Abstract

Acoustic-resolution photoacoustic microscopy (ARPAM) plays an important role in studying the microcirculation system of biological tissues with deep penetration. High lateral resolution of ARPAM is achieved by using a high numerical aperture acoustic transducer. The deteriorated lateral resolution in the out-of-focus region can be alleviated by synthetic aperture focusing technique (SAFT). Previously, we reported a three-dimensional (3D) deconvolution ARPAM to improve both lateral and axial resolutions in the focus region. In this study, we present our extension of resolution enhancement to the out-of-focus region based on two-dimensional SAFT combined with the 3D deconvolution (SAFT+Deconv). In both the focus and out-of-focus regions, depth-independent lateral resolution provided by SAFT, together with inherently depth-independent axial resolution, ensures a depth-independent point spread function for 3D deconvolution algorithm. Imaging of 10 μm polymer beads shows that SAFT+Deconv ARPAM improves the −6 dB lateral resolutions from 65–700 μm to 20–29 μm, and the −6 dB axial resolutions from 35–42 μm to 12–19 μm in an extended depth of focus (DOF) of ∼2 mm. The signal-to-noise ratio is also increased by 6–30 dB. The resolution enhancement in three dimensions is validated by in vivo imaging of a mouse’s dorsal subcutaneous microvasculature. Our results suggest that SAFT+Deconv ARPAM may allow fine spatial resolution with deep penetration and extended DOF for biomedical photoacoustic applications.

© 2017 Optical Society of America

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References

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2016 (2)

K. H. Song, E. W. Stein, J. A. Margenthaler, and L. V. Wang, “Delay-multiply-and-sum-based synthetic aperture focusing in photoacoustic microscopy,” J. Biomed. Opt. 21(3), 036010 (2016).
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[Crossref] [PubMed]

2014 (3)

2013 (2)

J. Chen, R. Lin, H. Wang, J. Meng, H. Zheng, and L. Song, “Blind-deconvolution optical-resolution photoacoustic microscopy in vivo,” Opt. Express 59(2), 7316–7327 (2013).
[Crossref]

J. Kim, S. An, S. Ahn, and B. Kim, “Depth-variant deconvolution of 3D widefield fluorescence microscopy using the penalized maximum likelihood estimation method,” Opt. Express 21(23), 27668–27681 (2013).
[Crossref]

2012 (6)

Z. Deng, X. Yang, H. Gong, and Q. Luo, “Adaptive synthetic-aperture focusing technique for microvasculature imaging using photoacoustic microscopy,” Opt. Express 20(7), 7555–7563 (2012).
[Crossref] [PubMed]

R. Ma, S. Söntges, S. Shoham, V. Ntziachristos, and D. Razansky, “Fast scanning coaxial optoacoustic microscopy,” Biomed. Opt. Express 3(7), 1724–1731 (2012).
[Crossref] [PubMed]

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[Crossref] [PubMed]

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[Crossref] [PubMed]

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 0612091 (2012).
[Crossref]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

2011 (4)

Z. Deng, X. Yang, H. Gong, and Q. Luo, “Two-dimensional synthetic-aperture focusing technique in photoacoustic microscopy,” J. Appl. Phys. 109(10), 104701 (2011).
[Crossref]

M. Laasmaa, M. Vendelin, and P. Peterson, “Application of regularized Richardson Lucy algorithm for deconvolution of confocal microscopy images,” J. Microsc. 243(2), 124–140 (2011).
[Crossref] [PubMed]

K. Jansen, A. F. Van Der Steen, H. M. van Beusekom, J.W. Oosterhuis, and G. van Soest, “Intravascular photoacoustic imaging of human coronary atherosclerosis,” Opt. Lett. 36(5), 597–599 (2011).
[Crossref] [PubMed]

S.-L. Chen, Z. Xie, P. L. Carson, X. Wang, and L. J. Guo, “In vivo flow speed measurement of capillaries by photoacoustic correlation spectroscopy,” Opt. Lett. 36(20), 4017–4019 (2011).
[Crossref] [PubMed]

2010 (1)

V. Ntziachristos, “Going deeper than microscopy: the optical imaging frontier in biology,” Nat. Methods 7(8), 603–614 (2010).
[Crossref] [PubMed]

2009 (2)

2008 (3)

2006 (3)

2005 (1)

2004 (2)

1994 (1)

R. L. White, “Image restoration using the damped richardson-lucy method,” Proc. SPIE 2198, 1342–1348 (1994).
[Crossref]

1989 (1)

B. Piwakowski and B. Delannoy, “Method for computing spatial pulse response: Time-domain approach,” J. Acoust. Soc. Am. 86(6), 2422–2432 (1989).
[Crossref]

1974 (1)

L. B. Lucy, “An iterative technique for the rectification of observed distributions,” Astronomical J. 79, 745 (1974).
[Crossref]

1972 (1)

W. H. Richardson, “Bayesian-based iterative method of image restoration,” J. Opt. Soc. Am. A 62(1), 55–59 (1972).
[Crossref]

Ahn, S.

