Compressive three-dimensional super-resolution microscopy with speckle-saturated fluorescence excitation

Nonlinear structured illumination microscopy (nSIM) is an effective approach for super-resolution wide-field fluorescence microscopy with a theoretically unlimited resolution. In nSIM, carefully designed, highly-contrasted illumination patterns are combined with the saturation of an optical transition to enable sub-diffraction imaging. While the technique proved useful for two-dimensional imaging, extending it to three-dimensions is challenging due to the fading of organic fluorophores under intense cycling conditions. Here, we present a compressed sensing approach that allows 3D sub-diffraction nSIM of cultured cells by saturating fluorescence excitation. Exploiting the natural orthogonality of speckles at different axial planes, 3D probing of the sample is achieved by a single two-dimensional scan. Fluorescence contrast under saturated excitation is ensured by the inherent high density of intensity minima associated with optical vortices in polarized speckle patterns. Compressed speckle microscopy is thus a simple approach that enables 3D super-resolved nSIM imaging with potentially considerably reduced acquisition time and photobleaching.Nonlinear structured illumination microscopy is a super-resolution technique that is challenging to extend to 3 dimensions. The authors obtain super-resolution image information in 3D from a 2D scan by exploiting orthogonal speckle illumination patterns and compressed sensing of the sparse fluorescence.

[1]  V. Emiliani,et al.  Superresolution Imaging of Optical Vortices in a Speckle Pattern. , 2016, Physical review letters.

[2]  J. Bertolotti,et al.  Exploiting speckle correlations to improve the resolution of wide-field fluorescence microscopy , 2014, 1410.2079.

[3]  Mark R. Dennis,et al.  Phase singularities in isotropic random waves , 2000, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[4]  I. Freund,et al.  Parameterization of anisotropic vortices , 1997 .

[5]  Irving S. Reed,et al.  On a moment theorem for complex Gaussian processes , 1962, IRE Trans. Inf. Theory.

[6]  Laura Waller,et al.  Structured illumination microscopy with unknown patterns and a statistical prior , 2016, Biomedical optics express.

[7]  Marc Teboulle,et al.  A Fast Iterative Shrinkage-Thresholding Algorithm for Linear Inverse Problems , 2009, SIAM J. Imaging Sci..

[8]  David L Donoho,et al.  Compressed sensing , 2006, IEEE Transactions on Information Theory.

[9]  M. Berry,et al.  Dislocations in wave trains , 1974, Proceedings of the Royal Society of London. A. Mathematical and Physical Sciences.

[10]  Parameterization and orbital angular momentum of anisotropic dislocations , 1996 .

[11]  Xiaoqing Xu,et al.  Extended depth-resolved imaging through a thin scattering medium with PSF manipulation , 2018, Scientific Reports.

[12]  I. Freund Looking through walls and around corners , 1990 .

[13]  M. Gustafsson Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[14]  D. Psaltis,et al.  Imaging blood cells through scattering biological tissue using speckle scanning microscopy. , 2013, Optics express.

[15]  G. Raposo,et al.  Myosin 1b promotes the formation of post-Golgi carriers by regulating actin assembly and membrane remodelling at the trans-Golgi network , 2011, Nature Cell Biology.

[16]  J. Lippincott-Schwartz,et al.  Imaging Intracellular Fluorescent Proteins at Nanometer Resolution , 2006, Science.

[17]  Sjoerd Stallinga,et al.  Studying different illumination patterns for resolution improvement in fluorescence microscopy. , 2015, Optics express.

[18]  O. Katz,et al.  Compressive ghost imaging , 2009, 0905.0321.

[19]  Hui Cao,et al.  Customizing Speckle Intensity Statistics , 2017, 1711.11128.

[20]  Xu Liu,et al.  Effects of polarization on the de-excitation dark focal spot in STED microscopy , 2010 .

[21]  Michael Unser,et al.  DeconvolutionLab2: An open-source software for deconvolution microscopy. , 2017, Methods.

[22]  S. Bernet,et al.  Lensless digital holography with diffuse illumination through a pseudo-random phase mask. , 2011, Optics express.

[23]  E.J. Candes,et al.  An Introduction To Compressive Sampling , 2008, IEEE Signal Processing Magazine.

[24]  François Chapeau-Blondeau,et al.  Exploiting the speckle noise for compressive imaging , 2011 .

[25]  E. Candès,et al.  Compressive fluorescence microscopy for biological and hyperspectral imaging , 2012, Proceedings of the National Academy of Sciences.

[26]  S. Hell,et al.  Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. , 1994, Optics letters.

[27]  Anne Sentenac,et al.  Structured illumination microscopy using unknown speckle patterns , 2012, Nature Photonics.

[28]  R. Heintzmann,et al.  Saturated patterned excitation microscopy--a concept for optical resolution improvement. , 2002, Journal of the Optical Society of America. A, Optics, image science, and vision.

[29]  S. Hell,et al.  Nanoscale resolution in GFP-based microscopy , 2006, Nature Methods.

