Abstract

The strong optical scattering of biological tissue confounds our ability to focus light deeply into the brain beyond depths of a few hundred microns. This challenge can be potentially overcome by exploiting wavefront shaping techniques which allow light to be focused through or inside scattering media. However, these techniques require the scattering medium to be static, as changes in the arrangement of the scatterers between the wavefront recording and playback steps reduce the fidelity of the focus that is formed. Furthermore, as the thickness of the scattering medium increases, the influence of the dynamic nature becomes more severe due to the growing number of scattering events experienced by each photon. In this paper, by examining the scattering dynamics in the mouse brain in vivo via multispeckle diffusing wave spectroscopy (MSDWS) using a custom fiber probe that simulates a point-like source within the brain, we investigate the relationship between this decorrelation time and the depth of the point-like light source inside the living mouse brain at depths up to 3.2 mm.

© 2017 Optical Society of America

Full Article  |  PDF Article

Corrections

Muhammad Mohsin Qureshi, Joshua Brake, Hee-Jae Jeon, Haowen Ruan, Yan Liu, Abdul Mohaimen Safi, Tae Joong Eom, Changhuei Yang, and Euiheon Chung, "In vivo study of optical speckle decorrelation time across depths in the mouse brain: erratum," Biomed. Opt. Express 8, 5039-5039 (2017)
https://www.osapublishing.org/boe/abstract.cfm?uri=boe-8-11-5039

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References

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2017 (3)

S. Rotter and S. Gigan, “Light fields in complex media: Mesoscopic scattering meets wave control,” Rev. Mod. Phys. 89, 015005 (2017).

Y. Liu, C. Ma, Y. Shen, J. Shi, and L. V. Wang, “Focusing light inside dynamic scattering media with millisecond digital optical phase conjugation,” Optica 4(2), 280–288 (2017).
[PubMed]

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

2016 (3)

2015 (7)

S. Sun, B. R. Hayes-Gill, D. He, Y. Zhu, and S. P. Morgan, “Multi-exposure laser speckle contrast imaging using a high frame rate CMOS sensor with a field programmable gate array,” Opt. Lett. 40(20), 4587–4590 (2015).
[PubMed]

D. Wang, E. H. Zhou, J. Brake, H. Ruan, M. Jang, and C. Yang, “Focusing through dynamic tissue with millisecond digital optical phase conjugation,” Optica 2(8), 728–735 (2015).
[PubMed]

C. Ma, F. Zhou, Y. Liu, and L. V. Wang, “Single-exposure optical focusing inside scattering media using binarized time-reversed adapted perturbation,” Optica 2, 869–876 (2015).

Y. Liu, P. Lai, C. Ma, X. Xu, A. A. Grabar, and L. V. Wang, “Optical focusing deep inside dynamic scattering media with near-infrared time-reversed ultrasonically encoded (TRUE) light,” Nat. Commun. 6, 5904 (2015).
[PubMed]

I. M. Vellekoop, “Feedback-based wavefront shaping,” Opt. Express 23(9), 12189–12206 (2015).
[PubMed]

H. Yu, J. Park, K. Lee, J. Yoon, K. Kim, S. Lee, and Y. Park, “Recent advances in wavefront shaping techniques for biomedical applications,” Curr. Appl. Phys. 15, 632–641 (2015).

R. Horstmeyer, H. Ruan, and C. Yang, “Guidestar-assisted wavefront-shaping methods for focusing light into biological tissue,” Nat. Photonics 9, 563–571 (2015).
[PubMed]

2014 (1)

2013 (1)

S. L. Jacques, “Optical Properties of Biological Tissues: A Review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[PubMed]

2012 (3)

2011 (4)

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).
[PubMed]

D. Akbulut, T. J. Huisman, E. G. van Putten, W. L. Vos, and A. P. Mosk, “Focusing light through random photonic media by binary amplitude modulation,” Opt. Express 19(5), 4017–4029 (2011).
[PubMed]

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
[PubMed]

