Abstract

Developing methods for high-density localization of multiple emitters is a promising approach for enhancing the temporal resolution of localization microscopy while maintaining a desired spatial resolution, but the widespread use of this approach is thus far mainly obstructed by the slow image analysis speed. Here we present a high-density localization method based on the combination of Graphics Processing Unit (GPU) parallel computation, multiple-emitter fitting, and model recommendation via Bayesian Information Criterion (BIC). This method, called PALMER, exhibits satisfactory localization accuracy comparable with the previous reported SSM_BIC method, while executes more than two orders of magnitudes faster. Meanwhile, compared to the conventional localization microscopy which is based on sparse emitter localization, high-density localization microscopy based the PALMER method allows a speed gain of up to ~14-fold in obtaining a super-resolution image with the same Nyquist resolution.

© 2012 OSA

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2012

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat Methods (2012), doi:.
[CrossRef] [PubMed]

2011

G. T. Dempsey, J. C. Vaughan, K. H. Chen, M. Bates, and X. W. Zhuang, “Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging,” Nat. Methods8(12), 1027–1036 (2011).
[CrossRef] [PubMed]

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods8(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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

S. A. Jones, S. H. Shim, J. He, and X. W. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods8(6), 499–505 (2011).
[CrossRef] [PubMed]

E. Pastrana, “Fast 3D super-resolution fluorescence microscopy,” Nat. Methods8(1), 46 (2011).
[CrossRef]

F. Huang, S. L. Schwartz, J. M. Byars, and K. A. Lidke, “Simultaneous multiple-emitter fitting for single molecule super-resolution imaging,” Biomed. Opt. Express2(5), 1377–1393 (2011).
[CrossRef] [PubMed]

T. W. Quan, H. Y. Zhu, X. M. Liu, Y. F. Liu, J. P. Ding, S. Q. Zeng, and Z. L. Huang, “High-density localization of active molecules using Structured Sparse Model and Bayesian Information Criterion,” Opt. Express19(18), 16963–16974 (2011).
[CrossRef] [PubMed]

2010

2009

K. R. Chi, “Super-resolution microscopy: breaking the limits,” Nat. Methods6(1), 15–18 (2009).
[CrossRef]

2008

H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Methods5(5), 417–423 (2008).
[CrossRef] [PubMed]

2007

S. W. Hell, “Far-field optical nanoscopy,” Science316(5828), 1153–1158 (2007).
[CrossRef] [PubMed]

M. A. T. Figueiredo, R. D. Nowak, and S. J. Wright, “Gradient projection for sparse reconstruction: application to compressed sensing and other inverse problems,” IEEE J. Sel. Top. Signal Process.1(4), 586–597 (2007).
[CrossRef]

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]

2005

K. Nienhaus, G. U. Nienhaus, J. Wiedenmann, and H. Nar, “Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP,” Proc. Natl. Acad. Sci. U.S.A.102(26), 9156–9159 (2005).
[CrossRef] [PubMed]

1996

Z. Gao, Y. Lai, and Z. Hu, “A generalized gradient projection method for optimization problems with equality and inequality constraints about arbitrary initial point,” Acta Appl. Math.12(1), 40–49 (1996).
[CrossRef]

1995

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

Bates, M.

G. T. Dempsey, J. C. Vaughan, K. H. Chen, M. Bates, and X. W. Zhuang, “Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging,” Nat. Methods8(12), 1027–1036 (2011).
[CrossRef] [PubMed]

Betzig, E.

H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Methods5(5), 417–423 (2008).
[CrossRef] [PubMed]

Bewersdorf, J.

D. Toomre and J. Bewersdorf, “A new wave of cellular imaging,” Annu. Rev. Cell Dev. Biol.26(1), 285–314 (2010).
[CrossRef] [PubMed]

Burnette, D. T.

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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

Byars, J. M.

Chen, K. H.

