Abstract

Light sheet fluorescence microscopy offers considerable potential to the cellular neuroscience community as it makes it possible to image extensive areas of neuronal structures, such as axons or dendrites, with a low light budget, thereby minimizing phototoxicity. However, the shallow depth of a light sheet, which is critical for achieving high contrast, well resolved images, adds a significant challenge if fast functional imaging is also required, as multiple images need to be collected across several image planes. Consequently, fast functional imaging of neurons is typically restricted to a small tissue volume where part of the neuronal structure lies within the plane of a single image. Here we describe a method by which fast functional imaging can be achieved across a much larger tissue volume; a custom-built light sheet microscope is presented that includes a synchronized galvo mirror and electrically tunable lens, enabling high speed acquisition of images across a configurable depth. We assess the utility of this technique by acquiring fast functional Ca2+ imaging data across a neuron’s dendritic arbour in mammalian brain tissue.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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References

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2017 (2)

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

M. Duocastella, G. Sancataldo, P. Saggau, P. Ramoino, P. Bianchini, and A. Diaspro, “Fast Inertia-Free Volumetric Light-Sheet Microscope,” ACS Photonics 4(7), 1797–1804 (2017).
[Crossref]

2016 (3)

2015 (4)

O. E. Olarte, J. Andilla, D. Artigas, and P. Loza-Alvarez, “Decoupled illumination detection in light sheet microscopy for fast volumetric imaging,” Optica 2(8), 702 (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, 7924 (2015).
[Crossref] [PubMed]

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

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

2013 (2)

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] [PubMed]

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

2012 (1)

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

2011 (2)

B. F. Grewe, F. F. Voigt, M. van ’t Hoff, and F. Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Express 2(7), 2035–2046 (2011).
[Crossref] [PubMed]

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

2008 (3)

T. F. Holekamp, D. Turaga, and T. E. Holy, “Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy,” Neuron 57(5), 661–672 (2008).
[Crossref] [PubMed]

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

C. Dunsby, “Optically sectioned imaging by oblique plane microscopy,” Opt. Express 16(25), 20306–20316 (2008).
[Crossref] [PubMed]

2007 (1)

C. E. J. Cheetham, M. S. L. Hammond, C. E. J. Edwards, and G. T. Finnerty, “Sensory experience alters cortical connectivity and synaptic function site specifically,” J. Neurosci. 27(13), 3456–3465 (2007).
[Crossref] [PubMed]

2002 (1)

N. L. Golding, N. P. Staff, and N. Spruston, “Dendritic spikes as a mechanism for cooperative long-term potentiation,” Nature 418(6895), 326–331 (2002).
[Crossref] [PubMed]

1999 (1)

N. Emptage, T. V. Bliss, and A. Fine, “Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines,” Neuron 22(1), 115–124 (1999).
[Crossref] [PubMed]

1991 (1)

L. Stoppini, P. A. Buchs, and D. Muller, “A simple method for organotypic cultures of nervous tissue,” J. Neurosci. Methods 37(2), 173–182 (1991).
[Crossref] [PubMed]

Ahrens, M. B.

Andalman, A.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Andilla, J.

Arganda-Carreras, I.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Artigas, D.

Bao, Z.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Bianchini, P.

M. Duocastella, G. Sancataldo, P. Saggau, P. Ramoino, P. Bianchini, and A. Diaspro, “Fast Inertia-Free Volumetric Light-Sheet Microscope,” ACS Photonics 4(7), 1797–1804 (2017).
[Crossref]

Bliss, T. V.

N. Emptage, T. V. Bliss, and A. Fine, “Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines,” Neuron 22(1), 115–124 (1999).
[Crossref] [PubMed]

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. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref] [PubMed]

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, 7924 (2015).
[Crossref] [PubMed]

Broxton, M.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Bruno, R. M.

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

Buchs, P. A.

L. Stoppini, P. A. Buchs, and D. Muller, “A simple method for organotypic cultures of nervous tissue,” J. Neurosci. Methods 37(2), 173–182 (1991).
[Crossref] [PubMed]

Burns, V. M.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Cardona, A.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Chan, D. C.