K. Deisseroth, “Optogenetics,” Nat. Methods 8(1), 26–29 (2011).
[PubMed]

2010 (3)

M. Cui and C. Yang, “Implementation of a digital optical phase conjugation system and its application to study the robustness of turbidity suppression by phase conjugation,” Opt. Express 18(4), 3444–3455 (2010).
[PubMed]

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

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the Transmission Matrix in Optics: An Approach to the Study and Control of Light Propagation in Disordered Media,” Phys. Rev. Lett. 104(10), 100601 (2010).
[PubMed]

2009 (1)

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

2008 (5)

R. Mostany and C. Portera-Cailliau, “A craniotomy surgery procedure for chronic brain imaging,” J. Vis. Exp. 12, 680 (2008).
[PubMed]

M. Medebach, N. Freiberger, and O. Glatter, “Dynamic light scattering in turbid nonergodic media,” Rev. Sci. Instrum. 79(7), 073907 (2008).
[PubMed]

A. B. Parthasarathy, W. J. Tom, A. Gopal, X. Zhang, and A. K. Dunn, “Robust flow measurement with multi-exposure speckle imaging,” Opt. Express 16(3), 1975–1989 (2008).
[PubMed]

Z. Yaqoob, D. Psaltis, M. S. Feld, and C. Yang, “Optical phase conjugation for turbidity suppression in biological samples,” Nat. Photonics 2(2), 110–115 (2008).
[PubMed]

I. M. Vellekoop and A. P. Mosk, “Phase control algorithms for focusing light through turbid media,” Opt. Commun. 281, 3071–3080 (2008).

2002 (2)

V. Viasnoff, F. Lequeux, and D. J. Pine, “Multispeckle diffusing-wave spectroscopy: A tool to study slow relaxation and time-dependent dynamics,” Rev. Sci. Instrum. 73, 2336–2344 (2002).

J. Li, G. Ku, and L. V. Wang, “Ultrasound-modulated optical tomography of biological tissue by use of contrast of laser speckles,” Appl. Opt. 41(28), 6030–6035 (2002).
[PubMed]

1999 (1)

1989 (1)

F. C. MacKintosh and S. John, “Diffusing-wave spectroscopy and multiple scattering of light in correlated random media,” Phys. Rev. B Condens. Matter 40(4), 2383–2406 (1989).
[PubMed]

1988 (1)

D. J. Pine, D. A. Weitz, P. M. Chaikin, and E. Herbolzheimer, “Diffusing wave spectroscopy,” Phys. Rev. Lett. 60(12), 1134–1137 (1988).
[PubMed]

1987 (1)

G. Maret and P. E. Wolf, “Multiple light scattering from disordered media. The effect of brownian motion of scatterers,” Z. Phys. B Condens. Matter 65, 409–413 (1987).

1976 (1)

Akbulut, D.

Akerboom, J.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Bargmann, C. I.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Boccara, A. C.

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the Transmission Matrix in Optics: An Approach to the Study and Control of Light Propagation in Disordered Media,” Phys. Rev. Lett. 104(10), 100601 (2010).
[PubMed]

Brake, J.

Caravaca-Aguirre, A. M.

Carminati, R.

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the Transmission Matrix in Optics: An Approach to the Study and Control of Light Propagation in Disordered Media,” Phys. Rev. Lett. 104(10), 100601 (2010).
[PubMed]

Chaikin, P. M.

D. J. Pine, D. A. Weitz, P. M. Chaikin, and E. Herbolzheimer, “Diffusing wave spectroscopy,” Phys. Rev. Lett. 60(12), 1134–1137 (1988).
[PubMed]

Chalasani, S. H.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Cheng, Y.-T.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

Chiappe, M. E.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Cho, A.

Choi, W.

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
[PubMed]

Choi, Y.

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
[PubMed]

Chung, E.

Conkey, D. B.

Cruz-Hernández, J. C.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

Cui, M.

Dasari, R. R.

