Superresolution microscope image reconstruction by spatiotemporal object decomposition and association: application in resolving t-tubule structure in skeletal muscle

Mingzhai Sun; Jiaqing Huang; Filiz Bunyak; Kristyn Gumpper; Gejing De; Matthew Sermersheim; George Liu; Pei-Hui Lin; Kannappan Palaniappan; Jianjie Ma

doi:10.1364/OE.22.012160

Superresolution microscope image reconstruction by spatiotemporal object decomposition and association: application in resolving t-tubule structure in skeletal muscle

Mingzhai Sun, Jiaqing Huang, Filiz Bunyak, Kristyn Gumpper, Gejing De, Matthew Sermersheim, George Liu, Pei-Hui Lin, Kannappan Palaniappan, and Jianjie Ma

Optics Express
Vol. 22,
Issue 10,
pp. 12160-12176
(2014)
•https://doi.org/10.1364/OE.22.012160

Get Citation
Copy Citation Text
Mingzhai Sun, Jiaqing Huang, Filiz Bunyak, Kristyn Gumpper, Gejing De, Matthew Sermersheim, George Liu, Pei-Hui Lin, Kannappan Palaniappan, and Jianjie Ma, "Superresolution microscope image reconstruction by spatiotemporal object decomposition and association: application in resolving t-tubule structure in skeletal muscle," Opt. Express 22, 12160-12176 (2014)

Export Citation
- BibTex
- Endnote (RIS)
- HTML
- Plain Text
Get PDF (3148 KB)
Set citation alerts
Save article

Related Topics
Table of Contents Category
- Image Processing
Optics & Photonics Topics
?

The topics in this list come from the OSA Optics and Photonics Topics applied to this article.
Previously assigned OCIS codes
- Biology and medicine (000.1430)
- Image processing (100.0100)
- Superresolution (100.6640)
- Multiframe image processing (110.4155)
- Microscopy (180.0180)

About this Article
History
- Original Manuscript: December 26, 2013
- Revised Manuscript: March 5, 2014
- Manuscript Accepted: April 1, 2014
- Published: May 13, 2014
Virtual Issues
Virtual Journal for Biomedical Optics Vol. 9, Iss. 7

Accessible

Open Access

Abstract

One key factor that limits resolution of single-molecule superresolution microscopy relates to the localization accuracy of the activated emitters, which is usually deteriorated by two factors. One originates from the background noise due to out-of-focus signals, sample auto-fluorescence, and camera acquisition noise; and the other is due to the low photon count of emitters at a single frame. With fast acquisition rate, the activated emitters can last multiple frames before they transiently switch off or permanently bleach. Effectively incorporating the temporal information of these emitters is critical to improve the spatial resolution. However, majority of the existing reconstruction algorithms locate the emitters frame by frame, discarding or underusing the temporal information. Here we present a new image reconstruction algorithm based on tracklets, short trajectories of the same objects. We improve the localization accuracy by associating the same emitters from multiple frames to form tracklets and by aggregating signals to enhance the signal to noise ratio. We also introduce a weighted mean-shift algorithm (WMS) to automatically detect the number of modes (emitters) in overlapping regions of tracklets so that not only well-separated single emitters but also individual emitters within multi-emitter groups can be identified and tracked. In combination with a maximum likelihood estimator method (MLE), we are able to resolve low to medium density of overlapping emitters with improved localization accuracy. We evaluate the performance of our method with both synthetic and experimental data, and show that the tracklet-based reconstruction is superior in localization accuracy, particularly for weak signals embedded in a strong background. Using this method, for the first time, we resolve the transverse tubule structure of the mammalian skeletal muscle.

Full Article | PDF Article

OSA Recommended Articles

Comparison between SOFI and STORM

Stefan Geissbuehler, Claudio Dellagiacoma, and Theo Lasser
Biomed. Opt. Express 2(3) 408-420 (2011)

3D multifocus astigmatism and compressed sensing (3D MACS) based superresolution reconstruction

Jiaqing Huang, Mingzhai Sun, Kristyn Gumpper, Yuejie Chi, and Jianjie Ma
Biomed. Opt. Express 6(3) 902-917 (2015)

Phase stretch transform for super-resolution localization microscopy

Tali Ilovitsh, Bahram Jalali, Mohammad H. Asghari, and Zeev Zalevsky
Biomed. Opt. Express 7(10) 4198-4209 (2016)