G. T. Dempsey, J. C. Vaughan, K. H. Chen, M. Bates, and X. W. Zhuang, “Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging,” Nat. Methods8(12), 1027–1036 (2011).
[CrossRef] [PubMed]

Cheng, Y.

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

Chi, K. R.

K. R. Chi, “Super-resolution microscopy: breaking the limits,” Nat. Methods6(1), 15–18 (2009).
[CrossRef]

Cox, S.

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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

Dempsey, G. T.

G. T. Dempsey, J. C. Vaughan, K. H. Chen, M. Bates, and X. W. Zhuang, “Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging,” Nat. Methods8(12), 1027–1036 (2011).
[CrossRef] [PubMed]

Ding, J. P.

Elnatan, D.

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat Methods (2012), doi:.
[CrossRef] [PubMed]

Figueiredo, M. A. T.

M. A. T. Figueiredo, R. D. Nowak, and S. J. Wright, “Gradient projection for sparse reconstruction: application to compressed sensing and other inverse problems,” IEEE J. Sel. Top. Signal Process.1(4), 586–597 (2007).
[CrossRef]

Galbraith, C. G.

H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Methods5(5), 417–423 (2008).
[CrossRef] [PubMed]

Galbraith, J. A.

H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Methods5(5), 417–423 (2008).
[CrossRef] [PubMed]

Gao, Z.

Z. Gao, Y. Lai, and Z. Hu, “A generalized gradient projection method for optimization problems with equality and inequality constraints about arbitrary initial point,” Acta Appl. Math.12(1), 40–49 (1996).
[CrossRef]

He, J.

S. A. Jones, S. H. Shim, J. He, and X. W. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods8(6), 499–505 (2011).
[CrossRef] [PubMed]

Hedde, P. N.

Heintzmann, R.

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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

Hell, S. W.

S. W. Hell, “Far-field optical nanoscopy,” Science316(5828), 1153–1158 (2007).
[CrossRef] [PubMed]

Holden, S. J.

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods8(4), 279–280 (2011).
[CrossRef] [PubMed]

Hu, Z.

Z. Gao, Y. Lai, and Z. Hu, “A generalized gradient projection method for optimization problems with equality and inequality constraints about arbitrary initial point,” Acta Appl. Math.12(1), 40–49 (1996).
[CrossRef]

Huang, B.

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat Methods (2012), doi:.
[CrossRef] [PubMed]

Huang, F.

Huang, Z. L.

Jones, G. E.

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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

Jones, S. A.

S. A. Jones, S. H. Shim, J. He, and X. W. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods8(6), 499–505 (2011).
[CrossRef] [PubMed]

Jovanovic-Talisman, T.

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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

Kapanidis, A. N.

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods8(4), 279–280 (2011).
[CrossRef] [PubMed]

Lai, Y.

Z. Gao, Y. Lai, and Z. Hu, “A generalized gradient projection method for optimization problems with equality and inequality constraints about arbitrary initial point,” Acta Appl. Math.12(1), 40–49 (1996).
[CrossRef]

Li, P. C.

Lidke, K. A.

Lippincott-Schwartz, J.

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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

Liu, X. M.

Liu, Y. F.

Long, F.

Luo, Q. M.

Monypenny, J.

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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

Nar, H.

K. Nienhaus, G. U. Nienhaus, J. Wiedenmann, and H. Nar, “Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP,” Proc. Natl. Acad. Sci. U.S.A.102(26), 9156–9159 (2005).
[CrossRef] [PubMed]

Nienhaus, G. U.

T. W. Quan, P. C. Li, F. Long, S. Q. Zeng, Q. M. Luo, P. N. Hedde, G. U. Nienhaus, and Z. L. Huang, “Ultra-fast, high-precision image analysis for localization-based super resolution microscopy,” Opt. Express18(11), 11867–11876 (2010).
[CrossRef] [PubMed]

K. Nienhaus, G. U. Nienhaus, J. Wiedenmann, and H. Nar, “Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP,” Proc. Natl. Acad. Sci. U.S.A.102(26), 9156–9159 (2005).
[CrossRef] [PubMed]

Nienhaus, K.