Cheetham, C. E. J.

C. E. J. Cheetham, M. S. L. Hammond, C. E. J. Edwards, and G. T. Finnerty, “Sensory experience alters cortical connectivity and synaptic function site specifically,” J. Neurosci. 27(13), 3456–3465 (2007).
[Crossref] [PubMed]

Christensen, R.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Colón-Ramos, D.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Deisseroth, K.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Dholakia, K.

Z. Yang, P. Haslehurst, S. Scott, N. Emptage, and K. Dholakia, “A compact light-sheet microscope for the study of the mammalian central nervous system,” Sci. Rep. 6(1), 26317 (2016).
[Crossref] [PubMed]

Diaspro, A.

M. Duocastella, G. Sancataldo, P. Saggau, P. Ramoino, P. Bianchini, and A. Diaspro, “Fast Inertia-Free Volumetric Light-Sheet Microscope,” ACS Photonics 4(7), 1797–1804 (2017).
[Crossref]

Du, Z.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Dunsby, C.

Duocastella, M.

M. Duocastella, G. Sancataldo, P. Saggau, P. Ramoino, P. Bianchini, and A. Diaspro, “Fast Inertia-Free Volumetric Light-Sheet Microscope,” ACS Photonics 4(7), 1797–1804 (2017).
[Crossref]

Edwards, C. E. J.

C. E. J. Cheetham, M. S. L. Hammond, C. E. J. Edwards, and G. T. Finnerty, “Sensory experience alters cortical connectivity and synaptic function site specifically,” J. Neurosci. 27(13), 3456–3465 (2007).
[Crossref] [PubMed]

Eliceiri, K.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Eliceiri, K. W.

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

Emptage, N.

Z. Yang, P. Haslehurst, S. Scott, N. Emptage, and K. Dholakia, “A compact light-sheet microscope for the study of the mammalian central nervous system,” Sci. Rep. 6(1), 26317 (2016).
[Crossref] [PubMed]

N. Emptage, T. V. Bliss, and A. Fine, “Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines,” Neuron 22(1), 115–124 (1999).
[Crossref] [PubMed]

Fahrbach, F. O.

Fine, A.

N. Emptage, T. V. Bliss, and A. Fine, “Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines,” Neuron 22(1), 115–124 (1999).
[Crossref] [PubMed]

Finnerty, G. T.

C. E. J. Cheetham, M. S. L. Hammond, C. E. J. Edwards, and G. T. Finnerty, “Sensory experience alters cortical connectivity and synaptic function site specifically,” J. Neurosci. 27(13), 3456–3465 (2007).
[Crossref] [PubMed]

Freeman, 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, 7924 (2015).
[Crossref] [PubMed]

Frise, E.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Ghitani, A.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Golding, N. L.

N. L. Golding, N. P. Staff, and N. Spruston, “Dendritic spikes as a mechanism for cooperative long-term potentiation,” Nature 418(6895), 326–331 (2002).
[Crossref] [PubMed]

Grewe, B. F.

Grosenick, L.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

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. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref] [PubMed]

Gu, S.

Hammond, M. S. L.

C. E. J. Cheetham, M. S. L. Hammond, C. E. J. Edwards, and G. T. Finnerty, “Sensory experience alters cortical connectivity and synaptic function site specifically,” J. Neurosci. 27(13), 3456–3465 (2007).
[Crossref] [PubMed]

Hartenstein, V.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Haslehurst, P.

Z. Yang, P. Haslehurst, S. Scott, N. Emptage, and K. Dholakia, “A compact light-sheet microscope for the study of the mammalian central nervous system,” Sci. Rep. 6(1), 26317 (2016).
[Crossref] [PubMed]

Helmchen, F.

Hillman, E. M. C.

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

Höckendorf, B.

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, 7924 (2015).
[Crossref] [PubMed]

Holekamp, T. F.

T. F. Holekamp, D. Turaga, and T. E. Holy, “Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy,” Neuron 57(5), 661–672 (2008).
[Crossref] [PubMed]

Holy, T. E.

