Abstract

Optical scattering has traditionally limited the ability to focus light inside scattering media such as biological tissue. Recently developed wavefront shaping techniques promise to overcome this limit by tailoring an optical wavefront to constructively interfere at a target location deep inside scattering media. To find such a wavefront solution, a “guidestar” mechanism is required to identify the target location. However, developing guidestars of practical usefulness is challenging, especially in biological tissue, which hinders the translation of wavefront shaping techniques. Here, we demonstrate a guidestar mechanism that relies on magnetic modulation of small particles. This guidestar method features an optical modulation efficiency of 29% and enables micrometer-scale focusing inside biological tissue with a peak intensity-to-background ratio (PBR) of 140; both numbers are one order of magnitude higher than those achieved with the ultrasound guidestar, a popular guidestar method. We also demonstrate that light can be focused on cells labeled with magnetic particles, and to different target locations by magnetically controlling the position of a particle. Since magnetic fields have a large penetration depth even through bone structures like the skull, this optical focusing method holds great promise for deep-tissue applications such as optogenetic modulation of neurons, targeted light-based therapy, and imaging.

© 2017 Optical Society of America

Full Article  |  PDF Article
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References

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2017 (3)

2016 (2)

Y. Shen, Y. Liu, C. Ma, and L. V. Wang, “Focusing light through biological tissue and tissue-mimicking phantoms up to 9.6 cm in thickness with digital optical phase conjugation,” J. Biomed. Opt. 21, 085001 (2016).
[Crossref]

J. Brake, M. Jang, and C. Yang, “Analyzing the relationship between decorrelation time and tissue thickness in acute rat brain slices using multispeckle diffusing wave spectroscopy,” J. Opt. Soc. Am. A 33, 270–275 (2016).
[Crossref]

2015 (15)

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).
[Crossref]

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, 72–85 (2015).
[Crossref]

K. Lee, J. Lee, J.-H. Park, J.-H. Park, and Y. Park, “One-wave optical phase conjugation mirror by actively coupling arbitrary light fields into a single-mode reflector,” Phys. Rev. Lett. 115, 153902 (2015).
[Crossref]

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

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

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).
[Crossref]

M. Kim, W. Choi, Y. Choi, C. Yoon, and W. Choi, “Transmission matrix of a scattering medium and its applications in biophotonics,” Opt. Express 23, 12648–12668 (2015).
[Crossref]

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, “Photoacoustically guided wavefront shaping for enhanced optical focusing in scattering media,” Nat. Photonics 9, 126–132 (2015).
[Crossref]

H. Ruan, M. Jang, and C. Yang, “Optical focusing inside scattering media with time-reversed ultrasound microbubble encoded light,” Nat. Commun. 6, 8968 (2015).
[Crossref]

B. D. Plouffe, S. K. Murthy, and L. H. Lewis, “Fundamentals and application of magnetic particles in cell isolation and enrichment: a review,” Rep. Prog. Phys. 78, 016601 (2015).
[Crossref]

E. E. White, A. Pai, Y. Weng, A. K. Suresh, D. Van Haute, T. Pailevanian, D. Alizadeh, A. Hajimiri, B. Badie, and J. M. Berlin, “Functionalized iron oxide nanoparticles for controlling the movement of immune cells,” Nanoscale 7, 7780–7789 (2015).
[Crossref]

R. Chen, G. Romero, M. G. Christiansen, A. Mohr, and P. Anikeeva, “Wireless magnetothermal deep brain stimulation,” Science 347, 1477–1480 (2015).
[Crossref]

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, 728–735 (2015).
[Crossref]

S. Kulkarni, B. Ramaswamy, E. Horton, S. Gangapuram, A. Nacev, D. Depireux, M. Shimoji, and B. Shapiro, “Quantifying the motion of magnetic particles in excised tissue: effect of particle properties and applied magnetic field,” J. Magn. Magn. Mater. 393, 243–252 (2015).
[Crossref]

