Abstract

Large scale simultaneous recording of fast patterns of neural activity remains challenging. Volumetric imaging modalities such as scanning-beam light-sheet microscopy (LSM) and wide-field light-field microscopy (WFLFM) fall short of the goal due to their complex calibration procedure, low spatial resolution, or high-photobleaching. Here, we demonstrate a hybrid light-sheet light-field microscopy (LSLFM) modality that yields high spatial resolution with simplified alignment of the imaging plane and the excitation plane. This new modality combines the selective excitation of light-sheet illumination with volumetric light-field imaging. This modality overcomes the current limitations of the scanning-beam LSM and WFLFM implementations. Compared with LSM, LSLFM captures volumetric data at a frame rate 50× lower than the rate of LSM and requires no dynamic calibration. Compared with WFLFM, LSLFM produces moderate improvements in spatial resolutions, 10 times improvement in the contrast when imaging fluorescent beads, and 3.2× the signal-to-noise ratio in the detection of neural activity when imaging live zebrafish expressing a genetically encoded calcium sensor.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2019 (2)

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

A. Giovannucci, J. Friedrich, P. Gunn, J. Kalfon, B. L. Brown, S. A. Koay, J. Taxidis, F. Najafi, J. L. Gauthier, and P. Zhou, “CaImAn an open source tool for scalable calcium imaging data analysis,” eLife 8, e38173 (2019).
[Crossref]

2018 (4)

M. A. Taylor, G. C. Vanwalleghem, I. A. Favre-Bulle, and E. K. Scott, “Diffuse light-sheet microscopy for stripe-free calcium imaging of neural populations,” J. Biophotonics 11(12), e201800088 (2018).
[Crossref]

O. Skocek, T. Nöbauer, L. Weilguny, F. M. Traub, C. N. Xia, M. I. Molodtsov, A. Grama, M. Yamagata, D. Aharoni, and D. D. Cox, “High-speed volumetric imaging of neuronal activity in freely moving rodents,” Nat. Methods 15(6), 429–432 (2018).
[Crossref]

W. Koroshetz, J. Gordon, A. Adams, A. Beckel-Mitchener, J. Churchill, G. Farber, M. Freund, J. Gnadt, N. S. Hsu, and N. Langhals, “The state of the NIH Brain initiative,” J. Neurosci. 38(29), 6427–6438 (2018).
[Crossref]

A.-K. Gustavsson, P. N. Petrov, M. Y. Lee, Y. Shechtman, and W. Moerner, “3D single-molecule super-resolution microscopy with a tilted light sheet,” Nat. Commun. 9(1), 123 (2018).
[Crossref]

2017 (3)

D. P. Ryan, E. A. Gould, G. J. Seedorf, O. Masihzadeh, S. H. Abman, S. Vijayaraghavan, W. B. Macklin, D. Restrepo, and D. P. Shepherd, “Automatic and adaptive heterogeneous refractive index compensation for light-sheet microscopy,” Nat. Commun. 8(1), 612 (2017).
[Crossref]

R. M. Power and J. Huisken, “A guide to light-sheet fluorescence microscopy for multiscale imaging,” Nat. Methods 14(4), 360–373 (2017).
[Crossref]

W. Yang and R. Yuste, “In vivo imaging of neural activity,” Nat. Methods 14(4), 349–359 (2017).
[Crossref]

2016 (3)

2015 (3)

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref]

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

W. C. Lemon, S. R. Pulver, B. Höckendorf, K. McDole, K. Branson, J. Freeman, and P. J. Keller, “Whole-central nervous system functional imaging in larval Drosophila,” Nat. Commun. 6(1), 7924 (2015).
[Crossref]

2014 (5)

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, and E. S. Boyden, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref]

Y. Gong, M. J. Wagner, J. Z. Li, and M. J. Schnitzer, “Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors,” Nat. Commun. 5(1), 3674 (2014).
[Crossref]

T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
[Crossref]

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

L. Tian, J. Wang, and L. Waller, “3D differential phase-contrast microscopy with computational illumination using an LED array,” Opt. Lett. 39(5), 1326–1329 (2014).
[Crossref]

2013 (5)

A. A. Bhandiwad, D. G. Zeddies, D. W. Raible, E. W. Rubel, and J. A. Sisneros, “Auditory sensitivity of larval zebrafish (Danio rerio) measured using a behavioral prepulse inhibition assay,” J. Exp. Biol. 216(18), 3504–3513 (2013).
[Crossref]