References

View by:
Article Order
|
Year
|
Author
|
Publication

M. Born and E. Wolf, Principles of Optics: Electromagnetic Theory of Propagation, Interference and Diffraction of Light, 7th ed. (Cambridge University, 1975).
S. W. Hell, “Far-field optical nanoscopy,” Science 316(5828), 1153–1158 (2007).
[Crossref] [PubMed]
B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
[Crossref] [PubMed]
G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
[Crossref] [PubMed]
K. R. Chi, “Microscopy: Ever-increasing resolution,” Nature 462(7273), 675–678 (2009).
[Crossref] [PubMed]
S. W. Hell and J. Wichmann, “Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy,” Opt. Lett. 19(11), 780–782 (1994).
[Crossref] [PubMed]
M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
[Crossref] [PubMed]
J. Fölling, M. Bossi, H. Bock, R. Medda, C. A. Wurm, B. Hein, S. Jakobs, C. Eggeling, and S. W. Hell, “Fluorescence nanoscopy by ground-state depletion and single-molecule return,” Nat. Methods 5(11), 943–945 (2008).
[Crossref] [PubMed]
T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, “Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI),” Proc. Natl. Acad. Sci. U.S.A. 106(52), 22287–22292 (2009).
[Crossref] [PubMed]
M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]
M. Heilemann, S. van de Linde, M. Schuttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem-Ger. Edit. 47(33), 6172–6176 (2008).
[Crossref]
M. Heilemann, S. van de Linde, A. Mukherjee, and M. Sauer, “Super-resolution imaging with small organic fluorophores,” Angew. Chem. Int. Ed. Engl. 48(37), 6903–6908 (2009).
[Crossref] [PubMed]
E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[Crossref] [PubMed]
S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91(11), 4258–4272 (2006).
[Crossref] [PubMed]
J. C. Vaughan, S. Jia, and X. Zhuang, “Ultrabright photoactivatable fluorophores created by reductive caging,” Nat. Methods 9(12), 1181–1184 (2012).
[Crossref] [PubMed]
A. Pertsinidis, K. Mukherjee, M. Sharma, Z. P. Pang, S. R. Park, Y. Zhang, A. T. Brunger, T. C. Südhof, and S. Chu, “Ultrahigh-resolution imaging reveals formation of neuronal SNARE/Munc18 complexes in situ,” Proc. Natl. Acad. Sci. U.S.A. 110(30), E2812–E2820 (2013).
[Crossref] [PubMed]
A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
[Crossref] [PubMed]
H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Methods 5(5), 417–423 (2008).
[Crossref] [PubMed]
S. A. Jones, S. H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[Crossref] [PubMed]
B. Zhang, J. Zerubia, and J. C. Olivo-Marin, “Gaussian approximations of fluorescence microscope point-spread function models,” Appl. Opt. 46(10), 1819–1829 (2007).
[Crossref] [PubMed]
S. Stallinga and B. Rieger, “Accuracy of the gaussian point spread function model in 2D localization microscopy,” Opt. Express 18(24), 24461–24476 (2010).
[Crossref] [PubMed]
F. Huang, S. L. Schwartz, J. M. Byars, and K. A. Lidke, “Simultaneous multiple-emitter fitting for single molecule super-resolution imaging,” Biomed. Opt. Express 2(5), 1377–1393 (2011).
[Crossref] [PubMed]
R. E. Thompson, D. R. Larson, and W. W. Webb, “Precise nanometer localization analysis for individual fluorescent probes,” Biophys. J. 82(5), 2775–2783 (2002).
[Crossref] [PubMed]
D. Sage, F. R. Neumann, F. Hediger, S. M. Gasser, and M. Unser, “Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics,” IEEE Trans. Image Process. 14(9), 1372–1383 (2005).
[Crossref] [PubMed]
J. L. Starck, F. Murtagh, and A. Bijaoui, “Multiresolution support applied to image filtering and restoration,” Graph Model Im. Pro. C. 57(5), 420–431 (1995).
[Crossref]
K. Fukunaga and L. Hostetler, “The estimation of the gradient of a density function, with applications in pattern recognition,” IEEE Trans. Inf. Theory 21(1), 32–40 (1975).
[Crossref]
Y. Cheng, “Mean shift, mode seeking, and clustering,” IEEE T. Pattern Anal. 17(8), 790–799 (1995).
[Crossref]
K. L. Wu and M. S. Yang, “Mean shift-based clustering,” Pattern Recognit. 40(11), 3035–3052 (2007).
[Crossref]
E. Meijering, I. Smal, O. Dzyubachyk, and J.-C. Olivo-Marin, “Time-lapse imaging,” Microsc. Img. Proc. 401-440 (2008).
E. Meijering, O. Dzyubachyk, and I. Smal, “Methods for cell and particle tracking,” Methods Enzymol. 504, 183–200 (2012).
[Crossref] [PubMed]
K. Jaqaman, D. Loerke, M. Mettlen, H. Kuwata, S. Grinstein, S. L. Schmid, and G. Danuser, “Robust single-particle tracking in live-cell time-lapse sequences,” Nat. Methods 5(8), 695–702 (2008).
[Crossref] [PubMed]
F. H. Li, X. B. Zhou, J. W. Ma, and S. T. C. Wong, “Multiple nuclei tracking using integer programming for quantitative cancer cell cycle analysis,” IEEE Trans. Med. Imaging 29(1), 96–105 (2010).
[Crossref] [PubMed]
T. Kanade, Z. Yin, R. Bise, S. Huh, and S. Eom, “Cell image analysis: algorithms, system and applications,” IEEE Work. App. Comp. (2011).
F. Bunyak, K. Palaniappan, S. K. Nath, T. L. Baskin, and G. Dong, “Quantitative cell motility for in vitro wound healing using level set-based active contour tracking,” I. S. Biomed. Imaging 1040–1043 (2006).
K. Palaniappan, F. Bunyak, S. Nath, and J. Goffeney, “Parallel Processing Strategies for Cell Motility and Shape Analysis,” High-Throughput Image Reconstruction and Analysis, Artech House Publisher, 39–87 (2009).
B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-Dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[Crossref] [PubMed]
M. Bates, S. A. Jones, and X. Zhuang, “Stochastic optical reconstruction microscopy (STORM): a method for superresolution fluorescence imaging,” Cold Spring Harb Protoc 2013(6), 498–520 (2013).
[Crossref] [PubMed]
H. Takeshima, M. Shimuta, S. Komazaki, K. Ohmi, M. Nishi, M. Iino, A. Miyata, and K. Kangawa, “Mitsugumin29, a novel synaptophysin family member from the triad junction in skeletal muscle,” Biochem. J. 331(Pt 1), 317–322 (1998).
[PubMed]
S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods 8(4), 279–280 (2011).
[Crossref] [PubMed]
L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat. Methods 9(7), 721–723 (2012).
[Crossref] [PubMed]
T. Quan, H. Zhu, X. Liu, Y. Liu, J. Ding, S. Zeng, and Z. L. Huang, “High-density localization of active molecules using Structured Sparse Model and Bayesian Information Criterion,” Opt. Express 19(18), 16963–16974 (2011).
[Crossref] [PubMed]
Y. Wang, T. Quan, S. Zeng, and Z. L. Huang, “PALMER: a method capable of parallel localization of multiple emitters for high-density localization microscopy,” Opt. Express 20(14), 16039–16049 (2012).
[Crossref] [PubMed]
H. P. Babcock, J. R. Moffitt, Y. Cao, and X. Zhuang, “Fast compressed sensing analysis for super-resolution imaging using L1-homotopy,” Opt. Express 21(23), 28583–28596 (2013).
[Crossref] [PubMed]
E. A. Mukamel, H. Babcock, and X. Zhuang, “Statistical deconvolution for superresolution fluorescence microscopy,” Biophys. J. 102(10), 2391–2400 (2012).
[Crossref] [PubMed]
Y. Deng, P. Coen, M. Sun, and J. W. Shaevitz, “Efficient multiple object tracking using mutually repulsive active membranes,” PLoS ONE 8(6), e65769 (2013).
[Crossref] [PubMed]
P. Dedecker, S. Duwé, R. K. Neely, and J. Zhang, “Localizer: fast, accurate, open-source, and modular software package for superresolution microscopy,” J. Biomed. Opt. 17(12), 126008 (2012).
[Crossref] [PubMed]
C. Franzini-Armstrong, J. E. Heuser, T. S. Reese, A. P. Somlyo, and A. V. Somlyo, “T-tubule swelling in hypertonic solutions: a freeze substitution study,” J. Physiol. 283, 133–140 (1978).
[PubMed]
E. Wagner, M. A. Lauterbach, T. Kohl, V. Westphal, G. S. B. Williams, J. H. Steinbrecher, J. H. Streich, B. Korff, H. T. M. Tuan, B. Hagen, S. Luther, G. Hasenfuss, U. Parlitz, M. S. Jafri, S. W. Hell, W. J. Lederer, and S. E. Lehnart, “Stimulated emission depletion live-cell super-resolution imaging shows proliferative remodeling of T-tubule membrane structures after myocardial infarction,” Circ. Res. 111(4), 402–414 (2012).
[Crossref] [PubMed]
S. Komazaki, M. Nishi, K. Kangawa, and H. Takeshima, “Immunolocalization of mitsugumin29 in developing skeletal muscle and effects of the protein expressed in amphibian embryonic cells,” Dev. Dyn. 215(2), 87–95 (1999).
[Crossref] [PubMed]
Z. Pan, D. Yang, R. Y. Nagaraj, T. A. Nosek, M. Nishi, H. Takeshima, H. Cheng, and J. Ma, “Dysfunction of store-operated calcium channel in muscle cells lacking mg29,” Nat. Cell Biol. 4(5), 379–383 (2002).
[Crossref] [PubMed]
S. Cox, E. Rosten, J. Monypenny, T. Jovanovic-Talisman, D. T. Burnette, J. Lippincott-Schwartz, G. E. Jones, and R. Heintzmann, “Bayesian localization microscopy reveals nanoscale podosome dynamics,” Nat. Methods 9(2), 195–200 (2011).
[Crossref] [PubMed]
E. Rosten, G. E. Jones, and S. Cox, “ImageJ plug-in for Bayesian analysis of blinking and bleaching,” Nat. Methods 10(2), 97–98 (2013).
[Crossref] [PubMed]
Y. S. Hu, X. Nan, P. Sengupta, J. Lippincott-Schwartz, and H. Cang, “Accelerating 3B single-molecule super-resolution microscopy with cloud computing,” Nat. Methods 10(2), 96–97 (2013).
[Crossref] [PubMed]

