Abstract

In deep tissue photoacoustic imaging, the spatial resolution is inherently limited by acoustic diffraction. Moreover, as the ultrasound attenuation increases with frequency, resolution is often traded off for penetration depth. Here, we report on super-resolution photoacoustic imaging by use of multiple speckle illumination. Specifically, we demonstrate experimentally that the analysis of second-order fluctuations of the photoacoustic images enables the resolution of optically absorbing structures beyond the acoustic diffraction limit, with a resolution enhancement of about 1.4. In addition, deconvolution was implemented to fully exploit the highest spatial frequencies available and resulted in an effective resolution enhancement of at least 1.6 in the lateral direction. Our method introduces a new framework that could potentially lead to deep tissue photoacoustic imaging with subacoustic resolution.

© 2016 Optical Society of America

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References

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H. Roitner, M. Haltmeier, R. Nuster, D. P. O’Leary, T. Berer, G. Paltauf, H. Grün, and P. Burgholzer, J. Biomed. Opt. 19, 056011 (2014).
[Crossref]

T. Chaigne, O. Katz, A. Boccara, M. Fink, E. Bossy, and S. Gigan, Nat. Photonics 8, 58 (2014).
[Crossref]

L. Wang, C. Zhang, and L. V. Wang, Phys. Rev. Lett. 113, 174301 (2014).
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2013 (3)

2012 (1)

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[Crossref]

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Boccara, A.

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Bossy, E.

T. Chaigne, O. Katz, A. Boccara, M. Fink, E. Bossy, and S. Gigan, Nat. Photonics 8, 58 (2014).
[Crossref]

J. Gateau, T. Chaigne, O. Katz, S. Gigan, and E. Bossy, Opt. Lett. 38, 5188 (2013).
[Crossref]

Burgholzer, P.

H. Roitner, M. Haltmeier, R. Nuster, D. P. O’Leary, T. Berer, G. Paltauf, H. Grün, and P. Burgholzer, J. Biomed. Opt. 19, 056011 (2014).
[Crossref]

Caravaca-Aguirre, A. M.

Chaigne, T.

T. Chaigne, O. Katz, A. Boccara, M. Fink, E. Bossy, and S. Gigan, Nat. Photonics 8, 58 (2014).
[Crossref]

J. Gateau, T. Chaigne, O. Katz, S. Gigan, and E. Bossy, Opt. Lett. 38, 5188 (2013).
[Crossref]

Chen, R.

Cho, Y.-W.

Chung, E.

Colyer, R.

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, Proc. Natl. Acad. Sci. U.S.A. 106, 22287 (2009).
[Crossref]

Conkey, D. B.

Danielli, A.

Dertinger, T.

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, Proc. Natl. Acad. Sci. U.S.A. 106, 22287 (2009).
[Crossref]

Dove, J. D.

Enderlein, J.

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, Proc. Natl. Acad. Sci. U.S.A. 106, 22287 (2009).
[Crossref]

Fink, M.

T. Chaigne, O. Katz, A. Boccara, M. Fink, E. Bossy, and S. Gigan, Nat. Photonics 8, 58 (2014).
[Crossref]

Gateau, J.

Gigan, S.

T. Chaigne, O. Katz, A. Boccara, M. Fink, E. Bossy, and S. Gigan, Nat. Photonics 8, 58 (2014).
[Crossref]

J. Gateau, T. Chaigne, O. Katz, S. Gigan, and E. Bossy, Opt. Lett. 38, 5188 (2013).
[Crossref]

Grün, H.

H. Roitner, M. Haltmeier, R. Nuster, D. P. O’Leary, T. Berer, G. Paltauf, H. Grün, and P. Burgholzer, J. Biomed. Opt. 19, 056011 (2014).
[Crossref]

Haltmeier, M.

H. Roitner, M. Haltmeier, R. Nuster, D. P. O’Leary, T. Berer, G. Paltauf, H. Grün, and P. Burgholzer, J. Biomed. Opt. 19, 056011 (2014).
[Crossref]

Hu, S.

L. V. Wang and S. Hu, Science 335, 1458 (2012).
[Crossref]

Huynh, E.

K. K. Ng, M. Shakiba, E. Huynh, R. A. Weersink, A. Roxin, B. C. Wilson, and G. Zheng, ACS Nano 8, 8363 (2014).
[Crossref]

Iyer, G.

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, Proc. Natl. Acad. Sci. U.S.A. 106, 22287 (2009).
[Crossref]

Jang, M.

