Volumetric optical coherence microscopy with a high space-bandwidth-time product enabled by hybrid adaptive optics

Siyang Liu; Jeffrey A. Mulligan; Steven G. Adie

doi:10.1364/BOE.9.003137

Biomedical Optics Express
Vol. 9,
Issue 7,
pp. 3137-3152
(2018)
•https://doi.org/10.1364/BOE.9.003137

Volumetric optical coherence microscopy with a high space-bandwidth-time product enabled by hybrid adaptive optics

Siyang Liu, Jeffrey A. Mulligan, and Steven G. Adie

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Siyang Liu, Jeffrey A. Mulligan, and Steven G. Adie, "Volumetric optical coherence microscopy with a high space-bandwidth-time product enabled by hybrid adaptive optics," Biomed. Opt. Express 9, 3137-3152 (2018)

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Abstract

Optical coherence microscopy (OCM) is a promising modality for high resolution imaging, but has limited ability to capture large-scale volumetric information about dynamic biological processes with cellular resolution. To enhance the throughput of OCM, we implemented a hybrid adaptive optics (hyAO) approach that combines computational adaptive optics with an intentionally aberrated imaging beam generated via hardware adaptive optics. Using hyAO, we demonstrate the depth-equalized illumination and collection ability of an astigmatic beam compared to a Gaussian beam for cellular-resolution imaging. With this advantage, we achieved volumetric OCM with a higher space-bandwidth-time product compared to Gaussian-beam acquisition that employed focus-scanning across depth. HyAO was also used to perform volumetric time-lapse OCM imaging of cellular dynamics over a 1mm × 1mm × 1mm field-of-view with 2 μm isotropic spatial resolution and 3-minute temporal resolution. As hyAO is compatible with both spectral-domain and swept-source beam-scanning OCM systems, significant further improvements in absolute volumetric throughput are possible by use of ultrahigh-speed swept sources.

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2018 (2)

S. Tozburun, C. Blatter, M. Siddiqui, E. F. J. Meijer, and B. J. Vakoc, “Phase-stable Doppler OCT at 19 MHz using a stretched-pulse mode-locked laser,” Biomed. Opt. Express 9(3), 952–961 (2018).
[Crossref] [PubMed]

P. Xiao, V. Mazlin, K. Grieve, J.-A. Sahel, M. Fink, and A. C. Boccara, “In vivo high-resolution human retinal imaging with wavefront-correctionless full-field OCT,” Optica 5(4), 409–412 (2018).
[Crossref]

2017 (10)

P. J. Marchand, A. Bouwens, D. Szlag, D. Nguyen, A. Descloux, M. Sison, S. Coquoz, J. Extermann, and T. Lasser, “Visible spectrum extended-focus optical coherence microscopy for label-free sub-cellular tomography,” Biomed. Opt. Express 8(7), 3343–3359 (2017).
[Crossref] [PubMed]

S. Coquoz, A. Bouwens, P. J. Marchand, J. Extermann, and T. Lasser, “Interferometric synthetic aperture microscopy for extended focus optical coherence microscopy,” Opt. Express 25(24), 30807–30819 (2017).
[Crossref] [PubMed]

L. Ginner, A. Kumar, D. Fechtig, L. M. Wurster, M. Salas, M. Pircher, and R. A. Leitgeb, “Noniterative digital aberration correction for cellular resolution retinal optical coherence tomography in vivo,” Optica 4(8), 924–931 (2017).
[Crossref]

J. A. Mulligan, F. Bordeleau, C. A. Reinhart-King, and S. G. Adie, “Measurement of dynamic cell-induced 3D displacement fields in vitro for traction force optical coherence microscopy,” Biomed. Opt. Express 8(2), 1152–1171 (2017).
[Crossref] [PubMed]

K. Karnowski, A. Ajduk, B. Wieloch, S. Tamborski, K. Krawiec, M. Wojtkowski, and M. Szkulmowski, “Optical coherence microscopy as a novel, non-invasive method for the 4D live imaging of early mammalian embryos,” Sci. Rep. 7(1), 4165 (2017).
[Crossref] [PubMed]

L. Yi, L. Sun, and W. Ding, “Multifocal spectral-domain optical coherence tomography based on Bessel beam for extended imaging depth,” J. Biomed. Opt. 22(10), 1–8 (2017).
[Crossref] [PubMed]

Y. Chen, L. A. Trinh, J. Fingler, and S. E. Fraser, “3D in vivo imaging with extended-focus optical coherence microscopy,” J. Biophotonics 10(11), 1411–1420 (2017).
[Crossref] [PubMed]

