Abstract

The precise localization of nanometric objects in three dimensions is essential to identify functional diffusion mechanisms in complex systems at the cellular or molecular level. However, most optical methods can achieve high temporal resolution and high localization precision only in two dimensions or over a limited axial (z) range. Here we develop a novel wide-field detection system based on an electrically tunable lens that can track multiple individual nanoscale emitters in three dimensions over a tunable axial range with nanometric localization precision. The optical principle of the technique is based on the simultaneous acquisition of two images with an extended depth of field while encoding the z position of the emitters via a lateral shift between images. We provide a theoretical framework for this approach and demonstrate tracking of free diffusing beads and GABAA receptors in live neurons. This approach allows getting nanometric localization precision up to an axial range above 10 μm with a high numerical aperture lens—quadruple that of a typical 3D tracking system. Synchronization or complex fitting procedures are not requested here, which leads to a suitable architecture for localizing single molecules in four dimensions, namely, three dimensions in real-time.

© 2017 Optical Society of America

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    [Crossref]

2016 (2)

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

M. Duocastella, C. Theriault, and C. B. Arnold, “Three-dimensional particle tracking via tunable color- encoded multiplexing,” Opt. Lett. 41, 863–864 (2016).
[Crossref]

2015 (3)

2014 (5)

M. Duocastella, G. Vicidomini, and A. Diaspro, “Simultaneous multiplane confocal microscopy using acoustic tunable lenses,” Opt. Express 22, 19293–19301 (2014).
[Crossref]

B. Biermann, S. Sokoll, J. Klueva, M. Missler, J. S. Wiegert, J.-B. Sibarita, and M. Heine, “Imaging of molecular surface dynamics in brain slices using single-particle tracking,” Nat. Commun. 5, 3024 (2014).
[Crossref]

L. Lanzano and E. Gratton, “Orbital single particle tracking on a commercial confocal microscope using piezoelectric stage feedback,” Methods Appl. Flouresc. 1, 024010 (2014).
[Crossref]

E. M. Petrini, T. Ravasenga, T. J. Hausrat, G. Iurilli, U. Olcese, V. Racine, J.-B. Sibarita, T. C. Jacob, S. J. Moss, F. Benfenati, P. Medini, M. Kneussel, and A. Barberis, “Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP,” Nat. Commun. 5, 3921 (2014).
[Crossref]

H. Deschout, F. Cella Zanacchi, M. Mlodzianoski, A. Diaspro, J. Bewersdorf, S. T. Hess, and K. Braeckmans, “Precisely and accurately localizing single emitters in fluorescence microscopy,” Nat. Methods 11, 253–266 (2014).
[Crossref]

2013 (3)

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

M. Duocastella and C. B. Arnold, “Enhanced depth of field laser processing using an ultra-high-speed axial scanner,” Appl. Phys. Lett. 102, 061113 (2013).
[Crossref]

D. Choquet and A. Triller, “The dynamic synapse,” Neuron 80, 691–703 (2013).
[Crossref]

2012 (1)

2011 (2)

S. Liu and H. Hua, “Extended depth-of-field microscopic imaging with a variable focus microscope objective,” Opt. Express 19, 353–362 (2011).
[Crossref]

A. Dupont and D. C. Lamb, “Nanoscale three-dimensional single particle tracking,” Nanoscale 3, 4532–4541 (2011).
[Crossref]

2010 (5)

M. F. Juette and J. Bewersdorf, “Three-dimensional tracking of single fluorescent particles with submillisecond temporal resolution,” Nano Lett. 10, 4657–4663 (2010).
[Crossref]

M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10, 211–218 (2010).
[Crossref]

J. L. Gregg, K. M. McGuire, D. C. Focht, and M. A. Model, “Measurement of the thickness and volume of adherent cells using transmission-through-dye microscopy,” Pflügers Arch. 460, 1097–1104 (2010).
[Crossref]

R. Bowman, G. Gibson, and M. Padgett, “Particle tracking stereomicroscopy in optical tweezers: control of trap shape,” Opt. Express 18, 11785–11790 (2010).
[Crossref]

X. Michalet, “Mean square displacement analysis of single-particle trajectories with localization error: Brownian motion in an isotropic medium,” Phys. Rev. E 82, 041914 (2010).
[Crossref]