R. Guduru, P. Liang, J. Hong, A. Rodzinski, A. Hadjikhani, J. Horstmyer, E. Levister, and S. Khizroev, “Magnetoelectric “spin” on stimulating the brain,” Nanomedicine 10, 2051–2061 (2015).
[Crossref]

2014 (7)

R. Mooney, L. Roma, D. Zhao, D. Van Haute, E. Garcia, S. U. Kim, A. J. Annala, K. S. Aboody, and J. M. Berlin, “Neural stem cell-mediated intratumoral delivery of gold nanorods improves photothermal therapy,” ACS Nano 8, 12450–12460 (2014).
[Crossref]

K. Birmingham, V. Gradinaru, P. Anikeeva, W. M. Grill, V. Pikov, B. McLaughlin, P. Pasricha, D. Weber, K. Ludwig, and K. Famm, “Bioelectronic medicines: a research roadmap,” Nat. Rev. Drug Discov. 13, 399–400 (2014).
[Crossref]

M. Jang, H. Ruan, H. Zhou, B. Judkewitz, and C. Yang, “Method for auto-alignment of digital optical phase conjugation systems based on digital propagation,” Opt. Express 22, 14054–14071 (2014).
[Crossref]

C. Ma, X. Xu, Y. Liu, and L. V. Wang, “Time-reversed adapted-perturbation (TRAP) optical focusing onto dynamic objects inside scattering media,” Nat. Photonics 8, 931–936 (2014).
[Crossref]

E. H. Zhou, H. Ruan, C. Yang, and B. Judkewitz, “Focusing on moving targets through scattering samples,” Optica 1, 227–232 (2014).
[Crossref]

H. Ruan, M. Jang, B. Judkewitz, and C. Yang, “Iterative time-reversed ultrasonically encoded light focusing in backscattering mode,” Sci. Rep. 4, 7156 (2014).
[Crossref]

J. W. Tay, P. Lai, Y. Suzuki, and L. V. Wang, “Ultrasonically encoded wavefront shaping for focusing into random media,” Sci. Rep. 4, 3918 (2014).
[Crossref]

2013 (5)

J. Jang, J. Lim, H. Yu, H. Choi, J. Ha, J.-H. Park, W.-Y. Oh, W. Jang, S. Lee, and Y. Park, “Complex wavefront shaping for optimal depth-selective focusing in optical coherence tomography,” Opt. Express 21, 2890–2902 (2013).
[Crossref]

T. Chaigne, O. Katz, A. C. Boccara, M. Fink, E. Bossy, and S. Gigan, “Controlling light in scattering media non-invasively using the photoacoustic transmission matrix,” Nat. Photonics 8, 58–64 (2013).
[Crossref]

H. Yu, T. R. Hillman, W. Choi, J. O. Lee, M. S. Feld, R. R. Dasari, and Y. Park, “Measuring large optical transmission matrices of disordered media,” Phys. Rev. Lett. 111, 153902 (2013).
[Crossref]

T. R. Hillman, T. Yamauchi, W. Choi, R. R. Dasari, M. S. Feld, Y. Park, and Z. Yaqoob, “Digital optical phase conjugation for delivering two-dimensional images through turbid media.,” Sci. Rep. 3, 1909 (2013).
[Crossref]

H. Ruan, M. L. Mather, and S. P. Morgan, “Pulsed ultrasound modulated optical tomography with harmonic lock-in holography detection,” J. Opt. Soc. Am. A 30, 1409–1416 (2013).
[Crossref]

2012 (4)

I. N. Papadopoulos, S. Farahi, C. Moser, and D. Psaltis, “Focusing and scanning light through a multimode optical fiber using digital phase conjugation.,” Opt. Express 20, 10583–10590 (2012).
[Crossref]

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).
[Crossref]

Y. M. Wang, B. Judkewitz, C. A. DiMarzio, and C. Yang, “Deep-tissue focal fluorescence imaging with digitally time-reversed ultrasound-encoded light,” Nat. Commun. 3, 928 (2012).
[Crossref]

