Abstract

Understanding how neural circuits control behavior requires monitoring a large population of neurons with high spatial resolution and volume rate. Here we report an axicon-based Bessel beam module with continuously adjustable depth of focus (CADoF), that turns frame rate into volume rate by extending the excitation focus in the axial direction while maintaining high lateral resolutions. Cost-effective and compact, this CADoF Bessel module can be easily integrated into existing two-photon fluorescence microscopes. Simply translating one of the relay lenses along its optical axis enabled continuous adjustment of the axial length of the Bessel focus. We used this module to simultaneously monitor activity of spinal projection neurons extending over 60 µm depth in larval zebrafish at 50 Hz volume rate with adjustable axial extent of the imaged volume.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (1)

B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: Manipulating ultrafast spatiotemporal foci in space and time,” Light Sci. Appl. 7(1), 17117 (2018).
[Crossref]

2017 (2)

A. Song, A. S. Charles, S. A. Koay, J. L. Gauthier, S. Y. Thiberge, J. W. Pillow, and D. W. Tank, “Volumetric two-photon imaging of neurons using stereoscopy (vtwins),” Nat. Methods 14(4), 420–426 (2017).
[Crossref] [PubMed]

R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
[Crossref] [PubMed]

2016 (3)

M. Z. Lin and M. J. Schnitzer, “Genetically encoded indicators of neuronal activity,” Nat. Neurosci. 19(9), 1142–1153 (2016).
[Crossref] [PubMed]

N. Ji, J. Freeman, and S. L. Smith, “Technologies for imaging neural activity in large volumes,” Nat. Neurosci. 19(9), 1154–1164 (2016).
[Crossref] [PubMed]

N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, e14472 (2016).
[Crossref] [PubMed]

2015 (3)

L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
[Crossref] [PubMed]

J. T. Lock, I. Parker, and I. F. Smith, “A comparison of fluorescent Ca2+ indicators for imaging local Ca2+ signals in cultured cells,” Cell Calcium 58(6), 638–648 (2015).
[Crossref] [PubMed]

W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
[Crossref] [PubMed]

2014 (4)

K. E. Severi, R. Portugues, J. C. Marques, D. M. O’Malley, M. B. Orger, and F. Engert, “Neural control and modulation of swimming speed in the larval zebrafish,” Neuron 83(3), 692–707 (2014).
[Crossref] [PubMed]

M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

L. Gao, L. Shao, B. C. Chen, and E. Betzig, “3d live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy,” Nat. Protoc. 9(5), 1083–1101 (2014).
[Crossref] [PubMed]

G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: Steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
[PubMed]

2013 (2)

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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

G. Thériault, Y. De Koninck, and N. McCarthy, “Extended depth of field microscopy for rapid volumetric two-photon imaging,” Opt. Express 21(8), 10095–10104 (2013).
[Crossref] [PubMed]

2012 (2)

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at khz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (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]

2011 (1)

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

2009 (2)

C. Satou, Y. Kimura, T. Kohashi, K. Horikawa, H. Takeda, Y. Oda, and S. Higashijima, “Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish,” J. Neurosci. 29(21), 6780–6793 (2009).
[Crossref] [PubMed]

T. Cizmár and K. Dholakia, “Tunable bessel light modes: Engineering the axial propagation,” Opt. Express 17(18), 15558–15570 (2009).
[Crossref] [PubMed]

2008 (5)

O. Brzobohatý, T. Cizmár, and P. Zemánek, “High quality quasi-Bessel beam generated by round-tip axicon,” Opt. Express 16(17), 12688–12700 (2008).
[Crossref] [PubMed]

T. Kohashi and Y. Oda, “Initiation of mauthner- or non-mauthner-mediated fast escape evoked by different modes of sensory input,” J. Neurosci. 28(42), 10641–10653 (2008).
[Crossref] [PubMed]

J. N. D. Kerr and W. Denk, “Imaging in vivo: Watching the brain in action,” Nat. Rev. Neurosci. 9(3), 195–205 (2008).
[Crossref] [PubMed]

M. B. Orger, A. R. Kampff, K. E. Severi, J. H. Bollmann, and F. Engert, “Control of visually guided behavior by distinct populations of spinal projection neurons,” Nat. Neurosci. 11(3), 327–333 (2008).
[Crossref] [PubMed]

