Abstract

We have developed an adaptive optics photoacoustic microscope (AO-PAM) for high-resolution imaging of biological tissues, especially the retina. To demonstrate the feasibility of AO-PAM we first designed the AO system to correct the wavefront errors of the illuminating light of PAM. The aberrations of the optical system delivering the illuminating light to the sample in PAM was corrected with a close-loop AO system consisting of a 141-element MEMS-based deformable mirror (DM) and a Shack-Hartmann (SH) wavefront sensor operating at 15 Hz. The photoacoustic signal induced by the illuminating laser beam was detected by a custom-built needle ultrasonic transducer. When the wavefront errors were corrected by the AO system, the lateral resolution of PAM was measured to be better than 2.5 µm using a low NA objective lens. We tested the system on imaging ex vivo ocular samples, e.g., the ciliary body and retinal pigment epithelium (RPE) of a pig eye. The AO-PAM images showed significant quality improvement. For the first time we were able to resolve single RPE cells with PAM.

© 2010 OSA

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2010 (6)

2009 (3)

2008 (3)

2007 (4)

2006 (6)

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Imaging acute thermal burns by photoacoustic microscopy,” J. Biomed. Opt. 11(5), 054033 (2006).
[CrossRef] [PubMed]

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]

Y. Zhang, S. Poonja, and A. Roorda, “MEMS-based adaptive optics scanning laser ophthalmoscopy,” Opt. Lett. 31(9), 1268–1270 (2006).
[CrossRef] [PubMed]

D. Merino, C. Dainty, A. Bradu, and A. G. Podoleanu, “Adaptive optics enhanced simultaneous en-face optical coherence tomography and scanning laser ophthalmoscopy,” Opt. Express 14(8), 3345–3353 (2006), http://www.opticsinfobase.org/oe/abstract.cfm?URI=oe-14-8-3345 .
[CrossRef] [PubMed]

D. X. Hammer, R. D. Ferguson, C. E. Bigelow, N. V. Iftimia, T. E. Ustun, and S. A. Burns, “Adaptive optics scanning laser ophthalmoscope for stabilized retinal imaging,” Opt. Express 14(8), 3354–3367 (2006), http://www.opticsinfobase.org/abstract.cfm?id=89323&CFID=113107704&CFTOKEN=11132256 .
[CrossRef] [PubMed]

Y. Zhang, B. Cense, J. Rha, R. S. Jonnal, W. Gao, R. J. Zawadzki, J. S. Werner, S. Jones, S. Olivier, and D. T. Miller, “High-speed volumetric imaging of cone photoreceptors with adaptive optics spectral-domain optical coherence tomography,” Opt. Express 14(10), 4380–4394 (2006), http://www.opticsinfobase.org/abstract.cfm?id=89918&CFID=113107704&CFTOKEN=11132256 .
[CrossRef] [PubMed]

2005 (2)

2004 (1)

2003 (1)

2002 (3)

A. Roorda, F. Romero-Borja, W. Donnelly Iii, H. Queener, T. Hebert, and M. Campbell, “Adaptive optics scanning laser ophthalmoscopy,” Opt. Express 10(9), 405–412 (2002), http://www.opticsinfobase.org/abstract.cfm?URI=OE-10-9-405 .
[PubMed]

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[CrossRef] [PubMed]

M. J. Booth, M. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[CrossRef] [PubMed]

2001 (2)

P. Artal, A. Guirao, E. Berrio, and D. R. Williams, “Compensation of corneal aberrations by the internal optics in the human eye,” J. Vis. 1(1), 1–8 (2001).
[CrossRef]

E. J. Fernández, I. Iglesias, and P. Artal, “Closed-loop adaptive optics in the human eye,” Opt. Lett. 26(10), 746–748 (2001).
[CrossRef]

1997 (2)

Albert, O.

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[CrossRef] [PubMed]

Artal, P.

Ballesta, J.

J. W. Cha, J. Ballesta, and P. T. C. So, “Shack-Hartmann wavefront-sensor-based adaptive optics system for multiphoton microscopy,” J. Biomed. Opt. 15(4), 046022 (2010).
[CrossRef] [PubMed]

Berrio, E.

P. Artal, A. Guirao, E. Berrio, and D. R. Williams, “Compensation of corneal aberrations by the internal optics in the human eye,” J. Vis. 1(1), 1–8 (2001).
[CrossRef]

Bigelow, C. E.

Booth, M. J.

M. J. Booth, M. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[CrossRef] [PubMed]

Bower, B. A.

Bradu, A.

Burns, D.

Burns, S. A.

Campbell, M.

Cense, B.

Cha, J. W.

J. W. Cha, J. Ballesta, and P. T. C. So, “Shack-Hartmann wavefront-sensor-based adaptive optics system for multiphoton microscopy,” J. Biomed. Opt. 15(4), 046022 (2010).
[CrossRef] [PubMed]

Choi, S.