B. Yin, C. Hyun, J. A. Gardecki, and G. J. Tearney, “Extended depth of focus for coherence-based cellular imaging,” Optica 4(8), 959–965 (2017).
[Crossref] [PubMed]

O. Thouvenin, C. Boccara, M. Fink, J. Sahel, M. Pâques, and K. Grieve, “Cell Motility as Contrast Agent in Retinal Explant Imaging With Full-Field Optical Coherence Tomography,” Invest. Ophthalmol. Vis. Sci. 58(11), 4605–4615 (2017).
[Crossref] [PubMed]

O. Thouvenin, K. Grieve, P. Xiao, C. Apelian, and A. C. Boccara, “En face coherence microscopy [Invited],” Biomed. Opt. Express 8(2), 622–639 (2017).
[Crossref] [PubMed]

2016 (8)

A. Curatolo, M. Villiger, D. Lorenser, P. Wijesinghe, A. Fritz, B. F. Kennedy, and D. D. Sampson, “Ultrahigh-resolution optical coherence elastography,” Opt. Lett. 41(1), 21–24 (2016).
[Crossref] [PubMed]

S. Tamborski, H. C. Lyu, H. Dolezyczek, M. Malinowska, G. Wilczynski, D. Szlag, T. Lasser, M. Wojtkowski, and M. Szkulmowski, “Extended-focus optical coherence microscopy for high-resolution imaging of the murine brain,” Biomed. Opt. Express 7(11), 4400–4414 (2016).
[Crossref] [PubMed]

A. Curatolo, P. R. T. Munro, D. Lorenser, P. Sreekumar, C. C. Singe, B. F. Kennedy, and D. D. Sampson, “Quantifying the influence of Bessel beams on image quality in optical coherence tomography,” Sci. Rep. 6(1), 23483 (2016).
[Crossref] [PubMed]

D. Hillmann, H. Spahr, C. Hain, H. Sudkamp, G. Franke, C. Pfäffle, C. Winter, and G. Hüttmann, “Aberration-free volumetric high-speed imaging of in vivo retina,” Sci. Rep. 6(1), 35209 (2016).
[Crossref] [PubMed]

Y. Xu, Y.-Z. Liu, S. A. Boppart, and P. S. Carney, “Automated interferometric synthetic aperture microscopy and computational adaptive optics for improved optical coherence tomography,” Appl. Opt. 55(8), 2034–2041 (2016).
[Crossref] [PubMed]

J. Notbohm, S. Banerjee, K. J. C. Utuje, B. Gweon, H. Jang, Y. Park, J. Shin, J. P. Butler, J. J. Fredberg, and M. C. Marchetti, “Cellular Contraction and Polarization Drive Collective Cellular Motion,” Biophys. J. 110(12), 2729–2738 (2016).
[Crossref] [PubMed]

L. Przybyla, J. N. Lakins, R. Sunyer, X. Trepat, and V. M. Weaver, “Monitoring developmental force distributions in reconstituted embryonic epithelia,” Methods 94, 101–113 (2016).
[Crossref] [PubMed]

P. Xiao, M. Fink, and A. C. Boccara, “Full-field spatially incoherent illumination interferometry: a spatial resolution almost insensitive to aberrations,” Opt. Lett. 41(17), 3920–3923 (2016).
[Crossref] [PubMed]

2015 (4)

D. J. Fechtig, B. Grajciar, T. Schmoll, C. Blatter, R. M. Werkmeister, W. Drexler, and R. A. Leitgeb, “Line-field parallel swept source MHz OCT for structural and functional retinal imaging,” Biomed. Opt. Express 6(3), 716–735 (2015).
[Crossref] [PubMed]

A. Kumar, T. Kamali, R. Platzer, A. Unterhuber, W. Drexler, and R. A. Leitgeb, “Anisotropic aberration correction using region of interest based digital adaptive optics in Fourier domain OCT,” Biomed. Opt. Express 6(4), 1124–1134 (2015).
[Crossref] [PubMed]

C. Costa, A. Bradu, J. Rogers, P. Phelan, and A. Podoleanu, “Swept source optical coherence tomography Gabor fusion splicing technique for microscopy of thick samples using a deformable mirror,” J. Biomed. Opt. 20(1), 016012 (2015).
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L. Tian, Z. Liu, L.-H. Yeh, M. Chen, J. Zhong, and L. Waller, “Computational illumination for high-speed in vitro Fourier ptychographic microscopy,” Optica 2(10), 904–911 (2015).
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2014 (5)