R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
[Crossref] [PubMed]

2007 (1)

2006 (2)

2002 (2)

E. Gahtan, N. Sankrithi, J. B. Campos, and D. M. O’Malley, “Evidence for a widespread brain stem escape network in larval zebrafish,” J. Neurophysiol. 87(1), 608–614 (2002).
[Crossref] [PubMed]

B. Depret, P. Verkerk, and D. Hennequin, “Characterization and modelling of the hollow beam produced by a real conical lens,” Opt. Commun. 211(1-6), 31–38 (2002).
[Crossref]

2001 (1)

E. Gahtan and D. M. O’Malley, “Rapid lesioning of large numbers of identified vertebrate neurons: Applications in zebrafish,” J. Neurosci. Methods 108(1), 97–110 (2001).
[Crossref] [PubMed]

1996 (1)

D. M. O’Malley, Y. H. Kao, and J. R. Fetcho, “Imaging the functional organization of zebrafish hindbrain segments during escape behaviors,” Neuron 17(6), 1145–1155 (1996).
[Crossref] [PubMed]

1992 (1)

1990 (2)

J. Nissanov, R. C. Eaton, and R. DiDomenico, “The motor output of the mauthner cell, a reticulospinal command neuron,” Brain Res. 517(1-2), 88–98 (1990).
[Crossref] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “2-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

1986 (2)

W. K. Metcalfe, B. Mendelson, and C. B. Kimmel, “Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva,” J. Comp. Neurol. 251(2), 147–159 (1986).
[Crossref] [PubMed]

B. Mendelson, “Development of reticulospinal neurons of the zebrafish. II. Early axonal outgrowth and cell body position,” J. Comp. Neurol. 251(2), 172–184 (1986).
[Crossref] [PubMed]

1977 (1)

S. J. Zottoli, “Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish,” J. Exp. Biol. 66(1), 243–254 (1977).
[PubMed]

1959 (1)

B. Richards and E. Wolf, “Electromagnetic diffraction in optical systems. Ii. Structure of the image field in an aplanatic system,” Proc. R. Soc. Lond. A Math. Phys. Sci. 253(1274), 358–379 (1959).
[Crossref]

1954 (1)

Arimoto, R.

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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Betzig, E.

L. Gao, L. Shao, B. C. Chen, and E. Betzig, “3d live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy,” Nat. Protoc. 9(5), 1083–1101 (2014).
[Crossref] [PubMed]

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

Bierfeld, J.

R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
[Crossref] [PubMed]

Bollmann, J. H.

M. B. Orger, A. R. Kampff, K. E. Severi, J. H. Bollmann, and F. Engert, “Control of visually guided behavior by distinct populations of spinal projection neurons,” Nat. Neurosci. 11(3), 327–333 (2008).
[Crossref] [PubMed]

Booth, M. J.

B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: Manipulating ultrafast spatiotemporal foci in space and time,” Light Sci. Appl. 7(1), 17117 (2018).
[Crossref]

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at khz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

E. J. Botcherby, R. Juskaitis, M. J. Booth, and T. Wilson, “Aberration-free optical refocusing in high numerical aperture microscopy,” Opt. Lett. 32(14), 2007–2009 (2007).
[Crossref] [PubMed]

Botcherby, E. J.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at khz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

E. J. Botcherby, R. Juskaitis, M. J. Booth, and T. Wilson, “Aberration-free optical refocusing in high numerical aperture microscopy,” Opt. Lett. 32(14), 2007–2009 (2007).
[Crossref] [PubMed]

Bourque, C.

R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
[Crossref] [PubMed]

Bowman, T.

R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
[Crossref] [PubMed]

Brzobohatý, O.

Burke, C.

R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
[Crossref] [PubMed]

Burns, C. E.

R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
[Crossref] [PubMed]

Campos, J. B.

E. Gahtan, N. Sankrithi, J. B. Campos, and D. M. O’Malley, “Evidence for a widespread brain stem escape network in larval zebrafish,” J. Neurophysiol. 87(1), 608–614 (2002).
[Crossref] [PubMed]

Castonguay, A.

G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: Steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
[PubMed]

Ceol, C.