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
[PubMed]

Deisseroth, K.

K. Deisseroth, “Optogenetics,” Nat. Methods 8(1), 26–29 (2011).
[PubMed]

Dunn, A. K.

Durian, D. J.

Fang-Yen, C.

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
[PubMed]

Feld, M. S.

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
[PubMed]

Z. Yaqoob, D. Psaltis, M. S. Feld, and C. Yang, “Optical phase conjugation for turbidity suppression in biological samples,” Nat. Photonics 2(2), 110–115 (2008).
[PubMed]

Feng, D. D.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

Fink, M.

A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6, 283–292 (2012).

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the Transmission Matrix in Optics: An Approach to the Study and Control of Light Propagation in Disordered Media,” Phys. Rev. Lett. 104(10), 100601 (2010).
[PubMed]

Freiberger, N.

M. Medebach, N. Freiberger, and O. Glatter, “Dynamic light scattering in turbid nonergodic media,” Rev. Sci. Instrum. 79(7), 073907 (2008).
[PubMed]

Gigan, S.

S. Rotter and S. Gigan, “Light fields in complex media: Mesoscopic scattering meets wave control,” Rev. Mod. Phys. 89, 015005 (2017).

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the Transmission Matrix in Optics: An Approach to the Study and Control of Light Propagation in Disordered Media,” Phys. Rev. Lett. 104(10), 100601 (2010).
[PubMed]

Glatter, O.

M. Medebach, N. Freiberger, and O. Glatter, “Dynamic light scattering in turbid nonergodic media,” Rev. Sci. Instrum. 79(7), 073907 (2008).
[PubMed]

Goodman, J. W.

Gopal, A.

Grabar, A. A.

Y. Liu, P. Lai, C. Ma, X. Xu, A. A. Grabar, and L. V. Wang, “Optical focusing deep inside dynamic scattering media with near-infrared time-reversed ultrasonically encoded (TRUE) light,” Nat. Commun. 6, 5904 (2015).
[PubMed]

Hayes-Gill, B. R.

He, D.

Herbolzheimer, E.

D. J. Pine, D. A. Weitz, P. M. Chaikin, and E. Herbolzheimer, “Diffusing wave spectroscopy,” Phys. Rev. Lett. 60(12), 1134–1137 (1988).
[PubMed]

Hires, S. A.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Horstmeyer, R.

R. Horstmeyer, H. Ruan, and C. Yang, “Guidestar-assisted wavefront-shaping methods for focusing light into biological tissue,” Nat. Photonics 9, 563–571 (2015).
[PubMed]

Horton, N. G.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[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).
[PubMed]

Huber, D.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Huisman, T. J.

Jacques, S. L.

S. L. Jacques, “Optical Properties of Biological Tissues: A Review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[PubMed]

Jang, M.

Jayaraman, V.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

John, S.

F. C. MacKintosh and S. John, “Diffusing-wave spectroscopy and multiple scattering of light in correlated random media,” Phys. Rev. B Condens. Matter 40(4), 2383–2406 (1989).
[PubMed]

Jouhanneau, J.-S.

I. N. Papadopoulos, J.-S. Jouhanneau, J. F. A. Poulet, and B. Judkewitz, “Scattering compensation by focus scanning holographic aberration probing (F-SHARP),” Nat. Photonics 11, 116–123 (2016).

Judkewitz, B.

I. N. Papadopoulos, J.-S. Jouhanneau, J. F. A. Poulet, and B. Judkewitz, “Scattering compensation by focus scanning holographic aberration probing (F-SHARP),” Nat. Photonics 11, 116–123 (2016).

M. Jang, H. Ruan, I. M. Vellekoop, B. Judkewitz, E. Chung, and C. Yang, “Relation between speckle decorrelation and optical phase conjugation (OPC)-based turbidity suppression through dynamic scattering media: a study on in vivo mouse skin,” Biomed. Opt. Express 6(1), 72–85 (2014).
[PubMed]

Kang, P.