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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Y. Xu, X. K. B. Chng, S. G. Adie, S. A. Boppart, and P. S. Carney, “Multifocal interferometric synthetic aperture microscopy,” Opt. Express 22(13), 16606–16618 (2014).
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H. Yu, J. Jang, J. Lim, J.-H. Park, W. Jang, J.-Y. Kim, and Y. Park, “Depth-enhanced 2-D optical coherence tomography using complex wavefront shaping,” Opt. Express 22(7), 7514–7523 (2014).
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Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
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Y.-Z. Liu, N. D. Shemonski, S. G. Adie, A. Ahmad, A. J. Bower, P. S. Carney, and S. A. Boppart, “Computed optical interferometric tomography for high-speed volumetric cellular imaging,” Biomed. Opt. Express 5(9), 2988–3000 (2014).
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2013 (5)

T. Klein, W. Wieser, L. Reznicek, A. Neubauer, A. Kampik, and R. Huber, “Multi-MHz retinal OCT,” Biomed. Opt. Express 4(10), 1890–1908 (2013).
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J. Jang, J. Lim, H. Yu, H. Choi, J. Ha, J.-H. Park, W.-Y. Oh, W. Jang, S. Lee, and Y. Park, “Complex wavefront shaping for optimal depth-selective focusing in optical coherence tomography,” Opt. Express 21(3), 2890–2902 (2013).
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A. Kumar, W. Drexler, and R. A. Leitgeb, “Subaperture correlation based digital adaptive optics for full field optical coherence tomography,” Opt. Express 21(9), 10850–10866 (2013).
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F. Huber, J. Schnauß, S. Rönicke, P. Rauch, K. Müller, C. Fütterer, and J. Käs, “Emergent complexity of the cytoskeleton: from single filaments to tissue,” Adv. Phys. 62(1), 1–112 (2013).
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G. Zheng, R. Horstmeyer, and C. Yang, “Wide-field, high-resolution Fourier ptychographic microscopy,” Nat. Photonics 7(9), 739–745 (2013).
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2012 (7)

C. Blatter, J. Weingast, A. Alex, B. Grajciar, W. Wieser, W. Drexler, R. Huber, and R. A. Leitgeb, “In situ structural and microangiographic assessment of human skin lesions with high-speed OCT,” Biomed. Opt. Express 3(10), 2636–2646 (2012).
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K.-S. Lee, H. Zhao, S. F. Ibrahim, N. Meemon, L. Khoudeir, and J. P. Rolland, “Three-dimensional imaging of normal skin and nonmelanoma skin cancer with cellular resolution using Gabor domain optical coherence microscopy,” J. Biomed. Opt. 17(12), 126006 (2012).
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V. J. Srinivasan, H. Radhakrishnan, J. Y. Jiang, S. Barry, and A. E. Cable, “Optical coherence microscopy for deep tissue imaging of the cerebral cortex with intrinsic contrast,” Opt. Express 20(3), 2220–2239 (2012).
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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).
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S. G. Adie, N. D. Shemonski, B. W. Graf, A. Ahmad, P. Scott Carney, and S. A. Boppart, “Guide-star-based computational adaptive optics for broadband interferometric tomography,” Appl. Phys. Lett. 101(22), 221117 (2012).
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N. Gjorevski and C. M. Nelson, “Mapping of Mechanical Strains and Stresses around Quiescent Engineered Three-Dimensional Epithelial Tissues,” Biophys. J. 103(1), 152–162 (2012).
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2011 (4)

F. Wetzel, S. Rönicke, K. Müller, M. Gyger, D. Rose, M. Zink, and J. Käs, “Single cell viability and impact of heating by laser absorption,” Eur. Biophys. J. 40(9), 1109–1114 (2011).
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O. P. Kocaoglu, S. Lee, R. S. Jonnal, Q. Wang, A. E. Herde, J. C. Derby, W. Gao, and D. T. Miller, “Imaging cone photoreceptors in three dimensions and in time using ultrahigh resolution optical coherence tomography with adaptive optics,” Biomed. Opt. Express 2(4), 748–763 (2011).
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D. Hillmann, C. Lührs, T. Bonin, P. Koch, and G. Hüttmann, “Holoscopy--holographic optical coherence tomography,” Opt. Lett. 36(13), 2390–2392 (2011).
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C. Blatter, B. Grajciar, C. M. Eigenwillig, W. Wieser, B. R. Biedermann, R. Huber, and R. A. Leitgeb, “Extended focus high-speed swept source OCT with self-reconstructive illumination,” Opt. Express 19(13), 12141–12155 (2011).
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2010 (4)