R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
[Crossref] [PubMed]

Charles, A. S.

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DiDomenico, R.

J. Nissanov, R. C. Eaton, and R. DiDomenico, “The motor output of the mauthner cell, a reticulospinal command neuron,” Brain Res. 517(1-2), 88–98 (1990).
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L. Gao, L. Shao, B. C. Chen, and E. Betzig, “3d live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy,” Nat. Protoc. 9(5), 1083–1101 (2014).
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L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
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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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: Manipulating ultrafast spatiotemporal foci in space and time,” Light Sci. Appl. 7(1), 17117 (2018).
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N. Ji, J. Freeman, and S. L. Smith, “Technologies for imaging neural activity in large volumes,” Nat. Neurosci. 19(9), 1154–1164 (2016).
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W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
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Juškaitis, R.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at khz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
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M. B. Orger, A. R. Kampff, K. E. Severi, J. H. Bollmann, and F. Engert, “Control of visually guided behavior by distinct populations of spinal projection neurons,” Nat. Neurosci. 11(3), 327–333 (2008).
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M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
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Kao, Y. H.

D. M. O’Malley, Y. H. Kao, and J. R. Fetcho, “Imaging the functional organization of zebrafish hindbrain segments during escape behaviors,” Neuron 17(6), 1145–1155 (1996).
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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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Kerlin, A.

R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
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J. N. D. Kerr and W. Denk, “Imaging in vivo: Watching the brain in action,” Nat. Rev. Neurosci. 9(3), 195–205 (2008).
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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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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W. K. Metcalfe, B. Mendelson, and C. B. Kimmel, “Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva,” J. Comp. Neurol. 251(2), 147–159 (1986).
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C. Satou, Y. Kimura, T. Kohashi, K. Horikawa, H. Takeda, Y. Oda, and S. Higashijima, “Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish,” J. Neurosci. 29(21), 6780–6793 (2009).
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N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, e14472 (2016).
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M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
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A. Song, A. S. Charles, S. A. Koay, J. L. Gauthier, S. Y. Thiberge, J. W. Pillow, and D. W. Tank, “Volumetric two-photon imaging of neurons using stereoscopy (vtwins),” Nat. Methods 14(4), 420–426 (2017).
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C. Satou, Y. Kimura, T. Kohashi, K. Horikawa, H. Takeda, Y. Oda, and S. Higashijima, “Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish,” J. Neurosci. 29(21), 6780–6793 (2009).
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T. Kohashi and Y. Oda, “Initiation of mauthner- or non-mauthner-mediated fast escape evoked by different modes of sensory input,” J. Neurosci. 28(42), 10641–10653 (2008).
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E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at khz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
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L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
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R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
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L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
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R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
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R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
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L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
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M. Z. Lin and M. J. Schnitzer, “Genetically encoded indicators of neuronal activity,” Nat. Neurosci. 19(9), 1142–1153 (2016).
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L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
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J. T. Lock, I. Parker, and I. F. Smith, “A comparison of fluorescent Ca2+ indicators for imaging local Ca2+ signals in cultured cells,” Cell Calcium 58(6), 638–648 (2015).
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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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
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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).
[Crossref] [PubMed]

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K. E. Severi, R. Portugues, J. C. Marques, D. M. O’Malley, M. B. Orger, and F. Engert, “Neural control and modulation of swimming speed in the larval zebrafish,” Neuron 83(3), 692–707 (2014).
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McCarthy, N.

Mcleod, J. H.

Mendelson, B.

W. K. Metcalfe, B. Mendelson, and C. B. Kimmel, “Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva,” J. Comp. Neurol. 251(2), 147–159 (1986).
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B. Mendelson, “Development of reticulospinal neurons of the zebrafish. II. Early axonal outgrowth and cell body position,” J. Comp. Neurol. 251(2), 172–184 (1986).
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W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
[Crossref] [PubMed]

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W. K. Metcalfe, B. Mendelson, and C. B. Kimmel, “Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva,” J. Comp. Neurol. 251(2), 147–159 (1986).
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T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

Mohar, B.

R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
[Crossref] [PubMed]

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J. Nissanov, R. C. Eaton, and R. DiDomenico, “The motor output of the mauthner cell, a reticulospinal command neuron,” Brain Res. 517(1-2), 88–98 (1990).
[Crossref] [PubMed]

O’Malley, D. M.