T. F. Holekamp, D. Turaga, and T. E. Holy, “Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy,” Neuron 57(5), 661–672 (2008).
[Crossref] [PubMed]

Huisken, J.

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

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

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] [PubMed]

Jenkins, M. W.

Kauvar, I.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Kaynig, V.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

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, 7924 (2015).
[Crossref] [PubMed]

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

Lacefield, C.

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

Lemon, W. C.

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, 7924 (2015).
[Crossref] [PubMed]

Longair, M.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Lovett-Barron, M.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Loza-Alvarez, P.

Ma, P.

Mann, R. S.

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

McDole, 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, 7924 (2015).
[Crossref] [PubMed]

Mendes, C. S.

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

Muller, D.

L. Stoppini, P. A. Buchs, and D. Muller, “A simple method for organotypic cultures of nervous tissue,” J. Neurosci. Methods 37(2), 173–182 (1991).
[Crossref] [PubMed]

Olarte, O. E.

Peterka, D. S.

Pietzsch, T.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Pitrone, P. G.

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

Power, R. M.

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

Preibisch, S.

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Pulver, S. R.

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, 7924 (2015).
[Crossref] [PubMed]

Quirin, S.

Ramoino, P.

M. Duocastella, G. Sancataldo, P. Saggau, P. Ramoino, P. Bianchini, and A. Diaspro, “Fast Inertia-Free Volumetric Light-Sheet Microscope,” ACS Photonics 4(7), 1797–1804 (2017).
[Crossref]

Rollins, A. M.

Rondeau, G.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Rueden, C.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Saalfeld, S.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Saggau, P.

M. Duocastella, G. Sancataldo, P. Saggau, P. Ramoino, P. Bianchini, and A. Diaspro, “Fast Inertia-Free Volumetric Light-Sheet Microscope,” ACS Photonics 4(7), 1797–1804 (2017).
[Crossref]

Sancataldo, G.

M. Duocastella, G. Sancataldo, P. Saggau, P. Ramoino, P. Bianchini, and A. Diaspro, “Fast Inertia-Free Volumetric Light-Sheet Microscope,” ACS Photonics 4(7), 1797–1804 (2017).
[Crossref]

Sankaran, S.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Santella, A.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Schindelin, J.

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Schmid, B.

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] [PubMed]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Schmidt, A. D.

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

Scott, S.

Z. Yang, P. Haslehurst, S. Scott, N. Emptage, and K. Dholakia, “A compact light-sheet microscope for the study of the mammalian central nervous system,” Sci. Rep. 6(1), 26317 (2016).
[Crossref] [PubMed]

Shroff, H.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Spruston, N.

N. L. Golding, N. P. Staff, and N. Spruston, “Dendritic spikes as a mechanism for cooperative long-term potentiation,” Nature 418(6895), 326–331 (2002).
[Crossref] [PubMed]

Staff, N. P.

N. L. Golding, N. P. Staff, and N. Spruston, “Dendritic spikes as a mechanism for cooperative long-term potentiation,” Nature 418(6895), 326–331 (2002).
[Crossref] [PubMed]

Stelzer, E. H. K.

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

Stoppini, L.

L. Stoppini, P. A. Buchs, and D. Muller, “A simple method for organotypic cultures of nervous tissue,” J. Neurosci. Methods 37(2), 173–182 (1991).
[Crossref] [PubMed]

Stuyvenberg, L.

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

Tinevez, J.-Y.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Tomancak, P.

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Tomer, R.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Turaga, D.

T. F. Holekamp, D. Turaga, and T. E. Holy, “Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy,” Neuron 57(5), 661–672 (2008).
[Crossref] [PubMed]

van ’t Hoff, M.

Vladimirov, N.

Voigt, F. F.

Voleti, V.

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

Watanabe, M.

Weber, M.

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

White, D. J.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Wittbrodt, J.

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

Wu, Y.

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Yang, C.-T.

Yang, S.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

Yang, Z.