J. P. Rolland, P. Meemon, S. Murali, K. P. Thompson, and K. S. Lee, “Gabor-based fusion technique for Optical Coherence Microscopy,” Opt. Express 18(4), 3632–3642 (2010).
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K. Ramser and D. Hanstorp, “Optical manipulation for single-cell studies,” J. Biophotonics 3(4), 187–206 (2010).
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B. W. Graf, S. G. Adie, and S. A. Boppart, “Correction of coherence gate curvature in high numerical aperture optical coherence imaging,” Opt. Lett. 35(18), 3120–3122 (2010).
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W. Wieser, B. R. Biedermann, T. Klein, C. M. Eigenwillig, and R. Huber, “Multi-megahertz OCT: High quality 3D imaging at 20 million A-scans and 4.5 GVoxels per second,” Opt. Express 18(14), 14685–14704 (2010).
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2009 (3)

X. Trepat, M. R. Wasserman, T. E. Angelini, E. Millet, D. A. Weitz, J. P. Butler, and J. J. Fredberg, “Physical forces during collective cell migration,” Nat. Phys. 5(6), 426–430 (2009).
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S. M. Rey, B. Považay, B. Hofer, A. Unterhuber, B. Hermann, A. Harwood, and W. Drexler, “Three- and four-dimensional visualization of cell migration using optical coherence tomography,” J. Biophotonics 2(6-7), 370–379 (2009).
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P. Friedl and D. Gilmour, “Collective cell migration in morphogenesis, regeneration and cancer,” Nat. Rev. Mol. Cell Biol. 10(7), 445–457 (2009).
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2008 (1)

K.-S. Lee and J. P. Rolland, “Bessel beam spectral-domain high-resolution optical coherence tomography with micro-optic axicon providing extended focusing range,” Opt. Lett. 33(15), 1696–1698 (2008).
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2007 (3)

T. S. Ralston, D. L. Marks, P. S. Carney, and S. A. Boppart, “Interferometric synthetic aperture microscopy,” Nat. Phys. 3(2), 129–134 (2007).
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F. C. Delori, R. H. Webb, and D. H. Sliney, “Maximum permissible exposures for ocular safety (ANSI 2000), with emphasis on ophthalmic devices,” J. Opt. Soc. Am. A 24(5), 1250–1265 (2007).
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A. G. Podoleanu, M. Seeger, G. M. Dobre, D. J. Webb, D. A. Jackson, and F. W. Fitzke, “Transversal and longitudinal images from the retina of the living eye using low coherence reflectometry,” J. Biomed. Opt. 3(1), 12–20 (1998).
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Supplementary Material (2)

Name	Description
Visualization 1	Volumetric visualization of fibroblast cell dynamics. The central part has 1mm × 1mm × 1mm field of view, and all the extracted parts have 0.25mm × 0.25mm × 0.25mm field of view.
Visualization 2	En face maximum intensity projection (400 µm slices) of fibroblast cell dynamics. Scale bar represents 50 µm for all sections.

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Fig. 1 System diagram for hybrid AO OCM. FC: 50-50 Fiber Coupler, PC: Polarization Controller, CL: Collimating Lens, M: Mirror, DM: Deformable Mirror, RP: Right-angle Prism, GMx and GMy: galvanometer mirror along x and y directions, OBJ: Objective Lens, S: Sample. All other unlabeled lenses are telescope pairs used for pupil conjugation.

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Fig. 2 Simulation results showing the depth-dependent incident beam intensity and reconstructed OCT signals for a Gaussian versus astigmatic beam. (a) Depth-dependent illumination profile obtained with the following beam types. Beam1: Gaussian beam illumination. Beam 2: Astigmatic beam with EPI. Beam 3: Astigmatic beam with EPII. (b) Reconstruction of depth-dependent collection profile with CAO. Signal A: Depth-dependent OCM signal from Beam 1. Signal B: CAO reconstruction of Signal A. Signal C: Depth-dependent OCM signal from Beam 3. Signal D: CAO reconstruction of Signal C. The dynamic range occupied by Gaussian and astigmatic beam is labelled on the right side.

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Fig. 3 Performance characterization of Gaussian versus astigmatic illumination beams in a resolution phantom, using ESI. (a-e) Comparison of cross-sectional energy distribution across depth, from maximum intensity projection of a 250μm slice. The bottom row is the depth-normalized version of the top row (method explained in Sect. 4.2), with (a) OCM with Gaussian beam, (b) CAO-OCM with Gaussian beam, (c) OCM with astigmatic beam, (d) CAO-OCM with astigmatic beam, and (e) focus scanning OCM fused from 18 volumes. Scale bars indicate 100 μm for all images. (f) Quantitative measurement of peak reconstructed OCT signal intensity. (g) FWHM resolution for hyAO and focus scanning OCM. Color-filled regions indicate ± one standard deviation. In (f) and (g), the depth axis matches the portion of the cross sectional images that are below the sample surface.

