Abstract

Aberrations and random scattering severely limit optical imaging in deep tissue. Adaptive optics can in principle drastically extend the penetration depth and improve the image quality. However, for random scattering media a large number of spatial modes need to be measured and controlled to restore a diffraction limited focus. Here, we present a parallel wavefront optimization method using backscattered light as a feedback. Spatial confinement of the feedback signal is realized with a confocal pinhole and coherence gating. We show in simulations and experiments that this approach enables focusing deep into tissue over up to six mean scattering path lengths. Experimentally the technique was tested on tissue phantoms and fixed brain slices.

© 2012 Optical Society of America

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2012 (2)

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
[CrossRef] [PubMed]

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).
[CrossRef] [PubMed]

2011 (2)

M. Cui, “Parallel wavefront optimization method for focusing light through random scattering media,” Opt. Lett. 36(6), 870–872 (2011).
[CrossRef] [PubMed]

D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
[CrossRef] [PubMed]

2010 (2)

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]

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]

2009 (2)

M. Cui, E. J. McDowell, and C. Yang, “Observation of polarization-gate based reconstruction quality improvement during the process of turbidity suppression by optical phase conjugation,” Appl. Phys. Lett. 95(12), 123702 (2009).
[CrossRef] [PubMed]

B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in light microscopy for neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
[CrossRef] [PubMed]

2007 (1)

M. Pircher and R. J. Zawadzki, “Combining adaptive optics with optical coherence tomography: unveiling the cellular structure of the human retina in vivo,” Expert Rev. Ophthalmol. 2(6), 1019–1035 (2007).
[CrossRef]

2006 (1)

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[CrossRef] [PubMed]

2005 (1)

P. H. Tomlins and R. K. Wang, “Theory, developments and applications of optical coherence tomography,” J. Phys. D. 38(15), 2519–2535 (2005).
[CrossRef]

2004 (1)

J. Mertz, “Nonlinear microscopy: new techniques and applications,” Curr. Opin. Neurobiol. 14(5), 610–616 (2004).
[CrossRef] [PubMed]

2003 (3)

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[CrossRef] [PubMed]

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys. 66(2), 239–303 (2003).
[CrossRef]

P. Marsh, D. Burns, and J. Girkin, “Practical implementation of adaptive optics in multiphoton microscopy,” Opt. Express 11(10), 1123–1130 (2003).
[CrossRef] [PubMed]

2002 (1)

M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A. F. Fercher, “In vivo human retinal imaging by Fourier domain optical coherence tomography,” J. Biomed. Opt. 7(3), 457–463 (2002).
[CrossRef] [PubMed]

2000 (1)

M. A. A. Neil, R. Juškaitis, M. J. Booth, T. Wilson, T. Tanaka, and S. Kawata, “Adaptive aberration correction in a two-photon microscope,” J. Microsc. 200(2), 105–108 (2000).
[CrossRef] [PubMed]

1999 (1)

1995 (3)

M. J. Yadlowsky, J. M. Schmitt, and R. F. Bonner, “Multiple scattering in optical coherence microscopy,” Appl. Opt. 34(25), 5699–5707 (1995).
[CrossRef] [PubMed]

A. Derode, P. Roux, and M. Fink, “Robust Acoustic Time Reversal with High-Order Multiple Scattering,” Phys. Rev. Lett. 75(23), 4206–4209 (1995).
[CrossRef] [PubMed]

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun. 117(1-2), 43–48 (1995).
[CrossRef]

1994 (1)

1991 (1)

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[CrossRef] [PubMed]

1974 (1)

Amblard, F.

Bajraszewski, T.

M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A. F. Fercher, “In vivo human retinal imaging by Fourier domain optical coherence tomography,” J. Biomed. Opt. 7(3), 457–463 (2002).
[CrossRef] [PubMed]

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]

Barry, S.

Beaurepaire, E.

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]

Bonner, R. F.

Booth, M. J.

M. A. A. Neil, R. Juškaitis, M. J. Booth, T. Wilson, T. Tanaka, and S. Kawata, “Adaptive aberration correction in a two-photon microscope,” J. Microsc. 200(2), 105–108 (2000).
[CrossRef] [PubMed]

Bridges, W. B.

Brown, W. P.

Brunner, P. T.

Burns, D.

Burns, L. D.

B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in light microscopy for neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
[CrossRef] [PubMed]

Cable, A. E.

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]

Chang, W.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Cui, M.