K. E. Severi, R. Portugues, J. C. Marques, D. M. O’Malley, M. B. Orger, and F. Engert, “Neural control and modulation of swimming speed in the larval zebrafish,” Neuron 83(3), 692–707 (2014).
[Crossref] [PubMed]

E. Gahtan, N. Sankrithi, J. B. Campos, and D. M. O’Malley, “Evidence for a widespread brain stem escape network in larval zebrafish,” J. Neurophysiol. 87(1), 608–614 (2002).
[Crossref] [PubMed]

E. Gahtan and D. M. O’Malley, “Rapid lesioning of large numbers of identified vertebrate neurons: Applications in zebrafish,” J. Neurosci. Methods 108(1), 97–110 (2001).
[Crossref] [PubMed]

D. M. O’Malley, Y. H. Kao, and J. R. Fetcho, “Imaging the functional organization of zebrafish hindbrain segments during escape behaviors,” Neuron 17(6), 1145–1155 (1996).
[Crossref] [PubMed]

Oda, Y.

C. Satou, Y. Kimura, T. Kohashi, K. Horikawa, H. Takeda, Y. Oda, and S. Higashijima, “Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish,” J. Neurosci. 29(21), 6780–6793 (2009).
[Crossref] [PubMed]

T. Kohashi and Y. Oda, “Initiation of mauthner- or non-mauthner-mediated fast escape evoked by different modes of sensory input,” J. Neurosci. 28(42), 10641–10653 (2008).
[Crossref] [PubMed]

Orger, M. B.

R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
[Crossref] [PubMed]

K. E. Severi, R. Portugues, J. C. Marques, D. M. O’Malley, M. B. Orger, and F. Engert, “Neural control and modulation of swimming speed in the larval zebrafish,” Neuron 83(3), 692–707 (2014).
[Crossref] [PubMed]

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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

M. B. Orger, A. R. Kampff, K. E. Severi, J. H. Bollmann, and F. Engert, “Control of visually guided behavior by distinct populations of spinal projection neurons,” Nat. Neurosci. 11(3), 327–333 (2008).
[Crossref] [PubMed]

Parker, I.

J. T. Lock, I. Parker, and I. F. Smith, “A comparison of fluorescent Ca2+ indicators for imaging local Ca2+ signals in cultured cells,” Cell Calcium 58(6), 638–648 (2015).
[Crossref] [PubMed]

Paulsen, O.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at khz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Piché, M.

Pillow, J. W.

A. Song, A. S. Charles, S. A. Koay, J. L. Gauthier, S. Y. Thiberge, J. W. Pillow, and D. W. Tank, “Volumetric two-photon imaging of neurons using stereoscopy (vtwins),” Nat. Methods 14(4), 420–426 (2017).
[Crossref] [PubMed]

Planchon, T. A.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

Portugues, R.

K. E. Severi, R. Portugues, J. C. Marques, D. M. O’Malley, M. B. Orger, and F. Engert, “Neural control and modulation of swimming speed in the larval zebrafish,” Neuron 83(3), 692–707 (2014).
[Crossref] [PubMed]

Pulver, S. R.

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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Renninger, S. L.

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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Richards, B.

B. Richards and E. Wolf, “Electromagnetic diffraction in optical systems. Ii. Structure of the image field in an aplanatic system,” Proc. R. Soc. Lond. A Math. Phys. Sci. 253(1274), 358–379 (1959).
[Crossref]

Roider, C.

B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: Manipulating ultrafast spatiotemporal foci in space and time,” Light Sci. Appl. 7(1), 17117 (2018).
[Crossref]

Roska, B.

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]

Rózsa, B.

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]

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Salter, P. S.

B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: Manipulating ultrafast spatiotemporal foci in space and time,” Light Sci. Appl. 7(1), 17117 (2018).
[Crossref]

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E. Gahtan, N. Sankrithi, J. B. Campos, and D. M. O’Malley, “Evidence for a widespread brain stem escape network in larval zebrafish,” J. Neurophysiol. 87(1), 608–614 (2002).
[Crossref] [PubMed]

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C. Satou, Y. Kimura, T. Kohashi, K. Horikawa, H. Takeda, Y. Oda, and S. Higashijima, “Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish,” J. Neurosci. 29(21), 6780–6793 (2009).
[Crossref] [PubMed]

Schmidt, M.