K. Nienhaus, G. U. Nienhaus, J. Wiedenmann, and H. Nar, “Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP,” Proc. Natl. Acad. Sci. U.S.A.102(26), 9156–9159 (2005).
[CrossRef] [PubMed]

Nowak, R. D.

M. A. T. Figueiredo, R. D. Nowak, and S. J. Wright, “Gradient projection for sparse reconstruction: application to compressed sensing and other inverse problems,” IEEE J. Sel. Top. Signal Process.1(4), 586–597 (2007).
[CrossRef]

Olivo-Marin, J. C.

Pastrana, E.

E. Pastrana, “Fast 3D super-resolution fluorescence microscopy,” Nat. Methods8(1), 46 (2011).
[CrossRef]

Quan, T. W.

Rieger, B.

Rosten, E.

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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

Schwartz, S. L.

Shim, S. H.

S. A. Jones, S. H. Shim, J. He, and X. W. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods8(6), 499–505 (2011).
[CrossRef] [PubMed]

Shroff, H.

H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Methods5(5), 417–423 (2008).
[CrossRef] [PubMed]

Stallinga, S.

Toomre, D.

D. Toomre and J. Bewersdorf, “A new wave of cellular imaging,” Annu. Rev. Cell Dev. Biol.26(1), 285–314 (2010).
[CrossRef] [PubMed]

Uphoff, S.

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods8(4), 279–280 (2011).
[CrossRef] [PubMed]

Vaughan, J. C.

G. T. Dempsey, J. C. Vaughan, K. H. Chen, M. Bates, and X. W. Zhuang, “Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging,” Nat. Methods8(12), 1027–1036 (2011).
[CrossRef] [PubMed]

Wiedenmann, J.

K. Nienhaus, G. U. Nienhaus, J. Wiedenmann, and H. Nar, “Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP,” Proc. Natl. Acad. Sci. U.S.A.102(26), 9156–9159 (2005).
[CrossRef] [PubMed]

Wright, S. J.

M. A. T. Figueiredo, R. D. Nowak, and S. J. Wright, “Gradient projection for sparse reconstruction: application to compressed sensing and other inverse problems,” IEEE J. Sel. Top. Signal Process.1(4), 586–597 (2007).
[CrossRef]

Zeng, S. Q.

Zerubia, J.

Zhang, B.

Zhang, W.

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat Methods (2012), doi:.
[CrossRef] [PubMed]

Zhu, H. Y.

Zhu, L.

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat Methods (2012), doi:.
[CrossRef] [PubMed]

Zhuang, X. W.

S. A. Jones, S. H. Shim, J. He, and X. W. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods8(6), 499–505 (2011).
[CrossRef] [PubMed]

G. T. Dempsey, J. C. Vaughan, K. H. Chen, M. Bates, and X. W. Zhuang, “Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging,” Nat. Methods8(12), 1027–1036 (2011).
[CrossRef] [PubMed]

Acta Appl. Math.

Z. Gao, Y. Lai, and Z. Hu, “A generalized gradient projection method for optimization problems with equality and inequality constraints about arbitrary initial point,” Acta Appl. Math.12(1), 40–49 (1996).
[CrossRef]

Annu. Rev. Cell Dev. Biol.

D. Toomre and J. Bewersdorf, “A new wave of cellular imaging,” Annu. Rev. Cell Dev. Biol.26(1), 285–314 (2010).
[CrossRef] [PubMed]

Appl. Opt.

Biomed. Opt. Express

IEEE J. Sel. Top. Signal Process.

M. A. T. Figueiredo, R. D. Nowak, and S. J. Wright, “Gradient projection for sparse reconstruction: application to compressed sensing and other inverse problems,” IEEE J. Sel. Top. Signal Process.1(4), 586–597 (2007).
[CrossRef]

IEEE Trans. Pattern Anal. Mach. Intell.