K. Si, R. Fiolka, and M. Cui, “Fluorescence imaging beyond the ballistic regime by ultrasound pulse guided digital phase conjugation,” Nat. Photonics 6, 657–661 (2012).
[Crossref]

2011 (3)

X. Xu, H. Liu, and L. V. Wang, “Time-reversed ultrasonically encoded optical focusing into scattering media,” Nat. Photonics 5, 154–157 (2011).
[Crossref]

C. S. S. R. Kumar and F. Mohammad, “Magnetic nanomaterials for hyperthermia-based therapy and controlled drug delivery,” Adv. Drug Deliv. Rev. 63, 789–808 (2011).
[Crossref]

F. Kong, R. H. Silverman, L. Liu, P. V. Chitnis, K. K. Lee, and Y. C. Chen, “Photoacoustic-guided convergence of light through optically diffusive media,” Opt. Lett. 36, 2053–2055 (2011).
[Crossref]

2010 (6)

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7, 141–147 (2010).
[Crossref]

I. M. Vellekoop and C. M. Aegerter, “Scattered light fluorescence microscopy: imaging through turbid layers,” Opt. Lett. 35, 1245–1247 (2010).
[Crossref]

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

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, 100601 (2010).
[Crossref]

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, 3444–3455 (2010).
[Crossref]

C. Hsieh, Y. Pu, R. Grange, and D. Psaltis, “Digital phase conjugation of second harmonic radiation emitted by nanoparticles in turbid media,” Opt. Express 18, 12283–12290 (2010).

2008 (2)

I. M. Vellekoop, E. G. van Putten, A. Lagendijk, and A. P. Mosk, “Demixing light paths inside disordered metamaterials,” Opt. Express 16, 67–80 (2008).
[Crossref]

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

2007 (1)

2005 (1)

B. Gleich and J. Weizenecker, “Tomographic imaging using the nonlinear response of magnetic particles,” Nature 435, 1214–1217 (2005).
[Crossref]

1997 (1)

1979 (1)

A. Schlegel, S. F. Alvarado, and P. Wachter, “Optical properties of magnetite (Fe3O4) related content optical properties of magnetite (Fe, O,),” J. Phys. C 12, 1157–1164 (1979).
[Crossref]

1966 (1)

Aboody, K. S.

R. Mooney, L. Roma, D. Zhao, D. Van Haute, E. Garcia, S. U. Kim, A. J. Annala, K. S. Aboody, and J. M. Berlin, “Neural stem cell-mediated intratumoral delivery of gold nanorods improves photothermal therapy,” ACS Nano 8, 12450–12460 (2014).
[Crossref]

Aegerter, C. M.

Alizadeh, D.

E. E. White, A. Pai, Y. Weng, A. K. Suresh, D. Van Haute, T. Pailevanian, D. Alizadeh, A. Hajimiri, B. Badie, and J. M. Berlin, “Functionalized iron oxide nanoparticles for controlling the movement of immune cells,” Nanoscale 7, 7780–7789 (2015).
[Crossref]

Alvarado, S. F.

A. Schlegel, S. F. Alvarado, and P. Wachter, “Optical properties of magnetite (Fe3O4) related content optical properties of magnetite (Fe, O,),” J. Phys. C 12, 1157–1164 (1979).
[Crossref]

Anikeeva, P.

R. Chen, G. Romero, M. G. Christiansen, A. Mohr, and P. Anikeeva, “Wireless magnetothermal deep brain stimulation,” Science 347, 1477–1480 (2015).
[Crossref]

K. Birmingham, V. Gradinaru, P. Anikeeva, W. M. Grill, V. Pikov, B. McLaughlin, P. Pasricha, D. Weber, K. Ludwig, and K. Famm, “Bioelectronic medicines: a research roadmap,” Nat. Rev. Drug Discov. 13, 399–400 (2014).
[Crossref]

Annala, A. J.

R. Mooney, L. Roma, D. Zhao, D. Van Haute, E. Garcia, S. U. Kim, A. J. Annala, K. S. Aboody, and J. M. Berlin, “Neural stem cell-mediated intratumoral delivery of gold nanorods improves photothermal therapy,” ACS Nano 8, 12450–12460 (2014).
[Crossref]

Badie, B.

