Abstract

Three-dimensional imaging in biological samples usually suffers from performance degradation caused by optical inhomogeneities. Here we proposed an approach to adaptive optics in fluorescence microscopy where the aberrations are measured by self-interference holographic recording and then corrected by a post-processing optimization procedure. In our approach, only one complex-value hologram is sufficient to measure and then correct the aberrations, which results in fast acquisition speed, lower exposure time, and the ability to image in three-dimensions without the need to scan the sample or any other element in the system. We show proof-of-principle experiments on a tissue phantom containing fluorescence particles. Furthermore, we present three-dimensional reconstructions of actin-labeled MCF7 breast cancer cells, showing improved resolution after the correction of aberrations. Both experiments demonstrate the validity of our method and show the great potential of non-scanning adaptive three-dimensional microscopy in imaging biological samples with improved resolution and signal-to-noise ratio.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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2017 (5)

2016 (4)

2015 (2)

D. Burke, B. Patton, F. Huang, J. Bewersdorf, and M. J. Booth, “Adaptive optics correction of specimen-induced aberrations in single-molecule switching microscopy,” Optica 2(2), 177–185 (2015).
[Crossref]

L. Miccio, P. Memmolo, F. Merola, P. A. Netti, and P. Ferraro, “Red blood cell as an adaptive optofluidic microlens,” Nat. Commun. 6(6502), 6502 (2015).
[Crossref] [PubMed]

2014 (2)

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

R. Kelner, B. Katz, and J. Rosen, “Optical sectioning using a digital Fresnel incoherent-holography-based confocal imaging system,” Optica 1(2), 70–74 (2014).
[Crossref] [PubMed]

2013 (1)

2012 (6)

S. Przibilla, S. Dartmann, A. Vollmer, S. Ketelhut, B. Greve, G. von Bally, and B. Kemper, “Sensing dynamic cytoplasm refractive index changes of adherent cells with quantitative phase microscopy using incorporated microspheres as optical probes,” J. Biomed. Opt. 17(9), 0970011 (2012).
[Crossref] [PubMed]

B. Katz, J. Rosen, R. Kelner, and G. Brooker, “Enhanced resolution and throughput of Fresnel incoherent correlation holography (FINCH) using dual diffractive lenses on a spatial light modulator (SLM),” Opt. Express 20(8), 9109–9121 (2012).
[Crossref] [PubMed]

R. Kelner and J. Rosen, “Spatially incoherent single channel digital Fourier holography,” Opt. Lett. 37(17), 3723–3725 (2012).
[Crossref] [PubMed]

T. J. Gould, D. Burke, J. Bewersdorf, and M. J. Booth, “Adaptive optics enables 3D STED microscopy in aberrating specimens,” Opt. Express 20(19), 20998–21009 (2012).
[Crossref] [PubMed]

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

M. K. Kim, “Adaptive optics by incoherent digital holography,” Opt. Lett. 37(13), 2694–2696 (2012).
[Crossref] [PubMed]

2010 (1)

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
[Crossref] [PubMed]

2009 (1)

2008 (1)

J. Rosen and G. Brooker, “Non-scanning motionless fluorescence three-dimensional holographic microscopy,” Nat. Photonics 2(3), 190–195 (2008).
[Crossref]

2007 (1)

2005 (1)

Adie, S. G.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Ahmad, A.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Barroso, Á.

F. Merola, Á. Barroso, L. Miccio, P. Memmolo, M. Mugnano, P. Ferraro, and C. Denz, “Biolens behavior of RBCs under optically-induced mechanical stress,” Cytometry A 91(5), 527–533 (2017).
[Crossref] [PubMed]

Betzig, E.

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
[Crossref] [PubMed]

Bewersdorf, J.

Bliek, L.

Bonora, S.

Booth, M. J.

Boppart, S. A.

P. Pande, Y. Z. Liu, F. A. South, and S. A. Boppart, “Automated computational aberration correction method for broadband interferometric imaging techniques,” Opt. Lett. 41(14), 3324–3327 (2016).
[Crossref] [PubMed]

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Brooker, G.

Brown, A. C. N.

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

Burke, D.

Carney, P. S.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Clegg, J. H.

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

Cuche, E.

Dartmann, S.

S. Przibilla, S. Dartmann, A. Vollmer, S. Ketelhut, B. Greve, G. von Bally, and B. Kemper, “Sensing dynamic cytoplasm refractive index changes of adherent cells with quantitative phase microscopy using incorporated microspheres as optical probes,” J. Biomed. Opt. 17(9), 0970011 (2012).
[Crossref] [PubMed]

Davis, D. M.

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

Denz, C.

