Abstract

A number of questions in system biology such as understanding how dynamics of neuronal networks are related to brain function require the ability to capture the functional dynamics of large cellular populations at high speed. Recently, this has driven the development of a number of parallel and high speed imaging techniques such as light-sculpting microscopy, which has been used to capture neuronal dynamics at the whole brain and single cell level in small model organisms. However, the broader applicability of light-sculpting microcopy is limited by the size of volumes for which high speed imaging can be obtained and scattering in brain tissue. Here, we present strategies for optimizing the present tradeoffs in light-sculpting microscopy. Various scanning modalities in light-sculpting microscopy are theoretically and experimentally evaluated, and strategies to maximize the obtainable volume speeds, and depth penetration in brain tissue using different laser systems are provided. Design-choices, important parameters and their trade-offs are experimentally demonstrated by performing calcium-imaging in acute mouse-brain slices. We further show that synchronization of line-scanning techniques with rolling-shutter read-out of the camera can reduce scattering effects and enhance image contrast at depth.

© 2015 Optical Society of America

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P. W. Winter and H. Shroff, “Faster fluorescence microscopy: advances in high speed biological imaging,” Curr. Opin. Chem. Biol. 20, 46–53 (2014).
[Crossref] [PubMed]

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

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[Crossref] [PubMed]

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[Crossref] [PubMed]

2013 (3)

H. Choi, E. Y. S. Yew, B. Hallacoglu, S. Fantini, C. J. R. Sheppard, and P. T. C. So, “Improvement of axial resolution and contrast in temporally focused widefield two-photon microscopy with structured light illumination,” Biomed. Opt. Express 4(7), 995–1005 (2013).
[Crossref] [PubMed]

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] [PubMed]

T. Schrödel, R. Prevedel, K. Aumayr, M. Zimmer, and A. Vaziri, “Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light,” Nat. Methods 10(10), 1013–1020 (2013).
[Crossref] [PubMed]

2012 (8)

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
[Crossref] [PubMed]

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
[Crossref] [PubMed]

L. C. Cheng, C. Y. Chang, C. Y. Lin, K. C. Cho, W. C. Yen, N. S. Chang, C. Xu, C. Y. Dong, and S. J. Chen, “Spatiotemporal focusing-based widefield multiphoton microscopy for fast optical sectioning,” Opt. Express 20(8), 8939–8948 (2012).
[Crossref] [PubMed]

F. O. Fahrbach and A. Rohrbach, “Propagation stability of self-reconstructing Bessel beams enables contrast-enhanced imaging in thick media,” Nat. Commun. 3, 632 (2012).
[Crossref] [PubMed]

L. Silvestri, A. Bria, L. Sacconi, G. Iannello, and F. S. Pavone, “Confocal light sheet microscopy: micron-scale neuroanatomy of the entire mouse brain,” Opt. Express 20(18), 20582–20598 (2012).
[Crossref] [PubMed]

E. Baumgart and U. Kubitscheck, “Scanned light sheet microscopy with confocal slit detection,” Opt. Express 20(19), 21805–21814 (2012).
[Crossref] [PubMed]

H. Dana and S. Shoham, “Remotely scanned multiphoton temporal focusing by axial grism scanning,” Opt. Lett. 37(14), 2913–2915 (2012).
[Crossref] [PubMed]

2010 (2)

A. Vaziri and C. V. Shank, “Ultrafast widefield optical sectioning microscopy by multifocal temporal focusing,” Opt. Express 18(19), 19645–19655 (2010).
[Crossref] [PubMed]

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

2008 (1)

G. Duemani Reddy, K. Kelleher, R. Fink, and P. Saggau, “Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity,” Nat. Neurosci. 11(6), 713–720 (2008).
[Crossref] [PubMed]

2005 (5)

2003 (1)

2002 (1)

A. N. Yaroslavsky, P. C. Schulze, I. V. Yaroslavsky, R. Schober, F. Ulrich, and H. J. Schwarzmaier, “Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range,” Phys. Med. Biol. 47(12), 2059–2073 (2002).
[Crossref] [PubMed]

2001 (2)

M. Oheim, E. Beaurepaire, E. Chaigneau, J. Mertz, and S. Charpak, “Two-photon microscopy in brain tissue: parameters influencing the imaging depth,” J. Neurosci. Methods 111(1), 29–37 (2001).
[Crossref] [PubMed]

Q. T. Nguyen, N. Callamaras, C. Hsieh, and I. Parker, “Construction of a two-photon microscope for video-rate Ca(2+) imaging,” Cell Calcium 30(6), 383–393 (2001).
[Crossref] [PubMed]

