 131–136 (2010).
[CrossRef] [PubMed]

K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt.8, 432–439 (2003).
[CrossRef] [PubMed]

Kurokawa, H.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14, 1481–1488 (2011).
[CrossRef] [PubMed]

Lee, S. J.

Léger, J. -F.

Levecq, X.

Lichtman, J. W.

J. Livet, T. A. Weissman, H. Kang, R. W. Draft, J. Lu, R. A. Bennis, J. R. Sanes, and J. W. Lichtman, “Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system,” Nature450, 56–62 (2007).
[CrossRef] [PubMed]

Livet, J.

J. Livet, T. A. Weissman, H. Kang, R. W. Draft, J. Lu, R. A. Bennis, J. R. Sanes, and J. W. Lichtman, “Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system,” Nature450, 56–62 (2007).
[CrossRef] [PubMed]

Loza-Alvarez, P.

Lu, J.

J. Livet, T. A. Weissman, H. Kang, R. W. Draft, J. Lu, R. A. Bennis, J. R. Sanes, and J. W. Lichtman, “Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system,” Nature450, 56–62 (2007).
[CrossRef] [PubMed]

Luengo-Oroz, M.

N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
[CrossRef]

Mack-Bucher, J.

M. Rueckel, J. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Nat. Acad. Sci.103, 17137–17142 (2006).
[CrossRef] [PubMed]

Marsh, P. N.

Milkie, D. E.

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods7, 141–147 (2009).
[CrossRef] [PubMed]

Miyawaki, A.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14, 1481–1488 (2011).
[CrossRef] [PubMed]

Neil, M. A. A.

M. J. Booth, M. A. A. Neil, R. Juškaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Nat. Acad. Sci.99, 5788–5792 (2002).
[CrossRef] [PubMed]

Nieto, M.

Noda, H.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14, 1481–1488 (2011).
[CrossRef] [PubMed]

Olarte, O. E.

Olivier, N.

N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
[CrossRef]

N. Olivier, D. Débarre, and E. Beaurepaire, “Dynamic aberration correction for multiharmonic microscopy,” Opt. Lett.34, 3145–3147 (2009).
[CrossRef] [PubMed]

Pena, A. -M.

H. Ait El Madani, E. Tancrède-Bohin, A. Bensussan, A. Colonna, A. Dupuy, M. Bagot, and A. -M. Pena, “In vivo multiphoton imaging of human skin: assessment of topical corticosteroid-induced epidermis atrophy and depigmentation,” J. Biomed. Opt.17, 026009 (2012).
[CrossRef]

Peyriéras, N.

N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
[CrossRef]

Porcar-Guezenec, R.

Riemann, I.

K. König and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt.8, 432–439 (2003).
[CrossRef] [PubMed]

Rueckel, M.

M. Rueckel, J. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Nat. Acad. Sci.103, 17137–17142 (2006).
[CrossRef] [PubMed]

Sakaue-Sawano, A.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14, 1481–1488 (2011).
[CrossRef] [PubMed]

Sanes, J. R.

J. Livet, T. A. Weissman, H. Kang, R. W. Draft, J. Lu, R. A. Bennis, J. R. Sanes, and J. W. Lichtman, “Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system,” Nature450, 56–62 (2007).
[CrossRef] [PubMed]

Santos, A.

N. Olivier, M. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy,” Science339, 967–971 (2010).
[CrossRef]

Sarntinoranont, M.

Sato, T. R.

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Nat. Acad. Sci.109, 22–27 (2012).
[CrossRef]

Savy, T.

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Supplementary Material (7)

» Media 1: AVI (11406 KB)     
» Media 2: AVI (3710 KB)     
» Media 3: AVI (4541 KB)     
» Media 4: AVI (1500 KB)     
» Media 5: AVI (1803 KB)     
» Media 6: AVI (10104 KB)     
» Media 7: AVI (47822 KB)     

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Figures (7)

Fig. 1
Fig. 1

Principle of spatially resolved modal aberration correction. (a), experimental setup. A titanium-sapphire laser (Ti:S) (Chameleon, Coherent Inc.) is used for excitation. The beam is reflected on a deformable mirror (DM) (Mirao 52e, Imagine Optic), scanned with galvanometric mirrors (General Scanning) and focussed using a 25x, 1.05NA, water immersion, coverslip-corrected objective (obj) (Olympus). 2PEF and second-harmonic signals are collected on photomultiplier tubes (PMT) (Photon Line) using dichroic beamsplitters (DBS) (Chroma) and short-pass emission filters (EF) (Semrock) to eliminate excitation light. (b), principle of aberration measurement. For each aberration mode i, P images are acquired with an amount of aberration bij (j=1..P) applied by the DM. Here, the example of Zernike astigmatism is shown. Metric M (here average image intensity) is subsequently calculated for each value of bi, and the initial amount of aberration, aim, is estimated as the opposite of the calculated maximum of the curve of M. (c), extension to spatially-resolved aberration measurement: each of the P images are divided in L×L pixel subregions, and M is calculated for each sub-region of coordinates (k,l) as a function of bij. The map of aberrations in mode i is obtained as the matrix {aim(k,l) = −bim(k,l)}kl where bim(k,l) is the position of the maximum of M.