Allen, T. J.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 0612091 (2012).
[Crossref]

Amirian, J. H.

An, S.

Beard, P. C.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 0612091 (2012).
[Crossref]

Cai, D.

Cai, X.

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Carson, P. L.

Chen, J.

J. Chen, R. Lin, H. Wang, J. Meng, H. Zheng, and L. Song, “Blind-deconvolution optical-resolution photoacoustic microscopy in vivo,” Opt. Express 59(2), 7316–7327 (2013).
[Crossref]

Chen, R.

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Chen, S.-L.

Chen, Z.

P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
[Crossref] [PubMed]

Cheng, J.-X.

P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
[Crossref] [PubMed]

Conchello, J.-A.

Delannoy, B.

B. Piwakowski and B. Delannoy, “Method for computing spatial pulse response: Time-domain approach,” J. Acoust. Soc. Am. 86(6), 2422–2432 (1989).
[Crossref]

Deng, Z.

Z. Deng, X. Yang, H. Gong, and Q. Luo, “Adaptive synthetic-aperture focusing technique for microvasculature imaging using photoacoustic microscopy,” Opt. Express 20(7), 7555–7563 (2012).
[Crossref] [PubMed]

Z. Deng, X. Yang, H. Gong, and Q. Luo, “Two-dimensional synthetic-aperture focusing technique in photoacoustic microscopy,” J. Appl. Phys. 109(10), 104701 (2011).
[Crossref]

Dhillon, A. P.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 0612091 (2012).
[Crossref]

Emelianov, S. Y.

Estrada, H.

Favazza, C.

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Gong, H.

Z. Deng, X. Yang, H. Gong, and Q. Luo, “Adaptive synthetic-aperture focusing technique for microvasculature imaging using photoacoustic microscopy,” Opt. Express 20(7), 7555–7563 (2012).
[Crossref] [PubMed]

Z. Deng, X. Yang, H. Gong, and Q. Luo, “Two-dimensional synthetic-aperture focusing technique in photoacoustic microscopy,” J. Appl. Phys. 109(10), 104701 (2011).
[Crossref]

Gong, X.

Guo, L. J.

Hall, A.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 0612091 (2012).
[Crossref]

Hu, S.

Huang, H.

Hui, J.

P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
[Crossref] [PubMed]

Jansen, K.

Jensen, J. A.

S. I. Nikolov and J. A. Jensen, “3D synthetic aperture imaging using a virtual source element in the elevation plane,” in Proceedings of IEEE Conference on Ultrasonics (Institute of Electrical and Electronics Engineers, 2000), pp. 1743–1747.

Kim, B.

Kim, J.

Kneipp, M.

Laasmaa, M.

M. Laasmaa, M. Vendelin, and P. Peterson, “Application of regularized Richardson Lucy algorithm for deconvolution of confocal microscopy images,” J. Microsc. 243(2), 124–140 (2011).
[Crossref] [PubMed]

Li, M.-L.

Li, P.-C.

Li, Z.

Liang, S.

P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
[Crossref] [PubMed]

Liang, Y.

Liao, C.-K.

Lin, R.

W. Song, W. Zheng, R. Liu, R. Lin, H. Huang, X. Gong, S. Yang, R. Zhang, and L. Song, “Reflection-mode in vivo photoacoustic microscopy with subwavelength lateral resolution,” Biomed. Opt. Express 5(12), 4235–4241 (2014).
[Crossref]

J. Chen, R. Lin, H. Wang, J. Meng, H. Zheng, and L. Song, “Blind-deconvolution optical-resolution photoacoustic microscopy in vivo,” Opt. Express 59(2), 7316–7327 (2013).
[Crossref]

Litovsky, S. H.

Liu, R.

Liu, Y.

Lucy, L. B.

L. B. Lucy, “An iterative technique for the rectification of observed distributions,” Astronomical J. 79, 745 (1974).
[Crossref]

Luo, Q.