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
[PubMed]

Kim, D.

Kim, K.

H. Yu, J. Park, K. Lee, J. Yoon, K. Kim, S. Lee, and Y. Park, “Recent advances in wavefront shaping techniques for biomedical applications,” Curr. Appl. Phys. 15, 632–641 (2015).

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).
[PubMed]

Ku, G.

Lagendijk, A.

A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6, 283–292 (2012).

Lai, P.

Y. Liu, P. Lai, C. Ma, X. Xu, A. A. Grabar, and L. V. Wang, “Optical focusing deep inside dynamic scattering media with near-infrared time-reversed ultrasonically encoded (TRUE) light,” Nat. Commun. 6, 5904 (2015).
[PubMed]

Lee, K.

H. Yu, J. Park, K. Lee, J. Yoon, K. Kim, S. Lee, and Y. Park, “Recent advances in wavefront shaping techniques for biomedical applications,” Curr. Appl. Phys. 15, 632–641 (2015).

Lee, K. J.

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
[PubMed]

Lee, S.

H. Yu, J. Park, K. Lee, J. Yoon, K. Kim, S. Lee, and Y. Park, “Recent advances in wavefront shaping techniques for biomedical applications,” Curr. Appl. Phys. 15, 632–641 (2015).

Lemieux, P.-A.

Lequeux, F.

V. Viasnoff, F. Lequeux, and D. J. Pine, “Multispeckle diffusing-wave spectroscopy: A tool to study slow relaxation and time-dependent dynamics,” Rev. Sci. Instrum. 73, 2336–2344 (2002).

Lerosey, G.

A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6, 283–292 (2012).

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the Transmission Matrix in Optics: An Approach to the Study and Control of Light Propagation in Disordered Media,” Phys. Rev. Lett. 104(10), 100601 (2010).
[PubMed]

Li, J.

Liu, Y.

Looger, L. L.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Ma, C.

MacKintosh, F. C.

F. C. MacKintosh and S. John, “Diffusing-wave spectroscopy and multiple scattering of light in correlated random media,” Phys. Rev. B Condens. Matter 40(4), 2383–2406 (1989).
[PubMed]

Mao, T.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Maret, G.

G. Maret and P. E. Wolf, “Multiple light scattering from disordered media. The effect of brownian motion of scatterers,” Z. Phys. B Condens. Matter 65, 409–413 (1987).

Mather, M. L.

McKinney, S. A.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Medebach, M.

M. Medebach, N. Freiberger, and O. Glatter, “Dynamic light scattering in turbid nonergodic media,” Rev. Sci. Instrum. 79(7), 073907 (2008).
[PubMed]

Morgan, S. P.

Mosk, A. P.

A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6, 283–292 (2012).

D. Akbulut, T. J. Huisman, E. G. van Putten, W. L. Vos, and A. P. Mosk, “Focusing light through random photonic media by binary amplitude modulation,” Opt. Express 19(5), 4017–4029 (2011).
[PubMed]

I. M. Vellekoop and A. P. Mosk, “Phase control algorithms for focusing light through turbid media,” Opt. Commun. 281, 3071–3080 (2008).

Mostany, R.

R. Mostany and C. Portera-Cailliau, “A craniotomy surgery procedure for chronic brain imaging,” J. Vis. Exp. 12, 680 (2008).
[PubMed]

Nishimura, N.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

Ntziachristos, V.

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

Ouzounov, D. G.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

Papadopoulos, I. N.

I. N. Papadopoulos, J.-S. Jouhanneau, J. F. A. Poulet, and B. Judkewitz, “Scattering compensation by focus scanning holographic aberration probing (F-SHARP),” Nat. Photonics 11, 116–123 (2016).

Park, J.

H. Yu, J. Park, K. Lee, J. Yoon, K. Kim, S. Lee, and Y. Park, “Recent advances in wavefront shaping techniques for biomedical applications,” Curr. Appl. Phys. 15, 632–641 (2015).

Park, Y.