[30]  M. Gustafsson Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy , 2000, Journal of microscopy.

[31]  Mark R. Dennis,et al.  Topology of light's darkness. , 2009, Physical review letters.

[32]  Brahim Lounis,et al.  Large parallelization of STED nanoscopy using optical lattices. , 2013, Optics express.

[33]  D. L. Donoho,et al.  Compressed sensing , 2006, IEEE Trans. Inf. Theory.

[34]  Ick,et al.  DiffuserCam : Lensless Single-exposure 3 D Imaging , 2017 .

[35]  J. Durnin Exact solutions for nondiffracting beams. I. The scalar theory , 1987 .

[36]  Patricia Bassereau,et al.  Catch-bond behaviour facilitates membrane tubulation by non-processive myosin 1b , 2014, Nature Communications.

[37]  Jong Chul Ye,et al.  Fluorescent microscopy beyond diffraction limits using speckle illumination and joint support recovery , 2013, Scientific Reports.

[38]  Jérôme Idier,et al.  Joint Reconstruction Strategy for Structured Illumination Microscopy With Unknown Illuminations , 2016, IEEE Transactions on Image Processing.

[39]  Alberto Diaspro,et al.  Strategies to maximize the performance of a STED microscope. , 2012, Optics express.

[40]  Zeev Zalevsky,et al.  The Limitations of Nonlinear Fluorescence Effect in Super Resolution Saturated Structured Illumination Microscopy System , 2011, Journal of Fluorescence.

[41]  M. R. Dennis Local phase structure of wave dislocation lines: twist and twirl , 2003 .

[42]  Christian Eggeling,et al.  Nanoscopy with more than 100,000 'doughnuts' , 2013, Nature Methods.

[43]  Steffen J Sahl,et al.  2000-fold parallelized dual-color STED fluorescence nanoscopy. , 2015, Optics express.

[44]  M. Carlier,et al.  Dimeric WH2 domains in Vibrio VopF promote actin filament barbed-end uncapping and assisted elongation , 2013, Nature Structural &Molecular Biology.

[45]  Isaac Freund,et al.  OPTICAL VORTICES IN GAUSSIAN RANDOM WAVE FIELDS : STATISTICAL PROBABILITY DENSITIES , 1994 .

[46]  Satoshi Kawata,et al.  High-resolution confocal microscopy by saturated excitation of fluorescence. , 2007, Physical review letters.

[47]  M. Gustafsson,et al.  Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. , 2008, Biophysical journal.

[48]  H. Rigneault,et al.  Complementary Speckle Patterns: Deterministic Interchange of Intrinsic Vortices and Maxima through Scattering Media. , 2016, Physical review letters.

[49]  P. Gestraud,et al.  Cdc42 controls the dilation of the exocytotic fusion pore by regulating membrane tension , 2014, Molecular biology of the cell.

[50]  James R Fienup,et al.  Phase retrieval algorithms: a personal tour [Invited]. , 2013, Applied optics.

[51]  Jerome Mertz,et al.  Optical sectioning microscopy with planar or structured illumination , 2011, Nature Methods.

[52]  Christian Eggeling,et al.  Breaking the diffraction barrier in fluorescence microscopy by optical shelving. , 2007, Physical review letters.

[53]  Laura Waller,et al.  DiffuserCam: Lensless Single-exposure 3D Imaging , 2017, ArXiv.

[54]  Giuliano Scarcelli,et al.  Memory-effect based deconvolution microscopy for super-resolution imaging through scattering media , 2016, Scientific Reports.

[55]  Hui Cao,et al.  Generating Non-Rayleigh Speckles with Tailored Intensity Statistics , 2014, 1401.7662.

[56]  Ales Benda,et al.  Optical saturation as a versatile tool to enhance resolution in confocal microscopy. , 2009, Biophysical journal.

[57]  Christian Eggeling,et al.  Major signal increase in fluorescence microscopy through dark-state relaxation , 2007, Nature Methods.

[58]  J. Bertolotti,et al.  Speckle correlation resolution enhancement of wide-field fluorescence imaging , 2015 .

[59]  Yonina C. Eldar,et al.  Photoacoustic imaging beyond the acoustic diffraction-limit with dynamic speckle illumination and sparse joint support recovery , 2016, Optics express.

[60]  J. Bertolotti,et al.  Non-invasive imaging through opaque scattering layers , 2012, Nature.

[61]  Zeev Zalevsky,et al.  Synthetic aperture superresolution by speckle pattern projection. , 2005, Optics express.

[62]  Keng C Chou,et al.  Review of Super-Resolution Fluorescence Microscopy for Biology , 2011, Applied spectroscopy.

[63]  Liang Gao,et al.  3D live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy , 2014, Nature Protocols.

[64]  Andreas Schönle,et al.  Resolution scaling in STED microscopy. , 2008, Optics express.

[65]  J. J. Macklin,et al.  Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution , 2011, Proceedings of the National Academy of Sciences.

[66]  Michael J Rust,et al.  Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) , 2006, Nature Methods.