Abstract

The in-vivo investigation of highly dynamic biological samples, for example the beating zebrafish heart, requires high-speed volume imaging techniques. Light-sheet microscopy is ideal for such samples as it records high-contrast images of entire planes within large samples at once. However, in order to obtain images of different planes, it has been necessary to move the sample relative to the fixed focal plane of the detection objective lens. This mechanical movement limits speed, precision and may be harmful to the sample. We have built a light-sheet microscope that uses remote focusing with an electrically tunable lens (ETL). Without moving specimen or objective we have thereby achieved flexible volume imaging at much higher speeds than previously reported. Our high-speed microscope delivers 3D snapshots of sensitive biological samples. As an example, we imaged 17 planes within a beating zebrafish heart at 510 frames per second, equivalent to 30 volume scans per second. Movements, shape changes and signals across the entire volume can be followed which has been impossible with existing reconstruction techniques.

© 2013 OSA

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    [CrossRef]
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2013

T.  Panier, S.  Romano, R.  Olive, T.  Pietri, G.  Sumbre, R.  Candelier, G.  Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy,” Front. Neural Circuits 7, 65 (2013).
[CrossRef] [PubMed]

C.  Skupsch, C.  Brücker, “Multiple-plane particle image velocimetry using a light-field camera,” Opt. Express 21, 1726–1740 (2013).
[CrossRef] [PubMed]

2012

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[CrossRef]

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

A.  Kaufmann, M.  Mickoleit, M.  Weber, J.  Huisken, “Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope,” Development 139, 3242–3247 (2012).
[CrossRef] [PubMed]

2011

B. F.  Grewe, F. F.  Voigt, M.  van’t Hoff, F.  Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Exp. 2, 2035–2046 (2011).
[CrossRef]

S.  Kumar, D.  Wilding, M. B.  Sikkel, A. R.  Lyon, K. T.  MacLeod, C.  Dunsby, “High-speed 2D and 3D fluorescence microscopy of cardiac myocytes,” Opt. Express 19, 13839–13847 (2011).
[CrossRef] [PubMed]

2010

2009

C.  Dunsby, “Optically sectioned imaging by oblique plane microscopy,” Opt. Express 16, 20306–20316 (2009).
[CrossRef]

J.  Huisken, D. Y. R.  Stainier, “Selective plane illumination microscopy techniques in developmental biology,” Development 136, 1963–1975 (2009).
[CrossRef] [PubMed]

M.  Levoy, Z.  Zhang, I.  McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Mic. 235, 144–162 (2009).
[CrossRef]

2008

E. J.  Botcherby, R.  Juškaitis, M. J.  Booth, T.  Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281, 880–887 (2008).
[CrossRef]

T. F.  Holekamp, D.  Turaga, T. E.  Holy, “Fast Three-Dimensional Fluorescence Imaging of Activity in Neural Populations by Objective-Coupled Planar Illumination Microscopy,” Neuron 57, 661–672 (2008).
[CrossRef] [PubMed]

S.  Ram, P.  Prabhat, J.  Chao, E. S.  Ward, 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] [PubMed]

2007

2006

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[CrossRef]

2004

J.  Huisken, J.  Swoger, F.  Del Bene, J.  Wittbrodt, E. H. K.  Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[CrossRef] [PubMed]

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Ankerhold, R.

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Booth, M. J.

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[CrossRef]

E. J.  Botcherby, R.  Juškaitis, M. J.  Booth, T.  Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281, 880–887 (2008).
[CrossRef]

Botcherby, E. J.

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[CrossRef]

E. J.  Botcherby, R.  Juškaitis, M. J.  Booth, T.  Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281, 880–887 (2008).
[CrossRef]

Brücker, C.

Candelier, R.

T.  Panier, S.  Romano, R.  Olive, T.  Pietri, G.  Sumbre, R.  Candelier, G.  Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy,” Front. Neural Circuits 7, 65 (2013).
[CrossRef] [PubMed]

Chao, J.

