Abstract

Two-photon excitation fluorescence microscopy is widely used to study the activity of neuronal circuits. However, the fast imaging is typically constrained to a single lateral plane for a standard microscope design. Given that cortical neuronal networks in a mouse brain are complex three-dimensional structures organised in six histologically defined layers which extend over many hundreds of micrometres, there is a strong demand for microscope systems that can record neuronal signalling in volumes. Henceforth, we developed a quasi-simultaneous multiplane imaging technique combining an acousto-optic deflector and static remote focusing to provide fast imaging of neurons from different axial positions inside the cortical layers without the need for mechanical disturbance of either the objective lens or the specimen. The hardware and the software are easily adaptable to existing two-photon microscopes. Here, we demonstrated that our imaging method can record, at high speed and high image contrast, the calcium dynamics of neurons in two different imaging planes separated axially with the in-focus and the refocused planes 120 µm and 250 µm below the brain surface respectively.

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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2018 (1)

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref] [PubMed]

2017 (3)

2016 (2)

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

M. Pachitariu, C. Stringer, S. Schröder, M. Dipoppa, L. F. Rossi, M. Carandini, and K. D. Harris, “Suite2p: beyond 10,000 neurons with standard two-photon microscopy,” bioRxiv 2016, 061507 (2016).

2015 (2)

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

2014 (4)

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[Crossref] [PubMed]

J. M. Jabbour, B. H. Malik, C. Olsovsky, R. Cuenca, S. Cheng, J. A. Jo, Y. S. L. Cheng, J. M. Wright, and K. C. Maitland, “Optical axial scanning in confocal microscopy using an electrically tunable lens,” Biomed. Opt. Express 5(2), 645–652 (2014).
[Crossref] [PubMed]

Y. Qi, M. Lei, Y. Yang, B. Yao, D. Dan, X. Yu, S. Yan, and T. Ye, “Remote-focusing microscopy with long working distance objective lenses,” Appl. Opt. 53(16), 3473–3478 (2014).
[Crossref] [PubMed]

E. Chong, T. Watson, and F. Festy, “Autocorrelation measurement of femtosecond laser pulses based on two-photon absorption in GaP photodiode,” Appl. Phys. Lett. 105(6), 062111 (2014).
[Crossref]

2013 (1)

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]

2012 (2)

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
[Crossref] [PubMed]

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]

2011 (3)

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]

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[Crossref] [PubMed]

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

2010 (2)

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

E. E. Hoover, M. D. Young, E. V. Chandler, A. Luo, J. J. Field, K. E. Sheetz, A. W. Sylvester, and J. A. Squier, “Remote focusing for programmable multi-layer differential multiphoton microscopy,” Biomed. Opt. Express 2(1), 113–122 (2010).
[Crossref] [PubMed]

2008 (4)

R. Carriles, K. E. Sheetz, E. E. Hoover, J. A. Squier, and V. Barzda, “Simultaneous multifocal, multiphoton, photon counting microscopy,” Opt. Express 16(14), 10364–10371 (2008).
[Crossref] [PubMed]

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

E. J. Botcherby, R. Juškaitis, M. J. Booth, and T. Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281(4), 880–887 (2008).
[Crossref]

Y. Kremer, J.-F. Léger, R. Lapole, N. Honnorat, Y. Candela, S. Dieudonné, and L. Bourdieu, “A spatio-temporally compensated acousto-optic scanner for two-photon microscopy providing large field of view,” Opt. Express 16(14), 10066–10076 (2008).
[Crossref] [PubMed]

2007 (3)

2006 (4)

V. Iyer, T. M. Hoogland, and P. Saggau, “Fast functional imaging of single neurons using random-access multiphoton (RAMP) microscopy,” J. Neurophysiol. 95(1), 535–545 (2006).
[Crossref] [PubMed]

K. Bi, S. Zeng, S. Xue, J. Sun, X. Lv, D. Li, and Q. Luo, “Position of the prism in a dispersion-compensated acousto-optic deflector for multiphoton imaging,” Appl. Opt. 45(33), 8560–8565 (2006).
[Crossref] [PubMed]

S. Zeng, X. Lv, C. Zhan, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Simultaneous compensation for spatial and temporal dispersion of acousto-optical deflectors for two-dimensional scanning with a single prism,” Opt. Lett. 31(8), 1091–1093 (2006).
[Crossref] [PubMed]

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

2003 (1)

V. Iyer, B. E. Losavio, and P. Saggau, “Compensation of spatial and temporal dispersion for acousto-optic multiphoton laser-scanning microscopy,” J. Biomed. Opt. 8(3), 460–471 (2003).
[Crossref] [PubMed]

1996 (1)

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

1988 (1)

1967 (1)

R. Dixon, “Acoustic diffraction of light in anisotropic media,” IEEE J. Quantum Electron. 3(2), 85–93 (1967).
[Crossref]

Amir, W.