F. O. Fahrbach, F. F. Voigt, B. Schmid, F. Helmchen, and J. Huisken, “Rapid 3D light-sheet microscopy with a tunable lens,” Opt. Express 21(18), 21010–21026 (2013).
[Crossref]

M. Broxton, L. Grosenick, S. Yang, N. Cohen, A. Andalman, K. Deisseroth, and M. Levoy, “Wave optics theory and 3-D deconvolution for the light field microscope,” Opt. Express 21(21), 25418–25439 (2013).
[Crossref]

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref]

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, and V. Jayaraman, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref]

2012 (1)

U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
[Crossref]

2008 (1)

2007 (1)

K. M. Kwan, E. Fujimoto, C. Grabher, B. D. Mangum, M. E. Hardy, D. S. Campbell, J. M. Parant, H. J. Yost, J. P. Kanki, and C. B. Chien, “The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs,” Dev. Dyn. 236(11), 3088–3099 (2007).
[Crossref]

2006 (1)

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph 25(3), 924–934 (2006).
[Crossref]

2005 (1)

R. Ng, M. Levoy, M. Brédif, G. Duval, M. Horowitz, and P. Hanrahan, “Light field photography with a hand-held plenoptic camera,” Computer Science Technical Report CSTR 2, 1–11 (2005).

2004 (1)

Z. Wang, A. C. Bovik, H. R. Sheikh, and E. P. Simoncelli, “Image quality assessment: from error visibility to structural similarity,” IEEE Trans. on Image Process. 13(4), 600–612 (2004).
[Crossref]

Abman, S. H.

D. P. Ryan, E. A. Gould, G. J. Seedorf, O. Masihzadeh, S. H. Abman, S. Vijayaraghavan, W. B. Macklin, D. Restrepo, and D. P. Shepherd, “Automatic and adaptive heterogeneous refractive index compensation for light-sheet microscopy,” Nat. Commun. 8(1), 612 (2017).
[Crossref]

Adams, A.

W. Koroshetz, J. Gordon, A. Adams, A. Beckel-Mitchener, J. Churchill, G. Farber, M. Freund, J. Gnadt, N. S. Hsu, and N. Langhals, “The state of the NIH Brain initiative,” J. Neurosci. 38(29), 6427–6438 (2018).
[Crossref]

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph 25(3), 924–934 (2006).
[Crossref]

B. Wilburn, N. Joshi, V. Vaish, E.-V. Talvala, E. Antunez, A. Barth, A. Adams, M. Horowitz, and M. Levoy, “High performance imaging using large camera arrays,” in ACM Trans. Graph, (ACM, 2005), 765–776.

Aharoni, D.

O. Skocek, T. Nöbauer, L. Weilguny, F. M. Traub, C. N. Xia, M. I. Molodtsov, A. Grama, M. Yamagata, D. Aharoni, and D. D. Cox, “High-speed volumetric imaging of neuronal activity in freely moving rodents,” Nat. Methods 15(6), 429–432 (2018).
[Crossref]

Ahrens, M. B.

S. Quirin, N. Vladimirov, C.-T. Yang, D. S. Peterka, R. Yuste, and M. B. Ahrens, “Calcium imaging of neural circuits with extended depth-of-field light-sheet microscopy,” Opt. Lett. 41(5), 855–858 (2016).
[Crossref]

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref]

Andalman, A.

Andreev, A.

T. V. Truong, D. B. Holland, S. Madaan, A. Andreev, J. V. Troll, D. E. Koo, K. Keomanee-Dizon, M. McFall-Ngai, and S. E. Fraser, “Selective volume illumination microscopy offers synchronous volumetric imaging with high contrast,” bioRxiv, 403303 (2018).

Antunez, E.

B. Wilburn, N. Joshi, V. Vaish, E.-V. Talvala, E. Antunez, A. Barth, A. Adams, M. Horowitz, and M. Levoy, “High performance imaging using large camera arrays,” in ACM Trans. Graph, (ACM, 2005), 765–776.

Arbeláez, P.

J. M. Wolff, D. Castro, P. Arbeláez, and M. Forero-Shelton, “Light-sheet enhanced resolution of light field microscopy for rapid imaging of large volumes,” in Three-Dimensional and Multidimensional Microscopy: Image Acquisition and Processing XXV, (International Society for Optics and Photonics, 2018), 104991U.

Baden, T.

L. Theis, P. Berens, E. Froudarakis, J. Reimer, M. R. Rosón, T. Baden, T. Euler, A. S. Tolias, and M. Bethge, “Benchmarking spike rate inference in population calcium imaging,” Neuron 90(3), 471–482 (2016).
[Crossref]

Baier, H.