Z. Deng, X. Yang, H. Gong, and Q. Luo, “Adaptive synthetic-aperture focusing technique for microvasculature imaging using photoacoustic microscopy,” Opt. Express 20(7), 7555–7563 (2012).
[Crossref] [PubMed]

Z. Deng, X. Yang, H. Gong, and Q. Luo, “Two-dimensional synthetic-aperture focusing technique in photoacoustic microscopy,” J. Appl. Phys. 109(10), 104701 (2011).
[Crossref]

Ma, R.

Ma, T.

P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
[Crossref] [PubMed]

Margenthaler, J. A.

K. H. Song, E. W. Stein, J. A. Margenthaler, and L. V. Wang, “Delay-multiply-and-sum-based synthetic aperture focusing in photoacoustic microscopy,” J. Biomed. Opt. 21(3), 036010 (2016).
[Crossref]

K. H. Song, E. W. Stein, J. A. Margenthaler, and L. V. Wang, “Noninvasive photoacoustic identification of sentinel lymph nodes containing methylene blue in vivo in a rat model,” J. Biomed. Opt. 13(5), 054033 (2008).
[Crossref] [PubMed]

Maslov, K.

Meng, J.

J. Chen, R. Lin, H. Wang, J. Meng, H. Zheng, and L. Song, “Blind-deconvolution optical-resolution photoacoustic microscopy in vivo,” Opt. Express 59(2), 7316–7327 (2013).
[Crossref]

Mu, G.

Nikolov, S. I.

S. I. Nikolov and J. A. Jensen, “3D synthetic aperture imaging using a virtual source element in the elevation plane,” in Proceedings of IEEE Conference on Ultrasonics (Institute of Electrical and Electronics Engineers, 2000), pp. 1743–1747.

Ntziachristos, V.

Oosterhuis, J.W.

Owen, J. S.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 0612091 (2012).
[Crossref]

Peterson, P.

M. Laasmaa, M. Vendelin, and P. Peterson, “Application of regularized Richardson Lucy algorithm for deconvolution of confocal microscopy images,” J. Microsc. 243(2), 124–140 (2011).
[Crossref] [PubMed]

Piwakowski, B.

B. Piwakowski and B. Delannoy, “Method for computing spatial pulse response: Time-domain approach,” J. Acoust. Soc. Am. 86(6), 2422–2432 (1989).
[Crossref]

Preza, C.

Razansky, D.

Richardson, W. H.

W. H. Richardson, “Bayesian-based iterative method of image restoration,” J. Opt. Soc. Am. A 62(1), 55–59 (1972).
[Crossref]

Roy, S.

P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
[Crossref] [PubMed]

Sethuraman, S.

Shoham, S.

Shung, K. K.

P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Slipchenko, M. N.

P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
[Crossref] [PubMed]

Smalling, R. W.

Song, K. H.

K. H. Song, E. W. Stein, J. A. Margenthaler, and L. V. Wang, “Delay-multiply-and-sum-based synthetic aperture focusing in photoacoustic microscopy,” J. Biomed. Opt. 21(3), 036010 (2016).
[Crossref]

K. H. Song, E. W. Stein, J. A. Margenthaler, and L. V. Wang, “Noninvasive photoacoustic identification of sentinel lymph nodes containing methylene blue in vivo in a rat model,” J. Biomed. Opt. 13(5), 054033 (2008).
[Crossref] [PubMed]

Song, L.

W. Song, W. Zheng, R. Liu, R. Lin, H. Huang, X. Gong, S. Yang, R. Zhang, and L. Song, “Reflection-mode in vivo photoacoustic microscopy with subwavelength lateral resolution,” Biomed. Opt. Express 5(12), 4235–4241 (2014).
[Crossref]

J. Chen, R. Lin, H. Wang, J. Meng, H. Zheng, and L. Song, “Blind-deconvolution optical-resolution photoacoustic microscopy in vivo,” Opt. Express 59(2), 7316–7327 (2013).
[Crossref]

Song, W.

Söntges, S.

Stein, E. W.