F. Merola, Á. Barroso, L. Miccio, P. Memmolo, M. Mugnano, P. Ferraro, and C. Denz, “Biolens behavior of RBCs under optically-induced mechanical stress,” Cytometry A 91(5), 527–533 (2017).
[Crossref] [PubMed]

Depeursinge, C.

Dunsby, C.

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

Emery, Y.

Ferraro, P.

F. Merola, Á. Barroso, L. Miccio, P. Memmolo, M. Mugnano, P. Ferraro, and C. Denz, “Biolens behavior of RBCs under optically-induced mechanical stress,” Cytometry A 91(5), 527–533 (2017).
[Crossref] [PubMed]

L. Miccio, P. Memmolo, F. Merola, P. A. Netti, and P. Ferraro, “Red blood cell as an adaptive optofluidic microlens,” Nat. Commun. 6(6502), 6502 (2015).
[Crossref] [PubMed]

French, P. M. W.

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

Gould, T. J.

Graf, B. W.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Greve, B.

S. Przibilla, S. Dartmann, A. Vollmer, S. Ketelhut, B. Greve, G. von Bally, and B. Kemper, “Sensing dynamic cytoplasm refractive index changes of adherent cells with quantitative phase microscopy using incorporated microspheres as optical probes,” J. Biomed. Opt. 17(9), 0970011 (2012).
[Crossref] [PubMed]

Hashimoto, N.

Heisler, M.

Huang, F.

Ji, N.

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
[Crossref] [PubMed]

Jian, Y.

Ju, M. J.

Kalkman, J.

Kashter, Y.

Katz, B.

Kelner, R.

Kemper, B.

S. Przibilla, S. Dartmann, A. Vollmer, S. Ketelhut, B. Greve, G. von Bally, and B. Kemper, “Sensing dynamic cytoplasm refractive index changes of adherent cells with quantitative phase microscopy using incorporated microspheres as optical probes,” J. Biomed. Opt. 17(9), 0970011 (2012).
[Crossref] [PubMed]

Ketelhut, S.

S. Przibilla, S. Dartmann, A. Vollmer, S. Ketelhut, B. Greve, G. von Bally, and B. Kemper, “Sensing dynamic cytoplasm refractive index changes of adherent cells with quantitative phase microscopy using incorporated microspheres as optical probes,” J. Biomed. Opt. 17(9), 0970011 (2012).
[Crossref] [PubMed]

Kim, M. K.

Knutsson, P.

Kurihara, M.

Lenz, M. O.

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

Liu, Y. Z.

Lupashin, V.

N. Siegel, V. Lupashin, B. Storrie, and G. Brooker, “High-magnification super-resolution FINCH microscopy using birefringent crystal lens interferometers,” Nat. Photonics 10(12), 802–808 (2016).
[Crossref] [PubMed]

Magistretti, P.

Man, T.

Marquet, P.

Memmolo, P.

F. Merola, Á. Barroso, L. Miccio, P. Memmolo, M. Mugnano, P. Ferraro, and C. Denz, “Biolens behavior of RBCs under optically-induced mechanical stress,” Cytometry A 91(5), 527–533 (2017).
[Crossref] [PubMed]

L. Miccio, P. Memmolo, F. Merola, P. A. Netti, and P. Ferraro, “Red blood cell as an adaptive optofluidic microlens,” Nat. Commun. 6(6502), 6502 (2015).
[Crossref] [PubMed]

Merola, F.

F. Merola, Á. Barroso, L. Miccio, P. Memmolo, M. Mugnano, P. Ferraro, and C. Denz, “Biolens behavior of RBCs under optically-induced mechanical stress,” Cytometry A 91(5), 527–533 (2017).
[Crossref] [PubMed]

L. Miccio, P. Memmolo, F. Merola, P. A. Netti, and P. Ferraro, “Red blood cell as an adaptive optofluidic microlens,” Nat. Commun. 6(6502), 6502 (2015).
[Crossref] [PubMed]

Miccio, L.

F. Merola, Á. Barroso, L. Miccio, P. Memmolo, M. Mugnano, P. Ferraro, and C. Denz, “Biolens behavior of RBCs under optically-induced mechanical stress,” Cytometry A 91(5), 527–533 (2017).
[Crossref] [PubMed]

L. Miccio, P. Memmolo, F. Merola, P. A. Netti, and P. Ferraro, “Red blood cell as an adaptive optofluidic microlens,” Nat. Commun. 6(6502), 6502 (2015).
[Crossref] [PubMed]

Milkie, D. E.

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
[Crossref] [PubMed]

Mugnano, M.

F. Merola, Á. Barroso, L. Miccio, P. Memmolo, M. Mugnano, P. Ferraro, and C. Denz, “Biolens behavior of RBCs under optically-induced mechanical stress,” Cytometry A 91(5), 527–533 (2017).
[Crossref] [PubMed]

Neil, M. A. A.