Ju, H.

Judkewitz, B.

Katz, O.

T. Chaigne, O. Katz, A. Boccara, M. Fink, E. Bossy, and S. Gigan, Nat. Photonics 8, 58 (2014).
[Crossref]

J. Gateau, T. Chaigne, O. Katz, S. Gigan, and E. Bossy, Opt. Lett. 38, 5188 (2013).
[Crossref]

Kim, Y.-H.

Lai, P.

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, Nat. Photonics 9, 126 (2015).
[Crossref]

Li, C.

C. Zhang, C. Li, and L. V. Wang, IEEE Photon. J. 2, 57 (2010).
[Crossref]

Maslov, K.

Murray, T. W.

Ng, K. K.

K. K. Ng, M. Shakiba, E. Huynh, R. A. Weersink, A. Roxin, B. C. Wilson, and G. Zheng, ACS Nano 8, 8363 (2014).
[Crossref]

Ntziachristos, V.

Nuster, R.

H. Roitner, M. Haltmeier, R. Nuster, D. P. O’Leary, T. Berer, G. Paltauf, H. Grün, and P. Burgholzer, J. Biomed. Opt. 19, 056011 (2014).
[Crossref]

O’Leary, D. P.

H. Roitner, M. Haltmeier, R. Nuster, D. P. O’Leary, T. Berer, G. Paltauf, H. Grün, and P. Burgholzer, J. Biomed. Opt. 19, 056011 (2014).
[Crossref]

Oh, J.-E.

Omar, M.

Paltauf, G.

H. Roitner, M. Haltmeier, R. Nuster, D. P. O’Leary, T. Berer, G. Paltauf, H. Grün, and P. Burgholzer, J. Biomed. Opt. 19, 056011 (2014).
[Crossref]

Piestun, R.

Rao, B.

Roitner, H.

H. Roitner, M. Haltmeier, R. Nuster, D. P. O’Leary, T. Berer, G. Paltauf, H. Grün, and P. Burgholzer, J. Biomed. Opt. 19, 056011 (2014).
[Crossref]

Roxin, A.

K. K. Ng, M. Shakiba, E. Huynh, R. A. Weersink, A. Roxin, B. C. Wilson, and G. Zheng, ACS Nano 8, 8363 (2014).
[Crossref]

Ruan, H.

Scarcelli, G.

Shakiba, M.

K. K. Ng, M. Shakiba, E. Huynh, R. A. Weersink, A. Roxin, B. C. Wilson, and G. Zheng, ACS Nano 8, 8363 (2014).
[Crossref]

Shung, K. K.

Soliman, D.

Tay, J. W.

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, Nat. Photonics 9, 126 (2015).
[Crossref]

Vellekoop, I. M.

Wang, L.

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, Nat. Photonics 9, 126 (2015).
[Crossref]

L. Wang, C. Zhang, and L. V. Wang, Phys. Rev. Lett. 113, 174301 (2014).
[Crossref]

Wang, L. V.

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, Nat. Photonics 9, 126 (2015).
[Crossref]

L. Wang, C. Zhang, and L. V. Wang, Phys. Rev. Lett. 113, 174301 (2014).
[Crossref]

L. V. Wang and S. Hu, Science 335, 1458 (2012).
[Crossref]

B. Rao, K. Maslov, A. Danielli, R. Chen, K. K. Shung, Q. Zhou, and L. V. Wang, Opt. Lett. 36, 1137 (2011).
[Crossref]

C. Zhang, C. Li, and L. V. Wang, IEEE Photon. J. 2, 57 (2010).
[Crossref]

Weersink, R. A.

K. K. Ng, M. Shakiba, E. Huynh, R. A. Weersink, A. Roxin, B. C. Wilson, and G. Zheng, ACS Nano 8, 8363 (2014).
[Crossref]

Weiss, S.

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, Proc. Natl. Acad. Sci. U.S.A. 106, 22287 (2009).
[Crossref]

Wilson, B. C.

K. K. Ng, M. Shakiba, E. Huynh, R. A. Weersink, A. Roxin, B. C. Wilson, and G. Zheng, ACS Nano 8, 8363 (2014).
[Crossref]

Yang, C.

Zhang, C.

L. Wang, C. Zhang, and L. V. Wang, Phys. Rev. Lett. 113, 174301 (2014).
[Crossref]

C. Zhang, C. Li, and L. V. Wang, IEEE Photon. J. 2, 57 (2010).
[Crossref]

Zheng, G.