2013 (6)

A. Pertsinidis, K. Mukherjee, M. Sharma, Z. P. Pang, S. R. Park, Y. Zhang, A. T. Brunger, T. C. Südhof, and S. Chu, “Ultrahigh-resolution imaging reveals formation of neuronal SNARE/Munc18 complexes in situ,” Proc. Natl. Acad. Sci. U.S.A. 110(30), E2812–E2820 (2013).
[Crossref] [PubMed]

M. Bates, S. A. Jones, and X. Zhuang, “Stochastic optical reconstruction microscopy (STORM): a method for superresolution fluorescence imaging,” Cold Spring Harb Protoc 2013(6), 498–520 (2013).
[Crossref] [PubMed]

H. P. Babcock, J. R. Moffitt, Y. Cao, and X. Zhuang, “Fast compressed sensing analysis for super-resolution imaging using L1-homotopy,” Opt. Express 21(23), 28583–28596 (2013).
[Crossref] [PubMed]

Y. Deng, P. Coen, M. Sun, and J. W. Shaevitz, “Efficient multiple object tracking using mutually repulsive active membranes,” PLoS ONE 8(6), e65769 (2013).
[Crossref] [PubMed]

E. Rosten, G. E. Jones, and S. Cox, “ImageJ plug-in for Bayesian analysis of blinking and bleaching,” Nat. Methods 10(2), 97–98 (2013).
[Crossref] [PubMed]

Y. S. Hu, X. Nan, P. Sengupta, J. Lippincott-Schwartz, and H. Cang, “Accelerating 3B single-molecule super-resolution microscopy with cloud computing,” Nat. Methods 10(2), 96–97 (2013).
[Crossref] [PubMed]

2012 (7)

P. Dedecker, S. Duwé, R. K. Neely, and J. Zhang, “Localizer: fast, accurate, open-source, and modular software package for superresolution microscopy,” J. Biomed. Opt. 17(12), 126008 (2012).
[Crossref] [PubMed]

E. A. Mukamel, H. Babcock, and X. Zhuang, “Statistical deconvolution for superresolution fluorescence microscopy,” Biophys. J. 102(10), 2391–2400 (2012).
[Crossref] [PubMed]

E. Wagner, M. A. Lauterbach, T. Kohl, V. Westphal, G. S. B. Williams, J. H. Steinbrecher, J. H. Streich, B. Korff, H. T. M. Tuan, B. Hagen, S. Luther, G. Hasenfuss, U. Parlitz, M. S. Jafri, S. W. Hell, W. J. Lederer, and S. E. Lehnart, “Stimulated emission depletion live-cell super-resolution imaging shows proliferative remodeling of T-tubule membrane structures after myocardial infarction,” Circ. Res. 111(4), 402–414 (2012).
[Crossref] [PubMed]

Y. Wang, T. Quan, S. Zeng, and Z. L. Huang, “PALMER: a method capable of parallel localization of multiple emitters for high-density localization microscopy,” Opt. Express 20(14), 16039–16049 (2012).
[Crossref] [PubMed]

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat. Methods 9(7), 721–723 (2012).
[Crossref] [PubMed]

E. Meijering, O. Dzyubachyk, and I. Smal, “Methods for cell and particle tracking,” Methods Enzymol. 504, 183–200 (2012).
[Crossref] [PubMed]

J. C. Vaughan, S. Jia, and X. Zhuang, “Ultrabright photoactivatable fluorophores created by reductive caging,” Nat. Methods 9(12), 1181–1184 (2012).
[Crossref] [PubMed]

2011 (5)

S. A. Jones, S. H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[Crossref] [PubMed]

F. Huang, S. L. Schwartz, J. M. Byars, and K. A. Lidke, “Simultaneous multiple-emitter fitting for single molecule super-resolution imaging,” Biomed. Opt. Express 2(5), 1377–1393 (2011).
[Crossref] [PubMed]

T. Quan, H. Zhu, X. Liu, Y. Liu, J. Ding, S. Zeng, and Z. L. Huang, “High-density localization of active molecules using Structured Sparse Model and Bayesian Information Criterion,” Opt. Express 19(18), 16963–16974 (2011).
[Crossref] [PubMed]

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods 8(4), 279–280 (2011).
[Crossref] [PubMed]