S.  Ram, P.  Prabhat, J.  Chao, E. S.  Ward, 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] [PubMed]

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Dahan, M.

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Dalgarno, H. I. C.

Dalgarno, P. A.

Darzacq, X.

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Débarre, D.

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[CrossRef]

Debrégeas, G.

T.  Panier, S.  Romano, R.  Olive, T.  Pietri, G.  Sumbre, R.  Candelier, G.  Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy,” Front. Neural Circuits 7, 65 (2013).
[CrossRef] [PubMed]

Del Bene, F.

J.  Huisken, J.  Swoger, F.  Del Bene, J.  Wittbrodt, E. H. K.  Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[CrossRef] [PubMed]

Dickinson, M. E.

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[CrossRef]

Dugast Darzacq, 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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Dunsby, C.

Forouhar, A. S.

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[CrossRef]

Fraser, S. E.

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[CrossRef]

Gharib, M.

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[CrossRef]

Greenaway, A. H.

Grewe, B. F.

B. F.  Grewe, F. F.  Voigt, M.  van’t Hoff, F.  Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Exp. 2, 2035–2046 (2011).
[CrossRef]

Gustafsson, M. G. L.

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Hajj, B.

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Helmchen, F.

B. F.  Grewe, F. F.  Voigt, M.  van’t Hoff, F.  Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Exp. 2, 2035–2046 (2011).
[CrossRef]

Holekamp, T. F.

T. F.  Holekamp, D.  Turaga, T. E.  Holy, “Fast Three-Dimensional Fluorescence Imaging of Activity in Neural Populations by Objective-Coupled Planar Illumination Microscopy,” Neuron 57, 661–672 (2008).
[CrossRef] [PubMed]

Holy, T. E.

T. F.  Holekamp, D.  Turaga, T. E.  Holy, “Fast Three-Dimensional Fluorescence Imaging of Activity in Neural Populations by Objective-Coupled Planar Illumination Microscopy,” Neuron 57, 661–672 (2008).
[CrossRef] [PubMed]

Huisken, J.

A.  Kaufmann, M.  Mickoleit, M.  Weber, J.  Huisken, “Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope,” Development 139, 3242–3247 (2012).
[CrossRef] [PubMed]

J.  Huisken, D. Y. R.  Stainier, “Selective plane illumination microscopy techniques in developmental biology,” Development 136, 1963–1975 (2009).
[CrossRef] [PubMed]

J.  Huisken, D. Y. R.  Stainier, “Even fluorescence excitation by multidirectional selective plane illumination microscopy (mSPIM),” Opt. Lett. 32, 2608–2610 (2007).
[CrossRef] [PubMed]

J.  Huisken, J.  Swoger, F.  Del Bene, J.  Wittbrodt, E. H. K.  Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[CrossRef] [PubMed]

Juškaitis, R.

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[CrossRef]

E. J.  Botcherby, R.  Juškaitis, M. J.  Booth, T.  Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281, 880–887 (2008).
[CrossRef]

Katsov, A. Y.

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Kaufmann, A.

A.  Kaufmann, M.  Mickoleit, M.  Weber, J.  Huisken, “Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope,” Development 139, 3242–3247 (2012).
[CrossRef] [PubMed]

Kohl, M. M.

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[CrossRef]

Kumar, S.

Lambert, R.

Levoy, M.

M.  Levoy, Z.  Zhang, I.  McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Mic. 235, 144–162 (2009).
[CrossRef]

Liebling, M.

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[CrossRef]

Logan, D. C.

Lyon, A. R.

MacLeod, K. T.

McDowall, I.

M.  Levoy, Z.  Zhang, I.  McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Mic. 235, 144–162 (2009).
[CrossRef]

Mickoleit, M.

A.  Kaufmann, M.  Mickoleit, M.  Weber, J.  Huisken, “Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope,” Development 139, 3242–3247 (2012).
[CrossRef] [PubMed]

Mizuguchi, G.

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Mueller, F.