B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: Manipulating ultrafast spatiotemporal foci in space and time,” Light Sci. Appl. 7(1), 17117 (2018).
[Crossref]

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M. Z. Lin and M. J. Schnitzer, “Genetically encoded indicators of neuronal activity,” Nat. Neurosci. 19(9), 1142–1153 (2016).
[Crossref] [PubMed]

Scholl, B.

R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
[Crossref] [PubMed]

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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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

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R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
[Crossref] [PubMed]

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R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
[Crossref] [PubMed]

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K. E. Severi, R. Portugues, J. C. Marques, D. M. O’Malley, M. B. Orger, and F. Engert, “Neural control and modulation of swimming speed in the larval zebrafish,” Neuron 83(3), 692–707 (2014).
[Crossref] [PubMed]

M. B. Orger, A. R. Kampff, K. E. Severi, J. H. Bollmann, and F. Engert, “Control of visually guided behavior by distinct populations of spinal projection neurons,” Nat. Neurosci. 11(3), 327–333 (2008).
[Crossref] [PubMed]

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L. Gao, L. Shao, B. C. Chen, and E. Betzig, “3d live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy,” Nat. Protoc. 9(5), 1083–1101 (2014).
[Crossref] [PubMed]

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E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at khz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Smith, I. F.

J. T. Lock, I. Parker, and I. F. Smith, “A comparison of fluorescent Ca2+ indicators for imaging local Ca2+ signals in cultured cells,” Cell Calcium 58(6), 638–648 (2015).
[Crossref] [PubMed]

Smith, S. L.

N. Ji, J. Freeman, and S. L. Smith, “Technologies for imaging neural activity in large volumes,” Nat. Neurosci. 19(9), 1154–1164 (2016).
[Crossref] [PubMed]

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N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, e14472 (2016).
[Crossref] [PubMed]

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A. Song, A. S. Charles, S. A. Koay, J. L. Gauthier, S. Y. Thiberge, J. W. Pillow, and D. W. Tank, “Volumetric two-photon imaging of neurons using stereoscopy (vtwins),” Nat. Methods 14(4), 420–426 (2017).
[Crossref] [PubMed]

Strauss, J.

B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: Manipulating ultrafast spatiotemporal foci in space and time,” Light Sci. Appl. 7(1), 17117 (2018).
[Crossref]

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W. Denk, J. H. Strickler, and W. W. Webb, “2-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
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B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: Manipulating ultrafast spatiotemporal foci in space and time,” Light Sci. Appl. 7(1), 17117 (2018).
[Crossref]

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R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
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W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
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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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

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N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, e14472 (2016).
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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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
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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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M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
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C. Satou, Y. Kimura, T. Kohashi, K. Horikawa, H. Takeda, Y. Oda, and S. Higashijima, “Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish,” J. Neurosci. 29(21), 6780–6793 (2009).
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M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
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W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
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Tang, J.

L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
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R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
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A. Song, A. S. Charles, S. A. Koay, J. L. Gauthier, S. Y. Thiberge, J. W. Pillow, and D. W. Tank, “Volumetric two-photon imaging of neurons using stereoscopy (vtwins),” Nat. Methods 14(4), 420–426 (2017).
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G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: Steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
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A. Song, A. S. Charles, S. A. Koay, J. L. Gauthier, S. Y. Thiberge, J. W. Pillow, and D. W. Tank, “Volumetric two-photon imaging of neurons using stereoscopy (vtwins),” Nat. Methods 14(4), 420–426 (2017).
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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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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, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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W. Denk, J. H. Strickler, and W. W. Webb, “2-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
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R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
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R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
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E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at khz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
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K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
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L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
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R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
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J. T. Lock, I. Parker, and I. F. Smith, “A comparison of fluorescent Ca2+ indicators for imaging local Ca2+ signals in cultured cells,” Cell Calcium 58(6), 638–648 (2015).
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Cell Stem Cell (1)

R. M. White, A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C. E. Burns, and L. I. Zon, “Transparent adult zebrafish as a tool for in vivo transplantation analysis,” Cell Stem Cell 2(2), 183–189 (2008).
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N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, e14472 (2016).
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M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

