Volume 7 Issue 4
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Jingyu Wang, Yongdeng Zhang. Adaptive optics in super-resolution microscopy[J]. Biophysics Reports, 2021, 7(4): 267-279. doi: 10.52601/bpr.2021.210015
Citation: Jingyu Wang, Yongdeng Zhang. Adaptive optics in super-resolution microscopy[J]. Biophysics Reports, 2021, 7(4): 267-279. doi: 10.52601/bpr.2021.210015

Adaptive optics in super-resolution microscopy

doi: 10.52601/bpr.2021.210015
Funds:  J. Wang is supported by John Fell Fund award (141/144), Wellcome Trust awards (105605/Z/14/Z and 107457/Z/15/Z). Y. Zhang is supported by Westlake Education Foundation.
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  • Corresponding author: zhangyongdeng@westlake.edu.cn (Y. Zhang)
  • Received Date: 01 June 2021
  • Accepted Date: 23 June 2021
  • Publish Date: 17 September 2021
  • Fluorescence microscopy has become a routine tool in biology for interrogating life activities with minimal perturbation. While the resolution of fluorescence microscopy is in theory governed only by the diffraction of light, the resolution obtainable in practice is also constrained by the presence of optical aberrations. The past two decades have witnessed the advent of super-resolution microscopy that overcomes the diffraction barrier, enabling numerous biological investigations at the nanoscale. Adaptive optics, a technique borrowed from astronomical imaging, has been applied to correct for optical aberrations in essentially every microscopy modality, especially in super-resolution microscopy in the last decade, to restore optimal image quality and resolution. In this review, we briefly introduce the fundamental concepts of adaptive optics and the operating principles of the major super-resolution imaging techniques. We highlight some recent implementations and advances in adaptive optics for active and dynamic aberration correction in super-resolution microscopy.
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  • [1]
    Ahn C, Hwang B, Nam K, Jin H, Woo T, Park JH (2019) Overcoming the penetration depth limit in optical microscopy: adaptive optics and wavefront shaping. J Innov Opt Health Sci 12: 1930002 doi: 10.1142/S1793545819300027
    [2]
    Angibaud J, Mascalchi P, Poujol C, Nagerl UV (2020) A simple tissue clearing method for increasing the depth penetration of STED microscopy of fixed brain slices. J Phys D-Appl Phys 53: 184001 doi: 10.1088/1361-6463/ab6f1b
    [3]
    Antonello J, Barbotin A, Chong EZ, Rittscher J, Booth MJ (2020a) Multi-scale sensorless adaptive optics: application to stimulated emission depletion microscopy. Opt Express 28: 16749−16763 doi: 10.1364/OE.393363
    [4]
    Antonello J, Burke D, Booth MJ (2017) Aberrations in stimulated emission depletion (STED) microscopy. Opt Commun 404: 203−209 doi: 10.1016/j.optcom.2017.06.037
    [5]
    Antonello J, Kromann EB, Burke D, Bewersdorf J, Booth MJ (2016) Coma aberrations in combined two- and three-dimensional STED nanoscopy. Opt Lett 41: 3631−3634 doi: 10.1364/OL.41.003631
    [6]
    Antonello J, Wang J, He C, Phillips M, Booth M (2020b) Interferometric calibration of a deformable mirror. Zenodo doi: 10.5281/zenodo.3714951
    [7]
    Arigovindan M, Sedat JW, Agard DA (2012) Effect of depth dependent spherical aberrations in 3D structured illumination microscopy. Opt Express 20: 6527−6541 doi: 10.1364/OE.20.006527
    [8]
    Baddeley D, Bewersdorf J (2018) Biological insight from super-resolution microscopy: what we can learn from localization-based images. Annu Rev Biochem 87: 965−989 doi: 10.1146/annurev-biochem-060815-014801
    [9]