2000 (1)

P. T. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-photon excitation fluorescence microscopy,” Annu. Rev. Biomed. Eng. 2(1), 399–429 (2000).
[Crossref] [PubMed]

1999 (1)

G. Y. Fan, H. Fujisaki, A. Miyawaki, R. K. Tsay, R. Y. Tsien, and M. H. Ellisman, “Video-Rate Scanning Two-Photon Excitation Fluorescence Microscopy and Ratio Imaging with Cameleons,” Biophys. J. 76(5), 2412–2420 (1999).
[Crossref] [PubMed]

1996 (1)

A. Taddeucci, F. Martelli, M. Barilli, M. Ferrari, and G. Zaccanti, “Optical properties of brain tissue,” J. Biomed. Opt. 1(1), 117–123 (1996).
[Crossref] [PubMed]

1941 (1)

L. G. Henyey and J. L. Greenstein, “Diffuse radiation in the galaxy,” Astrophys. J. 93, 70–83 (1941).
[Crossref]

Aggarwal, A.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
[Crossref] [PubMed]

Ahrens, M. B.

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] [PubMed]

Akerboom, J.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
[Crossref] [PubMed]

Aumayr, K.

T. Schrödel, R. Prevedel, K. Aumayr, M. Zimmer, and A. Vaziri, “Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light,” Nat. Methods 10(10), 1013–1020 (2013).
[Crossref] [PubMed]

Baier, H.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
[Crossref] [PubMed]

Bargmann, C. I.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
[Crossref] [PubMed]

Barilli, M.

A. Taddeucci, F. Martelli, M. Barilli, M. Ferrari, and G. Zaccanti, “Optical properties of brain tissue,” J. Biomed. Opt. 1(1), 117–123 (1996).
[Crossref] [PubMed]

Baumgart, E.

Beaurepaire, E.

M. Oheim, E. Beaurepaire, E. Chaigneau, J. Mertz, and S. Charpak, “Two-photon microscopy in brain tissue: parameters influencing the imaging depth,” J. Neurosci. Methods 111(1), 29–37 (2001).
[Crossref] [PubMed]

Berland, K. M.

P. T. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-photon excitation fluorescence microscopy,” Annu. Rev. Biomed. Eng. 2(1), 399–429 (2000).
[Crossref] [PubMed]

Borghuis, B. G.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
[Crossref] [PubMed]

Boyden, E. S.

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

Bria, A.

Brosh, I.

H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
[Crossref] [PubMed]

Calderón, N. C.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
[Crossref] [PubMed]

Callamaras, N.

Q. T. Nguyen, N. Callamaras, C. Hsieh, and I. Parker, “Construction of a two-photon microscope for video-rate Ca(2+) imaging,” Cell Calcium 30(6), 383–393 (2001).
[Crossref] [PubMed]

Chaigneau, E.

M. Oheim, E. Beaurepaire, E. Chaigneau, J. Mertz, and S. Charpak, “Two-photon microscopy in brain tissue: parameters influencing the imaging depth,” J. Neurosci. Methods 111(1), 29–37 (2001).
[Crossref] [PubMed]

Chang, C. Y.

Chang, N. S.

Charpak, S.

M. Oheim, E. Beaurepaire, E. Chaigneau, J. Mertz, and S. Charpak, “Two-photon microscopy in brain tissue: parameters influencing the imaging depth,” J. Neurosci. Methods 111(1), 29–37 (2001).
[Crossref] [PubMed]

Chen, S. J.

Chen, T. W.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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G. Duemani Reddy, K. Kelleher, R. Fink, and P. Saggau, “Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity,” Nat. Neurosci. 11(6), 713–720 (2008).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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Han, S.

Hasan, M. T.

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Q. T. Nguyen, N. Callamaras, C. Hsieh, and I. Parker, “Construction of a two-photon microscope for video-rate Ca(2+) imaging,” Cell Calcium 30(6), 383–393 (2001).
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X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
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B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
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B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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G. Duemani Reddy, K. Kelleher, R. Fink, and P. Saggau, “Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity,” Nat. Neurosci. 11(6), 713–720 (2008).
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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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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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Kim, D.

Kim, D. S.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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Kimmel, B. E.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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Konnerth, A.

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
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Kracun, S.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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Lagnado, L.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

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X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
[Crossref] [PubMed]

Li, J. M.

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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Lin, C. Y.

Looger, L. L.