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

Netti, P. A.

L. Miccio, P. Memmolo, F. Merola, P. A. Netti, and P. Ferraro, “Red blood cell as an adaptive optofluidic microlens,” Nat. Commun. 6(6502), 6502 (2015).
[Crossref] [PubMed]

Owald, D.

Owner-Petersen, M.

Pande, P.

Patton, B.

Patton, B. R.

Popovic, Z.

Przibilla, S.

S. Przibilla, S. Dartmann, A. Vollmer, S. Ketelhut, B. Greve, G. von Bally, and B. Kemper, “Sensing dynamic cytoplasm refractive index changes of adherent cells with quantitative phase microscopy using incorporated microspheres as optical probes,” J. Biomed. Opt. 17(9), 0970011 (2012).
[Crossref] [PubMed]

Rappaz, B.

Rosen, J.

A. Vijayakumar and J. Rosen, “Interferenceless coded aperture correlation holography-a new technique for recording incoherent digital holograms without two-wave interference,” Opt. Express 25(12), 13883–13896 (2017).
[Crossref] [PubMed]

A. Vijayakumar and J. Rosen, “Spectrum and space resolved 4D imaging by coded aperture correlation holography (COACH) with diffractive objective lens,” Opt. Lett. 42(5), 947–950 (2017).
[Crossref] [PubMed]

A. Vijayakumar, Y. Kashter, R. Kelner, and J. Rosen, “Coded aperture correlation holography-a new type of incoherent digital holograms,” Opt. Express 24(11), 12430–12441 (2016).
[Crossref] [PubMed]

R. Kelner, B. Katz, and J. Rosen, “Optical sectioning using a digital Fresnel incoherent-holography-based confocal imaging system,” Optica 1(2), 70–74 (2014).
[Crossref] [PubMed]

G. Brooker, N. Siegel, J. Rosen, N. Hashimoto, M. Kurihara, and A. Tanabe, “In-line FINCH super resolution digital holographic fluorescence microscopy using a high efficiency transmission liquid crystal GRIN lens,” Opt. Lett. 38(24), 5264–5267 (2013).
[Crossref] [PubMed]

R. Kelner and J. Rosen, “Spatially incoherent single channel digital Fourier holography,” Opt. Lett. 37(17), 3723–3725 (2012).
[Crossref] [PubMed]

B. Katz, J. Rosen, R. Kelner, and G. Brooker, “Enhanced resolution and throughput of Fresnel incoherent correlation holography (FINCH) using dual diffractive lenses on a spatial light modulator (SLM),” Opt. Express 20(8), 9109–9121 (2012).
[Crossref] [PubMed]

J. Rosen and G. Brooker, “Non-scanning motionless fluorescence three-dimensional holographic microscopy,” Nat. Photonics 2(3), 190–195 (2008).
[Crossref]

J. Rosen and G. Brooker, “Digital spatially incoherent Fresnel holography,” Opt. Lett. 32(8), 912–914 (2007).
[Crossref] [PubMed]

Sarunic, M. V.

Savell, A.

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

Siegel, N.

N. Siegel, V. Lupashin, B. Storrie, and G. Brooker, “High-magnification super-resolution FINCH microscopy using birefringent crystal lens interferometers,” Nat. Photonics 10(12), 802–808 (2016).
[Crossref] [PubMed]

G. Brooker, N. Siegel, J. Rosen, N. Hashimoto, M. Kurihara, and A. Tanabe, “In-line FINCH super resolution digital holographic fluorescence microscopy using a high efficiency transmission liquid crystal GRIN lens,” Opt. Lett. 38(24), 5264–5267 (2013).
[Crossref] [PubMed]

Sinclair, H. G.

M. O. Lenz, H. G. Sinclair, A. Savell, J. H. Clegg, A. C. N. Brown, D. M. Davis, C. Dunsby, M. A. A. Neil, and P. M. W. French, “3-D stimulated emission depletion microscopy with programmable aberration correction,” J. Biophotonics 7(1-2), 29–36 (2014).
[Crossref] [PubMed]

South, F. A.

Storrie, B.

N. Siegel, V. Lupashin, B. Storrie, and G. Brooker, “High-magnification super-resolution FINCH microscopy using birefringent crystal lens interferometers,” Nat. Photonics 10(12), 802–808 (2016).
[Crossref] [PubMed]

Tanabe, A.

Thaung, J.

Verhaegen, M.

Verstraete, H. R. G. W.

Vijayakumar, A.

Vollmer, A.