Anderson, D. J.

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

Annecchino, L. A.

R. Schuck, P. Quicke, C. Copeland, S. Garasto, L. A. Annecchino, J. K. Hwang, and S. Schultz, “Rapid three dimensional two photon neural population scanning,” in Proceedings of the 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (IEEE, 2015), pp. 5867–5870.
[Crossref]

Anselmi, F.

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

Arisaka, K.

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[Crossref] [PubMed]

Bando, Y.

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref] [PubMed]

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]

Barnstedt, O.

Barzda, V.

Bègue, A.

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

Betzig, E.

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
[Crossref] [PubMed]

Bi, K.

S. Zeng, X. Lv, K. Bi, C. Zhan, D. Li, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Analysis of the dispersion compensation of acousto-optic deflectors used for multiphoton imaging,” J. Biomed. Opt. 12(2), 024015 (2007).
[Crossref] [PubMed]

K. Bi, S. Zeng, S. Xue, J. Sun, X. Lv, D. Li, and Q. Luo, “Position of the prism in a dispersion-compensated acousto-optic deflector for multiphoton imaging,” Appl. Opt. 45(33), 8560–8565 (2006).
[Crossref] [PubMed]

Boilot, V.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Booth, M. J.

M. Žurauskas, O. Barnstedt, M. Frade-Rodriguez, S. Waddell, and M. J. Booth, “Rapid adaptive remote focusing microscope for sensing of volumetric neural activity,” Biomed. Opt. Express 8(10), 4369–4379 (2017).
[Crossref] [PubMed]

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. Juškaitis, M. J. Booth, and T. Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281(4), 880–887 (2008).
[Crossref]

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. Juškaitis, M. J. Booth, and T. Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281(4), 880–887 (2008).
[Crossref]

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]

Bourdieu, L.

Y. Kremer, J.-F. Léger, R. Lapole, N. Honnorat, Y. Candela, S. Dieudonné, and L. Bourdieu, “A spatio-temporally compensated acousto-optic scanner for two-photon microscopy providing large field of view,” Opt. Express 16(14), 10066–10076 (2008).
[Crossref] [PubMed]

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

Candela, Y.

Carandini, M.

M. Pachitariu, C. Stringer, S. Schröder, M. Dipoppa, L. F. Rossi, M. Carandini, and K. D. Harris, “Suite2p: beyond 10,000 neurons with standard two-photon microscopy,” bioRxiv 2016, 061507 (2016).

Carriles, R.

Carrillo-Reid, L.

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
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W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Chandler, E. V.

Chatenay, D.

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

Chen, D. F.

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

Chen, T. W.

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]

Chen, W. R.

S. Zeng, X. Lv, K. Bi, C. Zhan, D. Li, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Analysis of the dispersion compensation of acousto-optic deflectors used for multiphoton imaging,” J. Biomed. Opt. 12(2), 024015 (2007).
[Crossref] [PubMed]

S. Zeng, X. Lv, C. Zhan, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Simultaneous compensation for spatial and temporal dispersion of acousto-optical deflectors for two-dimensional scanning with a single prism,” Opt. Lett. 31(8), 1091–1093 (2006).
[Crossref] [PubMed]

Cheng, A.

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[Crossref] [PubMed]

Cheng, S.

Cheng, Y. S. L.

Chong, E.

E. Chong, T. Watson, and F. Festy, “Autocorrelation measurement of femtosecond laser pulses based on two-photon absorption in GaP photodiode,” Appl. Phys. Lett. 105(6), 062111 (2014).
[Crossref]

Chuong, A. S.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Clark, J.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
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Copeland, C.