E. E. White, A. Pai, Y. Weng, A. K. Suresh, D. Van Haute, T. Pailevanian, D. Alizadeh, A. Hajimiri, B. Badie, and J. M. Berlin, “Functionalized iron oxide nanoparticles for controlling the movement of immune cells,” Nanoscale 7, 7780–7789 (2015).
[Crossref]

Berlin, J. M.

E. E. White, A. Pai, Y. Weng, A. K. Suresh, D. Van Haute, T. Pailevanian, D. Alizadeh, A. Hajimiri, B. Badie, and J. M. Berlin, “Functionalized iron oxide nanoparticles for controlling the movement of immune cells,” Nanoscale 7, 7780–7789 (2015).
[Crossref]

R. Mooney, L. Roma, D. Zhao, D. Van Haute, E. Garcia, S. U. Kim, A. J. Annala, K. S. Aboody, and J. M. Berlin, “Neural stem cell-mediated intratumoral delivery of gold nanorods improves photothermal therapy,” ACS Nano 8, 12450–12460 (2014).
[Crossref]

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, 141–147 (2010).
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T. R. Hillman, T. Yamauchi, W. Choi, R. R. Dasari, M. S. Feld, Y. Park, and Z. Yaqoob, “Digital optical phase conjugation for delivering two-dimensional images through turbid media.,” Sci. Rep. 3, 1909 (2013).
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ACS Nano (1)

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Curr. Appl. Phys. (1)

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J. Biomed. Opt. (1)

Y. Shen, Y. Liu, C. Ma, and L. V. Wang, “Focusing light through biological tissue and tissue-mimicking phantoms up to 9.6 cm in thickness with digital optical phase conjugation,” J. Biomed. Opt. 21, 085001 (2016).
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Nanomedicine (1)

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H. Ruan, M. Jang, and C. Yang, “Optical focusing inside scattering media with time-reversed ultrasound microbubble encoded light,” Nat. Commun. 6, 8968 (2015).
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C. Ma, X. Xu, Y. Liu, and L. V. Wang, “Time-reversed adapted-perturbation (TRAP) optical focusing onto dynamic objects inside scattering media,” Nat. Photonics 8, 931–936 (2014).
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K. Si, R. Fiolka, and M. Cui, “Fluorescence imaging beyond the ballistic regime by ultrasound pulse guided digital phase conjugation,” Nat. Photonics 6, 657–661 (2012).
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X. Xu, H. Liu, and L. V. Wang, “Time-reversed ultrasonically encoded optical focusing into scattering media,” Nat. Photonics 5, 154–157 (2011).
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Nat. Rev. Drug Discov. (1)

K. Birmingham, V. Gradinaru, P. Anikeeva, W. M. Grill, V. Pikov, B. McLaughlin, P. Pasricha, D. Weber, K. Ludwig, and K. Famm, “Bioelectronic medicines: a research roadmap,” Nat. Rev. Drug Discov. 13, 399–400 (2014).
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Nature (1)

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Opt. Express (9)

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Phys. Rev. Lett. (3)

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Supplementary Material (5)

NameDescription
» Supplement 1       Supplemental document
» Visualization 1       Magnetic particles oscillate under an AC magnetic field of 25 Hz. This effect can serve as a guidestar for light to focus through scattering media using wavefront shaping techniques.
» Visualization 2       Magnetic particles oscillate under an AC magnetic field of 5 Hz. This effect can serve as a guidestar for light to focus through scattering media using wavefront shaping techniques.
» Visualization 3       A macrophage cell with magnetic particles oscillates under an AC magnetic field of 25 Hz. This effect can serve as a guidestar for light to focus through scattering media using wavefront shaping techniques.
» Visualization 4       A macrophage cell with magnetic particles oscillates under an AC magnetic field of 5 Hz. This effect can serve as a guidestar for light to focus through scattering media using wavefront shaping techniques.