Z. Yang, P. Haslehurst, S. Scott, N. Emptage, and K. Dholakia, “A compact light-sheet microscope for the study of the mammalian central nervous system,” Sci. Rep. 6(1), 26317 (2016).
[Crossref] [PubMed]

Yuste, R.

ACS Photonics (1)

M. Duocastella, G. Sancataldo, P. Saggau, P. Ramoino, P. Bianchini, and A. Diaspro, “Fast Inertia-Free Volumetric Light-Sheet Microscope,” ACS Photonics 4(7), 1797–1804 (2017).
[Crossref]

Biomed. Opt. Express (2)

Cell (1)

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function,” Cell 163(7), 1796–1806 (2015).
[Crossref] [PubMed]

J. Neurosci. (1)

C. E. J. Cheetham, M. S. L. Hammond, C. E. J. Edwards, and G. T. Finnerty, “Sensory experience alters cortical connectivity and synaptic function site specifically,” J. Neurosci. 27(13), 3456–3465 (2007).
[Crossref] [PubMed]

J. Neurosci. Methods (1)

L. Stoppini, P. A. Buchs, and D. Muller, “A simple method for organotypic cultures of nervous tissue,” J. Neurosci. Methods 37(2), 173–182 (1991).
[Crossref] [PubMed]

Nat. Commun. (1)

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, 7924 (2015).
[Crossref] [PubMed]

Nat. Methods (3)

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

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10(7), 598–599 (2013).
[Crossref] [PubMed]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Nat. Photonics (1)

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

Nature (1)

N. L. Golding, N. P. Staff, and N. Spruston, “Dendritic spikes as a mechanism for cooperative long-term potentiation,” Nature 418(6895), 326–331 (2002).
[Crossref] [PubMed]

Neuron (2)

N. Emptage, T. V. Bliss, and A. Fine, “Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines,” Neuron 22(1), 115–124 (1999).
[Crossref] [PubMed]

T. F. Holekamp, D. Turaga, and T. E. Holy, “Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy,” Neuron 57(5), 661–672 (2008).
[Crossref] [PubMed]

Opt. Express (2)

Opt. Lett. (1)

Optica (1)

Proc. Natl. Acad. Sci. U.S.A. (1)

Y. Wu, A. Ghitani, R. Christensen, A. Santella, Z. Du, G. Rondeau, Z. Bao, D. Colón-Ramos, and H. Shroff, “Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17708–17713 (2011).
[Crossref] [PubMed]

Sci. Rep. (1)

Z. Yang, P. Haslehurst, S. Scott, N. Emptage, and K. Dholakia, “A compact light-sheet microscope for the study of the mammalian central nervous system,” Sci. Rep. 6(1), 26317 (2016).
[Crossref] [PubMed]

Science (1)

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

Other (1)

R Core Team, R: a Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2015).

Supplementary Material (1)

NameDescription
» Visualization 1       The neuron was imaged by the light sheet microscope in single-plane mode with 594 nm illumination, 200 ms exposure, and 1 µm steps between each image in the stack. This video steps through this image stack at 4 frames per second.

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Figures (7)