M. Kunst, E. Laurell, N. Mokayes, A. Kramer, F. Kubo, A. M. Fernandes, D. Förster, M. Dal Maschio, and H. Baier, “A cellular-resolution atlas of the larval zebrafish brain,” Available at SSRN 3257346 (2018).

Balázs, B.

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

Baohan, A.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, and V. Jayaraman, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref]

Barth, A.

B. Wilburn, N. Joshi, V. Vaish, E.-V. Talvala, E. Antunez, A. Barth, A. Adams, M. Horowitz, and M. Levoy, “High performance imaging using large camera arrays,” in ACM Trans. Graph, (ACM, 2005), 765–776.

Beckel-Mitchener, A.

W. Koroshetz, J. Gordon, A. Adams, A. Beckel-Mitchener, J. Churchill, G. Farber, M. Freund, J. Gnadt, N. S. Hsu, and N. Langhals, “The state of the NIH Brain initiative,” J. Neurosci. 38(29), 6427–6438 (2018).
[Crossref]

Berens, P.

L. Theis, P. Berens, E. Froudarakis, J. Reimer, M. R. Rosón, T. Baden, T. Euler, A. S. Tolias, and M. Bethge, “Benchmarking spike rate inference in population calcium imaging,” Neuron 90(3), 471–482 (2016).
[Crossref]

Bethge, M.

L. Theis, P. Berens, E. Froudarakis, J. Reimer, M. R. Rosón, T. Baden, T. Euler, A. S. Tolias, and M. Bethge, “Benchmarking spike rate inference in population calcium imaging,” Neuron 90(3), 471–482 (2016).
[Crossref]

Bhandiwad, A. A.

A. A. Bhandiwad, D. G. Zeddies, D. W. Raible, E. W. Rubel, and J. A. Sisneros, “Auditory sensitivity of larval zebrafish (Danio rerio) measured using a behavioral prepulse inhibition assay,” J. Exp. Biol. 216(18), 3504–3513 (2013).
[Crossref]

Blau, S.

S. Soltanian-Zadeh, K. Sahingur, S. Blau, Y. Gong, and S. Farsiu, “Fast and robust active neuron segmentation in two-photon calcium imaging using spatiotemporal deep learning,” Proceedings of the National Academy of Sciences, 201812995 (2019).

Bouchard, M. B.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Bovik, A. C.

Z. Wang, A. C. Bovik, H. R. Sheikh, and E. P. Simoncelli, “Image quality assessment: from error visibility to structural similarity,” IEEE Trans. on Image Process. 13(4), 600–612 (2004).
[Crossref]

Boyden, E. S.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, and E. S. Boyden, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref]

Branson, K.

W. C. Lemon, S. R. Pulver, B. Höckendorf, K. McDole, K. Branson, J. Freeman, and P. J. Keller, “Whole-central nervous system functional imaging in larval Drosophila,” Nat. Commun. 6(1), 7924 (2015).
[Crossref]

Brédif, M.

R. Ng, M. Levoy, M. Brédif, G. Duval, M. Horowitz, and P. Hanrahan, “Light field photography with a hand-held plenoptic camera,” Computer Science Technical Report CSTR 2, 1–11 (2005).

Brown, B. L.

A. Giovannucci, J. Friedrich, P. Gunn, J. Kalfon, B. L. Brown, S. A. Koay, J. Taxidis, F. Najafi, J. L. Gauthier, and P. Zhou, “CaImAn an open source tool for scalable calcium imaging data analysis,” eLife 8, e38173 (2019).
[Crossref]

Broxton, M.

Bruno, R. M.

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T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
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T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
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J. M. Wolff, D. Castro, P. Arbeláez, and M. Forero-Shelton, “Light-sheet enhanced resolution of light field microscopy for rapid imaging of large volumes,” in Three-Dimensional and Multidimensional Microscopy: Image Acquisition and Processing XXV, (International Society for Optics and Photonics, 2018), 104991U.

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M. Kunst, E. Laurell, N. Mokayes, A. Kramer, F. Kubo, A. M. Fernandes, D. Förster, M. Dal Maschio, and H. Baier, “A cellular-resolution atlas of the larval zebrafish brain,” Available at SSRN 3257346 (2018).

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T. V. Truong, D. B. Holland, S. Madaan, A. Andreev, J. V. Troll, D. E. Koo, K. Keomanee-Dizon, M. McFall-Ngai, and S. E. Fraser, “Selective volume illumination microscopy offers synchronous volumetric imaging with high contrast,” bioRxiv, 403303 (2018).

