Journal of Innovative Optical Health Sciences, Volume. 12, Issue 4, 1930002(2019)
Overcoming the penetration depth limit in optical microscopy: Adaptive optics and wavefront shaping
[1] [1] C. Stosiek, O. Garaschuk, K. Holthoff, A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks," Proc. Natl. Acad. Sci. 100, 7319–7324 (2003).
[2] [2] A. Baohan et al., “Ultrasensitive fluorescent proteins for imaging neuronal activity," Nature 499, 295–300 (2013).
[3] [3] N. Vogt, “Neuroscience: All-optical electrophysiology in behaving animals," Nat. Methods 12, 101 (2015).
[4] [4] M. Scanziani, M. Hausser, “Electrophysiology in the age of light," Nature 461, 930–939 (2009).
[5] [5] S. Peron, K. Svoboda, “From cudgel to scalpel: Toward precise neural control with optogenetics," Nat. Methods 8, 30–34 (2011).
[6] [6] C. Tischbirek, A. Birkner, H. Jia, B. Sakmann, A. Konnerth, “Deep two-photon brain imaging with a red-shifted fluorometric Ca 2+ indicator," Proc. Natl. Acad. Sci. 112, 11377–11382 (2015).
[7] [7] C. Grienberger, A. Konnerth, “Imaging calcium in neurons," Neuron 73, 862–885 (2012).
[8] [8] H.-U. Dodt et al., “Ultramicroscopy: Threedimensional visualization of neuronal networks in the whole mouse brain," Nat. Methods 4, 331–336 (2007).
[9] [9] M. N. Economo et al., “A platform for brain-wide imaging and reconstruction of individual neurons," Elife 5, 1–22 (2016).
[10] [10] D. A. Dombeck, A. N. Khabbaz, F. Collman, T. L. Adelman, D. W. Tank, “Imaging large-scale neural activity with cellular resolution in awake, mobile mice," Neuron 56, 43–57 (2007).
[11] [11] B. R. Masters, P. T. C. So, E. Gratton, “Multiphoton excitation fluorescence microscopy and spectroscopy of in vivo human skin," Biophys. J. 72, 2405–2412 (1997).
[12] [12] R. Tomer et al., “SPED light sheet microscopy: Fast mapping of biological system structure and function," Cell 163, 1796–1806 (2015).
[13] [13] L. Sherman, J. Y. Ye, O. Albert, T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror," J. Microsc. 206, 65–71 (2002).
[14] [14] O. Katz, E. Small, Y. Silberberg, “Looking around corners and through thin turbid layers in real time with scattered incoherent light," Nat. Photonics 6, 549–553 (2012).
[15] [15] M. A. A. Neil et al.,“Adaptive aberration correction in a two-photon microscope," J. Microsc. 200, 105–108 (2000).
[16] [16] M. J. Booth, “Adaptive optics in microscopy," R. Soc. 365, 2829–2843 (2007).
[17] [17] C. Rodríguez, N. Ji, “Adaptive optical microscopy for neurobiology," Curr. Opin. Neurobiol. 50, 83–91 (2018).
[18] [18] N. Ji, “Adaptive optical fluorescence microscopy," Nat. Methods 14, 374–380 (2017).
[19] [19] R. Horstmeyer, H. Ruan, C. Yang, “Guidestarassisted wavefront-shaping methods for focusing light into biological tissue," Nat. Photonics 9, 563–571 (2015).
[20] [20] I. M. Vellekoop, “Feedback-based wavefront shaping," Opt. Express 23, 12189–12206 (2015).
[21] [21] H. Yu et al., “Depth-enhanced 2-D optical coherence tomography using complex wavefront shaping," Opt. Express 22, 7514–7523 (2014).
[22] [22] J. W. Goodman, Introduction to Fourier Optics. Roberts and Company Publishers (2005).
[23] [23] J. Vangindertael et al., “An introduction to optical super-resolution microscopy for the adventurous biologist An introduction to optical super-resolution microscopy for the adventurous biologist," Methods Appl. Fluoresc 6, 022003 (2018).
[24] [24] V. Ntziachristos, “Going deeper than microscopy: The optical imaging frontier in biology," Nat. Methods 7, 603–614 (2010).