H. Yu, J. Park, K. Lee, J. Yoon, K. Kim, S. Lee, and Y. Park, “Recent advances in wavefront shaping techniques for biomedical applications,” Curr. Appl. Phys. 15, 632–641 (2015).

Parthasarathy, A. B.

Petreanu, L.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Piestun, R.

Pine, D. J.

V. Viasnoff, F. Lequeux, and D. J. Pine, “Multispeckle diffusing-wave spectroscopy: A tool to study slow relaxation and time-dependent dynamics,” Rev. Sci. Instrum. 73, 2336–2344 (2002).

D. J. Pine, D. A. Weitz, P. M. Chaikin, and E. Herbolzheimer, “Diffusing wave spectroscopy,” Phys. Rev. Lett. 60(12), 1134–1137 (1988).
[PubMed]

Popoff, S. M.

S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the Transmission Matrix in Optics: An Approach to the Study and Control of Light Propagation in Disordered Media,” Phys. Rev. Lett. 104(10), 100601 (2010).
[PubMed]

Portera-Cailliau, C.

R. Mostany and C. Portera-Cailliau, “A craniotomy surgery procedure for chronic brain imaging,” J. Vis. Exp. 12, 680 (2008).
[PubMed]

Poulet, J. F. A.

I. N. Papadopoulos, J.-S. Jouhanneau, J. F. A. Poulet, and B. Judkewitz, “Scattering compensation by focus scanning holographic aberration probing (F-SHARP),” Nat. Photonics 11, 116–123 (2016).

Psaltis, D.

Z. Yaqoob, D. Psaltis, M. S. Feld, and C. Yang, “Optical phase conjugation for turbidity suppression in biological samples,” Nat. Photonics 2(2), 110–115 (2008).
[PubMed]

Reimer, J.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

Rotter, S.

S. Rotter and S. Gigan, “Light fields in complex media: Mesoscopic scattering meets wave control,” Rev. Mod. Phys. 89, 015005 (2017).

Ruan, H.

Schreiter, E. R.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Shen, Y.

Shi, J.

Sun, S.

Svoboda, K.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Tian, L.

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
[PubMed]

Tolias, A. S.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

Tom, W. J.

van Putten, E. G.

Vellekoop, I. M.

Viasnoff, V.

V. Viasnoff, F. Lequeux, and D. J. Pine, “Multispeckle diffusing-wave spectroscopy: A tool to study slow relaxation and time-dependent dynamics,” Rev. Sci. Instrum. 73, 2336–2344 (2002).

Vos, W. L.

Wang, D.

Wang, L. V.

Wang, M.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

Wang, T.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[PubMed]

Weitz, D. A.

D. J. Pine, D. A. Weitz, P. M. Chaikin, and E. Herbolzheimer, “Diffusing wave spectroscopy,” Phys. Rev. Lett. 60(12), 1134–1137 (1988).
[PubMed]

Wolf, P. E.

G. Maret and P. E. Wolf, “Multiple light scattering from disordered media. The effect of brownian motion of scatterers,” Z. Phys. B Condens. Matter 65, 409–413 (1987).

Xu, C.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[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).
[PubMed]

Xu, X.

Y. Liu, P. Lai, C. Ma, X. Xu, A. A. Grabar, and L. V. Wang, “Optical focusing deep inside dynamic scattering media with near-infrared time-reversed ultrasonically encoded (TRUE) light,” Nat. Commun. 6, 5904 (2015).
[PubMed]

Yang, C.

Yang, T. D.

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
[PubMed]

Yaqoob, Z.

Z. Yaqoob, D. Psaltis, M. S. Feld, and C. Yang, “Optical phase conjugation for turbidity suppression in biological samples,” Nat. Photonics 2(2), 110–115 (2008).
[PubMed]

Yeon, C.

Yoon, J.

H. Yu, J. Park, K. Lee, J. Yoon, K. Kim, S. Lee, and Y. Park, “Recent advances in wavefront shaping techniques for biomedical applications,” Curr. Appl. Phys. 15, 632–641 (2015).