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W. C. Lemon, S. R. Pulver, B. Höckendorf, K. McDole, K. Branson, J. Freeman, and P. J. Keller, “Whole-central nervous system functional imaging in larval Drosophila,” Nat. Commun. 6(1), 7924 (2015).
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A. Giovannucci, J. Friedrich, P. Gunn, J. Kalfon, B. L. Brown, S. A. Koay, J. Taxidis, F. Najafi, J. L. Gauthier, and P. Zhou, “CaImAn an open source tool for scalable calcium imaging data analysis,” eLife 8, e38173 (2019).
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N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
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W. Koroshetz, J. Gordon, A. Adams, A. Beckel-Mitchener, J. Churchill, G. Farber, M. Freund, J. Gnadt, N. S. Hsu, and N. Langhals, “The state of the NIH Brain initiative,” J. Neurosci. 38(29), 6427–6438 (2018).
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Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
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Y. Gong, M. J. Wagner, J. Z. Li, and M. J. Schnitzer, “Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors,” Nat. Commun. 5(1), 3674 (2014).
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S. Soltanian-Zadeh, K. Sahingur, S. Blau, Y. Gong, and S. Farsiu, “Fast and robust active neuron segmentation in two-photon calcium imaging using spatiotemporal deep learning,” Proceedings of the National Academy of Sciences, 201812995 (2019).

Gordon, J.

W. Koroshetz, J. Gordon, A. Adams, A. Beckel-Mitchener, J. Churchill, G. Farber, M. Freund, J. Gnadt, N. S. Hsu, and N. Langhals, “The state of the NIH Brain initiative,” J. Neurosci. 38(29), 6427–6438 (2018).
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K. M. Kwan, E. Fujimoto, C. Grabher, B. D. Mangum, M. E. Hardy, D. S. Campbell, J. M. Parant, H. J. Yost, J. P. Kanki, and C. B. Chien, “The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs,” Dev. Dyn. 236(11), 3088–3099 (2007).
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O. Skocek, T. Nöbauer, L. Weilguny, F. M. Traub, C. N. Xia, M. I. Molodtsov, A. Grama, M. Yamagata, D. Aharoni, and D. D. Cox, “High-speed volumetric imaging of neuronal activity in freely moving rodents,” Nat. Methods 15(6), 429–432 (2018).
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Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
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Grueber, W. B.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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Gunn, P.

A. Giovannucci, J. Friedrich, P. Gunn, J. Kalfon, B. L. Brown, S. A. Koay, J. Taxidis, F. Najafi, J. L. Gauthier, and P. Zhou, “CaImAn an open source tool for scalable calcium imaging data analysis,” eLife 8, e38173 (2019).
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T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
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U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
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R. Ng, M. Levoy, M. Brédif, G. Duval, M. Horowitz, and P. Hanrahan, “Light field photography with a hand-held plenoptic camera,” Computer Science Technical Report CSTR 2, 1–11 (2005).

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K. M. Kwan, E. Fujimoto, C. Grabher, B. D. Mangum, M. E. Hardy, D. S. Campbell, J. M. Parant, H. J. Yost, J. P. Kanki, and C. B. Chien, “The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs,” Dev. Dyn. 236(11), 3088–3099 (2007).
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Hillman, E. M.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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W. C. Lemon, S. R. Pulver, B. Höckendorf, K. McDole, K. Branson, J. Freeman, and P. J. Keller, “Whole-central nervous system functional imaging in larval Drosophila,” Nat. Commun. 6(1), 7924 (2015).
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R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, and E. S. Boyden, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
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T. V. Truong, D. B. Holland, S. Madaan, A. Andreev, J. V. Troll, D. E. Koo, K. Keomanee-Dizon, M. McFall-Ngai, and S. E. Fraser, “Selective volume illumination microscopy offers synchronous volumetric imaging with high contrast,” bioRxiv, 403303 (2018).

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M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph 25(3), 924–934 (2006).
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R. Ng, M. Levoy, M. Brédif, G. Duval, M. Horowitz, and P. Hanrahan, “Light field photography with a hand-held plenoptic camera,” Computer Science Technical Report CSTR 2, 1–11 (2005).