[25] [25] P. Theer, W. Denk, “On the fundamental imagingdepth limit in two-photon microscopy," J. Opt. Soc. Am. A 23, 3139 (2006).
[26] [26] F. Helmchen, W. Denk, “Deep tissue twophoton microscopy," Nat. Methods 2, 932–940 (2005).
[27] [27] N. G. Horton et al., “In vivo three-photon microscopy of subcortical structures within an intact mouse brain," Nat. Photonics 7, 205–209 (2013).
[28] [28] H. W. Babcock, “The possibility of compensating astronomical seeing," Astronomical Society of the Pacific 65, 229–236 (1953).
[29] [29] C. Max, “Introduction to adaptive optics and its history," tech. rep., NSF Center for Adaptive Optics, University of California at Santa Cruz and DOE Lawrence Livermore National Laboratory, 2001.
[30] [30] N. Devaney, Review of astronomical adaptive optics systems and plans, Proc. SPIE 6584, 658407 (2007).
[31] [31] J. M. Beckers, “Adaptive optics for astronomy: Principles, performance, and applications," Annu. Reo. Astron. Astrophy 31, 13–62 (1993).
[32] [32] R. Tyson, Principles of Adaptive Optics, 3rd Edition," CRC Press (2011).
[33] [33] A. Roorda, J. L. Duncan, “Adaptive Optics Ophthalmoscopy," Annu. Rev. Vis. Sci. 1, 19–50 (2015).
[34] [34] M. J. Booth, “Adaptive optical microscopy: The ongoing quest for a perfect image," Light Sci. Appl. 3, 1–7 (2014).
[35] [35] Y. Liu, C. Ma, Y. Shen, J. Shi, L. V. Wang, “Focusing light inside dynamic scattering media with millisecond digital optical phase conjugation," Optica 4, 280–288 (2017).
[36] [36] J.-H. Park, Z. Yu, K. Lee, P. Lai, Y. Park, “Perspective: Wavefront shaping techniques for controlling multiple light scattering in biological tissues: Toward in vivo applications," APL Photonics 3, 100901 (2018).
[37] [37] A. P. Mosk, A. Lagendijk, G. Lerosey, M. Fink, “Controlling waves in space and time for imaging and focusing in complex media," Nat. Photonics 6, 283–292 (2012).
[38] [38] R. Davies, M. Kasper, “Adaptive Optics for Astronomy," Annu. Rev. Astron. Astrophys. 50, 305–351 (2012).
[39] [39] I. M. Vellekoop, M. Cui, C. Yang, “Digital optical phase conjugation of fluorescence in turbid tissue," Appl. Phys. Lett. 101, 081108 (2012).
[40] [40] D. Akbulut, T. J. Huisman, E. G. van Putten, W. L. Vos, A. P. Mosk, “Focusing light through random photonic media by binary amplitude modulation," Opt. Express 19, 4017 (2011).
[41] [41] I. M. Vellekoop, C. M. Aegerter, “Scattered light fluorescence microscopy: Imaging through turbid layers," Opt. Lett. 35, 1245–1247 (2010).
[42] [42] M. J. Booth, M. A. A. Neil, R. Juskaitis, T. Wilson, “Adaptive aberration correction in a confocal microscope," Proc. Natl. Acad. Sci. 99, 5788–5792 (2002).
[43] [43] W. Zheng et al., “Adaptive optics improves multiphoton super-resolution imaging," Nat. Methods 14, 869–872 (2017).
[44] [44] R. Fiolka, K. Si, M. Cui, “Complex wavefront corrections for deep tissue focusing using low coherence backscattered light," Opt. Express 20, 16532–16543 (2012).
[45] [45] J. Jang et al., “Complex wavefront shaping for optimal depth-selective focusing in optical coherence tomography," Opt. Express 21, 2890–2902 (2013).
[46] [46] K. Wang et al., “Direct wavefront sensing for highresolution in vivo imaging in scattering tissue," Nat. Commun. 6, 1–6 (2015).
[47] [47] I. Yamaguchi, T. Zhang, “Phase-shifting digital holography," Opt. Lett. 22, 1268–1270 (1997).