Yu, H.

H. Yu, J. Park, K. Lee, J. Yoon, K. Kim, S. Lee, and Y. Park, “Recent advances in wavefront shaping techniques for biomedical applications,” Curr. Appl. Phys. 15, 632–641 (2015).

Zhang, X.

Zhou, E. H.

Zhou, F.

Zhu, Y.

Appl. Opt. (1)

Biomed. Opt. Express (1)

Curr. Appl. Phys. (1)

H. Yu, J. Park, K. Lee, J. Yoon, K. Kim, S. Lee, and Y. Park, “Recent advances in wavefront shaping techniques for biomedical applications,” Curr. Appl. Phys. 15, 632–641 (2015).

J. Biomed. Opt. (1)

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).
[PubMed]

J. Opt. Soc. Am. (1)

J. Opt. Soc. Am. A (2)

J. Opt. Soc. Korea (1)

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R. Mostany and C. Portera-Cailliau, “A craniotomy surgery procedure for chronic brain imaging,” J. Vis. Exp. 12, 680 (2008).
[PubMed]

Nat. Commun. (1)

Y. Liu, P. Lai, C. Ma, X. Xu, A. A. Grabar, and L. V. Wang, “Optical focusing deep inside dynamic scattering media with near-infrared time-reversed ultrasonically encoded (TRUE) light,” Nat. Commun. 6, 5904 (2015).
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V. Ntziachristos, “Going deeper than microscopy: the optical imaging frontier in biology,” Nat. Methods 7(8), 603–614 (2010).
[PubMed]

L. Tian, S. A. Hires, T. Mao, D. Huber, M. E. Chiappe, S. H. Chalasani, L. Petreanu, J. Akerboom, S. A. McKinney, E. R. Schreiter, C. I. Bargmann, V. Jayaraman, K. Svoboda, and L. L. Looger, “Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators,” Nat. Methods 6(12), 875–881 (2009).
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K. Deisseroth, “Optogenetics,” Nat. Methods 8(1), 26–29 (2011).
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[PubMed]

Nat. Photonics (4)

I. N. Papadopoulos, J.-S. Jouhanneau, J. F. A. Poulet, and B. Judkewitz, “Scattering compensation by focus scanning holographic aberration probing (F-SHARP),” Nat. Photonics 11, 116–123 (2016).

R. Horstmeyer, H. Ruan, and C. Yang, “Guidestar-assisted wavefront-shaping methods for focusing light into biological tissue,” Nat. Photonics 9, 563–571 (2015).
[PubMed]

A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6, 283–292 (2012).

Z. Yaqoob, D. Psaltis, M. S. Feld, and C. Yang, “Optical phase conjugation for turbidity suppression in biological samples,” Nat. Photonics 2(2), 110–115 (2008).
[PubMed]

Opt. Commun. (1)

I. M. Vellekoop and A. P. Mosk, “Phase control algorithms for focusing light through turbid media,” Opt. Commun. 281, 3071–3080 (2008).

Opt. Express (5)

Opt. Lett. (2)

Optica (3)

Phys. Med. Biol. (1)

S. L. Jacques, “Optical Properties of Biological Tissues: A Review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[PubMed]

Phys. Rev. B Condens. Matter (1)

F. C. MacKintosh and S. John, “Diffusing-wave spectroscopy and multiple scattering of light in correlated random media,” Phys. Rev. B Condens. Matter 40(4), 2383–2406 (1989).
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Phys. Rev. Lett. (3)

D. J. Pine, D. A. Weitz, P. M. Chaikin, and E. Herbolzheimer, “Diffusing wave spectroscopy,” Phys. Rev. Lett. 60(12), 1134–1137 (1988).
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S. M. Popoff, G. Lerosey, R. Carminati, M. Fink, A. C. Boccara, and S. Gigan, “Measuring the Transmission Matrix in Optics: An Approach to the Study and Control of Light Propagation in Disordered Media,” Phys. Rev. Lett. 104(10), 100601 (2010).
[PubMed]

Y. Choi, T. D. Yang, C. Fang-Yen, P. Kang, K. J. Lee, R. R. Dasari, M. S. Feld, and W. Choi, “Overcoming the diffraction limit using multiple light scattering in a highly disordered medium,” Phys. Rev. Lett. 107(2), 023902 (2011).
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S. Rotter and S. Gigan, “Light fields in complex media: Mesoscopic scattering meets wave control,” Rev. Mod. Phys. 89, 015005 (2017).