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Ober, R. J.

S.  Ram, P.  Prabhat, J.  Chao, E. S.  Ward, 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] [PubMed]

Olive, R.

T.  Panier, S.  Romano, R.  Olive, T.  Pietri, G.  Sumbre, R.  Candelier, G.  Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy,” Front. Neural Circuits 7, 65 (2013).
[CrossRef] [PubMed]

Panier, T.

T.  Panier, S.  Romano, R.  Olive, T.  Pietri, G.  Sumbre, R.  Candelier, G.  Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy,” Front. Neural Circuits 7, 65 (2013).
[CrossRef] [PubMed]

Paterson, L.

Paulsen, O.

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[CrossRef]

Pietri, T.

T.  Panier, S.  Romano, R.  Olive, T.  Pietri, G.  Sumbre, R.  Candelier, G.  Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy,” Front. Neural Circuits 7, 65 (2013).
[CrossRef] [PubMed]

Prabhat, P.

S.  Ram, P.  Prabhat, J.  Chao, E. S.  Ward, 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] [PubMed]

Putoud, A.

Ram, S.

S.  Ram, P.  Prabhat, J.  Chao, E. S.  Ward, 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] [PubMed]

Romano, S.

T.  Panier, S.  Romano, R.  Olive, T.  Pietri, G.  Sumbre, R.  Candelier, G.  Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy,” Front. Neural Circuits 7, 65 (2013).
[CrossRef] [PubMed]

Sikkel, M. B.

Skupsch, C.

Smith, C. W.

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Stainier, D. Y. R.

J.  Huisken, D. Y. R.  Stainier, “Selective plane illumination microscopy techniques in developmental biology,” Development 136, 1963–1975 (2009).
[CrossRef] [PubMed]

J.  Huisken, D. Y. R.  Stainier, “Even fluorescence excitation by multidirectional selective plane illumination microscopy (mSPIM),” Opt. Lett. 32, 2608–2610 (2007).
[CrossRef] [PubMed]

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Stelzer, E. H. K.

J.  Huisken, J.  Swoger, F.  Del Bene, J.  Wittbrodt, E. H. K.  Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[CrossRef] [PubMed]

Sumbre, G.

T.  Panier, S.  Romano, R.  Olive, T.  Pietri, G.  Sumbre, R.  Candelier, G.  Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy,” Front. Neural Circuits 7, 65 (2013).
[CrossRef] [PubMed]

Swoger, J.

J.  Huisken, J.  Swoger, F.  Del Bene, J.  Wittbrodt, E. H. K.  Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[CrossRef] [PubMed]

Towers, D. P.

Turaga, D.

T. F.  Holekamp, D.  Turaga, T. E.  Holy, “Fast Three-Dimensional Fluorescence Imaging of Activity in Neural Populations by Objective-Coupled Planar Illumination Microscopy,” Neuron 57, 661–672 (2008).
[CrossRef] [PubMed]

van’t Hoff, M.

B. F.  Grewe, F. F.  Voigt, M.  van’t Hoff, F.  Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Exp. 2, 2035–2046 (2011).
[CrossRef]

Voigt, F. F.

B. F.  Grewe, F. F.  Voigt, M.  van’t Hoff, F.  Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Exp. 2, 2035–2046 (2011).
[CrossRef]

Warburton, R. J.

Ward, E. S.

S.  Ram, P.  Prabhat, J.  Chao, E. S.  Ward, 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] [PubMed]

Weber, M.

A.  Kaufmann, M.  Mickoleit, M.  Weber, J.  Huisken, “Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope,” Development 139, 3242–3247 (2012).
[CrossRef] [PubMed]

Wilding, D.

Wilson, T.

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[CrossRef]

E. J.  Botcherby, R.  Juškaitis, M. J.  Booth, T.  Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281, 880–887 (2008).
[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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Wittbrodt, J.

J.  Huisken, J.  Swoger, F.  Del Bene, J.  Wittbrodt, E. H. K.  Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[CrossRef] [PubMed]

Wolleschensky, R.