2009 (5)

E. M. Petrini, J. Lu, L. Cognet, B. Lounis, M. D. Ehlers, and D. Choquet, “Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation,” Neuron 63, 92–105 (2009).
[Crossref]

Y. Sun, J. D. McKenna, J. M. Murray, E. M. Ostap, and Y. E. Goldman, “Parallax: high accuracy three-dimensional single molecule tracking using split images,” Nano Lett. 9, 2676–2682 (2009).
[Crossref]

M. J. Mlodzianoski, M. F. Juette, G. L. Beane, and J. Bewersdorf, “Experimental characterization of 3D localization techniques for particle-tracking and super-resolution microscopy,” Opt. Express 17, 8264–8277 (2009).
[Crossref]

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Y. Kalaidzidis, “Multiple objects tracking in fluorescence microscopy,” J. Math. Biol. 58, 57–80 (2009).
[Crossref]

2008 (5)

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

S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophys. J. 95, 6025–6043 (2008).
[Crossref]

H. Jin, D. A. Heller, and M. S. Strano, “Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells,” Nano Lett. 8, 1577–1585 (2008).
[Crossref]

I. Smal, K. Draegestein, N. Galjart, W. Niessen, and E. Meijering, “Particle filtering for multiple object tracking in dynamic fluorescence microscopy images: application to microtubule growth analysis,” IEEE Trans. Med. Imaging 27, 789–804 (2008).
[Crossref]

J. Yajima, K. Mizutani, and T. Nishizaka, “A torque component present in mitotic kinesin Eg5 revealed by three-dimensional tracking,” Nat. Struct. Mol. Biol. 15, 1119–1121 (2008).
[Crossref]

2007 (2)

B. Brandenburg and X. Zhuang, “Virus trafficking-learning from single-virus tracking,” Nat. Rev. Microbiol. 5, 197–208 (2007).
[Crossref]

E. Toprak, H. Balci, B. H. Blehm, and P. R. Selvin, “Three-dimensional particle tracking via bifocal imaging,” Nano Lett. 7, 2043–2045 (2007).
[Crossref]

2006 (1)

E. Meijering, I. Smal, and G. Danuser, “Tracking in molecular bioimaging,” IEEE Signal Process. Mag. 23(3), 46–53 (2006).
[Crossref]

2004 (1)

R. Dzakpasu and D. Axelrod, “Dynamic light scattering microscopy. A novel optical technique to image submicroscopic motions. II: Experimental applications,” Biophys. J. 87, 1288–1297 (2004).
[Crossref]

2003 (1)

Abrahamsson, S.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Agard, D. A.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Allgeyer, E. S.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Arnold, C. B.

M. Duocastella, C. Theriault, and C. B. Arnold, “Three-dimensional particle tracking via tunable color- encoded multiplexing,” Opt. Lett. 41, 863–864 (2016).
[Crossref]

M. Duocastella and C. B. Arnold, “Enhanced depth of field laser processing using an ultra-high-speed axial scanner,” Appl. Phys. Lett. 102, 061113 (2013).
[Crossref]

Axelrod, D.

R. Dzakpasu and D. Axelrod, “Dynamic light scattering microscopy. A novel optical technique to image submicroscopic motions. II: Experimental applications,” Biophys. J. 87, 1288–1297 (2004).
[Crossref]

Backer, A. S.

Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise 3D scan-free multiple-particle tracking over large axial ranges with Tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
[Crossref]

Badieirostami, M.

M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10, 211–218 (2010).
[Crossref]

Balci, H.

E. Toprak, H. Balci, B. H. Blehm, and P. R. Selvin, “Three-dimensional particle tracking via bifocal imaging,” Nano Lett. 7, 2043–2045 (2007).
[Crossref]

Barberis, A.

E. M. Petrini, T. Ravasenga, T. J. Hausrat, G. Iurilli, U. Olcese, V. Racine, J.-B. Sibarita, T. C. Jacob, S. J. Moss, F. Benfenati, P. Medini, M. Kneussel, and A. Barberis, “Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP,” Nat. Commun. 5, 3921 (2014).
[Crossref]

Bargmann, C. I.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Bates, M.

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

Beane, G. L.

Benfenati, F.