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W. Koroshetz, J. Gordon, A. Adams, A. Beckel-Mitchener, J. Churchill, G. Farber, M. Freund, J. Gnadt, N. S. Hsu, and N. Langhals, “The state of the NIH Brain initiative,” J. Neurosci. 38(29), 6427–6438 (2018).
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Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
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N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
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U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
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Jayaraman, V.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, and V. Jayaraman, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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B. Wilburn, N. Joshi, V. Vaish, E.-V. Talvala, E. Antunez, A. Barth, A. Adams, M. Horowitz, and M. Levoy, “High performance imaging using large camera arrays,” in ACM Trans. Graph, (ACM, 2005), 765–776.

Kalfon, J.

A. Giovannucci, J. Friedrich, P. Gunn, J. Kalfon, B. L. Brown, S. A. Koay, J. Taxidis, F. Najafi, J. L. Gauthier, and P. Zhou, “CaImAn an open source tool for scalable calcium imaging data analysis,” eLife 8, e38173 (2019).
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Kanki, J. P.

K. M. Kwan, E. Fujimoto, C. Grabher, B. D. Mangum, M. E. Hardy, D. S. Campbell, J. M. Parant, H. J. Yost, J. P. Kanki, and C. B. Chien, “The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs,” Dev. Dyn. 236(11), 3088–3099 (2007).
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R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, and E. S. Boyden, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
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Keller, P. J.

W. C. Lemon, S. R. Pulver, B. Höckendorf, K. McDole, K. Branson, J. Freeman, and P. J. Keller, “Whole-central nervous system functional imaging in larval Drosophila,” Nat. Commun. 6(1), 7924 (2015).
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T. V. Truong, D. B. Holland, S. Madaan, A. Andreev, J. V. Troll, D. E. Koo, K. Keomanee-Dizon, M. McFall-Ngai, and S. E. Fraser, “Selective volume illumination microscopy offers synchronous volumetric imaging with high contrast,” bioRxiv, 403303 (2018).

Kerr, R. A.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, and V. Jayaraman, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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Koay, S. A.

A. Giovannucci, J. Friedrich, P. Gunn, J. Kalfon, B. L. Brown, S. A. Koay, J. Taxidis, F. Najafi, J. L. Gauthier, and P. Zhou, “CaImAn an open source tool for scalable calcium imaging data analysis,” eLife 8, e38173 (2019).
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Koo, D. E.

T. V. Truong, D. B. Holland, S. Madaan, A. Andreev, J. V. Troll, D. E. Koo, K. Keomanee-Dizon, M. McFall-Ngai, and S. E. Fraser, “Selective volume illumination microscopy offers synchronous volumetric imaging with high contrast,” bioRxiv, 403303 (2018).

Koroshetz, W.

W. Koroshetz, J. Gordon, A. Adams, A. Beckel-Mitchener, J. Churchill, G. Farber, M. Freund, J. Gnadt, N. S. Hsu, and N. Langhals, “The state of the NIH Brain initiative,” J. Neurosci. 38(29), 6427–6438 (2018).
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Kramer, A.

M. Kunst, E. Laurell, N. Mokayes, A. Kramer, F. Kubo, A. M. Fernandes, D. Förster, M. Dal Maschio, and H. Baier, “A cellular-resolution atlas of the larval zebrafish brain,” Available at SSRN 3257346 (2018).

Krzic, U.

U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
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Kubo, F.

M. Kunst, E. Laurell, N. Mokayes, A. Kramer, F. Kubo, A. M. Fernandes, D. Förster, M. Dal Maschio, and H. Baier, “A cellular-resolution atlas of the larval zebrafish brain,” Available at SSRN 3257346 (2018).

Kunst, M.

M. Kunst, E. Laurell, N. Mokayes, A. Kramer, F. Kubo, A. M. Fernandes, D. Förster, M. Dal Maschio, and H. Baier, “A cellular-resolution atlas of the larval zebrafish brain,” Available at SSRN 3257346 (2018).

Kwan, K. M.

K. M. Kwan, E. Fujimoto, C. Grabher, B. D. Mangum, M. E. Hardy, D. S. Campbell, J. M. Parant, H. J. Yost, J. P. Kanki, and C. B. Chien, “The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs,” Dev. Dyn. 236(11), 3088–3099 (2007).
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Lacefield, C.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
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[Crossref]

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, and E. S. Boyden, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref]

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W. C. Lemon, S. R. Pulver, B. Höckendorf, K. McDole, K. Branson, J. Freeman, and P. J. Keller, “Whole-central nervous system functional imaging in larval Drosophila,” Nat. Commun. 6(1), 7924 (2015).
[Crossref]

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[Crossref]

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M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref]

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[Crossref]

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D. P. Ryan, E. A. Gould, G. J. Seedorf, O. Masihzadeh, S. H. Abman, S. Vijayaraghavan, W. B. Macklin, D. Restrepo, and D. P. Shepherd, “Automatic and adaptive heterogeneous refractive index compensation for light-sheet microscopy,” Nat. Commun. 8(1), 612 (2017).
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Schnitzer, M. J.