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

Nat Methods

L. Zhu, W. Zhang, D. Elnatan, and B. Huang, “Faster STORM using compressed sensing,” Nat Methods (2012), doi:.
[CrossRef] [PubMed]

Nat. Methods

K. R. Chi, “Super-resolution microscopy: breaking the limits,” Nat. Methods6(1), 15–18 (2009).
[CrossRef]

S. A. Jones, S. H. Shim, J. He, and X. W. Zhuang, “Fast, three-dimensional super-resolution imaging of live cells,” Nat. Methods8(6), 499–505 (2011).
[CrossRef] [PubMed]

E. Pastrana, “Fast 3D super-resolution fluorescence microscopy,” Nat. Methods8(1), 46 (2011).
[CrossRef]

H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Methods5(5), 417–423 (2008).
[CrossRef] [PubMed]

G. T. Dempsey, J. C. Vaughan, K. H. Chen, M. Bates, and X. W. Zhuang, “Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging,” Nat. Methods8(12), 1027–1036 (2011).
[CrossRef] [PubMed]

S. J. Holden, S. Uphoff, and A. N. Kapanidis, “DAOSTORM: an algorithm for high- density super-resolution microscopy,” Nat. Methods8(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. Methods9(2), 195–200 (2011).
[CrossRef] [PubMed]

Opt. Express

Proc. Natl. Acad. Sci. U.S.A.

K. Nienhaus, G. U. Nienhaus, J. Wiedenmann, and H. Nar, “Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP,” Proc. Natl. Acad. Sci. U.S.A.102(26), 9156–9159 (2005).
[CrossRef] [PubMed]

Science

S. W. Hell, “Far-field optical nanoscopy,” Science316(5828), 1153–1158 (2007).
[CrossRef] [PubMed]

Other

“GPU computing SDK, ” http://developer.nvidia.com/gpu-computing-sdk , accessed March 2012.

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Figures (5)

Fig. 1
Fig. 1

The entire image analysis routine for the PALMER method. Note that multiple images are processed in parallel through this routine.

Fig. 2
Fig. 2

Localization performance of the PALMER, SSM_BIC and DAOSTORM methods in analyzing simulated images with different emitter densities. Note that the background was 100 photons per pixel for all simulations, while the signals were for the total detected photons from individual emitters. Each date point was averaged from five independent measurements. The error bars in (e) and (f) are standard deviations.

Fig. 3
Fig. 3

Time consumptions of the PALMER and SSM_BIC methods in analyzing single image frame. Simulated images of 100 × 100 pixels were used, where the total detected signal from individual emitters was 350 photons and the background was 100 photons per pixel. Each data point was calculated from five sets of data.

Fig. 4
Fig. 4

Evaluation of the resolving capability of the PALMER method using simulated images with quarter-scale bitonal Siemens star pattern. (a) Image with ground-truth pattern. Wide-field image averaged from 1000 frames (b), a typical image frame (c) and a reconstructed super-resolution image from the PALMER method (d). The normalized intensity profile (green dots, averaged from 11 line pairs) of the green arc in (d) is shown in (e), which is further fitted with rectangular function (purple). (f) The dependence of the contrast on the structure width. The error bars in (f) show the standard errors. Note that the structures within the red dash box in (f) are irresolvable.

Fig. 5
Fig. 5

Localization performance of the PALMER and MaLiang methods in analyzing experimental images with high (a-e) and low (f-j) emitter density. TIRF image from a stack of 2000 image frames (a, f) and a single image frame (b, g). Super resolution images were reconstructed by the PALMER (c, h) and the MaLiang (d, i) method, respectively. Cross-sectional distributions of emitter localizations along the direction of the actins in the boxed region are shown (e, j), where the colors in the histograms are the same as those in the corresponding images. Scale bar: 2 μm.

Tables (1)

Tables Icon

Table 1 Nyquist resolution from reconstructed super-resolution images

Equations (1)

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S i,j =Poisson( k N A k exp(- (x- x ko ) 2 + (y- y ko ) 2 2 ω 2 ) +b)

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