Front. Cell. Neurosci. (1)

G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: Steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
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E. Gahtan, N. Sankrithi, J. B. Campos, and D. M. O’Malley, “Evidence for a widespread brain stem escape network in larval zebrafish,” J. Neurophysiol. 87(1), 608–614 (2002).
[Crossref] [PubMed]

J. Neurosci. (2)

C. Satou, Y. Kimura, T. Kohashi, K. Horikawa, H. Takeda, Y. Oda, and S. Higashijima, “Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish,” J. Neurosci. 29(21), 6780–6793 (2009).
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B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: Manipulating ultrafast spatiotemporal foci in space and time,” Light Sci. Appl. 7(1), 17117 (2018).
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Nat. Methods (4)

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]

L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
[Crossref] [PubMed]

A. Song, A. S. Charles, S. A. Koay, J. L. Gauthier, S. Y. Thiberge, J. W. Pillow, and D. W. Tank, “Volumetric two-photon imaging of neurons using stereoscopy (vtwins),” Nat. Methods 14(4), 420–426 (2017).
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T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
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Nat. Neurosci. (5)

M. Z. Lin and M. J. Schnitzer, “Genetically encoded indicators of neuronal activity,” Nat. Neurosci. 19(9), 1142–1153 (2016).
[Crossref] [PubMed]

M. B. Orger, A. R. Kampff, K. E. Severi, J. H. Bollmann, and F. Engert, “Control of visually guided behavior by distinct populations of spinal projection neurons,” Nat. Neurosci. 11(3), 327–333 (2008).
[Crossref] [PubMed]

R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
[Crossref] [PubMed]

N. Ji, J. Freeman, and S. L. Smith, “Technologies for imaging neural activity in large volumes,” Nat. Neurosci. 19(9), 1154–1164 (2016).
[Crossref] [PubMed]

W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
[Crossref] [PubMed]

Nat. Protoc. (1)

L. Gao, L. Shao, B. C. Chen, and E. Betzig, “3d live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy,” Nat. Protoc. 9(5), 1083–1101 (2014).
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Supplementary Material (5)

NameDescription
» Code 1       Supplementary Codes contain four codes: PSFofBesselBeam_Axicon.m, maskDesign.m, demo1.m, and demo2.m. The code “maskDesign.m” generates four masks with the inner and the outer diameters located at 1/e, 1/(5e), 1/(10e) and 1/(15e) of the peak amplitu
» Visualization 1       Simulation of PSF as a function of displacement of lens L2. Displacing Lens L2 (e.g., changing relative displacement D from – 20 mm to 20 mm) alters the amplitude and phase distribution on the back focal plane of the objective, axial, and lateral PSF
» Visualization 2       Functional movies with variable depth of focus. An acoustomechanical stimulus was delivered at 0 s. The Gaussian focus had 2.6 um axial FWHM. The short (displacement of lens L2 D = 12 mm), medium (D = 0 mm) and long Bessel (D = -12 mm) foci has 14 um
» Visualization 3       Gaussian 3D stack for data in Figure 5 scanning from 100 um to 166 um below the dorsal surface (relative depth z = 0 ~ 66 um). The field of view was 366 um × 214 um.
» Visualization 4       Phase pattern on pupil plane is critical to extend the focus. All parameters were the same as in Visualization 1, except that the phase on the back pupil plane (at the bottom-left panel) was forced to be constant here.

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Figures (5)