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref]

Y. Gong, M. J. Wagner, J. Z. Li, and M. J. Schnitzer, “Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors,” Nat. Commun. 5(1), 3674 (2014).
[Crossref]

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T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, and V. Jayaraman, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref]

Schrödel, T.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, and E. S. Boyden, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref]

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M. A. Taylor, G. C. Vanwalleghem, I. A. Favre-Bulle, and E. K. Scott, “Diffuse light-sheet microscopy for stripe-free calcium imaging of neural populations,” J. Biophotonics 11(12), e201800088 (2018).
[Crossref]

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D. P. Ryan, E. A. Gould, G. J. Seedorf, O. Masihzadeh, S. H. Abman, S. Vijayaraghavan, W. B. Macklin, D. Restrepo, and D. P. Shepherd, “Automatic and adaptive heterogeneous refractive index compensation for light-sheet microscopy,” Nat. Commun. 8(1), 612 (2017).
[Crossref]

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B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

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A.-K. Gustavsson, P. N. Petrov, M. Y. Lee, Y. Shechtman, and W. Moerner, “3D single-molecule super-resolution microscopy with a tilted light sheet,” Nat. Commun. 9(1), 123 (2018).
[Crossref]

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Z. Wang, A. C. Bovik, H. R. Sheikh, and E. P. Simoncelli, “Image quality assessment: from error visibility to structural similarity,” IEEE Trans. on Image Process. 13(4), 600–612 (2004).
[Crossref]

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D. P. Ryan, E. A. Gould, G. J. Seedorf, O. Masihzadeh, S. H. Abman, S. Vijayaraghavan, W. B. Macklin, D. Restrepo, and D. P. Shepherd, “Automatic and adaptive heterogeneous refractive index compensation for light-sheet microscopy,” Nat. Commun. 8(1), 612 (2017).
[Crossref]

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Z. Wang, A. C. Bovik, H. R. Sheikh, and E. P. Simoncelli, “Image quality assessment: from error visibility to structural similarity,” IEEE Trans. on Image Process. 13(4), 600–612 (2004).
[Crossref]

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A. A. Bhandiwad, D. G. Zeddies, D. W. Raible, E. W. Rubel, and J. A. Sisneros, “Auditory sensitivity of larval zebrafish (Danio rerio) measured using a behavioral prepulse inhibition assay,” J. Exp. Biol. 216(18), 3504–3513 (2013).
[Crossref]

Skocek, O.

O. Skocek, T. Nöbauer, L. Weilguny, F. M. Traub, C. N. Xia, M. I. Molodtsov, A. Grama, M. Yamagata, D. Aharoni, and D. D. Cox, “High-speed volumetric imaging of neuronal activity in freely moving rodents,” Nat. Methods 15(6), 429–432 (2018).
[Crossref]

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S. Soltanian-Zadeh, K. Sahingur, S. Blau, Y. Gong, and S. Farsiu, “Fast and robust active neuron segmentation in two-photon calcium imaging using spatiotemporal deep learning,” Proceedings of the National Academy of Sciences, 201812995 (2019).

Streichan, S. J.

U. Krzic, S. Gunther, T. E. Saunders, S. J. Streichan, and L. Hufnagel, “Multiview light-sheet microscope for rapid in toto imaging,” Nat. Methods 9(7), 730–733 (2012).
[Crossref]

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T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, and V. Jayaraman, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref]

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B. Wilburn, N. Joshi, V. Vaish, E.-V. Talvala, E. Antunez, A. Barth, A. Adams, M. Horowitz, and M. Levoy, “High performance imaging using large camera arrays,” in ACM Trans. Graph, (ACM, 2005), 765–776.

Taxidis, J.