S. Cox, E. Rosten, J. Monypenny, T. Jovanovic-Talisman, D. T. Burnette, J. Lippincott-Schwartz, G. E. Jones, and R. Heintzmann, “Bayesian localization microscopy reveals nanoscale podosome dynamics,” Nat. Methods 9(2), 195–200 (2011).
[Crossref] [PubMed]

2010 (4)

F. H. Li, X. B. Zhou, J. W. Ma, and S. T. C. Wong, “Multiple nuclei tracking using integer programming for quantitative cancer cell cycle analysis,” IEEE Trans. Med. Imaging 29(1), 96–105 (2010).
[Crossref] [PubMed]

S. Stallinga and B. Rieger, “Accuracy of the gaussian point spread function model in 2D localization microscopy,” Opt. Express 18(24), 24461–24476 (2010).
[Crossref] [PubMed]

A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
[Crossref] [PubMed]

G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
[Crossref] [PubMed]

2009 (4)

K. R. Chi, “Microscopy: Ever-increasing resolution,” Nature 462(7273), 675–678 (2009).
[Crossref] [PubMed]

B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
[Crossref] [PubMed]

T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, “Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI),” Proc. Natl. Acad. Sci. U.S.A. 106(52), 22287–22292 (2009).
[Crossref] [PubMed]

M. Heilemann, S. van de Linde, A. Mukherjee, and M. Sauer, “Super-resolution imaging with small organic fluorophores,” Angew. Chem. Int. Ed. Engl. 48(37), 6903–6908 (2009).
[Crossref] [PubMed]

2008 (5)

M. Heilemann, S. van de Linde, M. Schuttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, and M. Sauer, “Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes,” Angew. Chem-Ger. Edit. 47(33), 6172–6176 (2008).
[Crossref]

H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Methods 5(5), 417–423 (2008).
[Crossref] [PubMed]

J. Fölling, M. Bossi, H. Bock, R. Medda, C. A. Wurm, B. Hein, S. Jakobs, C. Eggeling, and S. W. Hell, “Fluorescence nanoscopy by ground-state depletion and single-molecule return,” Nat. Methods 5(11), 943–945 (2008).
[Crossref] [PubMed]

K. Jaqaman, D. Loerke, M. Mettlen, H. Kuwata, S. Grinstein, S. L. Schmid, and G. Danuser, “Robust single-particle tracking in live-cell time-lapse sequences,” Nat. Methods 5(8), 695–702 (2008).
[Crossref] [PubMed]

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-Dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[Crossref] [PubMed]

2007 (3)

K. L. Wu and M. S. Yang, “Mean shift-based clustering,” Pattern Recognit. 40(11), 3035–3052 (2007).
[Crossref]

S. W. Hell, “Far-field optical nanoscopy,” Science 316(5828), 1153–1158 (2007).
[Crossref] [PubMed]

B. Zhang, J. Zerubia, and J. C. Olivo-Marin, “Gaussian approximations of fluorescence microscope point-spread function models,” Appl. Opt. 46(10), 1819–1829 (2007).
[Crossref] [PubMed]

2006 (3)

E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, “Imaging intracellular fluorescent proteins at nanometer resolution,” Science 313(5793), 1642–1645 (2006).
[Crossref] [PubMed]

S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91(11), 4258–4272 (2006).
[Crossref] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

2005 (1)

D. Sage, F. R. Neumann, F. Hediger, S. M. Gasser, and M. Unser, “Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics,” IEEE Trans. Image Process. 14(9), 1372–1383 (2005).
[Crossref] [PubMed]

2002 (2)

R. E. Thompson, D. R. Larson, and W. W. Webb, “Precise nanometer localization analysis for individual fluorescent probes,” Biophys. J. 82(5), 2775–2783 (2002).
[Crossref] [PubMed]

Z. Pan, D. Yang, R. Y. Nagaraj, T. A. Nosek, M. Nishi, H. Takeshima, H. Cheng, and J. Ma, “Dysfunction of store-operated calcium channel in muscle cells lacking mg29,” Nat. Cell Biol. 4(5), 379–383 (2002).
[Crossref] [PubMed]

2000 (1)

M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
[Crossref] [PubMed]

1999 (1)

S. Komazaki, M. Nishi, K. Kangawa, and H. Takeshima, “Immunolocalization of mitsugumin29 in developing skeletal muscle and effects of the protein expressed in amphibian embryonic cells,” Dev. Dyn. 215(2), 87–95 (1999).
[Crossref] [PubMed]

1998 (1)

H. Takeshima, M. Shimuta, S. Komazaki, K. Ohmi, M. Nishi, M. Iino, A. Miyata, and K. Kangawa, “Mitsugumin29, a novel synaptophysin family member from the triad junction in skeletal muscle,” Biochem. J. 331(Pt 1), 317–322 (1998).
[PubMed]

1995 (2)

J. L. Starck, F. Murtagh, and A. Bijaoui, “Multiresolution support applied to image filtering and restoration,” Graph Model Im. Pro. C. 57(5), 420–431 (1995).
[Crossref]

Y. Cheng, “Mean shift, mode seeking, and clustering,” IEEE T. Pattern Anal. 17(8), 790–799 (1995).
[Crossref]

1994 (1)

S. W. Hell and J. Wichmann, “Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy,” Opt. Lett. 19(11), 780–782 (1994).
[Crossref] [PubMed]

1978 (1)

C. Franzini-Armstrong, J. E. Heuser, T. S. Reese, A. P. Somlyo, and A. V. Somlyo, “T-tubule swelling in hypertonic solutions: a freeze substitution study,” J. Physiol. 283, 133–140 (1978).
[PubMed]

1975 (1)

K. Fukunaga and L. Hostetler, “The estimation of the gradient of a density function, with applications in pattern recognition,” IEEE Trans. Inf. Theory 21(1), 32–40 (1975).
[Crossref]

Babcock, H.

E. A. Mukamel, H. Babcock, and X. Zhuang, “Statistical deconvolution for superresolution fluorescence microscopy,” Biophys. J. 102(10), 2391–2400 (2012).
[Crossref] [PubMed]

Babcock, H. P.

Bates, M.

B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
[Crossref] [PubMed]

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-Dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[Crossref] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

Betzig, E.

Bijaoui, A.

J. L. Starck, F. Murtagh, and A. Bijaoui, “Multiresolution support applied to image filtering and restoration,” Graph Model Im. Pro. C. 57(5), 420–431 (1995).
[Crossref]

Bock, H.