S. Przibilla, S. Dartmann, A. Vollmer, S. Ketelhut, B. Greve, G. von Bally, and B. Kemper, “Sensing dynamic cytoplasm refractive index changes of adherent cells with quantitative phase microscopy using incorporated microspheres as optical probes,” J. Biomed. Opt. 17(9), 0970011 (2012).
[Crossref] [PubMed]

von Bally, G.

S. Przibilla, S. Dartmann, A. Vollmer, S. Ketelhut, B. Greve, G. von Bally, and B. Kemper, “Sensing dynamic cytoplasm refractive index changes of adherent cells with quantitative phase microscopy using incorporated microspheres as optical probes,” J. Biomed. Opt. 17(9), 0970011 (2012).
[Crossref] [PubMed]

Wahl, D.

Wan, Y.

Wang, D.

Wu, F.

Appl. Opt. (1)

Biomed. Opt. Express (1)

Cytometry A (1)

F. Merola, Á. Barroso, L. Miccio, P. Memmolo, M. Mugnano, P. Ferraro, and C. Denz, “Biolens behavior of RBCs under optically-induced mechanical stress,” Cytometry A 91(5), 527–533 (2017).
[Crossref] [PubMed]

J. Biomed. Opt. (1)

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Supplementary Material (1)

NameDescription
» Visualization 1       Adaptive non-scanning three-dimensional reconstructions of MCF7 cells using the proposed method.

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Figures (10)

Fig. 1
Fig. 1 Schematic of the fluorescence self-interference digital holography system used in the simulations.
Fig. 2
Fig. 2 (a) Simulated reconstructed image of USAF resolution test target using back-propagation algorithm with astigmatism (z3), coma (z9) and spherical aberrations (z12) in the system. (b) AO corrected image obtained using the proposed method.
Fig. 3
Fig. 3 Schematic drawing of the custom-built FINCH inverted microscopic imaging system. L1 and L2, lens (f1 = 200 mm, f2 = 150 mm); DM, dichroic mirror; Fex and Fem, filters; SLM, spatial light modulator; P1 and P2, polarizers; OBJ, objective lens; sm-fiber, single mode fiber.
Fig. 4
Fig. 4 (a) Schematic of AO optimization procedure of the experimental data with astigmatism (z3) aberration in the system. Reconstructed image (b) before and (c) after the AO correction using the proposed method. Only the central area of the reconstructed images is shown.
Fig. 5
Fig. 5 Experimental results with astigmatism (z3), coma (z9) and spherical aberrations (z12) in the system. (a) Aberrated wide-field image. (b) Conventional FINCH reconstructed image using back-propagation algorithm. (c) AO corrected image after using the proposed method. (d) - (f) Correspond to magnified image of the central area of (a)-(c).
Fig. 6
Fig. 6 Phase of the complex-value hologram of the microsphere sample.
Fig. 7
Fig. 7 Reconstructed images at (a1)-(a3) depths of 76μm and (b1)-(b3) 120μm in the sample. (a1), (b1) and (a3), (b3) are the magnified images of the areas labeled by red and green rectangles in (a2) and (b2). In (a1), (a3), (b1) and (b3), in-focus microspheres are indicated by the red arrows and yellow labels. The white scale bar indicates 10μm.
Fig. 8
Fig. 8 Effect of aberration correction on reconstructed image of microsphere 1 and microsphere 2 (both located at a depth of 76μm in the sample) and microsphere 3 (located at 120μm). Top row: reconstructed focal-plane images obtained using the back-propagation reconstruction method. Bottom row: reconstructed images with additional computational AO correction. Insets: phase masks used for the AO correction. Images are magnified 20 times using the image interpolation toolbox of the Matlab. The white scale bar indicates 880nm.
Fig. 9
Fig. 9 Reconstructed images of actin-labeled MCF7 breast cancer cells (a)(b) before and (c)(d) after AO correction on different layers within the cell. Yellow arrows indicate the in-focus actin structures before/after AO correction. The scale bar indicates 24μm (see Visualization).
Fig. 10
Fig. 10 Wide-field fluorescence image of the actin-labeled MCF7 breast cancer cells.

Equations (6)

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U SLM =Q( 1 z s )Q( 1 f )Q( 1 d s ),
I i = | Q( 1 z s )Q( 1 f )Q( 1 d s ) e j φ a Q( 1 z h ) +Q( 1 z s )Q( 1 f )Q( 1 d s ) e j φ a Q( 1 f SLM )Q( 1 z h ) e j θ i | 2
H a =(En) H p =(En)[Q( 1 z r )Ψ],
R a = H a Q( 1 z r )=(En)[Q( 1 z r )Ψ]Q( 1 z r ).
R AO = F 1 [F( R a ) e j φ AO ],
φ AO = m=1 k c m z m .

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