Fig. 2
Fig. 2

Calibration of the accuracy of the spatially resolved aberration measurement. (a), example of test sample used for calibration (fixed, stained pine root slice). The green rectangles indicate the locations of the smaller regions over which aberrations were measured iteratively. Scale bar, 100μm. (b), aberration map obtained on the sample in (a) for astigmatism (z=5, see Appendix A). The green rectangles mark the same location as in (a), and delimitate the region over which the aberration map was averaged to compare the spatially-resolved measurement with the iterative result. (c), Error in the spatially resolved measurements as a function of the total amount of aberrations in the 11 Zernike modes under investigation (z=5 to 15, see Appendix A), estimated as the difference between the spatially-resolved value at a given location and the iterative (accurate) local measurement at the same location (green rectangles in (a) and (b)). Both axes are expressed in terms of rms value of the phase profile, or equivalently of the norm of the Zernike coefficient vector. Results for each sample are plotted with a different symbol and colour. The black line is a quadratic fit to the data [9].

Fig. 3
Fig. 3

Aberration measurements on human skin biopsies. (a)–(d), blue (410–490nm) and red (500–600nm) endogenous 2PEF signals and SHG signal (390nm, shown in green) recorded at 10μm (a), 35μm (b), 60μm (c) and 105μm (d) below skin surface. The strong aberrations introduced by the stratum corneum are evidenced by the darker pattern in deeper images (white ellipses). Media 1 shows the structure of the sample as a function of depth. Scale bar, 100μm. (e), endogenous fluorescence signal at a depth of 80μm (top), and the corresponding recorded spherical aberration amplitude (middle) and total aberration amplitude (bottom). Aberrations increase as a function of depth ( Media 2) and reflect the structure of the superficial layer. The blue areas in the middle images and the black areas in the bottom images correspond to an absence of measurement due to a lack of signal from the sample. Scale bar, 100μm. (f), XZ reslice of the data along the middle of the yellow box in (a). The 2PEF and SHG signals are strongly attenuated under the stratum corneum folds (orange arrow) compared with the surrounding regions. (a)–(d) and (f) share the same colour scale shown below (f). (g) and Media 3, 3D reconstruction of the boxed area in (a). The excitation cones corresponding to the effective NA used for imaging (0.95) are plotted for the two positions corresponding to the red and orange boxed area in (a). The corresponding images are shown as inset at 80μm deep, demonstrating the correlation between the distortion of the excitation wavefront by the skin ridges and the loss of image resolution. Scale bar, 15μm.

Fig. 4
Fig. 4

Aberration measurement on fixed mouse hippocampus mounted in PBS. (a) and Media 4, endogenous 2PEF image at a depth of 80μm. (b), corresponding total aberration map, and (c) superposition of (a) and (b). (d)–(f), aberration coefficient maps for (d) astigmatism (z=5), (e) coma (z=8) and (f) spherical aberration (z=11). The 3 maps share the same colour scale. (g) and Media 5, region of the tissue modelled for aberration simulation (top), corresponding to the yellow bow in (a). Dotted circle, limit of the excitation cone at the surface of the tissue. Arrow, line along which aberrations were calculated. bottom, model used for the 3D refractive index map. Left, xy image 10μm below the surface of the tissue; right, xz reslice. Scale bars, 100μm.(h)–(j), experimental (blue) and simulated aberration profile with (purple) and without (green) index variation within the tissue at a depth of 80μm. (h), astigmatism; (i), coma; (j), spherical aberration. (k), residual aberration profile at the same depth after correction of 0 (black), 11 (red) and 32 (orange) Zernike modes.

Fig. 5
Fig. 5

Aberration measurement on fixed Brainbow mouse hippocampus mounted in Vec-tashield. (a) and Media 6, CFP and endogenous 2PEF image at depths of 10, 100 and 200μm. (b)–(d), aberration coefficient maps for (b), astigmatism (z=5); (c), coma (z=8); (d), spherical aberration (z=11). The three maps share the same colour scale. (e), maps of the total aberration amplitude. Scale bar, 100μm. At each depth, measurement of the 11 aberration maps took about 6 minutes and induced ≈ 7% decrease of the fluorescent signal due to photobleaching.

Fig. 6
Fig. 6

Deep imaging within fixed mouse hippocampus. (a) and Media 7, comparison of 2PEF imaging over a 400 × 400 × 420μm volume of a PBS-mounted (left and a Vectashield-mounted (right) sample. The lines on the images indicate the location of the three visualised planes. Top, xy view (cut along the orange lines); middle, xz view (cut along the yellow lines); bottom, yz view (cut along the blue lines). Scale bar, 100μm. (b), residual aberration correction on a Vectashield-mounted sample. Within a 100 × 100μm aplanetism region, the quality of images can be maintained throughout the tissue by adjusting the correction phase. Scale bar, 50μm.

Fig. 7
Fig. 7

Aberration correction over a large area. (a), 2PEF image of a Vectashield-embedded brain slide 150μm below the surface. Scale bar, 100μm. (b) (resp. (c)), map of the Strehl ratio after spatially unresolved aberration correction over the green boxed region in (a)(resp. the entire area in (a)). (d), Strehl ratio in the green boxed region after correction over a region centred on this boxed region and of varying size. The dotted line is the lower limit for diffraction-limited focussing and the solid line is the value achieved after correction over the entire image. (e)–(g), Strehl ratio map after spatially resolved correction over (e), 9; (f), 25; and (g), 64 subregions. (h), percentage of the image area for which the Strehl ratio is above 0.8 as a function of the number of subregions used for spatially resolved correction. (b)–(g) maps share the same colour scale and pixel size (10μm).

Tables (1)

Tables Icon

Table 1 Zernike modes 1 to 15 and numbering scheme. The modes are expressed over the unit disk as functions of r and θ with 0 < r < 1 and 0 < θ < 2π.

Equations (2)

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d c = N tot + P B F ,
S ( a ) = exp [ a 2 ] = exp [ i = 1 N a i 2 ]

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