Bonifacino, J. S.

Bossi, M.

Brunger, A. T.

Burnette, D. T.

Byars, J. M.

Cang, H.

Cao, Y.

Cheng, H.

Cheng, Y.

Y. Cheng, “Mean shift, mode seeking, and clustering,” IEEE T. Pattern Anal. 17(8), 790–799 (1995).
[Crossref]

Chi, K. R.

K. R. Chi, “Microscopy: Ever-increasing resolution,” Nature 462(7273), 675–678 (2009).
[Crossref] [PubMed]

Chu, S.

A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
[Crossref] [PubMed]

Coen, P.

Y. Deng, P. Coen, M. Sun, and J. W. Shaevitz, “Efficient multiple object tracking using mutually repulsive active membranes,” PLoS ONE 8(6), e65769 (2013).
[Crossref] [PubMed]

Colyer, R.

Cox, S.

E. Rosten, G. E. Jones, and S. Cox, “ImageJ plug-in for Bayesian analysis of blinking and bleaching,” Nat. Methods 10(2), 97–98 (2013).
[Crossref] [PubMed]

Danuser, G.

Davidson, M.

G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
[Crossref] [PubMed]

Davidson, M. W.

Dedecker, P.

Deng, Y.

Y. Deng, P. Coen, M. Sun, and J. W. Shaevitz, “Efficient multiple object tracking using mutually repulsive active membranes,” PLoS ONE 8(6), e65769 (2013).
[Crossref] [PubMed]

Dertinger, T.

Ding, J.

Duwé, S.

Dzyubachyk, O.

E. Meijering, O. Dzyubachyk, and I. Smal, “Methods for cell and particle tracking,” Methods Enzymol. 504, 183–200 (2012).
[Crossref] [PubMed]

Eggeling, C.

Elnatan, D.

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat. Methods 9(7), 721–723 (2012).
[Crossref] [PubMed]

Enderlein, J.

Fölling, J.

Franzini-Armstrong, C.

Fukunaga, K.

K. Fukunaga and L. Hostetler, “The estimation of the gradient of a density function, with applications in pattern recognition,” IEEE Trans. Inf. Theory 21(1), 32–40 (1975).
[Crossref]

Galbraith, C. G.

Galbraith, J. A.

Gasser, S. M.

Girirajan, T. P. K.

Grinstein, S.

Gustafsson, M. G.

M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
[Crossref] [PubMed]

Hagen, B.

Hasenfuss, G.

He, J.

S. A. Jones, S. H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[Crossref] [PubMed]

Hediger, F.

Heilemann, M.

M. Heilemann, S. van de Linde, A. Mukherjee, and M. Sauer, “Super-resolution imaging with small organic fluorophores,” Angew. Chem. Int. Ed. Engl. 48(37), 6903–6908 (2009).
[Crossref] [PubMed]

Hein, B.

Heintzmann, R.

Hell, S. W.

S. W. Hell, “Far-field optical nanoscopy,” Science 316(5828), 1153–1158 (2007).
[Crossref] [PubMed]

Hess, H. F.

Hess, S. T.

Heuser, J. E.

Holden, S. J.

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods 8(4), 279–280 (2011).
[Crossref] [PubMed]

Hostetler, L.

K. Fukunaga and L. Hostetler, “The estimation of the gradient of a density function, with applications in pattern recognition,” IEEE Trans. Inf. Theory 21(1), 32–40 (1975).
[Crossref]

Hu, Y. S.

Huang, B.

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat. Methods 9(7), 721–723 (2012).
[Crossref] [PubMed]

B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
[Crossref] [PubMed]

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-Dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[Crossref] [PubMed]

Huang, F.

Huang, Z. L.

Iino, M.

Iyer, G.

Jafri, M. S.

Jakobs, S.

Jaqaman, K.

Jia, S.

J. C. Vaughan, S. Jia, and X. Zhuang, “Ultrabright photoactivatable fluorophores created by reductive caging,” Nat. Methods 9(12), 1181–1184 (2012).
[Crossref] [PubMed]

Jones, G. E.

E. Rosten, G. E. Jones, and S. Cox, “ImageJ plug-in for Bayesian analysis of blinking and bleaching,” Nat. Methods 10(2), 97–98 (2013).
[Crossref] [PubMed]

Jones, S. A.

S. A. Jones, S. H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[Crossref] [PubMed]

Jovanovic-Talisman, T.

Kangawa, K.

Kapanidis, A. N.

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods 8(4), 279–280 (2011).
[Crossref] [PubMed]

Kasper, R.

Kohl, T.

Komazaki, S.

Korff, B.

Kuwata, H.

Larson, D. R.

R. E. Thompson, D. R. Larson, and W. W. Webb, “Precise nanometer localization analysis for individual fluorescent probes,” Biophys. J. 82(5), 2775–2783 (2002).
[Crossref] [PubMed]

Lauterbach, M. A.

Lederer, W. J.

Lehnart, S. E.

Li, F. H.

Lidke, K. A.

Lindwasser, O. W.

Lippincott-Schwartz, J.

G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
[Crossref] [PubMed]

Liu, X.

Liu, Y.

Loerke, D.

Luther, S.

Ma, J.

Ma, J. W.

Manley, S.

G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
[Crossref] [PubMed]

Mason, M. D.

Medda, R.

Meijering, E.

E. Meijering, O. Dzyubachyk, and I. Smal, “Methods for cell and particle tracking,” Methods Enzymol. 504, 183–200 (2012).
[Crossref] [PubMed]

Mettlen, M.

Miyata, A.

Moffitt, J. R.

Monypenny, J.

Mukamel, E. A.

E. A. Mukamel, H. Babcock, and X. Zhuang, “Statistical deconvolution for superresolution fluorescence microscopy,” Biophys. J. 102(10), 2391–2400 (2012).
[Crossref] [PubMed]

Mukherjee, A.

M. Heilemann, S. van de Linde, A. Mukherjee, and M. Sauer, “Super-resolution imaging with small organic fluorophores,” Angew. Chem. Int. Ed. Engl. 48(37), 6903–6908 (2009).
[Crossref] [PubMed]

Mukherjee, K.

Murtagh, F.

J. L. Starck, F. Murtagh, and A. Bijaoui, “Multiresolution support applied to image filtering and restoration,” Graph Model Im. Pro. C. 57(5), 420–431 (1995).
[Crossref]

Nagaraj, R. Y.

Nan, X.