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K. H. Song, E. W. Stein, J. A. Margenthaler, and L. V. Wang, “Delay-multiply-and-sum-based synthetic aperture focusing in photoacoustic microscopy,” J. Biomed. Opt. 21(3), 036010 (2016).
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P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
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K. H. Song, E. W. Stein, J. A. Margenthaler, and L. V. Wang, “Delay-multiply-and-sum-based synthetic aperture focusing in photoacoustic microscopy,” J. Biomed. Opt. 21(3), 036010 (2016).
[Crossref]

K. H. Song, E. W. Stein, J. A. Margenthaler, and L. V. Wang, “Noninvasive photoacoustic identification of sentinel lymph nodes containing methylene blue in vivo in a rat model,” J. Biomed. Opt. 13(5), 054033 (2008).
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M. Laasmaa, M. Vendelin, and P. Peterson, “Application of regularized Richardson Lucy algorithm for deconvolution of confocal microscopy images,” J. Microsc. 243(2), 124–140 (2011).
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H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[Crossref] [PubMed]

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J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
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L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
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Opt. Express (5)

Opt. Lett. (7)

Proc. SPIE (1)

R. L. White, “Image restoration using the damped richardson-lucy method,” Proc. SPIE 2198, 1342–1348 (1994).
[Crossref]

Sci. Rep. (1)

P. Wang, T. Ma, M. N. Slipchenko, S. Liang, J. Hui, K. K. Shung, S. Roy, M. Sturek, Q. Zhou, Z. Chen, and J.-X. Cheng, “High-speed intravascular photoacoustic imaging of lipid-laden atherosclerotic plaque enabled by a 2-khz barium nitrite raman laser,” Sci. Rep. 4, 6889 (2014).
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L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012).
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S. I. Nikolov and J. A. Jensen, “3D synthetic aperture imaging using a virtual source element in the elevation plane,” in Proceedings of IEEE Conference on Ultrasonics (Institute of Electrical and Electronics Engineers, 2000), pp. 1743–1747.

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Figures (9)

Fig. 1
Fig. 1 Schematic of 2D SAFT.
Fig. 2
Fig. 2 XY MAPs of the object at seven positions: (a) Original images, (b) 2D SAFT images, and (c) SAFT+Deconv images. The middle object (#4) is placed in the focal zone, the other six objects are placed above (#1–#3) and below (#5–#7) the focal zone. The scale in (a) is 200 μm, while the scales in (b) and (c) are 50 μm for better visualization.
Fig. 3
Fig. 3 Profile analysis of three images (#7) along red dashed lines in Fig. 2.
Fig. 4
Fig. 4 XY MAPs of five 25-μm tungsten wires: (a) Original image, (b) 2D SAFT image, and (c) SAFT+Deconv image.
Fig. 5
Fig. 5 YZ MAPs of five 25-μm tungsten wires: (a) Original image, (b) 2D SAFT image, and (c) SAFT+Deconv image.
Fig. 6
Fig. 6 (a) Lateral profile along the line L1 in Fig. 4. (b) Axial profile along the line L3 in Fig. 5. (c)–(e) XZ cross-sectional images from the region labeled by the line L3 in Fig. 5.
Fig. 7
Fig. 7 3D rendering display of five 25-μm tungsten wires: (a) Original image, (b) 2D SAFT image, and (c) SAFT+Deconv image.
Fig. 8
Fig. 8 XY MAPs of in vivo imaging of a mouse’s dorsal subcutaneous vessels: (a) Original image, (b) 2D SAFT image, (c) SAFT+Deconv image, (d) Deconvolution image, and (e) Depth-encoded XY MAP.
Fig. 9
Fig. 9 (a)–(c) are XZ cross-sectional images from slices labeled by white dashed lines L1 in Figs. 8(a)–8(c), respectively.

Tables (1)

Tables Icon

Table 1 Resolutions and SNR improvements in SAFT+Deconv ARPAM

Equations (5)

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S SAFT ( x i , y j , t i j ) = i , j = 1 circle S ( x i , y j , t i j Δ t i j ) SIR ( x i x i , y j y j , t i j ) ,
CF ( x i , y j , t i j ) = | i , j = 1 circle S ( x i , y j , t i j Δ t i j ) SIR ( x i x i , y j y j , t i j ) | 2 N i , j = 1 circle | S ( x i , y j , t i j Δ t i j ) SIR ( x i x i , y j y j , t i j ) | 2 ,
S SAFT _ CT ( x i , y j , t i j ) = S SAFT ( x i , y j , t i j ) CF ( x i , y j , t i j ) .
g ( x , y , z ) = h ( x , y , z ) o ( x , y , z ) + n ( x , y , z ) ,
o i + 1 ( x , y , z ) = [ g ( x , y , z ) h ( x , y , z ) o i ( x , y , z ) h ( x , y , z ) ] o i ( x , y , z ) ,

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