J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
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A. Taddeucci, F. Martelli, M. Barilli, M. Ferrari, and G. Zaccanti, “Optical properties of brain tissue,” J. Biomed. Opt. 1(1), 117–123 (1996).
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G. Y. Fan, H. Fujisaki, A. Miyawaki, R. K. Tsay, R. Y. Tsien, and M. H. Ellisman, “Video-Rate Scanning Two-Photon Excitation Fluorescence Microscopy and Ratio Imaging with Cameleons,” Biophys. J. 76(5), 2412–2420 (1999).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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Nguyen, Q. T.

Q. T. Nguyen, N. Callamaras, C. Hsieh, and I. Parker, “Construction of a two-photon microscope for video-rate Ca(2+) imaging,” Cell Calcium 30(6), 383–393 (2001).
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M. Oheim, E. Beaurepaire, E. Chaigneau, J. Mertz, and S. Charpak, “Two-photon microscopy in brain tissue: parameters influencing the imaging depth,” J. Neurosci. Methods 111(1), 29–37 (2001).
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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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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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Oron, D.

Pak, N.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
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H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
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Parker, I.

Q. T. Nguyen, N. Callamaras, C. Hsieh, and I. Parker, “Construction of a two-photon microscope for video-rate Ca(2+) imaging,” Cell Calcium 30(6), 383–393 (2001).
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Pavone, F. S.

Peterka, D. S.

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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T. Schrödel, R. Prevedel, K. Aumayr, M. Zimmer, and A. Vaziri, “Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light,” Nat. Methods 10(10), 1013–1020 (2013).
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S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
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R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
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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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X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
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F. O. Fahrbach and A. Rohrbach, “Propagation stability of self-reconstructing Bessel beams enables contrast-enhanced imaging in thick media,” Nat. Commun. 3, 632 (2012).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
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T. Schrödel, R. Prevedel, K. Aumayr, M. Zimmer, and A. Vaziri, “Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light,” Nat. Methods 10(10), 1013–1020 (2013).
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A. N. Yaroslavsky, P. C. Schulze, I. V. Yaroslavsky, R. Schober, F. Ulrich, and H. J. Schwarzmaier, “Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range,” Phys. Med. Biol. 47(12), 2059–2073 (2002).
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Sheppard, C. J. R.

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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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A. N. Yaroslavsky, P. C. Schulze, I. V. Yaroslavsky, R. Schober, F. Ulrich, and H. J. Schwarzmaier, “Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range,” Phys. Med. Biol. 47(12), 2059–2073 (2002).
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Varga, Z.

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
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R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
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T. Schrödel, R. Prevedel, K. Aumayr, M. Zimmer, and A. Vaziri, “Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light,” Nat. Methods 10(10), 1013–1020 (2013).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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J. Akerboom, T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderón, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. H. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger, “Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging,” J. Neurosci. 32(40), 13819–13840 (2012).
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S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
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Q. T. Nguyen, N. Callamaras, C. Hsieh, and I. Parker, “Construction of a two-photon microscope for video-rate Ca(2+) imaging,” Cell Calcium 30(6), 383–393 (2001).
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Figures (5)

Fig. 1
Fig. 1

Experimental setup and various modalities of light sculpting microscopy. A. Principle of temporal focusing. The grating disperses the laser pulse in its spectral components, which are refocused by a telescope in time and space formed by the temporal focusing lens (TF-lens) and the objective at the image plane in the sample. The dashed lines illustrate the spatial and temporal dispersion of the pulse at various points along the axial direction B. Schematic of the setup including its various modalities. The laser beam, from either a Ti:Sa source or an amplified system, is expanded via lenses and directed towards a pair of galvo mirrors, after which, depending on the scanning modality either no lens (wide-field), a cylindrical scan lens (fcyl – line-scan 1D-LS) or a spherical scan lens (fsp – spiral-scan 2D-SS) are employed. C. Left panel illustrates the schematics of various excitation modalities, including wide-field (top), line-scan 1D-LS (middle) and spiral-scan 2D-SS (bottom). Note that in the spiral scan configuration the small spot (diameter d~4-8 µm) being scanned is also a temporally focused disc. The middle panel shows the resulting excitation pattern taken with a fluorescent plastic slide, with cross sections along the x- and y-axis shown in the right panel. D. A typical axial scan of a single, 500 nm fluorescent bead in the spiral scan configuration, indicating the axial resolution. The asymmetry is due to background fluorescence. Scale bars are 50 µm in C.