R. Schuck, P. Quicke, C. Copeland, S. Garasto, L. A. Annecchino, J. K. Hwang, and S. Schultz, “Rapid three dimensional two photon neural population scanning,” in Proceedings of the 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (IEEE, 2015), pp. 5867–5870.
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Cuenca, R.

Dan, D.

Débarre, D.

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]

Dieudonné, S.

Y. Kremer, J.-F. Léger, R. Lapole, N. Honnorat, Y. Candela, S. Dieudonné, and L. Bourdieu, “A spatio-temporally compensated acousto-optic scanner for two-photon microscopy providing large field of view,” Opt. Express 16(14), 10066–10076 (2008).
[Crossref] [PubMed]

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

Dipoppa, M.

M. Pachitariu, C. Stringer, S. Schröder, M. Dipoppa, L. F. Rossi, M. Carandini, and K. D. Harris, “Suite2p: beyond 10,000 neurons with standard two-photon microscopy,” bioRxiv 2016, 061507 (2016).

Dixon, R.

R. Dixon, “Acoustic diffraction of light in anisotropic media,” IEEE J. Quantum Electron. 3(2), 85–93 (1967).
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Draviam, V. M.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
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Duemani Reddy, G.

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

Egolf, L.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Emiliani, V.

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

Festy, F.

E. Chong, T. Watson, and F. Festy, “Autocorrelation measurement of femtosecond laser pulses based on two-photon absorption in GaP photodiode,” Appl. Phys. Lett. 105(6), 062111 (2014).
[Crossref]

Field, J. J.

Fink, R.

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

Funahashi, A.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Garasto, S.

R. Schuck, P. Quicke, C. Copeland, S. Garasto, L. A. Annecchino, J. K. Hwang, and S. Schultz, “Rapid three dimensional two photon neural population scanning,” in Proceedings of the 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (IEEE, 2015), pp. 5867–5870.
[Crossref]

Garner, A. R.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Gengyo-Ando, K.

Gerber, D.

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

Golshani, P.

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[Crossref] [PubMed]

Gonçalves, J. T.

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
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Grewe, B. F.

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

Harris, K. D.

M. Pachitariu, C. Stringer, S. Schröder, M. Dipoppa, L. F. Rossi, M. Carandini, and K. D. Harris, “Suite2p: beyond 10,000 neurons with standard two-photon microscopy,” bioRxiv 2016, 061507 (2016).

Helmchen, F.

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

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Hiroi, N.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
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Honnorat, N.

Hoogland, T. M.

V. Iyer, T. M. Hoogland, and P. Saggau, “Fast functional imaging of single neurons using random-access multiphoton (RAMP) microscopy,” J. Neurophysiol. 95(1), 535–545 (2006).
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Hoover, E. E.

Hwang, J. K.

R. Schuck, P. Quicke, C. Copeland, S. Garasto, L. A. Annecchino, J. K. Hwang, and S. Schultz, “Rapid three dimensional two photon neural population scanning,” in Proceedings of the 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (IEEE, 2015), pp. 5867–5870.
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Iyer, V.

V. Iyer, T. M. Hoogland, and P. Saggau, “Fast functional imaging of single neurons using random-access multiphoton (RAMP) microscopy,” J. Neurophysiol. 95(1), 535–545 (2006).
[Crossref] [PubMed]

V. Iyer, B. E. Losavio, and P. Saggau, “Compensation of spatial and temporal dispersion for acousto-optic multiphoton laser-scanning microscopy,” J. Biomed. Opt. 8(3), 460–471 (2003).
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Jabbour, J. M.

Jackson, J.

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
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Jacques, S. L.

S. Zeng, X. Lv, K. Bi, C. Zhan, D. Li, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Analysis of the dispersion compensation of acousto-optic deflectors used for multiphoton imaging,” J. Biomed. Opt. 12(2), 024015 (2007).
[Crossref] [PubMed]

S. Zeng, X. Lv, C. Zhan, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Simultaneous compensation for spatial and temporal dispersion of acousto-optical deflectors for two-dimensional scanning with a single prism,” Opt. Lett. 31(8), 1091–1093 (2006).
[Crossref] [PubMed]

Jayaraman, V.

T. W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, 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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Ji, N.

N. Ji, “Adaptive optical fluorescence microscopy,” Nat. Methods 14(4), 374–380 (2017).
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N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
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Jo, J. A.