Fig. 1
Fig. 1 Inverted light sheet microscope modified for fast volume scanning. a: The control signals applied to the electrically tuneable lens (ETL) and the galvo mirror. These move the light sheet and the focal plane of the detection objective in synchrony through a 20 µm traverse in the Z axis. In practice the control signals need to be separated by a phase difference (P) because of the lag time required for the ETL to respond to the signal. b: Diagram illustrating how fast volume scanning builds up a deeper image volume. In the left panel is shown the position of the light sheet illuminating a neuronal dendrite at consecutive moments as it scans through a complete cycle covering 20 µm in the Z axis. The right panel shows the effective image depth acquired over the course of a 20 ms camera exposure. c: Schematic diagram of the modified inverted LSM described in this paper.
Fig. 2
Fig. 2 Example Ca2+ events detected using fast volume-scanning LSM. Upper left panel: maximum intensity projection of a portion of the basal dendritic arbour of a pyramidal neuron in a rat hippocampal brain slice. The neuron was filled with Alexa Fluor 594 (AF594) and Ca2+-sensitive dye Oregon Green BAPTA-1 (OGB-1), and imaged with 594 nm illumination. The volume shown in this image has a depth of 160 µm. Lower left panel: average intensity projection of a fast volume scan acquired from the same neuron using 488 nm illumination. The volume scanned has a depth of ~20 µm. The volume was imaged for a duration of 10 sec, with the whole volume being scanned once every 20 ms (50 volumes/sec). Right panel: shows changes in OGB-1 fluorescence at various regions of interest (a-h) during a 3 sec period of the scan starting at the 2 sec time point (grey). Ca2+ transient events are clearly visible in some but not all of the traces, and have been fitted with a rise/decay function (orange; see Methods). Note that the first candidate event in trace (f) did not pass the criteria to be identified as an event (light orange; see Fig. 6).
Fig. 3
Fig. 3 Further example Ca2+ events detected using fast volume-scanning LSM. This figure shows other Ca2+ events taken from the same 10 sec fast volume scan that is shown in Fig. 2. Left panel: average intensity projection of a fast volume scan acquired using 488 nm illumination, showing a small segment of the dendritic arbour of the same pyramidal neuron depicted in Fig. 2, filled with OGB-1. The volume scanned was ~20 µm deep. Right hand panel: changes in OGB-1 fluorescence at various regions of interest (a-g), during the final 2 sec of the 10 sec scan (grey). Ca2+ transient events are clearly visible in some but not all of the traces, and have been fitted with a rise/decay function (orange; see Methods).
Fig. 4
Fig. 4 Example Ca2+ event detected using single-plane LSFM. Left panel: average intensity projection of a single-plane LSFM scan acquired from the same neuron as shown in Fig. 2 and Fig. 3 using 488 nm illumination. The image was acquired over 10 sec, with an exposure time of 20 ms (50 volumes/sec). Compare with Fig. 2 – here only short lengths of dendrite are in focus. Right panel: changes in OGB-1 fluorescence at various regions of interest (a-d) during a 2 sec period of the scan starting at the 1.5 sec time point (grey). A Ca2+ transient event is apparent in one of the traces, and has been fitted with a rise/decay function (orange; see Methods).
Fig. 5
Fig. 5 Our fast volume-scanning LSM is also capable of acquiring high resolution structural images. Upper left panel: maximum intensity projection of a portion of the basal dendritic arbour of the same hippocampal pyramidal neuron shown in Figs. 2-4. The neuron was filled with AF594 and imaged with 594 nm illumination and 200 ms exposure time. The image stack was built up of 320 image steps at intervals of 0.5 µm, hence the image has a depth in the Z axis of 160 µm. Panels a, b, c and d are details of various parts of this field of view, cropped from the same image stack. The 20 µm scale bar in panel a applies to all 4 of these panels. Panel a is a single image slice, panels b, c and d are maximum intensity projections of 4, 4, and 7 contiguous slices respectively.
Fig. 6
Fig. 6 Illustration of criteria used to identify Ca2+ events. The events shown in Fig. 2 and Fig. 3 are plotted again along with the preceding 1 second baseline period. The mean baseline is shown (orange) along with an estimate of noise (grey) calculated as ± root mean square (RMS) of the baseline signal. Candidate events were fitted with a rise/decay function (see Methods). Each candidate event was accepted (green) if its amplitude exceeded mean baseline + RMS. One example is shown of a candidate event which narrowly missed being identified as an event (red).
Fig. 7
Fig. 7 Sectioning properties of the LSM in the Z-axis. Maximum intensity projection of a region of interest of the same neuron shown in previous figures. The neuron was imaged by the LSM in single-plane mode with 594 nm illumination, 200 ms exposure, and 1 µm steps in the Z-axis between each image in the stack. The associated video steps through this image stack at 4 frames per second (see Visualization 1).

Tables (1)

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Table 1 Time constants of Ca2+ events detected with volume-scanning or single-plane LSFM are comparable.

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