Neely, R. K.

Neumann, F. R.

Nishi, M.

Nosek, T. A.

Ohmi, K.

Olenych, S.

Olivo-Marin, J. C.

B. Zhang, J. Zerubia, and J. C. Olivo-Marin, “Gaussian approximations of fluorescence microscope point-spread function models,” Appl. Opt. 46(10), 1819–1829 (2007).
[Crossref] [PubMed]

Pan, Z.

Pang, Z. P.

Park, S. R.

Parlitz, U.

Patterson, G.

G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
[Crossref] [PubMed]

Patterson, G. H.

Pertsinidis, A.

A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
[Crossref] [PubMed]

Quan, T.

Reese, T. S.

Rieger, B.

S. Stallinga and B. Rieger, “Accuracy of the gaussian point spread function model in 2D localization microscopy,” Opt. Express 18(24), 24461–24476 (2010).
[Crossref] [PubMed]

Rosten, E.

E. Rosten, G. E. Jones, and S. Cox, “ImageJ plug-in for Bayesian analysis of blinking and bleaching,” Nat. Methods 10(2), 97–98 (2013).
[Crossref] [PubMed]

Rust, M. J.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

Sage, D.

Sauer, M.

M. Heilemann, S. van de Linde, A. Mukherjee, and M. Sauer, “Super-resolution imaging with small organic fluorophores,” Angew. Chem. Int. Ed. Engl. 48(37), 6903–6908 (2009).
[Crossref] [PubMed]

Schmid, S. L.

Schuttpelz, M.

Schwartz, S. L.

Seefeldt, B.

Sengupta, P.

Shaevitz, J. W.

Y. Deng, P. Coen, M. Sun, and J. W. Shaevitz, “Efficient multiple object tracking using mutually repulsive active membranes,” PLoS ONE 8(6), e65769 (2013).
[Crossref] [PubMed]

Sharma, M.

Shim, S. H.

S. A. Jones, S. H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[Crossref] [PubMed]

Shimuta, M.

Shroff, H.

Smal, I.

E. Meijering, O. Dzyubachyk, and I. Smal, “Methods for cell and particle tracking,” Methods Enzymol. 504, 183–200 (2012).
[Crossref] [PubMed]

Somlyo, A. P.

Somlyo, A. V.

Sougrat, R.

Stallinga, S.

S. Stallinga and B. Rieger, “Accuracy of the gaussian point spread function model in 2D localization microscopy,” Opt. Express 18(24), 24461–24476 (2010).
[Crossref] [PubMed]

Starck, J. L.

J. L. Starck, F. Murtagh, and A. Bijaoui, “Multiresolution support applied to image filtering and restoration,” Graph Model Im. Pro. C. 57(5), 420–431 (1995).
[Crossref]

Steinbrecher, J. H.

Streich, J. H.

Südhof, T. C.

Sun, M.

Y. Deng, P. Coen, M. Sun, and J. W. Shaevitz, “Efficient multiple object tracking using mutually repulsive active membranes,” PLoS ONE 8(6), e65769 (2013).
[Crossref] [PubMed]

Takeshima, H.

Thompson, R. E.

R. E. Thompson, D. R. Larson, and W. W. Webb, “Precise nanometer localization analysis for individual fluorescent probes,” Biophys. J. 82(5), 2775–2783 (2002).
[Crossref] [PubMed]

Tinnefeld, P.

Tuan, H. T. M.

Unser, M.

Uphoff, S.

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods 8(4), 279–280 (2011).
[Crossref] [PubMed]

van de Linde, S.

M. Heilemann, S. van de Linde, A. Mukherjee, and M. Sauer, “Super-resolution imaging with small organic fluorophores,” Angew. Chem. Int. Ed. Engl. 48(37), 6903–6908 (2009).
[Crossref] [PubMed]

Vaughan, J. C.

J. C. Vaughan, S. Jia, and X. Zhuang, “Ultrabright photoactivatable fluorophores created by reductive caging,” Nat. Methods 9(12), 1181–1184 (2012).
[Crossref] [PubMed]

Wagner, E.

Wang, W.

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-Dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[Crossref] [PubMed]

Wang, Y.

Webb, W. W.

R. E. Thompson, D. R. Larson, and W. W. Webb, “Precise nanometer localization analysis for individual fluorescent probes,” Biophys. J. 82(5), 2775–2783 (2002).
[Crossref] [PubMed]

Weiss, S.

Westphal, V.

Wichmann, J.

Williams, G. S. B.

Wong, S. T. C.

Wu, K. L.

K. L. Wu and M. S. Yang, “Mean shift-based clustering,” Pattern Recognit. 40(11), 3035–3052 (2007).
[Crossref]

Wurm, C. A.

Yang, D.

Yang, M. S.

K. L. Wu and M. S. Yang, “Mean shift-based clustering,” Pattern Recognit. 40(11), 3035–3052 (2007).
[Crossref]

Zeng, S.

Zerubia, J.

B. Zhang, J. Zerubia, and J. C. Olivo-Marin, “Gaussian approximations of fluorescence microscope point-spread function models,” Appl. Opt. 46(10), 1819–1829 (2007).
[Crossref] [PubMed]

Zhang, B.

B. Zhang, J. Zerubia, and J. C. Olivo-Marin, “Gaussian approximations of fluorescence microscope point-spread function models,” Appl. Opt. 46(10), 1819–1829 (2007).
[Crossref] [PubMed]

Zhang, J.

Zhang, W.

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat. Methods 9(7), 721–723 (2012).
[Crossref] [PubMed]

Zhang, Y.

A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
[Crossref] [PubMed]

Zhou, X. B.

Zhu, H.

Zhu, L.

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat. Methods 9(7), 721–723 (2012).
[Crossref] [PubMed]

Zhuang, X.