A. Giovannucci, J. Friedrich, P. Gunn, J. Kalfon, B. L. Brown, S. A. Koay, J. Taxidis, F. Najafi, J. L. Gauthier, and P. Zhou, “CaImAn an open source tool for scalable calcium imaging data analysis,” eLife 8, e38173 (2019).
[Crossref]

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M. A. Taylor, G. C. Vanwalleghem, I. A. Favre-Bulle, and E. K. Scott, “Diffuse light-sheet microscopy for stripe-free calcium imaging of neural populations,” J. Biophotonics 11(12), e201800088 (2018).
[Crossref]

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L. Theis, P. Berens, E. Froudarakis, J. Reimer, M. R. Rosón, T. Baden, T. Euler, A. S. Tolias, and M. Bethge, “Benchmarking spike rate inference in population calcium imaging,” Neuron 90(3), 471–482 (2016).
[Crossref]

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Tian, L.

Tolias, A. S.

L. Theis, P. Berens, E. Froudarakis, J. Reimer, M. R. Rosón, T. Baden, T. Euler, A. S. Tolias, and M. Bethge, “Benchmarking spike rate inference in population calcium imaging,” Neuron 90(3), 471–482 (2016).
[Crossref]

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O. Skocek, T. Nöbauer, L. Weilguny, F. M. Traub, C. N. Xia, M. I. Molodtsov, A. Grama, M. Yamagata, D. Aharoni, and D. D. Cox, “High-speed volumetric imaging of neuronal activity in freely moving rodents,” Nat. Methods 15(6), 429–432 (2018).
[Crossref]

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T. V. Truong, D. B. Holland, S. Madaan, A. Andreev, J. V. Troll, D. E. Koo, K. Keomanee-Dizon, M. McFall-Ngai, and S. E. Fraser, “Selective volume illumination microscopy offers synchronous volumetric imaging with high contrast,” bioRxiv, 403303 (2018).

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T. V. Truong, D. B. Holland, S. Madaan, A. Andreev, J. V. Troll, D. E. Koo, K. Keomanee-Dizon, M. McFall-Ngai, and S. E. Fraser, “Selective volume illumination microscopy offers synchronous volumetric imaging with high contrast,” bioRxiv, 403303 (2018).

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B. Wilburn, N. Joshi, V. Vaish, E.-V. Talvala, E. Antunez, A. Barth, A. Adams, M. Horowitz, and M. Levoy, “High performance imaging using large camera arrays,” in ACM Trans. Graph, (ACM, 2005), 765–776.

Vanwalleghem, G. C.

M. A. Taylor, G. C. Vanwalleghem, I. A. Favre-Bulle, and E. K. Scott, “Diffuse light-sheet microscopy for stripe-free calcium imaging of neural populations,” J. Biophotonics 11(12), e201800088 (2018).
[Crossref]

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T. Vettenburg, H. I. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11(5), 541–544 (2014).
[Crossref]

Vijayaraghavan, S.

D. P. Ryan, E. A. Gould, G. J. Seedorf, O. Masihzadeh, S. H. Abman, S. Vijayaraghavan, W. B. Macklin, D. Restrepo, and D. P. Shepherd, “Automatic and adaptive heterogeneous refractive index compensation for light-sheet microscopy,” Nat. Commun. 8(1), 612 (2017).
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Voigt, F. F.

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M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Wagner, M. J.

Y. Gong, M. J. Wagner, J. Z. Li, and M. J. Schnitzer, “Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors,” Nat. Commun. 5(1), 3674 (2014).
[Crossref]

Wagner, N.

N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16(6), 497–500 (2019).
[Crossref]

Waller, L.

Wang, J.

Wang, K.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

Wang, Z.

Z. Wang, A. C. Bovik, H. R. Sheikh, and E. P. Simoncelli, “Image quality assessment: from error visibility to structural similarity,” IEEE Trans. on Image Process. 13(4), 600–612 (2004).
[Crossref]

Wardill, T. J.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, and V. Jayaraman, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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Figures (7)