Juskaitis, R.

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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E. J. Botcherby, R. Juškaitis, M. J. Booth, and T. Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281(4), 880–887 (2008).
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Kampa, B. M.

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

Kandel, E. R.

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

Kasper, H.

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

Kelleher, K.

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

Kerr, R. A.

T. W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, 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]

Kim, D. S.

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]

Klapoetke, N. C.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Kohl, M. M.

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]

Kremer, Y.

Y. Kremer, J.-F. Léger, R. Lapole, N. Honnorat, Y. Candela, S. Dieudonné, and L. Bourdieu, “A spatio-temporally compensated acousto-optic scanner for two-photon microscopy providing large field of view,” Opt. Express 16(14), 10066–10076 (2008).
[Crossref] [PubMed]

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

Krichevsky, O.

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

Kubota, H.

Langer, D.

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

Lapole, R.

Léger, J. F.

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

Léger, J.-F.

Lei, M.

Li, D.

S. Zeng, X. Lv, K. Bi, C. Zhan, D. Li, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Analysis of the dispersion compensation of acousto-optic deflectors used for multiphoton imaging,” J. Biomed. Opt. 12(2), 024015 (2007).
[Crossref] [PubMed]

K. Bi, S. Zeng, S. Xue, J. Sun, X. Lv, D. Li, and Q. Luo, “Position of the prism in a dispersion-compensated acousto-optic deflector for multiphoton imaging,” Appl. Opt. 45(33), 8560–8565 (2006).
[Crossref] [PubMed]

Li, L.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Looger, L. 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]

Losavio, B. E.

V. Iyer, B. E. Losavio, and P. Saggau, “Compensation of spatial and temporal dispersion for acousto-optic multiphoton laser-scanning microscopy,” J. Biomed. Opt. 8(3), 460–471 (2003).
[Crossref] [PubMed]

Luo, A.

Luo, Q.

Lv, X.

Madisen, L.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Maitland, K. C.

Malik, B. H.

Mayford, M.

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

Mercer, E. H.

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

Miller, J. E.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Monetti, C.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Motegi, Y.

Nakai, J.

Nakai, Y.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Nakashima, T.

Nakazawa, M.

Niino, Y.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Nonaka, S.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Ogden, D.

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

Ohkura, M.

Oku, H.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Olsovsky, C.

Orger, M. B.

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]

Ozeki, M.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Pachitariu, M.

M. Pachitariu, C. Stringer, S. Schröder, M. Dipoppa, L. F. Rossi, M. Carandini, and K. D. Harris, “Suite2p: beyond 10,000 neurons with standard two-photon microscopy,” bioRxiv 2016, 061507 (2016).

Paninski, L.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[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]

Peterka, D. S.

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref] [PubMed]

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[Crossref] [PubMed]

Planchon, T. A.

Pnevmatikakis, E.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Portera-Cailliau, C.

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[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]

Qi, Y.

Quicke, P.

R. Schuck, P. Quicke, C. Copeland, S. Garasto, L. A. Annecchino, J. K. Hwang, and S. Schultz, “Rapid three dimensional two photon neural population scanning,” in Proceedings of the 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (IEEE, 2015), pp. 5867–5870.
[Crossref]

Quirin, S.

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[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]

Rossi, L. F.

M. Pachitariu, C. Stringer, S. Schröder, M. Dipoppa, L. F. Rossi, M. Carandini, and K. D. Harris, “Suite2p: beyond 10,000 neurons with standard two-photon microscopy,” bioRxiv 2016, 061507 (2016).

Saggau, P.

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

V. Iyer, T. M. Hoogland, and P. Saggau, “Fast functional imaging of single neurons using random-access multiphoton (RAMP) microscopy,” J. Neurophysiol. 95(1), 535–545 (2006).
[Crossref] [PubMed]

V. Iyer, B. E. Losavio, and P. Saggau, “Compensation of spatial and temporal dispersion for acousto-optic multiphoton laser-scanning microscopy,” J. Biomed. Opt. 8(3), 460–471 (2003).
[Crossref] [PubMed]

Salomé, R.

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

Sato, M.

Sato, T. R.

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
[Crossref] [PubMed]

Schreiter, E. 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]

Schröder, S.