K. K. Ng, M. Shakiba, E. Huynh, R. A. Weersink, A. Roxin, B. C. Wilson, and G. Zheng, ACS Nano 8, 8363 (2014).
[Crossref]

Zhou, Q.

ACS Nano (1)

K. K. Ng, M. Shakiba, E. Huynh, R. A. Weersink, A. Roxin, B. C. Wilson, and G. Zheng, ACS Nano 8, 8363 (2014).
[Crossref]

Biomed. Opt. Express (1)

IEEE Photon. J. (1)

C. Zhang, C. Li, and L. V. Wang, IEEE Photon. J. 2, 57 (2010).
[Crossref]

Interface Focus (1)

P. Beard, Interface Focus 1, 602 (2011).
[Crossref]

J. Biomed. Opt. (1)

H. Roitner, M. Haltmeier, R. Nuster, D. P. O’Leary, T. Berer, G. Paltauf, H. Grün, and P. Burgholzer, J. Biomed. Opt. 19, 056011 (2014).
[Crossref]

Nat. Photonics (2)

T. Chaigne, O. Katz, A. Boccara, M. Fink, E. Bossy, and S. Gigan, Nat. Photonics 8, 58 (2014).
[Crossref]

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, Nat. Photonics 9, 126 (2015).
[Crossref]

Opt. Express (1)

Opt. Lett. (4)

Phys. Rev. Lett. (1)

L. Wang, C. Zhang, and L. V. Wang, Phys. Rev. Lett. 113, 174301 (2014).
[Crossref]

Proc. Natl. Acad. Sci. U.S.A. (1)

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, Proc. Natl. Acad. Sci. U.S.A. 106, 22287 (2009).
[Crossref]

Science (1)

L. V. Wang and S. Hu, Science 335, 1458 (2012).
[Crossref]

Other (1)

M. Bertero and P. Boccacci, Introduction to Inverse Problems in Imaging (CRC Press, 1998).

Supplementary Material (1)

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Figures (5)

Fig. 1.
Fig. 1.

Experimental setup. A 5 ns laser pulse is focused onto a rotating diffuser. Each resulting speckle pattern (scale bar 200 μm, speckle grain size 30 μm ) illuminates a collection of absorbing beads, generating ultrasound detected with a linear ultrasonic array.

Fig. 2.
Fig. 2.

(a) Photograph of sample 1 (randomly positioned 100 μm diameter beads). (b) Mean PA image over 100 speckle realizations, mimicking uniform illumination. Inset: mean PA image of a single isolated bead. (c) Variance image over 100 speckle realizations. Inset: variance image of a single isolated bead. Scale bars: 300 μm.

Fig. 3.
Fig. 3.

(a) Photograph of sample 2. The distances between 100 μm diameter beads (center to center) were 120, 140, and 200 μm along the z direction (from top to bottom), and 250, 200, and 160 μm along the x direction (from left to right). The four 50 μm diameter beads used to estimate the PSF are also slightly visible (see Fig. S1 in Supplement 1). (b) Mean PA image over 100 speckle realizations, mimicking uniform illumination. (c) Square root of the variance image over 100 speckle realizations. Scale bars: 500 μm.

Fig. 4.
Fig. 4.

(a) Mean image deconvolved by the PSF; white dashed lines indicates the cross-sections. (b) Square root of the variance image deconvolved by the squared PSF. (c) Horizontal cross-sections: deconvolved mean image (blue) and square root of deconvolved variance image (red). (d) Vertical cross-sections: deconvolved mean image (blue) and square root of deconvolved variance image (red). Scale bars: 500 μm.

Fig. 5.
Fig. 5.

(a) Mean image deconvolved by the PSF. (b) Square root of the variance image deconvolved by the squared PSF; white dashed lines indicate the cross-section direction. (c) Photograph of sample 3. (d) Cross-sections. Blue curve, mean image; red curve, square root of variance image. Scale bars: 200 μm.

Equations (4)

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A ( r ) = [ μ a ( r ) × I ( r ) ] * h ( r ) ,
A ( r ) = I 0 × [ μ a ( r ) * h ( r ) ] ,
σ 2 [ A ] ( r ) μ a 2 ( r ) * h 2 ( r ) .
J ( x ) : = h 2 * x σ 2 [ A ] ^ 2 + α x 2 subject to x 0 ,

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