E. A. Mukamel, H. Babcock, and X. Zhuang, “Statistical deconvolution for superresolution fluorescence microscopy,” Biophys. J. 102(10), 2391–2400 (2012).
[Crossref] [PubMed]

J. C. Vaughan, S. Jia, and X. Zhuang, “Ultrabright photoactivatable fluorophores created by reductive caging,” Nat. Methods 9(12), 1181–1184 (2012).
[Crossref] [PubMed]

S. A. Jones, S. H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[Crossref] [PubMed]

B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
[Crossref] [PubMed]

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-Dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[Crossref] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

Angew. Chem-Ger. Edit. (1)

Angew. Chem. Int. Ed. Engl. (1)

M. Heilemann, S. van de Linde, A. Mukherjee, and M. Sauer, “Super-resolution imaging with small organic fluorophores,” Angew. Chem. Int. Ed. Engl. 48(37), 6903–6908 (2009).
[Crossref] [PubMed]

Annu. Rev. Biochem. (1)

B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
[Crossref] [PubMed]

Annu. Rev. Phys. Chem. (1)

G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
[Crossref] [PubMed]

Appl. Opt. (1)

B. Zhang, J. Zerubia, and J. C. Olivo-Marin, “Gaussian approximations of fluorescence microscope point-spread function models,” Appl. Opt. 46(10), 1819–1829 (2007).
[Crossref] [PubMed]

Biochem. J. (1)

Biomed. Opt. Express (1)

Biophys. J. (3)

R. E. Thompson, D. R. Larson, and W. W. Webb, “Precise nanometer localization analysis for individual fluorescent probes,” Biophys. J. 82(5), 2775–2783 (2002).
[Crossref] [PubMed]

E. A. Mukamel, H. Babcock, and X. Zhuang, “Statistical deconvolution for superresolution fluorescence microscopy,” Biophys. J. 102(10), 2391–2400 (2012).
[Crossref] [PubMed]

Circ. Res. (1)

Cold Spring Harb Protoc (1)

Dev. Dyn. (1)

Graph Model Im. Pro. C. (1)

J. L. Starck, F. Murtagh, and A. Bijaoui, “Multiresolution support applied to image filtering and restoration,” Graph Model Im. Pro. C. 57(5), 420–431 (1995).
[Crossref]

IEEE T. Pattern Anal. (1)

Y. Cheng, “Mean shift, mode seeking, and clustering,” IEEE T. Pattern Anal. 17(8), 790–799 (1995).
[Crossref]

IEEE Trans. Image Process. (1)

IEEE Trans. Inf. Theory (1)

K. Fukunaga and L. Hostetler, “The estimation of the gradient of a density function, with applications in pattern recognition,” IEEE Trans. Inf. Theory 21(1), 32–40 (1975).
[Crossref]

IEEE Trans. Med. Imaging (1)

J. Biomed. Opt. (1)

J. Microsc. (1)

M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
[Crossref] [PubMed]

J. Physiol. (1)

Methods Enzymol. (1)

E. Meijering, O. Dzyubachyk, and I. Smal, “Methods for cell and particle tracking,” Methods Enzymol. 504, 183–200 (2012).
[Crossref] [PubMed]

Nat. Cell Biol. (1)

Nat. Methods (11)

E. Rosten, G. E. Jones, and S. Cox, “ImageJ plug-in for Bayesian analysis of blinking and bleaching,” Nat. Methods 10(2), 97–98 (2013).
[Crossref] [PubMed]

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods 8(4), 279–280 (2011).
[Crossref] [PubMed]

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat. Methods 9(7), 721–723 (2012).
[Crossref] [PubMed]

J. C. Vaughan, S. Jia, and X. Zhuang, “Ultrabright photoactivatable fluorophores created by reductive caging,” Nat. Methods 9(12), 1181–1184 (2012).
[Crossref] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[Crossref] [PubMed]

S. A. Jones, S. H. Shim, J. He, and X. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods 8(6), 499–505 (2011).
[Crossref] [PubMed]

Nature (2)

A. Pertsinidis, Y. Zhang, and S. Chu, “Subnanometre single-molecule localization, registration and distance measurements,” Nature 466(7306), 647–651 (2010).
[Crossref] [PubMed]

K. R. Chi, “Microscopy: Ever-increasing resolution,” Nature 462(7273), 675–678 (2009).
[Crossref] [PubMed]

Opt. Express (4)

S. Stallinga and B. Rieger, “Accuracy of the gaussian point spread function model in 2D localization microscopy,” Opt. Express 18(24), 24461–24476 (2010).
[Crossref] [PubMed]

Opt. Lett. (1)

Pattern Recognit. (1)

K. L. Wu and M. S. Yang, “Mean shift-based clustering,” Pattern Recognit. 40(11), 3035–3052 (2007).
[Crossref]

PLoS ONE (1)

Y. Deng, P. Coen, M. Sun, and J. W. Shaevitz, “Efficient multiple object tracking using mutually repulsive active membranes,” PLoS ONE 8(6), e65769 (2013).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (2)

Science (3)

S. W. Hell, “Far-field optical nanoscopy,” Science 316(5828), 1153–1158 (2007).
[Crossref] [PubMed]

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-Dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[Crossref] [PubMed]

Other (5)

T. Kanade, Z. Yin, R. Bise, S. Huh, and S. Eom, “Cell image analysis: algorithms, system and applications,” IEEE Work. App. Comp. (2011).

F. Bunyak, K. Palaniappan, S. K. Nath, T. L. Baskin, and G. Dong, “Quantitative cell motility for in vitro wound healing using level set-based active contour tracking,” I. S. Biomed. Imaging 1040–1043 (2006).

K. Palaniappan, F. Bunyak, S. Nath, and J. Goffeney, “Parallel Processing Strategies for Cell Motility and Shape Analysis,” High-Throughput Image Reconstruction and Analysis, Artech House Publisher, 39–87 (2009).

E. Meijering, I. Smal, O. Dzyubachyk, and J.-C. Olivo-Marin, “Time-lapse imaging,” Microsc. Img. Proc. 401-440 (2008).

M. Born and E. Wolf, Principles of Optics: Electromagnetic Theory of Propagation, Interference and Diffraction of Light, 7th ed. (Cambridge University, 1975).

Cited By

OSA participates in Crossref's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.

Click here to see a list of articles that cite this paper

Fig. 1 Illustration of the tracklet-based superresolution microscope image reconstruction algorithm. (a). Flowchart of the analysis procedure. (b). 2D blob detection with LoG filter. Masks of the candidate emitters, both disjoint single emitters and the overlapping multi-emitters, are identified through the LoG filter. (c). 3D spatiotemporal labeling through coarse tracking. (d). WMS decomposition of the emitter candidates. (e). Tracklet generation through the fine tracking processing. Tracklets are scored according to the percentage of the overlap regions with neighboring tracklets. (f). Re-estimation of the positions through MLE. The final positions of the emitters are refined by MLE fitting of the integrated image through combining of the frames belonging to the same tracklets.