[48] [48] M. Takeda, H. Ina, S. Kobayashi, “Fourier-transform method of fringe-pattern analysis for computer-based topography and interferometry," J. Opt. Soc. Am. 72, 156–160 (1982).
[49] [49] D. R. Neal, J. Copland, D. A. Neal, “Shack-Hartmann wavefront sensor precision and accuracy," Proc. SPIE 4779, 148–160 (2002).
[50] [50] R. A. Muller, A. Bu±ngton, “Real-time correction of atmospherically degraded telescope images through image sharpening," J. Opt. Soc. Am. 64, 1200–1210 (1974).
[51] [51] M. J. Booth, “Wavefront sensorless adaptive optics for large aberrations," Opt. Lett. 32, 5–7 (2007).
[52] [52] W. Lee, “Binary computer-generated holograms," Appl. Opt. 18, 3661–3669 (1979).
[53] [53] P. Marsh, D. Burns, J. Girkin, “Practical implementation of adaptive optics in multiphoton microscopy," Opt. Exp. 11, 1123–1130 (2003).
[54] [54] M. Skorsetz, P. Artal, J. M. Bueno, “Performance evaluation of a sensorless adaptive optics multiphoton microscope," J. Microsc. 261, 249–258 (2016).
[55] [55] M. Booth, “Wave front sensor-less adaptive optics: A model-based approach using sphere packings," Opt. Express 14, 1339–1352 (2006).
[56] [56] M. J. Booth, M. A. A. Neil, T. Wilson, “Aberration correction for confocal imaging in refractive-indexmismatched media," J. Microsc. 192, 90–98 (1998).
[57] [57] R. Bhatt, S. K. Mishra, D. Mohan, A. Sharma, A. K. Gupta, “Differential modal Zernike wavefront sensor employing a computer-generated hologram: A proposal," Appl. Opt. 48, 6458–6465 (2009).
[58] [58] J. H. Park, L. Kong, Y. Zhou, M. Cui, “Large-fieldof-view imaging by multi-pupil adaptive optics," Nat. Methods 14, 581–583 (2017).
[59] [59] N. A. Roddier, “Atmospheric wavefront simulation using Zernike polynomials," Opt. Eng. 29, 1174–1180 (1990).
[60] [60] V. Lakshminarayanan, A. Fleck, “Zernike polynomials: A guide," J. Mod. Opt. 58, 545–561 (2011).
[61] [61] N. Ji, D. E. Milkie, E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues," Nat. Methods 7, 141–147 (2010).
[62] [62] S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue," Proc. Natl. Acad. Sci. U. S. A., Vol. 109, pp. 7175–7180 (2012).
[63] [63] N. D. Shemonski et al., “Three-dimensional motion correction using speckle and phase for in vivo computed optical interferometric tomography," Biomed. Opt. Express 5, 4131–4143 (2014).
[64] [64] D. J. Wahl et al., “Wavefront sensorless adaptive optics fluorescence biomicroscope for in vivo retinal imaging in mice," Biomed. Opt. Express 7, 1–12 (2016).
[65] [65] T.-L. Liu et al., “Observing the cell in its native state: Imaging subcellular dynamics in multicellular organisms," Science (80-.). 360, 1–13 (2018).
[66] [66] E. Betzig et al., “Imaging intracellular fluorescent proteins at nanometer resolution," Science (80-.).313, 1642–1645 (2006).
[67] [67] M. J. Rust, M. Bates, X. Zhuang, “Sub-diffractionlimit imaging by stochastic optical reconstruction microscopy (STORM)," Nat. Methods 3, 793–795 (2006).
[68] [68] M. G. L. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy," J. Microsc. 198, 82–87 (2000).
[69] [69] S. W. Hell, J. Wichmann, “Breaking the diffraction resolution limit by stimulated emission: Stimulated-emission-depletion fluorescence microscopy," Opt. Lett. 19, 780–782 (1994).
[70] [70] R. McGorty, J. Schnitzbauer, W. Zhang, B. Huang, “Correction of depth-dependent aberrations in 3D single-molecule localization and superresolution microscopy," Opt. Lett. 39, 275 (2014).