Choi, S. S.

Chui, T. Y.

Dainty, C.

Donnelly Iii, W.

Drexler, W.

Elsner, A. E.

Evans, J. W.

Fawzi, A.

Fercher, A. F.

Ferguson, D.

Ferguson, R. D.

Fernández, E. J.

Gao, W.

Girkin, J.

Girkin, J. M.

J. M. Girkin, S. Poland, and A. J. Wright, “Adaptive optics for deeper imaging of biological samples,” Curr. Opin. Biotechnol. 20(1), 106–110 (2009).
[CrossRef] [PubMed]

Guirao, A.

P. Artal, A. Guirao, E. Berrio, and D. R. Williams, “Compensation of corneal aberrations by the internal optics in the human eye,” J. Vis. 1(1), 1–8 (2001).
[CrossRef]

Hammer, D. X.

Hebert, T.

Hermann, B.

Hitzenberger, C. K.

Hu, J.

Hu, S.

Iftimia, N. V.

Iglesias, I.

Izatt, J. A.

Jiang, M.

Jiao, S.

Jones, S.

Jones, S. M.

Jonnal, R.

Jonnal, R. S.

Juskaitis, R.

M. J. Booth, M. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[CrossRef] [PubMed]

Kurokawa, K.

Laut, S.

Li, K. Y.

Li, L.

Liang, J.

Liu, T.

Makita, S.

Marsh, P.

Maslov, K.

B. Rao, L. Li, K. Maslov, and L. Wang, “Hybrid-scanning optical-resolution photoacoustic microscopy for in vivo vasculature imaging,” Opt. Lett. 35(10), 1521–1523 (2010).
[CrossRef] [PubMed]

K. Maslov, H. F. Zhang, S. Hu, and L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protoc. 2(4), 797–804 (2007).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Imaging acute thermal burns by photoacoustic microscopy,” J. Biomed. Opt. 11(5), 054033 (2006).
[CrossRef] [PubMed]

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]

Merino, D.

Miller, D.

Miller, D. T.

Neil, M. A.

M. J. Booth, M. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[CrossRef] [PubMed]

Norris, T. B.

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[CrossRef] [PubMed]

Oliver, S. S.

Olivier, S.

Olivier, S. S.

Pircher, M.

Podoleanu, A. G.

Poland, S.

J. M. Girkin, S. Poland, and A. J. Wright, “Adaptive optics for deeper imaging of biological samples,” Curr. Opin. Biotechnol. 20(1), 106–110 (2009).
[CrossRef] [PubMed]

Poonja, S.

Prieto, P. M.

Puliafito, C. A.

Queener, H.

Rao, B.

Rha, J.

Romero-Borja, F.

Roorda, A.

Sasaki, K.

Sattmann, H.

Sherman, L.

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[CrossRef] [PubMed]

Shung, K. K.

So, P. T. C.

J. W. Cha, J. Ballesta, and P. T. C. So, “Shack-Hartmann wavefront-sensor-based adaptive optics system for multiphoton microscopy,” J. Biomed. Opt. 15(4), 046022 (2010).
[CrossRef] [PubMed]

Song, H.

Stoica, G.

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]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Imaging acute thermal burns by photoacoustic microscopy,” J. Biomed. Opt. 11(5), 054033 (2006).
[CrossRef] [PubMed]

Tumbar, R.

Unterhuber, A.

Ustun, T. E.

Wang, J.

Wang, L.

Wang, L. V.

S. Hu and L. V. Wang, “Photoacoustic imaging and characterization of the microvasculature,” J. Biomed. Opt. 15(1), 011101 (2010).
[CrossRef] [PubMed]

K. Maslov, H. F. Zhang, S. Hu, and L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protoc. 2(4), 797–804 (2007).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Imaging acute thermal burns by photoacoustic microscopy,” J. Biomed. Opt. 11(5), 054033 (2006).
[CrossRef] [PubMed]

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]

Wei, Q.

Werner, J. S.

Williams, D. R.

Wilson, T.

M. J. Booth, M. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[CrossRef] [PubMed]

Wright, A. J.

J. M. Girkin, S. Poland, and A. J. Wright, “Adaptive optics for deeper imaging of biological samples,” Curr. Opin. Biotechnol. 20(1), 106–110 (2009).
[CrossRef] [PubMed]

Xie, Z.

Yamanari, M.

Yasuno, Y.

Ye, J. Y.

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[CrossRef] [PubMed]

Zawadzki, R. J.

Zhang, H. F.