Fig. 1
Fig. 1 Design and characterization of the axicon-based CADoF Bessel module. (a) Optical schematics of the Bessel module incorporating an axicon. Two translating mirrors (TM1 and TM2) switch between the Gaussian and Bessel imaging modalities. D is defined as 0 mm when the mask is at the front focal plane of L2, and positive when L2 moves away from the mask. (b) Experimental axial PSFs with D = −12 mm, 0 mm, and 12 mm, respectively. Varying D leads to variable (c) lateral FWHM, (d) axial FWHM, (e) peak signal of PSF, and (f) post-objective power. Data in (c-e) were collected from nine 0.2-μm-diameter beads, and data in (f) are averages of four measurements. Lateral FWHMs in (c) were measured at the peak axial locations. Error bars represent standard deviations. Simulation data in (c) and (d) were linearly fitted (R2> 0.995). Excitation light was linearly polarized along x axis for simulation. Focal lengths of L1 to L5: 80 mm, 150 mm, 200 mm, 35.2 mm, and 200 mm, respectively. The apex angle of the axicon was 178°. The 1/e2 diameter of the beam at the axicon was 2.8 mm. Objective: Leica, 0.95 NA, 25X; wavelength: 940 nm. The annular aperture mask had an outer diameter of 1.312 mm and an inner diameter of 1.208 mm.
Fig. 2
Fig. 2 Engineering Bessel foci by displacing Lens L2. (a) 2D and (b) 1D (along x direction) representations of the amplitude and phase of the pupil function at the objective back focal plane, (c) axial and (d) lateral two-photon excitation PSFs for D = −20 mm, 0 mm, and 20 mm, respectively. Same parameters as described in the caption of Fig. 1. (See Visualization 1 for pupil function and PSF during continuously displacing Lens L2 from – 20 mm to 20 mm.)
Fig. 3
Fig. 3 Annular aperture masks alter the axial profile of the Bessel focus. (a-d) the axial PSFs measured without mask (red line), with Mask 1 (blue line), with Mask 2 (black line), together with the simulated PSF (dashed line) for Axicons 1-4, respectively. All axicons have the same apex angle (178°). Axicons 1 and 2: 1-APX-2-H254-P, ALTECHNA; Axicon 3: XFL25-010-U-B, ASPHERICON. Outer diameter: 1.429 mm, inner diameter: 1.091 mm for Mask 1; Outer diameter: 1.312 mm, inner diameter: 1.208 mm for Mask 2. Theoretical transmission ratio through Mask 1 and Mask 2 for perfect axicons: 99% and 90%, respectively.
Fig. 4
Fig. 4 Scanning Bessel foci with variable axial lengths probes varying volumes of spinal projection neurons in vivo. Reticulospinal and vestibulospinal neurons labeled with Alexa Fluor 488 in a larval zebrafish were imaged by scanning either (a,b) Gaussian or (c-j) Bessel foci. Left panels: neuron images; Right panels: axial profiles of 2-μm-diameter beads. (a) An image acquired using Gaussian focus at the relative depth of 18 μm (114 μm from the surface) contains 38 neurons. (b) Mean intensity projection over 74 μm axial range (absolute depth from 96 μm to 170 μm), color-coded by relative depths. (c-j) Volumetric images acquired by scanning Bessel foci with different axial lengths. Longer foci revealed more structures, e.g., (c) 65 neurons; (g): 87 neurons and (j): 108 neurons. Arrowheads (same color code as in b) in each image point to example new structures (neurons or axons) compared to the previous image. Axicon 1 and Mask 1 were employed here.
Fig. 5
Fig. 5 50 Hz volumetric functional calcium imaging of volumes of spinal projection neurons in zebrafish larvae. (a) Image acquired by Gaussian focus scanning at 127 μm from the dorsal surface of the head (relative depth z = 17 μm). (b) Averaged calcium transients of neurons evoked by the acoustomechanical tapping stimuli. (c), (e), and (g) were volumetric images obtained by scanning a short (14 μm axial FWHM), medium (24 μm axial FWHM), and long (39 μm axial FWHM) Bessel foci, respectively. (d), (f), and (h) were averaged calcium transients of responsive neurons. An acoustomechanical stimulus was delivered at 0 s. The Gaussian focus had 2.6 μm axial FWHM. The short (displacement of lens L2 D = 12 mm), medium (D = 0 mm) and long Bessel (D = −12 mm) foci has 14 μm, 24 μm and 39 μm axial FWHMs. The field of view was 366 μm × 214 μm. (See Visualization 2 for the functional movies.) (i) and (j) Mean intensity projections of a 66-μm-thick image stack acquired by Gaussian focus scanning (see Visualization 3 for the Gaussian 3D stack). Color in (i) encodes relative depth. Eleven trials were averaged in (b), (d), (f), and (h). Shadow represents standard deviations. Post-objective power: (a) 38 mW, (c) 97 mW, (e) 110 mW and (g) 132 mW.

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