[71] [71] A. Diezmann, M. Y. von, M. Lee, D. Lew, W. E. Moerner, “Correcting field-dependent aberrations with nanoscale accuracy in three-dimensional single-molecule localization microscopy," Optica 2, 985 (2015).
[72] [72] B. Thomas, A. Wolstenholme, S. N. E. Chaudhari, T. Kipreos, P. Kner, “Enhanced resolution through thick tissue with structured illumination and adaptive optics," J. Biomed. Opt. 20, 26006 (2015).
[73] [73] M. Arigovindan, J. W. Sedat, D. A. Agard, “Effect of depth dependent spherical aberrations in 3D structured illumination microscopy," Opt. Express 20, 6527–6541 (2012).
[74] [74] M. O. Lenz et al., “3-D stimulated emission depletion microscopy with programmable aberration correction," J. Biophotonics 7, 29–36 (2014).
[75] [75] B. R. Patton et al., “Three-dimensional STED microscopy of aberrating tissue using dual adaptive optics," Opt. Express 24, 8862–8876 (2016).
[76] [76] M. Booth, D. Andrade, D. Burke, B. Patton, M. Zurauskas, “Aberrations and adaptive optics in super-resolution microscopy," Microscopy 64, 251–261 (2015).
[77] [77] T. J. Gould, D. Burke, J. Bewersdorf, M. J. Booth, “Adaptive optics enables 3D STED microscopy in aberrating specimens," Opt. Express 20, 20998–21009 (2012).
[78] [78] H. Yu, K. Lee, Y. Park, “Ultrahigh enhancement of light focusing through disordered media controlled by mega-pixel modes," Opt. Express 25, 8036–8047 (2017).
[79] [79] I. M. Vellekoop, A. P. Mosk, “Focusing coherent light through opaque strongly scattering media," Opt. Lett. 32, 2309–2311 (2007).
[80] [80] M. Cui, 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).
[81] [81] I. N. Papadopoulos, S. Farahi, C. Moser, D. Psaltis, “Focusing and scanning light through a multimode optical fiber using digital phase conjugation," Opt. Express 20, 10583–10590 (2012).
[82] [82] T. R. Hillman et al., “Digital optical phase conjugation for delivering two-dimensional images through turbid media," Sci. Rep. 3, 1–5 (2013).
[83] [83] D. Wang et al., “Focusing through dynamic tissue with millisecond digital optical phase conjugation," Optica 2, 728–735 (2015).
[84] [84] J. Tang, R. N. Germain, M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique," Proc. Natl. Acad. Sci., Vol. 109, pp. 8434–8439 (2012).
[85] [85] J.-H. Park, W. Sun, M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull," Proc. Natl. Acad. Sci. 112, 9236–9241 (2015).
[86] [86] V. Szabo, C. Ventalon, V. De Sars, J. Bradley, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope," Neuron 84, 1157–1169 (2014).
[87] [87] R. P. J. Barretto et al., “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy," Nat. Med. 17, 223–229 (2011).
[88] [88] M. E. Bocarsly et al., “Minimally invasive microendoscopy system for in vivo functional imaging of deep nuclei in the mouse brain," Biomed. Opt. Express 6, 4546–4556 (2015).
[89] [89] S. L. Resendez et al., “Visualization of cortical, subcortical and deep brain neural circuit dynamics during naturalistic mammalian behavior with head-mounted microscopes and chronically implanted lenses," Nat. Protocols 11, 566–597 (2016).
[90] [90] Y. Choi et al., “Scanner-free and wide-field endoscopic imaging by using a single multimode optical fiber," Phys. Rev. Lett. 109, 1–5 (2012).
[91] [91] T. Cizmar, K. Dholakia, “Exploiting multimode waveguides for pure fibre-based imaging," Nat. Commun. 1027, 1–9 (2012).
[92] [92] M. Pl€oschner, T. Tyc, T. Cizmar, “Seeing through chaos in multimode fibres," Nat. Photonics 9, 529–535 (2015).
[93] [93] S. A. Vasquez-Lopez et al., “Subcellular spatial resolution achieved for deep-brain imaging in vivo using a minimally invasive multimode fiber," Light Sci. Appl. 7, 1–6 (2018).