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
[CrossRef] [PubMed]

M. Cui, “Parallel wavefront optimization method for focusing light through random scattering media,” Opt. Lett. 36(6), 870–872 (2011).
[CrossRef] [PubMed]

M. Cui, E. J. McDowell, and C. Yang, “Observation of polarization-gate based reconstruction quality improvement during the process of turbidity suppression by optical phase conjugation,” Appl. Phys. Lett. 95(12), 123702 (2009).
[CrossRef] [PubMed]

Denk, W.

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[CrossRef] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Derode, A.

A. Derode, P. Roux, and M. Fink, “Robust Acoustic Time Reversal with High-Order Multiple Scattering,” Phys. Rev. Lett. 75(23), 4206–4209 (1995).
[CrossRef] [PubMed]

Drexler, W.

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys. 66(2), 239–303 (2003).
[CrossRef]

El-Zaiat, S. Y.

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun. 117(1-2), 43–48 (1995).
[CrossRef]

Fercher, A. F.

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys. 66(2), 239–303 (2003).
[CrossRef]

M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A. F. Fercher, “In vivo human retinal imaging by Fourier domain optical coherence tomography,” J. Biomed. Opt. 7(3), 457–463 (2002).
[CrossRef] [PubMed]

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun. 117(1-2), 43–48 (1995).
[CrossRef]

Fink, M.

A. Derode, P. Roux, and M. Fink, “Robust Acoustic Time Reversal with High-Order Multiple Scattering,” Phys. Rev. Lett. 75(23), 4206–4209 (1995).
[CrossRef] [PubMed]

Flotte, T.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Fujimoto, J. G.

J. A. Izatt, M. R. Hee, G. M. Owen, E. A. Swanson, and J. G. Fujimoto, “Optical coherence microscopy in scattering media,” Opt. Lett. 19(8), 590–592 (1994).
[CrossRef] [PubMed]

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Germain, R. N.

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
[CrossRef] [PubMed]

Ghosh, K. K.

B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in light microscopy for neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
[CrossRef] [PubMed]

Girkin, J.

Gregory, K.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Hee, M. R.

J. A. Izatt, M. R. Hee, G. M. Owen, E. A. Swanson, and J. G. Fujimoto, “Optical coherence microscopy in scattering media,” Opt. Lett. 19(8), 590–592 (1994).
[CrossRef] [PubMed]

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Hitzenberger, C. K.

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys. 66(2), 239–303 (2003).
[CrossRef]

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun. 117(1-2), 43–48 (1995).
[CrossRef]

Horton, N. G.

D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
[CrossRef] [PubMed]

Huang, D.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Izatt, J. A.

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]

Jiang, J. Y.

Juškaitis, R.

M. A. A. Neil, R. Juškaitis, M. J. Booth, T. Wilson, T. Tanaka, and S. Kawata, “Adaptive aberration correction in a two-photon microscope,” J. Microsc. 200(2), 105–108 (2000).
[CrossRef] [PubMed]

Kamp, G.

A. F. Fercher, C. K. Hitzenberger, G. Kamp, and S. Y. El-Zaiat, “Measurement of intraocular distances by backscattering spectral interferometry,” Opt. Commun. 117(1-2), 43–48 (1995).
[CrossRef]

Kawata, S.

M. A. A. Neil, R. Juškaitis, M. J. Booth, T. Wilson, T. Tanaka, and S. Kawata, “Adaptive aberration correction in a two-photon microscope,” J. Microsc. 200(2), 105–108 (2000).
[CrossRef] [PubMed]

Kobat, D.

D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
[CrossRef] [PubMed]

Kowalczyk, A.

M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A. F. Fercher, “In vivo human retinal imaging by Fourier domain optical coherence tomography,” J. Biomed. Opt. 7(3), 457–463 (2002).
[CrossRef] [PubMed]

Lasser, T.

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys. 66(2), 239–303 (2003).
[CrossRef]

Lazzara, S. P.

Leitgeb, R.

M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A. F. Fercher, “In vivo human retinal imaging by Fourier domain optical coherence tomography,” J. Biomed. Opt. 7(3), 457–463 (2002).
[CrossRef] [PubMed]

Lin, C. P.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Mack-Bucher, J. A.

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[CrossRef] [PubMed]

Marsh, P.

McDowell, E. J.