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Fig. 4 Comparison of cross sectional energy distribution across depth in grape imaging, from maximum intensity projection of a 10 μm slice, in EPI. (a) OCM with Gaussian beam, (b) CAO-OCM with Gaussian beam, (c) OCM with astigmatic beam, (d) CAO-OCM with astigmatic beam, (e) Focus scanning OCM fused from 18 volumes. The line plots indicate the normalized intensity profile in the image at four depths, labelled by arrows with corresponding color, with black dashed arrow representing the focal plane position for the standard Gaussian acquisition. All images are depth-normalized with the same method as in the phantom results in Fig. 3. Scale bars indicate 100 μm for all images. A gamma correction with γ = 0.7 was applied to all images.

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Fig. 5 Volumetric visualization of fibroblast cell dynamics. (a) the entire volume with 1 mm × 1mm × 1mm FOV, extracted from Supplementary Visualization 1. (b) cell exhibits upward motion in a 30 min duration, (c) cell exhibits rapid sideways motion in a 6 min duration. Both (b) and (c) cover a 0.25mm × 0.25mm × 0.25mm volume, with the initial time point indicated by the cyan channel and final time point by the red channel.

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Fig. 6 En face maximum intensity projection (400 μm slices) of fibroblast cell dynamics. (a) the entire 1mm × 1mm FOV, extracted from Supplementary Visualization 2. (b) cell extending filopodia across a 1 hour duration, (c) cell undergoing migration over a 263 minute period. Scale bar represents 50 μm for all groups.

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Tables (1)

Table 1 Summary of different illumination approaches used for comparing Gaussian and astigmatic beams in the simulation and experiments.

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Equations (7)

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I_{ill} (z; k) = = \frac{2 P_{inc}}{π w^{2} (z)},

g (x, y, z; k) = \iint_{- \infty}^{\infty} G (k_{x}, k_{y}, z = 0; k) e^{i ϕ (k_{x}, k_{y})} e^{i k_{z} z} e^{i (k_{x} x + k_{y} y)} d k_{x} d k_{y} .

h (x, y, z; k) = \sqrt{P_{inc}} g_{ill} (x, y, z; k) g_{col} (x, y, z; k) = \sqrt{P_{inc}} g^{2} (x, y, z; k)

H (k_{x}, k_{y}, z; k) = \iint_{- \infty}^{\infty} h (x, y, z; k) e^{- i (k_{x} x + k_{y} y)} d x d y

h_{ac} (x, y, z; k) = \iint_{- \infty}^{\infty} H (k_{x}, k_{y}, z; k) e^{i ϕ_{ac} (k_{x}, k_{y}, z)} e^{i (k_{x} x + k_{y} y)} d k_{x} d k_{y}

I_{rec} (z; k) \propto \max_{x, y} {{| h (x, y, z; k) |}^{2}},

I_{rec,ac} (z; k) \propto \max_{x, y} {{| h_{ac} (x, y, z; k) |}^{2}} .

		Incident power onto the sample	$I_{ill,max}$	$I_{rec,max}$
Equal peak intensity (EPII)	Gaussian beam	P₀/α (α⁻¹ laser power reduction)	$\propto P_{0}$	$\propto α P_{0}$
Equal peak intensity (EPII)	Astigmatic beam	P₀	$\propto P_{0}$	$\propto P_{0}$
Inter-mediate	Gaussian beam	P₀/α (attenuated by α)	$\propto P_{0}$	$\propto P_{0}$ (attenuated by α)
Inter-mediate	Astigmatic beam	P₀	$\propto P_{0}$	$\propto P_{0}$
Equivalent signal (ESI)	Gaussian beam	$P_{0} / \sqrt{α}$ (attenuated by α^1/2)	$\propto \sqrt{α} P_{0}$	$\propto α P_{0}$ (attenuated by α^1/2)
Equivalent signal (ESI)	Astigmatic beam	P₀	$\propto P_{0}$	$\propto P_{0}$
Equalpower (EPI)	Gaussian beam	P₀	$\propto α P_{0}$	$\propto α^{2} P_{0}$
Equalpower (EPI)	Astigmatic beam	P₀	$\propto P_{0}$	$\propto P_{0}$

Abstract

References

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