[94] [94] P. Lai, L. Wang, J. W. Tay, L. V. Wang, “Photoacoustically guided wavefront shaping for enhanced optical focusing in scattering media," Nat. Photonics 9, 126–132 (2015).
[95] [95] T. Chaigne et al., “Controlling light in scattering media non-invasively using the photoacoustic transmission matrix," Nat. Photonics 8, 58–64 (2013).
[96] [96] F. Kong et al., “Photoacoustic-guided convergence of light through optically diffusive media," Opt. Lett. 36, 2053–2055 (2011).
[97] [97] X. Xu, H. Liu, L. V. Wang, “Time-reversed ultrasonically encoded optical focusing into scattering media," Nat. Photonics 5, 154–157 (2011).
[98] [98] J. W. Tay, P. Lai, Y. Suzuki, L. V. Wang, “Ultrasonically encoded wavefront shaping for focusing into random media," Sci. Rep. 4, 1–5 (2014).
[99] [99] C.-L. Hsieh, Y. Pu, R. Grange, D. Psaltis, “Digital phase conjugation of second harmonic radiation emitted by nanoparticles in turbid media," Opt. Express 18, 12283–12290 (2010).
[100] [100] C.-L. Hsieh, Y. Pu, R. Grange, G. Laporte, D. Psaltis, “Imaging through turbid layers by scanning the phase conjugated second harmonic radiation from a nanoparticle," Opt. Express 18, 20723–20731 (2010).
[101] [101] A. M. Caravaca-Aguirre et al., “High contrast three-dimensional photoacoustic imaging through scattering media by localized optical fluence enhancement," Opt. Express 21, 26671–26676 (2013).
[102] [102] C. Ma, X. Xu, Y. Liu, L. V. Wang, “Time-reversed adapted-perturbation (TRAP) optical focusing onto dynamic objects inside scattering media," Nat. Photonics 8, 931–936 (2014).
[103] [103] M. A. Pinkert, L. R. Salkowski, P. J. Keely, “Review of quantitative multiscale imaging of breast cancer," J. Med. Imaging 5, 10901–10911 (2018).
[104] [104] A. Roorda, F. Romero-Borja, W. J. D. III, H. Queener, “Adaptive optics scanning laser ophthalmoscopy," Opt. Exp. 10, 405–412 (2002).
[105] [105] M. Fink, “Time reversal of ultrasonic fields — Part I: basic principles," IEEE Trans. Ultrason. Ferroelectr. Freq. Control 39, 555–566 (1992).
[106] [106] M. Fink et al., “Time-reversed acoustics," Rep. Prog. Phys. 63, 1933–1995 (2000).
[107] [107] B. Judkewitz, R. Horstmeyer, I. M. Vellekoop, I. N. Papadopoulos, C. Yang, “Translation correlations in anisotropically scattering media," Nat. Phys. 11, 684–689 (2015).
[108] [108] G. Osnabrugge, R. Horstmeyer, I.N. Papadopoulos, B. Judkewitz, I. M. Vellekoop, “Generalized optical memory effect," Optica 4, 886 (2017).
[109] [109] E. Marchetti et al., “On-sky testing of the multiconjugate adaptive optics demonstrator," The Messenger 129, 8–13 (2007).
[110] [110] E. Marchetti, N. N. Hubin, E. Fedrigo, J. Brynnel, B. Delabre, “MAD the ESO multi-conjugate adaptive optics demonstrator," Adapt. Opt. Syst. Technol. II 4839, 317–328 (2003).
[111] [111] J. Mertz, H. Paudel, T. G. Bifano, “Field of view advantage of conjugate adaptive optics in microscopy applications," Appl. Opt. 54, 3498–3506 (2015).
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Cheolwoo Ahn, Byungjae Hwang, Kibum Nam, Hyungwon Jin, Taeseong Woo. Overcoming the penetration depth limit in optical microscopy: Adaptive optics and wavefront shaping[J]. Journal of Innovative Optical Health Sciences, 2019, 12(4): 1930002
Received: Mar. 30, 2019
Accepted: May. 19, 2019
Published Online: Sep. 3, 2019
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