    Bancelin S, Mercier L, Murana E, Nägerl UV (2021) Aberration correction in stimulated emission depletion microscopy to increase imaging depth in living brain tissue. Neurophotonics 8(3): 035001 doi: 10.1117/1.NPh.8.3.035001
    [10]
    Banerjee K, Rajaeipour P, Ataman C, Zappe H (2018) Optofluidic adaptive optics. Appl Opt 57: 6338−6344 doi: 10.1364/AO.57.006338
    [11]
    Belthangady C, Royer LA (2019) Applications, promises, and pitfalls of deep learning for fluorescence image reconstruction. Nat Methods 16: 1215−1225 doi: 10.1038/s41592-019-0458-z
    [12]
    Blom H, Widengren J (2017) Stimulated emission depletion microscopy. Chem Rev 117: 7377−7427 doi: 10.1021/acs.chemrev.6b00653
    [13]
    Booth M, Andrade D, Burke D, Patton B, Zurauskas M (2015) Aberrations and adaptive optics in super-resolution microscopy. Microscopy (Oxf) 64: 251−261
    [14]
    Booth MJ (2014) Adaptive optical microscopy: the ongoing quest for a perfect image. Light-Sci Appl 3 : e165−e165
    [15]
    Burke D, Patton B, Huang F, Bewersdorf J, Booth MJ (2015) Adaptive optics correction of specimen-induced aberrations in single-molecule switching microscopy. Optica 2: 177−185 doi: 10.1364/OPTICA.2.000177
    [16]
    Cabriel C, Bourg N, Dupuis G, Leveque-Fort S (2018) Aberration-accounting calibration for 3D single-molecule localization microscopy. Opt Lett 43: 174−177 doi: 10.1364/OL.43.000174
    [17]
    Carlini L, Holden SJ, Douglass KM, Manley S (2015) Correction of a depth-dependent lateral distortion in 3D super-resolution imaging. PLoS One 10: e0142949 doi: 10.1371/journal.pone.0142949
    [18]
    Chiu CP, Chiang TJ, Chen JK, Chang FC, Ko FH, Chu CW, Kuo SW, Fan SK (2012) Liquid lenses and driving mechanisms: a review. J Adhesion Sci Technol 26: 1773−1788 doi: 10.1163/156856111X600514
    [19]
    Coles BC, Webb SE, Schwartz N, Rolfe DJ, Martin-Fernandez M, Lo Schiavo V (2016) Characterisation of the effects of optical aberrations in single molecule techniques. Biomed Opt Express 7: 1755−1767 doi: 10.1364/BOE.7.001755
    [20]
    Dai Y, Antonello J, Booth MJ (2019) Calibration of a phase-only spatial light modulator for both phase and retardance modulation. Opt Express 27: 17912−17926 doi: 10.1364/OE.27.017912
    [21]
    Debarre D, Botcherby EJ, Booth MJ, Wilson T (2008) Adaptive optics for structured illumination microscopy. Opt Express 16: 9290−9305 doi: 10.1364/OE.16.009290
    [22]
    Deng S, Liu L, Cheng Y, Li R, Xu Z (2009) Investigation of the influence of the aberration induced by a plane interface on STED microscopy. Opt Express 17: 1714−1725 doi: 10.1364/OE.17.001714
    [23]
    Deng S, Liu L, Cheng Y, Li R, Xu Z (2010) Effects of primary aberrations on the fluorescence depletion patterns of STED microscopy. Opt Express 18: 1657−1666 doi: 10.1364/OE.18.001657
    [24]
    Deng Y, Shaevitz JW (2009) Effect of aberration on height calibration in three-dimensional localization-based microscopy and particle tracking. Appl Opt 48: 1886−1890 doi: 10.1364/AO.48.001886
    [25]
    Egner A, Geisler C, Siegmund R (2020). STED Nanoscopy. In Salditt T, Egner A and Luke DR (eds). Nanoscale Photonic Imaging. Cham: Springer International Publishing. pp 3-34
    [26]
    Gorlitz F, Guldbrand S, Runcorn TH, Murray RT, Jaso-Tamame AL, Sinclair HG, Martinez-Perez E, Taylor JR, Neil MAA, Dunsby C, French PMW (2018) easySLM-STED: stimulated emission depletion microscopy with aberration correction, extended field of view and multiple beam scanning. J Biophotonics 11: e201800087 doi: 10.1002/jbio.201800087
    [27]
    Gould TJ, Burke D, Bewersdorf J, Booth MJ (2012) Adaptive optics enables 3D STED microscopy in aberrating specimens. Opt Express 20: 20998−21009 doi: 10.1364/OE.20.020998
    [28]
    Gould TJ, Kromann EB, Burke D, Booth MJ, Bewersdorf J (2013) Auto-aligning stimulated emission depletion microscope using adaptive optics. Opt Lett 38: 1860−1862 doi: 10.1364/OL.38.001860