Fig. 2
Fig. 2

Trading off area versus imaging speed and fluorescence for different excitation modalities. A. Theoretical estimates and experimental measurements of the fluorescence signal as a function of the excited area for different combinations of laser systems and excitation modalities. Numbers indicate parameter configurations at which experimental data were obtained with the respective images shown in D. Dashed lines indicate regions for which the scanning speed of the galvo mirrors would not be sufficient. The values on the y-axis are typical signal intensities for practical calcium imaging with N a > 1 10 7 representing an empirical lower bound (dashed grey line). B. Time required for scanning an area in order to achieve N a ~ 3 10 8 hence sufficient signal for imaging as discussed in the main text. Coloring identical to A. C. Isolines for sufficient fluorescence signal ( N a ~ 3 10 8 ) during different image exposure times in dependence on scanned and non-scanned directions for a line-scan configuration ( w ~3 µm ) using an amplifier system. D. Images of convallaria rhizome, taken with different configurations at 10% of available power and t exp = 10 ms exposure time per plane. The scale bar applies to all subfigures.

Fig. 3
Fig. 3

Ca2+-imaging of acute mouse brain slices at various imaging depths, and using different TeFo excitation modalities. Individual somata as well as neuropil can clearly be seen at different depths as indicated in the top right corner. A. Amplifier 1D-LS TeFo. B. Amplifier WF TeFo. C. Ti:Sa 2D-SS TeFo. All images were taken with an exposure time of 10 ms and no frame averaging has been performed for A-C. D. Extracted Ca2+-signal from an acute brain slice that showed brief and sporadic spontaneous activity imaged with 200 µm FOV 2D-SS TeFo. The blue trace shows the baseline of an inactive neuron, while the black trace corresponds to another neuron showing brief bursts of activity. Thick lines show the 50 ms moving average of the raw extracted fluorescence signal, plotted as a relative fluorescence change dF/F. See the main text for a discussion. Scale bar is 50 µm across all images.

Fig. 4
Fig. 4

Theoretical estimation of the rolling shutter effect on image quality in scattering media. A. Schematic drawing of the detection path. Scattered photons (dashed lines) are typically excluded by the rolling shutter. B. Ground truth object including circles with 30, 15, 7.5 and 2.5 µm diameter and orthogonal grids of 2 µm spacing. C. Simulated effect of scattering through scattering tissue ( μ s =20/mm ) on image quality for different imaging depths. D. Scattering kernel ( μ s =20/mm ) for different imaging depths. Note the different scaling in the inset zooms. E. The same scattering kernels in the spatial frequency domain. F. Improvement of the scattering kernel by using the rolling shutter effect for an imaging depth of 50 µm for different rolling shutter widths. The curves vary little between 25 and 100 µm imaging depth, as illustrated by the red band for the 3 µm line-width. G. Rolling shutter simulation of the ground truth object for different imaging depths and rolling shutter line widths.

Fig. 5
Fig. 5

Experimental demonstration of improved Ca2+-imaging quality in scattering tissue by using line-scan TeFo illumination in combination with rolling shutter readout (sample: GCaMP6m-expressing neurons in the amygdala of acute mouse brain slices). Single images with an exposure time of 10 ms taken without rolling shutter (A-C) and with rolling shutter (D-F) at different depths (d) in the tissue. All images are an excerpt of a larger 200x200 µm FOV. G-I. Analysis of spatial frequency components in the acquired images. The frequency plots show which spatial frequencies are amplified in comparison with the non-rolling shutter-image, shown for different widths of the rolling shutter, w RS . The maximum of the gain around 0.1-0.2 µm−1 shows the improvement for a band of spatial frequencies corresponding to 5-10 µm sized features. Best choices for the rolling shutter width vary in dependence on imaging depth and were assessed by visual inspection: 1.2 µm for D, 3.0 µm for E and 5.9 µm for F (in (I) no data were acquired for w RS =1.2 µm ). Scalebars are 10 μm and apply to all subfigures.

Tables (2)

Tables Icon

Table 1 Summary of achievable field-of-views (FOV) in fast functional imaging experiments using the various scanning modalities discussed in the main text. Note that the plane exposure time, t exp , was fixed at 10 ms in all cases. The right column gives the main limitations when further trying to increase FOV for the various configurations. X denotes that in practice the laser source is not properly suited for the scanning modality.

Tables Icon

Table 2 Overview of possible scanning configuration and laser sources for given FOVs and frame rates. Nomenclature is identical to the main text. Green: expected signal intensity >108, i.e. sufficient signal for typical brain samples. Orange: expected signal levels of 107-108, empirical lower bound for practical calcium imaging.

Equations (3)

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N a ~ P 0 2 f τ ( λ A ) 2 Δt ,
I= x M[ K( G( x )W ) ]= K RS W,
K ^ RS =FT( K RS )=FT( I )/FT( W )

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