M. Cui, E. J. McDowell, and C. Yang, “Observation of polarization-gate based reconstruction quality improvement during the process of turbidity suppression by optical phase conjugation,” Appl. Phys. Lett. 95(12), 123702 (2009).
[CrossRef] [PubMed]

Mertz, J.

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]

Moreaux, L.

Mukamel, E. A.

B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in light microscopy for neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
[CrossRef] [PubMed]

Neil, M. A. A.

M. A. A. Neil, R. Juškaitis, M. J. Booth, T. Wilson, T. Tanaka, and S. Kawata, “Adaptive aberration correction in a two-photon microscope,” J. Microsc. 200(2), 105–108 (2000).
[CrossRef] [PubMed]

Nussmeier, T. A.

O’Meara, T. R.

Owen, G. M.

Pircher, M.

M. Pircher and R. J. Zawadzki, “Combining adaptive optics with optical coherence tomography: unveiling the cellular structure of the human retina in vivo,” Expert Rev. Ophthalmol. 2(6), 1019–1035 (2007).
[CrossRef]

Puliafito, C. A.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Radhakrishnan, H.

Roux, P.

A. Derode, P. Roux, and M. Fink, “Robust Acoustic Time Reversal with High-Order Multiple Scattering,” Phys. Rev. Lett. 75(23), 4206–4209 (1995).
[CrossRef] [PubMed]

Rueckel, M.

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[CrossRef] [PubMed]

Sanguinet, J. A.

Schmitt, J. M.

Schnitzer, M. J.

B. A. Wilt, L. D. Burns, E. T. Wei Ho, K. K. Ghosh, E. A. Mukamel, and M. J. Schnitzer, “Advances in light microscopy for neuroscience,” Annu. Rev. Neurosci. 32(1), 435–506 (2009).
[CrossRef] [PubMed]

Schuman, J. S.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

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]

Srinivasan, V. J.

Stinson, W. G.

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Figures (7)

Fig. 1
Fig. 1

Simulation of the wavefront optimization. (a)-(d) Light intensity distribution at the focal plane in a tissue phantom with a mean scattering path length of 4.5 after 0, 1, 2 and 3 wavefront optimization iterations. (e)-(h) Light intensity distribution at the focal plane in a tissue phantom with a mean scattering path length of 6 after 0, 1, 2 and 3 wavefront optimization iterations

Fig. 2
Fig. 2

Experimental setup: BS, beamsplitter, PBS, polarizing beamsplitter, QWP, quarter waveplate.

Fig. 3
Fig. 3

(a) Distorted focus after propagation through a tissue phantom, as imaged in transmission. A uniform phase profile was displayed on the SLM. A gamma correction with a factor of 0.5 was applied to better highlight the weak features of the distorted focus. (b) Corrected focus after three wavefront optimization iterations. A magnified view of the focus is shown in the inset. (c) Pseudo incoherent widefield image of the target bead layer as imaged in transmission. (d) Wavefront correction corresponding to image (b).

Fig. 4
Fig. 4

Focusing onto scattering sources inside the brain: (a) Distorted focus after propagation through a 300 micron thick fixed brain section, as imaged in transmission. A uniform phase profile was displayed on the SLM. (b) Corrected focus after three wavefront optimization iterations. (c) Wavefront correction corresponding to image (b). (d) Cross section through the corrected (solid line) and uncorrected focus (dashed line) corresponding to the images shown in (b) and (a), respectively. (e) Distorted focus after propagation through a 500 micron thick fixed brain section. A uniform phase profile was displayed on the SLM. (f) Corrected focus after three wavefront optimization iterations. (g) Wavefront correction corresponding to image (f). (h) Cross section through the corrected (solid line) and uncorrected focus (dashed line) corresponding to the images shown in (e) and (f), respectively.

Fig. 5
Fig. 5

Focusing through brain tissue on a polystyrene bead: (a) Distorted focus after propagation through a 500 micron thick fixed brain section, as imaged in transmission. A uniform phase profile was displayed on the SLM. A gamma correction with factor 0.5 was applied to the image. (b) Corrected focus after three wavefront optimization iterations. (c) Wavefront correction corresponding to image (b).

Fig. 6
Fig. 6

Lateral shift dependence of the corrected focus through a 300 micron thick fixed brain slice: (a) Corrected focus as observed in transmission for different lateral shifts. Scale bar: 5 microns. (b) Applied wavefront correction. The phase is indicated in radians.

Fig. 7
Fig. 7

Peak intensity of the corrected focus versus lateral displacement measured on a 300 micron thick brain slice.

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