H. F. Zhang, J. Wang, Q. Wei, T. Liu, S. Jiao, and C. A. Puliafito, “Collecting back-reflected photons in photoacoustic microscopy,” Opt. Express 18(2), 1278–1282 (2010), http://www.opticsinfobase.org/abstract.cfm?URI=oe-18-2-1278 .
[CrossRef] [PubMed]

S. Jiao, M. Jiang, J. Hu, A. Fawzi, Q. Zhou, K. K. Shung, C. A. Puliafito, and H. F. Zhang, “Photoacoustic ophthalmoscopy for in vivo retinal imaging,” Opt. Express 18(4), 3967–3972 (2010), http://www.opticsinfobase.org/abstract.cfm?URI=oe-18-4-3967 .
[CrossRef] [PubMed]

S. Jiao, Z. Xie, H. F. Zhang, and C. A. Puliafito, “Simultaneous multimodal imaging with integrated photoacoustic microscopy and optical coherence tomography,” Opt. Lett. 34(19), 2961–2963 (2009).
[CrossRef] [PubMed]

Z. Xie, S. Jiao, H. F. Zhang, and C. A. Puliafito, “Laser-scanning optical-resolution photoacoustic microscopy,” Opt. Lett. 34(12), 1771–1773 (2009).
[CrossRef] [PubMed]

K. Maslov, H. F. Zhang, S. Hu, and L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protoc. 2(4), 797–804 (2007).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Imaging acute thermal burns by photoacoustic microscopy,” J. Biomed. Opt. 11(5), 054033 (2006).
[CrossRef] [PubMed]

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]

Zhang, Y.

Zhao, M.

Zhou, Q.

Curr. Opin. Biotechnol. (1)

J. M. Girkin, S. Poland, and A. J. Wright, “Adaptive optics for deeper imaging of biological samples,” Curr. Opin. Biotechnol. 20(1), 106–110 (2009).
[CrossRef] [PubMed]

J. Biomed. Opt. (3)

J. W. Cha, J. Ballesta, and P. T. C. So, “Shack-Hartmann wavefront-sensor-based adaptive optics system for multiphoton microscopy,” J. Biomed. Opt. 15(4), 046022 (2010).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Imaging acute thermal burns by photoacoustic microscopy,” J. Biomed. Opt. 11(5), 054033 (2006).
[CrossRef] [PubMed]

S. Hu and L. V. Wang, “Photoacoustic imaging and characterization of the microvasculature,” J. Biomed. Opt. 15(1), 011101 (2010).
[CrossRef] [PubMed]

J. Microsc. (1)

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[CrossRef] [PubMed]

J. Opt. Soc. Am. A (6)

J. Vis. (1)

P. Artal, A. Guirao, E. Berrio, and D. R. Williams, “Compensation of corneal aberrations by the internal optics in the human eye,” J. Vis. 1(1), 1–8 (2001).
[CrossRef]

Nat. Biotechnol. (1)

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]

Nat. Protoc. (1)

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protoc. 2(4), 797–804 (2007).
[CrossRef] [PubMed]

Opt. Express (10)

A. Roorda, F. Romero-Borja, W. Donnelly Iii, H. Queener, T. Hebert, and M. Campbell, “Adaptive optics scanning laser ophthalmoscopy,” Opt. Express 10(9), 405–412 (2002), http://www.opticsinfobase.org/abstract.cfm?URI=OE-10-9-405 .
[PubMed]

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

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Other (2)

Thorlabs, “Operation Manual of AOkit,” http://www.thorlabs.com/NewGroupPage9.cfm?ObjectGroup_ID=3208

Thorlabs, “Operation Manual of Optical Wavefront Sensor,” http://www.thorlabs.com/NewGroupPage9.cfm?ObjectGroup_ID=2946

Supplementary Material (1)

» Media 1: MPG (1842 KB)     

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Figures (5)

Fig. 1
Fig. 1

Schematic of the experimental AO-PAM system. ND: neutral density filter; PD: photodiode; D: diaphragm; L1-L4: achromatic lenses; DM: deformable mirror; SH: Shack-Hartmann wavefront sensor; BS: pellicle beamsplitter (reflection: 8%, transmission 92%); UT: ultrasonic transducer.

Fig. 2
Fig. 2

(a) The first four order Zernike coefficients without/within AO, (b) corresponding PSF without AO, (c) corresponding PSF with AO.

Fig. 3
Fig. 3

(a) – (c) Images of Group 6 and 7 of the USAF 1951 Chart: (a) Light microscopy image, (b) MAP of the PAM image without AO, (c) MAP of the PAM image of the same target with AO. d: measured edge response; e: PSF calculated from the data in (d) without AO; f: PSF calculated from the data in (d) with AO.

Fig. 4
Fig. 4

MAP of the PAM images of the ciliary body of a pig eye: (a) without AO, (b) with AO, (c) (Media 1) 3D rendering of the PAM data set. The area outlined in each image was enlarged and shown as pointed by the arrows.

Fig. 5
Fig. 5

MAP of the PAM images of the RPE of the pig eye: (a) without AO, (b) with AO.

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