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Figures (5)

Fig. 1.
Fig. 1. Principle of magnetic-particle-guided optical focusing. (a) A magnetic particle is embedded in a piece of scattering tissue. A portion of the impinging laser beam interacts with the particle and the resulting tagged light is detected interferometrically using the camera of a DOPC system. (b) After capturing the field of the tagged light, the conjugate wavefront is displayed on the spatial light modulator (SLM) of the DOPC system. The reconstructed conjugate light field then retraces the scattering paths and forms a focus at the location of the magnetic particle. Panels (c) and (d) show two methods to separate the tagged light field from the background unmodulated light. The field subtraction method in (c) captures two optical fields before and after a magnetic field displaces the magnetic particle. The differential field nullifies the contribution from the background, which is not scattered by the particle. The frequency modulation method shown in (d) uses an AC magnetic field to make the magnetic particle oscillate, which shifts the frequency of the light, which interacts with the particle. By matching the frequency of a planar reference beam with that of the tagged light, the DOPC system detects the tagged light field via phase-shifting holography. (e) After imprinting the conjugate wavefront of the tagged light on a planar reference beam using the SLM, the conjugate wave forms a bright focus on top of a dim background at the location of the magnetic particle inside the scattering medium.
Fig. 2.
Fig. 2. Magnetic-particle-guided optical focusing with the field subtraction method. (a) Schematic of the setup to record the field of the tagged light. (b) Schematic of the setup for playback of the tagged field and observation of the focus. In this step, the tissue on the left side was removed and an imaging system was used to observe the light intensity distribution on the magnetic particle plane. Panels (c) and (d) show bright-field images of the particles with the magnetic field in different directions. (e) The focus observed with the setup shown in (b). (f) Control experiment: no focus was observed when the magnetic fields were turned off and the experiment was repeated. Scale bar, 5 μm.
Fig. 3.
Fig. 3. Magnetic-particle-guided optical focusing with the frequency modulation method. The electromagnets were driven by 25 Hz rectangular waves. Images were captured with the setup shown in Fig. 2(b). The focus achieved when the reference beam frequency was shifted by (a) 25 Hz (fundamental frequency), (b) 50 Hz (second harmonic), and (c) 75 Hz (third harmonic) relative to the laser frequency. (d) Control experiment: no focus was observed when the reference beam frequency was shifted by 30 Hz (frequency mismatch). Scale bar, 5 μm.
Fig. 4.
Fig. 4. Focusing light onto a targeted cell that endocytosed magnetic particles of 453 nm diameter. Panels (a) and (b) show bright-field images of a cell under two magnetic fields. (c) Focus achieved by the field subtraction method. (d) Focus achieved by the frequency modulation method (fm=25  Hz). (e) Control experiment: no focus was observed when the SLM pattern was circularly shifted by 10×10 pixels after obtaining the result in (d). Scale bar, 5 μm.
Fig. 5.
Fig. 5. Focusing light to different target locations by controlling the positions of the magnetic particles using an external magnetic field. The magnetic particles were driven to the target locations inside a microfluidic channel based on the position feedback from the observation microscope [Fig. 2(b)]. After reaching each target location, the magnetic particles were covered by the scattering samples on both sides as shown in Fig. 2(a), and the DOPC process was performed to create a focus through the scattering sample on the DOPC system side. Then, the scattering sample on the observation microscope side was removed [Fig. 2(b)], and the focus was observed directly. Scale bar, 5 μm.

Equations (4)

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Ep=αΔE*T=α[(Em_2*Em_1*)T*]T=αβ(Em_2*Em_1*).
Em(t)=f(t)Aexp[i(2πf0t+φ0)],
f(t)=n=1sin(πnτfm)nπ{exp[i(2πnfmt+φm)]+exp[i(2πnfmt+φm)]}+τfm.
Em(t)=n=1Anπsin(πnτfm)exp{i[2π(f0+nfm)t+φ0+φm]}+n=1Anπsin(πnτfm)exp{i[2π(f0nfm)t+φ0φm]}+τfmAexp[i(2πf0t+φ0)].

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