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Zhang, Z.

M.  Levoy, Z.  Zhang, I.  McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Mic. 235, 144–162 (2009).
[CrossRef]

Zimmermann, B.

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[CrossRef]

Biomed. Opt. Exp.

B. F.  Grewe, F. F.  Voigt, M.  van’t Hoff, F.  Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Exp. 2, 2035–2046 (2011).
[CrossRef]

Biophys. J.

S.  Ram, P.  Prabhat, J.  Chao, E. S.  Ward, 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] [PubMed]

Dev. Dynam.

M.  Liebling, A. S.  Forouhar, R.  Wolleschensky, B.  Zimmermann, R.  Ankerhold, S. E.  Fraser, M.  Gharib, M. E.  Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dynam. 235, 2940–2948 (2006).
[CrossRef]

Development

J.  Huisken, D. Y. R.  Stainier, “Selective plane illumination microscopy techniques in developmental biology,” Development 136, 1963–1975 (2009).
[CrossRef] [PubMed]

A.  Kaufmann, M.  Mickoleit, M.  Weber, J.  Huisken, “Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope,” Development 139, 3242–3247 (2012).
[CrossRef] [PubMed]

Front. Neural Circuits

T.  Panier, S.  Romano, R.  Olive, T.  Pietri, G.  Sumbre, R.  Candelier, G.  Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy,” Front. Neural Circuits 7, 65 (2013).
[CrossRef] [PubMed]

J. Mic.

M.  Levoy, Z.  Zhang, I.  McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Mic. 235, 144–162 (2009).
[CrossRef]

Nat. Methods

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, M. G. L.  Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[CrossRef] [PubMed]

Neuron

T. F.  Holekamp, D.  Turaga, T. E.  Holy, “Fast Three-Dimensional Fluorescence Imaging of Activity in Neural Populations by Objective-Coupled Planar Illumination Microscopy,” Neuron 57, 661–672 (2008).
[CrossRef] [PubMed]

Opt. Commun.

E. J.  Botcherby, R.  Juškaitis, M. J.  Booth, T.  Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281, 880–887 (2008).
[CrossRef]

Opt. Express

Opt. Lett.

P. Natl Acad. Sci. USA

E. J.  Botcherby, C. W.  Smith, M. M.  Kohl, D.  Débarre, M. J.  Booth, R.  Juškaitis, O.  Paulsen, T.  Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” P. Natl Acad. Sci. USA 109, 2919–2924 (2012).
[CrossRef]

Science

J.  Huisken, J.  Swoger, F.  Del Bene, J.  Wittbrodt, E. H. K.  Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[CrossRef] [PubMed]

Supplementary Material (4)

» Media 1: MOV (11580 KB)     
» Media 2: MOV (894 KB)     
» Media 3: MOV (2512 KB)     
» Media 4: MOV (8427 KB)     

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Figures (9)

Fig. 1
Fig. 1

Three different approaches to volume imaging in SPIM. (a) Volume image data in SPIM can be recorded by scanning the object through the stationary light sheet and aligned focal plane of the detection objective. Alternatively, the light sheet can be scanned through the sample by synchronized adjustment of the focal plane, either by repositioning the detection lens (b) or remote focusing (c), e.g. by a tunable lens to image the illuminated plane onto the camera.

Fig. 2
Fig. 2

A SPIM setup has been modified to include a scan mirror and an ETL lens: The light sheet is generated by focusing a line into the back focal plane of the illumination lens using a cylindrical lens. A motorized scan mirror displaces the light sheet along the detection optical axis. The image plane is displaced by changing the focal length of the ETL in-between the two relay lenses. Illumination light is shown in blue, fluorescence in green.