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G. Maret and P. E. Wolf, “Multiple light scattering from disordered media. The effect of brownian motion of scatterers,” Z. Phys. B Condens. Matter 65, 409–413 (1987).

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T. Laforest, A. Dupret, A. Verdant, F. Ramaz, S. Gigan, G. Tessier, and E. B. A. La Guillaume, “A 4000 Hz CMOS image sensor with in-pixel processing for light measurement and modulation,” 2013 IEEE 11th Int. New Circuits Syst. Conf. NEWCAS 2013 1–4 (2013).

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Figures (4)

Fig. 1
Fig. 1 Diagram of the experimental setup. (a) The experimental setup consisted of a Helium-neon laser coupled to a custom-made fiber probe. The fiber probe was covered with white ZnO paint to simulate a diffuse point-like source in the tissue. (b) The speckle pattern on the surface of the brain was imaged to an sCMOS sensor using a microscope objective and tube lens. A linear polarizer helped to maximize the contrast of the captured speckle pattern, and the iris ensured an adequate speckle size on the sensor. (c) A zoomed view of the mouse brain and fiber tip. The fiber tip was inserted at a 45-degree angle into the mouse brain through a gap between the skull and the cover glass which formed the cranial window. Then, the fiber was advanced from a depth d of 1.1 mm to 3.2 mm below the brain surface, and a series of speckle patterns were recorded at each depth to analyze the decorrelation time.
Fig. 2
Fig. 2 Characterization of diffusing fiber tip light distribution and imaging region. (a) The custom fiber tip probe is made of a 105-µm diameter multimode fiber covered with white paint to create a diffuse, point-like source in the brain tissue. (b) To characterize the distribution of light exiting the fiber tip, we measured the light intensity profile in the x-y (red) and y-z (blue) planes. (c) A white light image of the pial surface of the brain with the locations of subregions of interest for analysis shown for each penetration depth. The imaging regions of interest and the insertion site were chosen to avoid major pial blood vessels. (d-e) The orthogonal (d) and in-plane (e) light intensity distributions. The solid line traces the mean of five measurements, and the error bars indicate the standard deviation of the measurements. Scale bars: 200 µm in (a) 1mm in (c).
Fig. 3
Fig. 3 Decorrelation curves for different fiber tip depths. The decorrelation curves from 1.1 mm, 1.8 mm, 2.5 mm, and 3.2 mm were calculated by penetrating the respective depth into the mouse brain tissue using the fiber probe and capturing a time series of speckle patterns. Then, using the procedure explained above, g 2 ( t ) was calculated and plotted for each thickness. In the plot above, every 5th data point of the mean curve is shown for clarity, and the solid lines indicate the fit of the mean data points. Each thickness consists of a total of 14 traces across three mice. Shaded areas indicate the 95% confidence intervals for the mean of the data at each time point.
Fig. 4
Fig. 4 Decorrelation time as a function of fiber tip penetration depth. As the fiber tip penetrates deeper into the brain tissue, the decorrelation time decreases due to the increasing number of scattering events. The error bars indicate the standard error of the mean of the decorrelation times over the 14 total data sets from three mice at each depth.

Equations (2)

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g 2 ( τ )= I( t 0 )I( t 0 +τ ) I( t 0 )I( t 0 +τ )
g 2 ( t )=a×exp( 2× t b )+c×exp( 2× t d )+( e+1 ),

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