    [29]
    Hacker M, Stobrawa G, Sauerbrey R, Buckup T, Motzkus M, Wildenhain M, Gehner A (2003) Micromirror SLM for femtosecond pulse shaping in the ultraviolet. Appl Phys B-Lasers Opt 76: 711−714 doi: 10.1007/s00340-003-1180-0
    [30]
    Hao X, Allgeyer ES, Lee D-R, Antonello J, Watters K, Gerdes JA, Schroeder LK, Bottanelli F, Zhao J, Kidd P, Lessard MD, Rothman JE, Cooley L, Biederer T, Booth MJ, Bewersdorf J (2021) Three-dimensional adaptive optical nanoscopy for thick specimen imaging at sub-50-nm resolution. Nat Methods 18: 688−693 doi: 10.1038/s41592-021-01149-9
    [31]
    Heintzmann R, Huser T (2017) Super-resolution structured illumination microscopy. Chem Rev 117: 13890−13908 doi: 10.1021/acs.chemrev.7b00218
    [32]
    Hu L, Hu S, Gong W, Si K (2019) Learning-based Shack-Hartmann wavefront sensor for high-order aberration detection. Opt Express 27: 33504−33517 doi: 10.1364/OE.27.033504
    [33]
    Hu SW, Hu LJ, Gong W, Li ZH, and Si K (2021) Deep learning based wavefront sensor for complex wavefront detection in adaptive optical microscopes. Front Inform TechnolElectron Eng doi: 10.1631/FITEE.2000422
    [34]
    Izeddin I, El Beheiry M, Andilla J, Ciepielewski D, Darzacq X, Dahan M (2012) PSF shaping using adaptive optics for three-dimensional single-molecule super-resolution imaging and tracking. Opt Express 20: 4957−4967 doi: 10.1364/OE.20.004957
    [35]
    Ji N (2017) Adaptive optical fluorescence microscopy. Nat Methods 14: 374−380 doi: 10.1038/nmeth.4218
    [36]
    Lenz MO, Sinclair HG, Savell A, Clegg JH, Brown AC, Davis DM, Dunsby C, Neil MA, French PM (2014) 3-D stimulated emission depletion microscopy with programmable aberration correction. J Biophotonics 7: 29−36 doi: 10.1002/jbio.201300041
    [37]
    Li Y, Wu YL, Hoess P, Mund M, Ries J (2019) Depth-dependent PSF calibration and aberration correction for 3D single-molecule localization. Biomed Opt Express 10: 2708−2718 doi: 10.1364/BOE.10.002708
    [38]
    Lin R, Kipreos ET, Zhu J, Khang CH, Kner P (2021) Subcellular three-dimensional imaging deep through multicellular thick samples by structured illumination microscopy and adaptive optics. Nat Commun 12: 3148 doi: 10.1038/s41467-021-23449-6
    [39]
    Liu S, Kromann EB, Krueger WD, Bewersdorf J, Lidke KA (2013) Three dimensional single molecule localization using a phase retrieved pupil function. Opt Express 21: 29462−29487 doi: 10.1364/OE.21.029462
    [40]
    Liu X, Tu SJ, Xu Y, Song HY, Liu WJ, Liu QL, Kuang CF, Liu X, Hao X (2020) Aberrations in structured illumination microscopy: a theoretical analysis. Front Phys doi: 10.3389/fphy.2019.00254
    [41]
    Mahajan VN (1994) Zernike circle polynomials and optical aberrations of systems with circular pupils. Appl Opt 33: 8121 doi: 10.1364/AO.33.008121
    [42]
    McGorty R, Schnitzbauer J, Zhang W, Huang B (2014) Correction of depth-dependent aberrations in 3D single-molecule localization and super-resolution microscopy. Opt Lett 39: 275−278 doi: 10.1364/OL.39.000275
    [43]
    Mertz J, Paudel H, Bifano TG (2015) Field of view advantage of conjugate adaptive optics in microscopy applications. Appl Opt 54: 3498−3506 doi: 10.1364/AO.54.003498
    [44]
    Mlodzianoski MJ, Cheng-Hathaway PJ, Bemiller SM, McCray TJ, Liu S, Miller DA, Lamb BT, Landreth GE, Huang F (2018) Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections. Nat Methods 15: 583−586 doi: 10.1038/s41592-018-0053-8
    [45]
    Mockl L, Moerner WE (2020) Super-resolution microscopy with single molecules in biology and beyond-essentials, current trends, and future challenges. J Am Chem Soc 142: 17828−17844 doi: 10.1021/jacs.0c08178