E. M. Petrini, T. Ravasenga, T. J. Hausrat, G. Iurilli, U. Olcese, V. Racine, J.-B. Sibarita, T. C. Jacob, S. J. Moss, F. Benfenati, P. Medini, M. Kneussel, and A. Barberis, “Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP,” Nat. Commun. 5, 3921 (2014).
[Crossref]

Bewersdorf, J.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

H. Deschout, F. Cella Zanacchi, M. Mlodzianoski, A. Diaspro, J. Bewersdorf, S. T. Hess, and K. Braeckmans, “Precisely and accurately localizing single emitters in fluorescence microscopy,” Nat. Methods 11, 253–266 (2014).
[Crossref]

M. F. Juette and J. Bewersdorf, “Three-dimensional tracking of single fluorescent particles with submillisecond temporal resolution,” Nano Lett. 10, 4657–4663 (2010).
[Crossref]

M. J. Mlodzianoski, M. F. Juette, G. L. Beane, and J. Bewersdorf, “Experimental characterization of 3D localization techniques for particle-tracking and super-resolution microscopy,” Opt. Express 17, 8264–8277 (2009).
[Crossref]

Biermann, B.

B. Biermann, S. Sokoll, J. Klueva, M. Missler, J. S. Wiegert, J.-B. Sibarita, and M. Heine, “Imaging of molecular surface dynamics in brain slices using single-particle tracking,” Nat. Commun. 5, 3024 (2014).
[Crossref]

Biteen, J. S.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Blehm, B. H.

E. Toprak, H. Balci, B. H. Blehm, and P. R. Selvin, “Three-dimensional particle tracking via bifocal imaging,” Nano Lett. 7, 2043–2045 (2007).
[Crossref]

Bonora, S.

Booth, M. J.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Bortolozzo, U.

Bowman, R.

Braeckmans, K.

H. Deschout, F. Cella Zanacchi, M. Mlodzianoski, A. Diaspro, J. Bewersdorf, S. T. Hess, and K. Braeckmans, “Precisely and accurately localizing single emitters in fluorescence microscopy,” Nat. Methods 11, 253–266 (2014).
[Crossref]

Brandenburg, B.

B. Brandenburg and X. Zhuang, “Virus trafficking-learning from single-virus tracking,” Nat. Rev. Microbiol. 5, 197–208 (2007).
[Crossref]

Cella Zanacchi, F.

H. Deschout, F. Cella Zanacchi, M. Mlodzianoski, A. Diaspro, J. Bewersdorf, S. T. Hess, and K. Braeckmans, “Precisely and accurately localizing single emitters in fluorescence microscopy,” Nat. Methods 11, 253–266 (2014).
[Crossref]

Chao, J.

S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophys. J. 95, 6025–6043 (2008).
[Crossref]

Chen, D.

Chen, J.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Choquet, D.

D. Choquet and A. Triller, “The dynamic synapse,” Neuron 80, 691–703 (2013).
[Crossref]

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S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophys. J. 95, 6025–6043 (2008).
[Crossref]

Racine, V.

E. M. Petrini, T. Ravasenga, T. J. Hausrat, G. Iurilli, U. Olcese, V. Racine, J.-B. Sibarita, T. C. Jacob, S. J. Moss, F. Benfenati, P. Medini, M. Kneussel, and A. Barberis, “Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP,” Nat. Commun. 5, 3921 (2014).
[Crossref]

Ram, S.

S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophys. J. 95, 6025–6043 (2008).
[Crossref]

Ravasenga, T.

E. M. Petrini, T. Ravasenga, T. J. Hausrat, G. Iurilli, U. Olcese, V. Racine, J.-B. Sibarita, T. C. Jacob, S. J. Moss, F. Benfenati, P. Medini, M. Kneussel, and A. Barberis, “Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP,” Nat. Commun. 5, 3921 (2014).
[Crossref]

Residori, S.

Rivera-Molina, F. E.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Rothman, J. E.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Saavedra, G.

Sabine, L.

L. Sabine and A. Triller, “Neurotransmitter dynamics,” in The Dynamic Synapse: Molecular Methods in Ionotropic Receptor Biology, J. T. Kittler and S. J. Moss, eds. (CRC Press/Taylor & Francis, 2006).

Sahl, S. J.

Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise 3D scan-free multiple-particle tracking over large axial ranges with Tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
[Crossref]

Sanchez-Ortiga, E.

Schroeder, L. K.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Selvin, P. R.

E. Toprak, H. Balci, B. H. Blehm, and P. R. Selvin, “Three-dimensional particle tracking via bifocal imaging,” Nano Lett. 7, 2043–2045 (2007).
[Crossref]

Shechtman, Y.

Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise 3D scan-free multiple-particle tracking over large axial ranges with Tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
[Crossref]

Sibarita, J.-B.

E. M. Petrini, T. Ravasenga, T. J. Hausrat, G. Iurilli, U. Olcese, V. Racine, J.-B. Sibarita, T. C. Jacob, S. J. Moss, F. Benfenati, P. Medini, M. Kneussel, and A. Barberis, “Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP,” Nat. Commun. 5, 3921 (2014).
[Crossref]

B. Biermann, S. Sokoll, J. Klueva, M. Missler, J. S. Wiegert, J.-B. Sibarita, and M. Heine, “Imaging of molecular surface dynamics in brain slices using single-particle tracking,” Nat. Commun. 5, 3024 (2014).
[Crossref]

Sirinakis, G.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Smal, I.

I. Smal, K. Draegestein, N. Galjart, W. Niessen, and E. Meijering, “Particle filtering for multiple object tracking in dynamic fluorescence microscopy images: application to microtubule growth analysis,” IEEE Trans. Med. Imaging 27, 789–804 (2008).
[Crossref]

E. Meijering, I. Smal, and G. Danuser, “Tracking in molecular bioimaging,” IEEE Signal Process. Mag. 23(3), 46–53 (2006).
[Crossref]

Sokoll, S.

B. Biermann, S. Sokoll, J. Klueva, M. Missler, J. S. Wiegert, J.-B. Sibarita, and M. Heine, “Imaging of molecular surface dynamics in brain slices using single-particle tracking,” Nat. Commun. 5, 3024 (2014).
[Crossref]

Soule, P.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Speidel, M.

Stallinga, S.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Strano, M. S.

H. Jin, D. A. Heller, and M. S. Strano, “Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells,” Nano Lett. 8, 1577–1585 (2008).
[Crossref]

Sun, Y.

Y. Sun, J. D. McKenna, J. M. Murray, E. M. Ostap, and Y. E. Goldman, “Parallax: high accuracy three-dimensional single molecule tracking using split images,” Nano Lett. 9, 2676–2682 (2009).
[Crossref]

Theriault, C.

Thompson, M. A.

M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10, 211–218 (2010).
[Crossref]

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Toomre, D.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Toprak, E.

E. Toprak, H. Balci, B. H. Blehm, and P. R. Selvin, “Three-dimensional particle tracking via bifocal imaging,” Nano Lett. 7, 2043–2045 (2007).
[Crossref]

Triller, A.

D. Choquet and A. Triller, “The dynamic synapse,” Neuron 80, 691–703 (2013).
[Crossref]

L. Sabine and A. Triller, “Neurotransmitter dynamics,” in The Dynamic Synapse: Molecular Methods in Ionotropic Receptor Biology, J. T. Kittler and S. J. Moss, eds. (CRC Press/Taylor & Francis, 2006).

Twieg, R. J.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Vicidomini, G.

Wang, W.

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

Ward, E. S.

S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophys. J. 95, 6025–6043 (2008).
[Crossref]

Weiss, L. E.

Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise 3D scan-free multiple-particle tracking over large axial ranges with Tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
[Crossref]

Wiegert, J. S.

B. Biermann, S. Sokoll, J. Klueva, M. Missler, J. S. Wiegert, J.-B. Sibarita, and M. Heine, “Imaging of molecular surface dynamics in brain slices using single-particle tracking,” Nat. Commun. 5, 3024 (2014).
[Crossref]

Wisniewski, J.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Wu, C.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Xu, G.

Yajima, J.

J. Yajima, K. Mizutani, and T. Nishizaka, “A torque component present in mitotic kinesin Eg5 revealed by three-dimensional tracking,” Nat. Struct. Mol. Biol. 15, 1119–1121 (2008).
[Crossref]

Yu, B.

Zhang, Y.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

Zhuang, X.