M. Pachitariu, C. Stringer, S. Schröder, M. Dipoppa, L. F. Rossi, M. Carandini, and K. D. Harris, “Suite2p: beyond 10,000 neurons with standard two-photon microscopy,” bioRxiv 2016, 061507 (2016).

Schuck, R.

R. Schuck, P. Quicke, C. Copeland, S. Garasto, L. A. Annecchino, J. K. Hwang, and S. Schultz, “Rapid three dimensional two photon neural population scanning,” in Proceedings of the 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (IEEE, 2015), pp. 5867–5870.
[Crossref]

Schultz, S.

R. Schuck, P. Quicke, C. Copeland, S. Garasto, L. A. Annecchino, J. K. Hwang, and S. Schultz, “Rapid three dimensional two photon neural population scanning,” in Proceedings of the 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (IEEE, 2015), pp. 5867–5870.
[Crossref]

Sheetz, K. E.

Shimaoka, D.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Shrestha, R.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Smith, C. W.

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]

Squier, J. A.

Stringer, C.

M. Pachitariu, C. Stringer, S. Schröder, M. Dipoppa, L. F. Rossi, M. Carandini, and K. D. Harris, “Suite2p: beyond 10,000 neurons with standard two-photon microscopy,” bioRxiv 2016, 061507 (2016).

Sun, J.

Sun, Y.

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]

Svoboda, K.

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]

Sylvester, A. W.

Tamura, N.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Taniguchi, A.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Tanimoto, R.

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Tom, C.

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

Tonegawa, S.

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

Tsien, J. Z.

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

van ’t Hoff, M.

van der Bourg, A.

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Ventalon, C.

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

Voigt, F. F.

Waddell, S.

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).
[Crossref] [PubMed]

Watson, T.

E. Chong, T. Watson, and F. Festy, “Autocorrelation measurement of femtosecond laser pulses based on two-photon absorption in GaP photodiode,” Appl. Phys. Lett. 105(6), 062111 (2014).
[Crossref]

Wilson, T.

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. Juškaitis, M. J. Booth, and T. Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281(4), 880–887 (2008).
[Crossref]

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]

Wright, J. M.

Wyart, C.

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

Xiong, W.

S. Zeng, X. Lv, K. Bi, C. Zhan, D. Li, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Analysis of the dispersion compensation of acousto-optic deflectors used for multiphoton imaging,” J. Biomed. Opt. 12(2), 024015 (2007).
[Crossref] [PubMed]

S. Zeng, X. Lv, C. Zhan, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Simultaneous compensation for spatial and temporal dispersion of acousto-optical deflectors for two-dimensional scanning with a single prism,” Opt. Lett. 31(8), 1091–1093 (2006).
[Crossref] [PubMed]

Xue, S.

Yagi, S.

Yan, S.

Yang, W.

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref] [PubMed]

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Yang, Y.

Yao, B.

Ye, T.

Young, M. D.

Yu, X.

Yuste, R.

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref] [PubMed]

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[Crossref] [PubMed]

Zeng, S.

Zhan, C.

S. Zeng, X. Lv, K. Bi, C. Zhan, D. Li, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Analysis of the dispersion compensation of acousto-optic deflectors used for multiphoton imaging,” J. Biomed. Opt. 12(2), 024015 (2007).
[Crossref] [PubMed]

S. Zeng, X. Lv, C. Zhan, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Simultaneous compensation for spatial and temporal dispersion of acousto-optical deflectors for two-dimensional scanning with a single prism,” Opt. Lett. 31(8), 1091–1093 (2006).
[Crossref] [PubMed]

Žurauskas, M.

Appl. Opt. (2)

Appl. Phys. Lett. (1)

E. Chong, T. Watson, and F. Festy, “Autocorrelation measurement of femtosecond laser pulses based on two-photon absorption in GaP photodiode,” Appl. Phys. Lett. 105(6), 062111 (2014).
[Crossref]

Biomed. Opt. Express (5)

bioRxiv (1)

M. Pachitariu, C. Stringer, S. Schröder, M. Dipoppa, L. F. Rossi, M. Carandini, and K. D. Harris, “Suite2p: beyond 10,000 neurons with standard two-photon microscopy,” bioRxiv 2016, 061507 (2016).