    [46]
    Nishizaki Y, Valdivia M, Horisaki R, Kitaguchi K, Saito M, Tanida J, Vera E (2019) Deep learning wavefront sensing. Opt Express 27: 240−251 doi: 10.1364/OE.27.000240
    [47]
    Park JH, Kong L, Zhou Y, Cui M (2017) Large-field-of-view imaging by multi-pupil adaptive optics. Nat Methods 14: 581−583 doi: 10.1038/nmeth.4290
    [48]
    Park JH, Sun W, Cui M (2015) High-resolution in vivo imaging of mouse brain through the intact skull. Proc Natl Acad Sci USA 112: 9236−9241 doi: 10.1073/pnas.1505939112
    [49]
    Patton BR, Burke D, Owald D, Gould TJ, Bewersdorf J, Booth MJ (2016) Three-dimensional STED microscopy of aberrating tissue using dual adaptive optics. Opt Express 24: 8862−8876 doi: 10.1364/OE.24.008862
    [50]
    Pozzi P, Quintavalla M, Wong AB, Borst JGG, Bonora S, Verhaegen M (2020) Plug-and-play adaptive optics for commercial laser scanning fluorescence microscopes based on an adaptive lens. Opt Lett 45: 3585−3588 doi: 10.1364/OL.396998
    [51]
    Prakash K, Diederich B, Reichelt S, Heintzmann R, Schermelleh L (2021) Super-resolution structured illumination microscopy: past, present and future. Philos Trans A Math Phys Eng Sci 379: 20200143
    [52]
    Rodriguez C, Ji N (2018) Adaptive optical microscopy for neurobiology. Curr Opin Neurobiol 50: 83−91 doi: 10.1016/j.conb.2018.01.011
    [53]
    Saha D, Schmidt U, Zhang Q, Barbotin A, Hu Q, Ji N, Booth MJ, Weigert M, Myers EW (2020) Practical sensorless aberration estimation for 3D microscopy with deep learning. Opt Express 28: 29044−29053 doi: 10.1364/OE.401933
    [54]
    Sahl SJ, Hell SW, Jakobs S (2017) Fluorescence nanoscopy in cell biology. Nat Rev Mol Cell Biol 18: 685−701
    [55]
    Sauer M, Heilemann M (2017) Single-molecule localization microscopy in eukaryotes. Chem Rev 117: 7478−7509 doi: 10.1021/acs.chemrev.6b00667
    [56]
    Schermelleh L, Ferrand A, Huser T, Eggeling C, Sauer M, Biehlmaier O, Drummen GPC (2019) Super-resolution microscopy demystified. Nat Cell Biol 21: 72−84 doi: 10.1038/s41556-018-0251-8
    [57]
    Siemons M, Hulleman CN, Thorsen RO, Smith CS, and Stallinga S (2018) High precision wavefront control in point spread function engineering for single emitter localization. Opt Express 26: 8397−8416 doi: 10.1364/OE.26.008397
    [58]
    Siemons ME, Hanemaaijer NAK, Kole MHP, Kapitein LC (2021) Robust adaptive optics for localization microscopy deep in complex tissue. Nat Commun 12(1): 3407 doi: 10.1038/s41467-021-23647-2
    [59]
    Sigal YM, Zhou R, Zhuang X (2018) Visualizing and discovering cellular structures with super-resolution microscopy. Science 361: 880−887 doi: 10.1126/science.aau1044
    [60]
    Sulai YN, Dubra A (2014) Non-common path aberration correction in an adaptive optics scanning ophthalmoscope. Biomed Opt Express 5(9): 3059−3073 doi: 10.1364/BOE.5.003059
    [61]
    Tehrani KF, Xu J, Zhang Y, Shen P, Kner P (2015) Adaptive optics stochastic optical reconstruction microscopy (AO-STORM) using a genetic algorithm. Opt Express 23: 13677−13692 doi: 10.1364/OE.23.013677
    [62]
    Tehrani KF, Zhang Y, Shen P, Kner P (2017) Adaptive optics stochastic optical reconstruction microscopy (AO-STORM) by particle swarm optimization. Biomed Opt Express 8: 5087−5097 doi: 10.1364/BOE.8.005087
    [63]
    Thomas B, Wolstenholme A, Chaudhari SN, Kipreos ET, Kner P (2015) Enhanced resolution through thick tissue with structured illumination and adaptive optics. J Biomed Opt 20: 26006 doi: 10.1117/1.JBO.20.2.026006
    [64]
    Tian L, Hunt B, Bell MAL, Yi J, Smith JT, Ochoa M, Intes X, Durr NJ (2021) Deep learning in biomedical optics. Lasers Surg Med doi: 10.1002/lsm.23414
    [65]