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

B. Brandenburg and X. Zhuang, “Virus trafficking-learning from single-virus tracking,” Nat. Rev. Microbiol. 5, 197–208 (2007).
[Crossref]

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M. Duocastella and C. B. Arnold, “Enhanced depth of field laser processing using an ultra-high-speed axial scanner,” Appl. Phys. Lett. 102, 061113 (2013).
[Crossref]

Biophys. J. (2)

R. Dzakpasu and D. Axelrod, “Dynamic light scattering microscopy. A novel optical technique to image submicroscopic motions. II: Experimental applications,” Biophys. J. 87, 1288–1297 (2004).
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S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophys. J. 95, 6025–6043 (2008).
[Crossref]

Cell (1)

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3D imaging of whole cells,” Cell 166, 1028–1040 (2016).
[Crossref]

IEEE Signal Process. Mag. (1)

E. Meijering, I. Smal, and G. Danuser, “Tracking in molecular bioimaging,” IEEE Signal Process. Mag. 23(3), 46–53 (2006).
[Crossref]

IEEE Trans. Med. Imaging (1)

I. Smal, K. Draegestein, N. Galjart, W. Niessen, and E. Meijering, “Particle filtering for multiple object tracking in dynamic fluorescence microscopy images: application to microtubule growth analysis,” IEEE Trans. Med. Imaging 27, 789–804 (2008).
[Crossref]

J. Display Technol. (1)

J. Math. Biol. (1)

Y. Kalaidzidis, “Multiple objects tracking in fluorescence microscopy,” J. Math. Biol. 58, 57–80 (2009).
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L. Lanzano and E. Gratton, “Orbital single particle tracking on a commercial confocal microscope using piezoelectric stage feedback,” Methods Appl. Flouresc. 1, 024010 (2014).
[Crossref]

Nano Lett. (6)

M. F. Juette and J. Bewersdorf, “Three-dimensional tracking of single fluorescent particles with submillisecond temporal resolution,” Nano Lett. 10, 4657–4663 (2010).
[Crossref]

E. Toprak, H. Balci, B. H. Blehm, and P. R. Selvin, “Three-dimensional particle tracking via bifocal imaging,” Nano Lett. 7, 2043–2045 (2007).
[Crossref]

M. A. Thompson, M. D. Lew, M. Badieirostami, and W. E. Moerner, “Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function,” Nano Lett. 10, 211–218 (2010).
[Crossref]

H. Jin, D. A. Heller, and M. S. Strano, “Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells,” Nano Lett. 8, 1577–1585 (2008).
[Crossref]

Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise 3D scan-free multiple-particle tracking over large axial ranges with Tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
[Crossref]

Y. Sun, J. D. McKenna, J. M. Murray, E. M. Ostap, and Y. E. Goldman, “Parallax: high accuracy three-dimensional single molecule tracking using split images,” Nano Lett. 9, 2676–2682 (2009).
[Crossref]

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A. Dupont and D. C. Lamb, “Nanoscale three-dimensional single particle tracking,” Nanoscale 3, 4532–4541 (2011).
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Nat. Commun. (2)

E. M. Petrini, T. Ravasenga, T. J. Hausrat, G. Iurilli, U. Olcese, V. Racine, J.-B. Sibarita, T. C. Jacob, S. J. Moss, F. Benfenati, P. Medini, M. Kneussel, and A. Barberis, “Synaptic recruitment of gephyrin regulates surface GABAA receptor dynamics for the expression of inhibitory LTP,” Nat. Commun. 5, 3921 (2014).
[Crossref]

B. Biermann, S. Sokoll, J. Klueva, M. Missler, J. S. Wiegert, J.-B. Sibarita, and M. Heine, “Imaging of molecular surface dynamics in brain slices using single-particle tracking,” Nat. Commun. 5, 3024 (2014).
[Crossref]

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H. Deschout, F. Cella Zanacchi, M. Mlodzianoski, A. Diaspro, J. Bewersdorf, S. T. Hess, and K. Braeckmans, “Precisely and accurately localizing single emitters in fluorescence microscopy,” Nat. Methods 11, 253–266 (2014).
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S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2013).
[Crossref]

Nat. Rev. Microbiol. (1)