Cell (1)

J. Z. Tsien, D. F. Chen, D. Gerber, C. Tom, E. H. Mercer, D. J. Anderson, M. Mayford, E. R. Kandel, and S. Tonegawa, “Subregion-and cell type–restricted gene knockout in mouse brain,” Cell 87, 1317–1326 (1996).

eLife (1)

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref] [PubMed]

Front. Neural Circuits (1)

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[Crossref] [PubMed]

IEEE J. Quantum Electron. (1)

R. Dixon, “Acoustic diffraction of light in anisotropic media,” IEEE J. Quantum Electron. 3(2), 85–93 (1967).
[Crossref]

J. Biomed. Opt. (2)

V. Iyer, B. E. Losavio, and P. Saggau, “Compensation of spatial and temporal dispersion for acousto-optic multiphoton laser-scanning microscopy,” J. Biomed. Opt. 8(3), 460–471 (2003).
[Crossref] [PubMed]

S. Zeng, X. Lv, K. Bi, C. Zhan, D. Li, W. R. Chen, W. Xiong, S. L. Jacques, and Q. Luo, “Analysis of the dispersion compensation of acousto-optic deflectors used for multiphoton imaging,” J. Biomed. Opt. 12(2), 024015 (2007).
[Crossref] [PubMed]

J. Neurophysiol. (1)

V. Iyer, T. M. Hoogland, and P. Saggau, “Fast functional imaging of single neurons using random-access multiphoton (RAMP) microscopy,” J. Neurophysiol. 95(1), 535–545 (2006).
[Crossref] [PubMed]

J. Neurosci. Methods (1)

R. Salomé, Y. Kremer, S. Dieudonné, J. F. Léger, O. Krichevsky, C. Wyart, D. Chatenay, and L. Bourdieu, “Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors,” J. Neurosci. Methods 154(1-2), 161–174 (2006).
[Crossref] [PubMed]

Nat. Methods (3)

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[Crossref] [PubMed]

N. Ji, “Adaptive optical fluorescence microscopy,” Nat. Methods 14(4), 374–380 (2017).
[Crossref] [PubMed]

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

Nat. Neurosci. (1)

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

Nature (1)

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]

Neuron (2)

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, and C. Monetti, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85, 942–958 (2015).

Opt. Commun. (1)

E. J. Botcherby, R. Juškaitis, M. J. Booth, and T. Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281(4), 880–887 (2008).
[Crossref]

Opt. Express (2)

Opt. Lett. (4)

Proc. Natl. Acad. Sci. U.S.A. (3)

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

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]

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
[Crossref] [PubMed]

Rev. Sci. Instrum. (1)

Y. Nakai, M. Ozeki, T. Hiraiwa, R. Tanimoto, A. Funahashi, N. Hiroi, A. Taniguchi, S. Nonaka, V. Boilot, R. Shrestha, J. Clark, N. Tamura, V. M. Draviam, and H. Oku, “High-speed microscopy with an electrically tunable lens to image the dynamics of in vivo molecular complexes,” Rev. Sci. Instrum. 86(1), 013707 (2015).
[Crossref] [PubMed]

Other (4)

R. Schuck, P. Quicke, C. Copeland, S. Garasto, L. A. Annecchino, J. K. Hwang, and S. Schultz, “Rapid three dimensional two photon neural population scanning,” in Proceedings of the 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (IEEE, 2015), pp. 5867–5870.
[Crossref]

M. Minsky and S. Papert, Perceptrons: An Essay in Computational Geometry (MIT Press, 1969).

P. Dayan and L. F. Abbott, Theoretical neuroscience (MIT Press, 2001), Vol. 806.

D. Gibson, Photon Lines (personal communication, 2018).

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Figures (9)