    Turcotte R, Liang Y, Tanimoto M, Zhang Q, Li Z, Koyama M, Betzig E, Ji N (2019) Dynamic super-resolution structured illumination imaging in the living brain. Proc Natl Acad Sci USA 116: 9586−9591 doi: 10.1073/pnas.1819965116
    [66]
    Urban NT, Willig KI, Hell SW, Nagerl UV (2011) STED nanoscopy of actin dynamics in synapses deep inside living brain slices. Biophys J 101: 1277−1284 doi: 10.1016/j.bpj.2011.07.027
    [67]
    Velasco MGM, Zhang MY, Antonello J, Yuan P, Allgeyer ES, May D, M'Saad O, Kidd P, Barentine AES, Greco V, Grutzendler J, Booth MJ, Bewersdorf J (2021) 3D super-resolution deep-tissue imaging in living mice. Optica 8: 442−450 doi: 10.1364/OPTICA.416841
    [68]
    Vicidomini G, Bianchini P, Diaspro A (2018) STED super-resolved microscopy. Nat Methods 15: 173−182 doi: 10.1038/nmeth.4593
    [69]
    von Diezmann A, Lee MY, Lew MD, Moerner WE (2015) Correcting field-dependent aberrations with nanoscale accuracy in three-dimensional single-molecule localization microscopy. Optica 2: 985−993 doi: 10.1364/OPTICA.2.000985
    [70]
    Wahl DJ, Zhang P, Mocci J, Quintavalla M, Muradore R, Jian Y, Bonora S, Sarunic MV, Zawadzki RJ (2019) Adaptive optics in the mouse eye: wavefront sensing based vs. image-guided aberration correction. Biomed Opt Express 10: 4757−4774
    [71]
    Wang Z, Cai Y, Liang Y, Dan D, Yao B, Lei M (2018) Aberration correction method based on double-helix point spread function. J Biomed Opt 24: 1−11
    [72]
    Wright AJ, Burns D, Patterson BA, Poland SP, Valentine GJ, Girkin JM (2005) Exploration of the optimisation algorithms used in the implementation of adaptive optics in confocal and multiphoton microscopy. Microsc Res Tech 67: 36−44 doi: 10.1002/jemt.20178
    [73]
    Wu Y, Shroff H (2018) Faster, sharper, and deeper: structured illumination microscopy for biological imaging. Nat Methods 15: 1011−1019 doi: 10.1038/s41592-018-0211-z
    [74]
    Xu F, Ma D, MacPherson KP, Liu S, Bu Y, Wang Y, Tang Y, Bi C, Kwok T, Chubykin AA, Yin P, Calve S, Landreth GE, Huang F (2020) Three-dimensional nanoscopy of whole cells and tissues with in situ point spread function retrieval. Nat Methods 17: 531−540 doi: 10.1038/s41592-020-0816-x
    [75]
    Zdankowski P, McGloin D, Swedlow JR (2019) Full volume super-resolution imaging of thick mitotic spindle using 3D AO STED microscope. Biomed Opt Express 10: 1999−2009 doi: 10.1364/BOE.10.001999
    [76]
    Zdankowski P, Trusiak M, McGloin D, Swedlow JR (2020) Numerically enhanced stimulated emission depletion microscopy with adaptive optics for deep-tissue super-resolved imaging. ACS Nano 14: 394−405 doi: 10.1021/acsnano.9b05891
    [77]
    Zhang P, Liu S, Chaurasia A, Ma D, Mlodzianoski MJ, Culurciello E, Huang F (2018) Analyzing complex single-molecule emission patterns with deep learning. Nat Methods 15: 913−916 doi: 10.1038/s41592-018-0153-5
    [78]
    Zhang Y, Wu C, Song Y, Si K, Zheng Y, Hu L, Chen J, Tang L, Gong W (2019) Machine learning based adaptive optics for doughnut-shaped beam. Opt Express 27: 16871−16881 doi: 10.1364/OE.27.016871
    [79]
    Zheng W, Wu Y, Winter P, Shroff H (2018) Adaptive optics improves multiphoton super-resolution imaging. Proceedings Volume 10502, Adaptive Optics and Wavefront Control for Biological Systems IV doi: https://doi.org/10.1117/12.2288155
    [80]
    Zheng Y, Chen J, Wu C, Gong W, Si K (2021) Adaptive optics for structured illumination microscopy based on deep learning. Cytometry A 99: 622−631 doi: 10.1002/cyto.a.24319
    [81]
    Zurauskas M, Dobbie IM, Parton RM, Phillips MA, Gohler A, Davis I, Booth MJ (2019) IsoSense: frequency enhanced sensorless adaptive optics through structured illumination. Optica 6: 370−379 doi: 10.1364/OPTICA.6.000370
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