Fig. 1.
Fig. 1. Conceptual schematics show that the LSLFM simplified the detection (vs. LSM) and limited the illumination to the region of interest for volumetric imaging (vs. WFLFM). (a) LSM used a scanning light-sheet excitation matched to an imaging plane modulated by an ETL. Dark green: excitation laser beam. Light green: Scanning volume of light-sheet. Dark blue and light blue lines represent the imaging paths focused at two positions controlled by the ETL that matched the excitation planes. (b) WFLFM used wide-field illumination and light-field imaging. (c) LSLFM used a scanning light-sheet for excitation and a micro-lens array for light-field imaging. (d) Schematic drawing shows the imaging setup.
Fig. 2.
Fig. 2. Dynamic calibration synchronized the displacement of the light-sheet with the focus shift of ETL. (a) The flow chart outlines the dynamic calibration procedures. Calibration of amplitude and phase identified the best peak voltage (V+out), trough voltage (V-out), and phase (Pout) for the sine wave applied to the galvo mirror. (b) Left: To calibrate the amplitude, we applied different peak and trough voltages in combination, and maximized the total pixel intensity over one cycle of the light-sheet scanning. Right: Once we obtained the optimal voltage input combination (V+out = 60 mV and V-out = −60 mV), we found the phase (Pout = 95°) that likewise maximized the pixel intensity. (c) The computed light-sheet position over one cycle of scanning matched the physical position determined by sample translation. (d) The intensity difference between the images taken in one half cycle using either the scanning-beam or the sample translational LSM was minimal.
Fig. 3.
Fig. 3. Schematic shows the reconstruction procedures of (a) light-sheet and (b) light-field imaging. In LSM reconstruction, we set a series of reference frames from data within the first scanning cycle and computed the similarity of all other frames to this set of reference frames. We then combined the frames showing the highest similarity in each cycle (labeled with red dots) sequentially over time, forming the reconstructed sequence of frames for each layer within our imaging depth. Light-field imaging acquired only one frame for each imaging volume. We first reconstructed each depth in the volume individually, and then combined these reconstructed images sequentially. Similarly, we repeated the same reconstruction procedure for all the imaging depths.
Fig. 4.
Fig. 4. Imaging of sub-diffraction beads demonstrated that LSLFM imaged with finer resolution than WFLFM. Images of individual 0.5 µm beads and the intensity profiles along the dashed lines obtained with (a) WFLFM, (b) LSLFM, and (c) LSM. Fits to Gaussian profiles determined the FWHM. Scale bar: 5 µm. (d) Comparison of FWHM between the three tested imaging modalities (mean ± std.). The lateral and axial FWHMs for LSLFM were smaller than those of the WFLFM, *p < 0.05 (n = 6, two-sided Wilcoxon rank-sum test).
Fig. 5.
Fig. 5. LSLFM produced higher contrast and lower background than WFLFM when imaging sub-diffraction beads. Bead images acquired at different depths within a 32 µm deep volume using (a) WFLSM, (b) LSLFM, (c) direct light-field imaging and (d) scanning-beam LSM. Scale bar: 50 µm. WFLFM did not clearly reveal the individual beads due to the high background. In contrast, LSLFM clearly showed the individual beads over different depths, similar to the results of direct-light-field imaging and LSM. The white arrows in panel (b) indicate beads that appeared in multiple planes due to the blurring of the axial point spread function in the LSLFM image. The same beads were not seen in the images of direct-light-field imaging and LSM. Quantitative analysis of the beads’ (e) absolute signal intensity, (f) background intensity, and (g) Weber contrast for the four imaging modalities (n = 5, mean ± std.).
Fig. 6.
Fig. 6. LSLFM imaging of the zebrafish brain expressing GCaMP6s in vivo produced more detail than WFLFM imaging. Images of the zebrafish brain acquired with (a) WFLFM, (b) LSLFM, (c) direct light-field imaging, and (d) LSM at depths of −16 µm, 0 µm, and 16 µm. LSLFM revealed the structure of sub-regions within the larval zebrafish brain, comparable to direct light-field imaging. WFLFM failed to resolve such structure due to the high background. Right: We quantified the feature size as the distance between the half feature heights. Scale bar: 50 µm.
Fig. 7.
Fig. 7. LSLFM imaging of the zebrafish brain during auditory stimulus improves the quality of recorded calcium transients compared to WFLFM. (a) Active neurons and the fluorescence traces acquired with WFLFM (left), LSLFM (middle) and LSM (right). Top row: Image of depth-encoded labeling of active neurons (colored masks) on top of brain structures (grayscale); Middle row: an enlarged view of the regions labeled with red boxes in the top images. The intensity corresponds to the normalized difference between the mean image of the frames with calcium transients and the mean image of the frames without neuron transients. Bottom row: Fluorescence traces from the same five representative neurons at different depths (−16 µm, −8 µm, 0 µm, 8 µm and 16 µm). Gray bars indicate auditory stimulus. (b) SNR comparison between neurons imaged with WFLFM, LSLFM, and LSM (mean ± std., n = 460, 558, and 648 neurons for WFLFM, LSLFM and LSM, respectively. ** p < 0.01, two-sided Wilcoxon rank-sum test). (c) Fluorescent beads imaged with LSM under the identical condition as the fish experiments. All scale bars are 20 µm.

Equations (2)

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D ETL f relay 1 f tube × D obj ,
P ls = f scan × f ex f tube × tan ( V 0.8 )