Fig. 1
Fig. 1 Pre-compensation of spatial dispersion in AOD using SF11 prism. (a) Schematic of pairing prism-AOD configuration for AOD dispersion compensation. The arrow on the AOD depicts the propagation of acoustic wave and α is the apex angle of SF11 prism i.e. 60°. (b) Calculated spatial dispersion constant of SF11 prism as a function of incident angle of 900 nm laser. The red dotted line is the intrinsic spatial dispersion constant of AOD acting as 1D scanner. The intersection point is the compensation instance where both dispersion constants cancel and the corresponding angle of incidence of the laser is 55.6°.
Fig. 2
Fig. 2 Calculated negative GDD provided by prism-AOD pre-compensation scheme as a function of spatial separation. The red dotted line shows the matching GDD value to that of material dispersion in AOD alone and thus, the intersection point is the predicted optimum distance between the prism and the AOD for restoring the pulse width of the laser tuned to 900 nm.
Fig. 3
Fig. 3 Schematic diagram of remote focusing configuration in which the back pupil plane of the objective is reimaged onto the pupil plane of the remote focusing lens by a 4f system. The translation of the rightmost lens in the refocusing system along the optical axis affords the axial scanning of the focal spot, without direct mechanical movement of the objective lens, as guided by the simple illustration of the marginal ray paths. Inset depicts the shape of the laser wavefront when collimated or refocused away from the nominal focal plane.
Fig. 4
Fig. 4 Far field beam profiling in uncompensated and spatial dispersion compensated AOD settings. (a) Uncompensated laser beam spot focused by achromatic doublet with 60 mm focal length. (b) AOD dispersion compensated laser focal spot. (c) Comparison between uncompensated and compensated beam intensity lineshapes. Scale bar represents 50 µm.
Fig. 5
Fig. 5 Pulse width measurements of diffracted laser beam at varying degree of temporal dispersion compensation. (a) Measured interferometric autocorrelation (IAC) trace with fitted Gaussian function for the laser beam without dispersion compensation. (b) IAC trace and associated Gaussian fit for compensated laser beam at minimum temporal dispersion. The laser pulse duration was calculated from dividing full-width-at-half-maximum (FWHM) of IAC by a factor of 1.41 [34]. (c) Progression of measured laser pulse width as a function of prism-AOD distance.
Fig. 6
Fig. 6 Simplified schematic diagram of multiplane functional imaging system. MOM: Moveable Objective Microscope with closely coupled green and red fluorescence detectors; WP1, WP2: half-wave plates; P1: SF11 equilateral prism; AOD: acousto-optic deflector; BD: beam dump; AL1, AL2: aspheric lenses; PBS: polarising beamsplitter; L1, L2: achromatic doublets; OBJ: objective lens. Insets depict the optical focal switch between two planes separated by z distance and the partially-filled back aperture of excitation objective lens. Laser Path A represents the nominal in-focus beam path and Laser Path B represents the refocusing beam path.
Fig. 7
Fig. 7 Investigation of two-photon excitation from the remote focusing. (a) FWHM of axial point spread function at varying refocusing depths derived from imaging 0.5 µm yellow-green fluorescent beads embedded in 10% (w/v) agarose gel. (b) Measured fluorescence intensity, that IPSF is the sum of PSF intensity over axial FWHM, at different refocusing depths. Error bars shown in both figures represent the standard error of the mean.
Fig. 8
Fig. 8 In vivo multiplane calcium imaging of neuronal circuit expressing GCaMP6s in the mouse parietal cortex region. Time-averaged fluorescence images of neurons at (a) the in-focus plane, 120 µm below the brain surface and (d) the refocused plane, 250 µm below brain surface. (b), (e) Regions of interest corresponding to the neurons in (a) and (d) with the location of five representative cells highlighted in red. (c), (f) Representative fluorescence traces from the five marked neurons at the in-focus and the refocused planes. (g), (h) Signal-to-noise ratio derived from the fluorescence transients at the in-focus and the refocused planes with the corresponding peaks labelled with asterisk sign (*).
Fig. 9
Fig. 9 Simplified schematic diagram of expanded concept of quasi-simultaneous multiplane multiphoton imaging technique using AOD optical switching and remote focusing. The frame rate will be ~7 fps at respective focal planes.

Equations (11)

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θ 1st = λf V
σ AOD = d θ 1st dλ = f V
σ AOD + σ prism =0
σ prism = dβ dn dn dλ
Δτ Δλ = λLf cV dβ dn dn dλ
GD D prismAOD = Δτ Δλ λ 2 2πc
ϕ(ρ)= n objective kz( 1 s 2 ρ 2 2 s 4 ρ 4 8 + )
θ objective = θ refocusing
N A objective N A refocusing = n objective n refocusing
z= n refocusing n objective Z refocusing
τ out = τ in 1+ (4ln2(GD D AOD +GD D prismAOD )) τ in 4 2

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