B. Brandenburg and X. Zhuang, “Virus trafficking-learning from single-virus tracking,” Nat. Rev. Microbiol. 5, 197–208 (2007).
[Crossref]

Nat. Struct. Mol. Biol. (1)

J. Yajima, K. Mizutani, and T. Nishizaka, “A torque component present in mitotic kinesin Eg5 revealed by three-dimensional tracking,” Nat. Struct. Mol. Biol. 15, 1119–1121 (2008).
[Crossref]

Neuron (2)

D. Choquet and A. Triller, “The dynamic synapse,” Neuron 80, 691–703 (2013).
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E. M. Petrini, J. Lu, L. Cognet, B. Lounis, M. D. Ehlers, and D. Choquet, “Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation,” Neuron 63, 92–105 (2009).
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S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Science (1)

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319, 810–813 (2008).
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L. Sabine and A. Triller, “Neurotransmitter dynamics,” in The Dynamic Synapse: Molecular Methods in Ionotropic Receptor Biology, J. T. Kittler and S. J. Moss, eds. (CRC Press/Taylor & Francis, 2006).

Supplementary Material (3)

NameDescription
» Supplement 1: PDF (3058 KB)      Supplemental information
» Visualization 1: AVI (1830 KB)      3D tracking of a free-diffusing bead in water
» Visualization 2: AVI (4317 KB)      3D tracking of a GABAA receptor in the membrane of a living neuron

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Figures (4)

Fig. 1.
Fig. 1. Schematic of the working principle of the tracking approach. (a) Red beams show the effect of the tunable lens in a standard on-axis image formation system. For an infinity corrected system, the focal length of an ETL placed in the conjugate plane of the detection objective can be varied to compensate for any degree of divergence for rays coming from focal planes at different z positions (bottom). This enables the formation of focused images at the camera sensor for particles located at different z positions, preventing the loss of out-of-focus tracking precision. By inserting an off-axis displacement of the ETL relative to the optical axis, the same holds (green beam). However, in this case, there is an additional steering effect that depends on the value of the ETL focal length needed to bring the image into focus. This produces an encoding of the axial position into a lateral shift. (b) Snapshot of a sample of fluorescent beads acquired with the tracking system. The false colors correspond to the aligned (red) and decentered (green) channels. (c) Experimental PSF for each channel with the ETL off (standard acquisition system) and ETL on. Scale bar is 2 μm. (d) Lateral shift induced in the green channel for a single bead as a function of the axial position. Note that the red channel does not move.

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Fig. 2.
Fig. 2. Characterization of the localization precision of the 3D tracking technique. (a) Lateral separation between the two channels ( Δ y ), in pixels, for a 500 nm bead attached to a glass coverslip and translated in steps of 0.5 μm every 50 acquisitions. The experiment was repeated for two different settings: a value of C corresponding to 2.7 px/μm (blue line) for a total axial range of 12 μm and to 5.1 px/μm (red line) for an axial range of 2 μm. The inset shows the linear dependence of Δ y as a function of the axial position for each case. (b) Plot of the x – y – z position of the tracked bead in (a) along the entire axial range for the two studied configurations. The values have been calculated relative to the average position in each axial plane. (c) Localization precision along the three directions of space extracted from (b).

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Fig. 3.
Fig. 3. Measurement of the 3D free-diffusion coefficient of microspheres in water. (a) 3D trajectory of single fluorescent bead (500 nm size) tracked in water at room temperature. The 3D position of the fluorescent particle was measured every 0.1 s for 100 s. (b) Representative MSD plot for the freely diffusing particle shown in (a).

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Fig. 4.
Fig. 4. Diffusion of GABAA receptors in the membrane of living neurons. (a) Representative time-color-coded trajectory of an individual α 1 -containing GABAA receptor diffusing on a soma of a cultured hippocampal neuron. The trajectory tracking the QD fluorescence has been superimposed on the neuronal soma image acquired with transmitted light microscopy. Scale bar is 2 μm. (b) Same receptor trajectory shown in (a) rendered in three dimensions and shown on a time-coded scale. In ∼ 45    s the receptor explores a considerable portion of the somatic region spanning ∼ 4 – 6    μm in both the x – y and z axes.

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Equations (2)

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

Δ y = C z = f t Δ d M R 2 f o 2 z ,
σ z = 2 C σ y .

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