Download Full Size | PPT Slide | PDF

Fig. 2 Effect of the stabilization factor in the Gaussian kernel. (a) WMS decomposition with a small stabilization factor underestimates the number of emitters. True positions of the emitters are labeled with circles and the estimated positions are labeled with crosses. (b) WMS decomposition with a large stabilization factor overestimates the number of modes. (c) WMS decomposition with the right stabilization factor renders the right number of emitters. (d) Mode detection using WMS on an image acquired via a 60x objective yields good match with raw data. Scale bars: 300 nm. (e) The stabilization factor is determined using the correlation method (Eq. (9), section 3.1). (f) The recall (percentage of detected modes) does not change significantly with the background noise or the photon levels as tested via simulation. At each condition, the value of the stabilization parameter was adjusted accordingly so that the correlation coefficient is 0.95.

Download Full Size | PPT Slide | PDF

Fig. 3 Performance of WMS on resolving emitter pairs and high density of emitters with overlapping. (a) and (b), WMS is able to resolve an emitter pair when the distances between them are 200 nm and 300 nm respectively. True positions of the emitters are labeled with circles and the estimated positions are labeled with crosses. (c). WMS is able to resolve the right number of emitters when the emitter density is as high as 3 emitters per micrometer square. Scale bars: 300 nm.

Download Full Size | PPT Slide | PDF

Fig. 4 (a). Illustration of three tracklets generated from the simulation. The yellow one is an isolated tracklet while the other two have significant overlapping in time. (b, c). Two individual frames from the two overlapping tracklets as shown in (a). The true positions of the emitters are labeled with circles and the estimates are labeled as crosses. Due to the low signal noise ratio, the estimates deviate from the true positions. (d). By aggregating all the support regions of the tracklets, the signal is significantly increased. Now the estimate positions (crosses) overlap with the true locations of the emitters. Scale bars: 300 nm.

Download Full Size | PPT Slide | PDF

Fig. 5 Tracklet based reconstruction is able to resolve overlapping multi-emitters with improved localization accuracy. (a). Reconstructed image using the SA method. Due to the high density of emitters at the central part of the image, SA is not able to resolve the overlapping emitters, which results in very low number of detected emitters. (b). Tracklet-based reconstruction of the same image. Comparing with (a), the central part of the image is well reconstructed. (c). Image reconstructed with the combined SA method as defined in the main text. (d). Line profiles of the selected regions as shown in (a), (b), and (c). The black curve represents the line profile of the selected region in (A), and the blue curve is from (b), and red is from (c). The blue curve has smaller width, demonstrating the smaller localization uncertainty with the tracklet-based method. Scale bar: 300 nm.

Download Full Size | PPT Slide | PDF

Fig. 6 Microtubule images in HeLa cells. (a). Image reconstructed using the tracklet-based method from 50,000 frames. (b). Image reconstructed using the same data set as in (a) but with the SA method. Structures are discontinuous, particularly at crossing regions where emitter density is high. Scale bars: 300 nm. (c, d, e). Line profiles of the selected regions in (a) and (b). The tracklet-based method is able to resolve two structures as close as 38 nm, which is not resolvable with the SA method due to insufficient localization of emitters.

Download Full Size | PPT Slide | PDF

Fig. 7 T-tubule structures in rat FDB fiber. (a) Epifluorescence image of MG29-labelled T-tubule network in rat skeletal muscle. Scale bar: 2 μm. (b) Overlay of the epifluorescence image (red) of the T-tubule and the corresponding superresolution image (green). Scale bar: 1 μm. (c). The line profiles of the selected region in (b). The green curve corresponds to the line profile from the superresolution image, which shows clearly the distance between the two T-tubule membranes is about 82 nm. The conventional epifluorescence image completely misses the fine structure (red curve).

Download Full Size | PPT Slide | PDF

Equations (10)

Equations on this page are rendered with MathJax. Learn more.

f (x, y) = \frac{1}{2 π σ^{2}} e^{- \frac{{(x - x_{0})}^{2} + {(y - y_{0})}^{2}}{2 σ^{2}}}

\begin{matrix} μ (x_{k}, y_{k}) = \sum_{i}^{N} \frac{I_{i}}{4} \times (e r f (\frac{x_{k} - x_{i} + \frac{1}{2}}{\sqrt{2} σ}) - e r f (\frac{x_{k} - x_{i} - \frac{1}{2}}{\sqrt{2} σ})) \\ \times (e r f (\frac{y_{k} - y_{i} + \frac{1}{2}}{\sqrt{2} σ}) - e r f (\frac{y_{k} - y_{i} - \frac{1}{2}}{\sqrt{2} σ})) \end{matrix}

Φ_{k} (x, y) = P o i s (μ_{k}) + G (η, σ_{G}) .

L o G (x, y) = - \frac{1}{π σ^{4}} (1 - \frac{x^{2} + y^{2}}{2 σ^{2}}) e^{- \frac{x^{2} + y^{2}}{2 σ^{2}}}

{\hat{f}}_{H} (x) = \sum_{j = 1}^{n} h ({‖ x - x_{j} ‖}^{2}) w (x_{j})

\begin{matrix} \nabla {\hat{f}}_{H} (x) = \sum_{j = 1}^{n} k ({‖ x - x_{j} ‖}^{2}) (x_{j} - x) w (x_{j}) \\ = [\sum_{j = 1}^{n} k ({‖ x - x_{j} ‖}^{2}) w (x_{j})] \\ \times [\frac{\sum_{j = 1}^{n} k ({‖ x - x_{j} ‖}^{2}) w (x_{j}) x_{j}}{\sum_{j = 1}^{n} k ({‖ x - x_{j} ‖}^{2}) w (x_{j})} - x] \end{matrix}

x = m_{H} (x) = \frac{\sum_{j = 1}^{n} k ({‖ x - x_{j} ‖}^{2}) w (x_{j}) x_{j}}{\sum_{j = 1}^{n} k ({‖ x - x_{j} ‖}^{2}) w (x_{j})}

G^{p} (x) = {[g ({‖ x - x_{j} ‖}^{2})]}^{p} = {[e x p {- \frac{{‖ x - x_{j} ‖}^{2}}{2 β^{2}}}]}^{p}

{\hat{f}}_{H}^{p} (x_{i}) = {\sum_{j = 1}^{n} h (‖ x_{i} - x_{j} ‖)}^{p} w (x_{j})

P_{i j} (b_{j} | c_{i}) = e^{- \frac{‖ {\vec{r}}_{c} - {\vec{r}}_{b} ‖}{σ}}