Fig. 3
Fig. 3

The ETL-SPIM setup exhibits a wide scan range and good image quality across almost the whole field. (a) The ETL’s refractive power DETL = 1/fETL as a function of the applied current (measurement by Optotune AG). (b, c) The dependence of the position of the focal plane on currents IETL for the 10×/0.3 lens (b) and the 20×/0.5 lens (c). (d–f) A grating with a period of 100μm imaged with a 20×/0.5 lens for three different currents: (d) IETL = 0mA, (e) IETL = 160mA, and (f) IETL = 320mA. The red crosses indicate the lower/right edge of the line that were located to measure the magnification and the distortion.

Fig. 4
Fig. 4

The dynamic behavior of the ETL in response to different driving signals. (a) The image plane is scanned by applying a sawtooth current IETL. The maximum intensity of the image is shown in red. Peaks can be observed whenever the image plane and the light-sheet zLS coincide. (b) The maximum value taken of the images p(t) plotted against the position of the light-sheet zLS and the time point within each ETL-period trel. The line at −90μm for trel ≈ 0μm and 100μm is an artifact created by an out-of-focus cluster of spheres. (c–f) max(p(trel, zLS)) for sawtooth signals IETL at νETL = 20Hz (c), νETL = 40Hz (d), a lowpass-filtered sawtooth at νETL = 40Hz (e) and a sine at νETL = 40Hz (f).

Fig. 5
Fig. 5

Frequency-dependent amplitude for the 20× objective and phase of the focal length of the ETL. The amplitude (a) and the phase shift (b) of the axial position of the image plane. The ETL was driven with a sinusoidal signal. The crosses mark measurement results. Exponentially decaying functions were fitted to the data.

Fig. 6
Fig. 6

Large volume scan with an ETL through the head of a zebrafish ( Media 1). (a) Slowly varying ramp signals can be used for remote scanning through large volumes. Thin optical sections are recorded by flashing the illumination only for a short time when the rolling shutter exposes the full camera chip. (b,c) A stack of images of the vascular system in the brain of a zebrafish imaged by remote scanning (blood cells in red, vasculature in green). The figure shows a maximum projection along the detection axis overlaid with a bright-field image (b) and a three-dimensional rendering (c) which is also shown in Media 1. The data was recorded with the 10× lens.

Fig. 7
Fig. 7

Dynamic calibration ensures perfect overlap of the light sheet and the image plane over the full period for high-speed volume scans ( Media 2). (a) Maximum projection of the image stack across the light sheet axis y over one period. Media 2 shows the full images. (b) Driving signals for the ETL, IETL, and the piezo-mirror UPM. (c) Quality parameter j that measures the overlap over one period for different parameters uj and ϕj grouped in five subsets depending on the offset U0,j which is changed in steps dU. The maximum value is reached for U0 = Uc, ϕ = ϕc and u = uc and marked by an arrow. The image stack shown in (a) was recorded with these parameters. The data was recorded with the 20× lens.

Fig. 8
Fig. 8

Sinusoidal driving signals offer two possibilities to increase either spatial or temporal sampling. The green plot indicates the position of the image plane along the optical axis (vertical axis) over time (horizontal axis). The camera records images with constant temporal spacing. The timepoints are marked by red dots and the number i of the frame within the ETL period. m indicates the overall number of frames. In the two cases shown, either: (a) Each plane is imaged twice during each period, e.g. i = 1 and 14, i = 2 and 13, ..., or (b) planes imaged in the second half are lying between the planes imaged in the first half of each period.

Fig. 9
Fig. 9

Movies of multiple planes in a beating zebrafish heart can be acquired synchronously ( Media 3 & Media 4). (a,b,c) Three series of images taken in different planes. The temporal spacing between two frames taken in the same plane is 1/fETL = 1/30s. The corresponding movie is available as Media 3. The relative positions of the planes along the detection axis z can be inferred from Fig. 8(b) where the corresponding frames are marked by *. Scalebar: 50 μm. (b) A three-dimensional reconstruction. Units are microns. The corresponding movie is available as Media 4).

Equations (2)

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δ z det = 1 M det 2 n f r 2 f ETL , eff .
f r f TL d ETL d BFP .

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