Abstract

Recently, we presented a new approach to create high-speed amplitude modulation of femtosecond laser pulses and tag multiple excitation beams with specific modulation frequencies. In this work, we discuss the utility of this method to record calcium signals in brain tissue with two-photon frequency-division multiplexing (2P-FDM) microscopy. While frequency-multiplexed imaging appears slightly inferior in terms of image quality as compared to conventional two-photon laser scanning microscopy due to shot noise-induced cross-talk between frequency channels, applying this technique to record average signals from regions of interest (ROI) such as neuronal cell bodies was found to be promising. We use phase information associated with each pixel or waveform within a selected ROI to phase-align and recombine the signals into one extended amplitude-modulated waveform. This procedure narrows the frequency detection window, effectively decreasing noise contributions from other frequency channels. Using theoretical analysis, numerical simulations, and in vitro imaging, we demonstrate a reduction of cross-talk by more than an order of magnitude and predict the usefulness of 2P-FDM for functional studies of brain activity.

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

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2017 (4)

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

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]

D. Tsyboulski, N. Orlova, and P. Saggau, “Amplitude modulation of femtosecond laser pulses in the megahertz range for frequency-multiplexed two-photon imaging,” Opt. Express 25(8), 9435–9442 (2017).
[Crossref] [PubMed]

2016 (7)

J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
[Crossref] [PubMed]

K. Podgorski and G. Ranganathan, “Brain heating induced by near-infrared lasers during multiphoton microscopy,” J. Neurophysiol. 116(3), 1012–1023 (2016).
[Crossref] [PubMed]

R. Prevedel, A. J. Verhoef, A. J. Pernía-Andrade, S. Weisenburger, B. S. Huang, T. Nöbauer, A. Fernández, J. E. Delcour, P. Golshani, A. Baltuska, and A. Vaziri, “Fast volumetric calcium imaging across multiple cortical layers using sculpted light,” Nat. Methods 13(12), 1021–1028 (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]

J. N. Stirman, I. T. Smith, M. W. Kudenov, and S. L. Smith, “Wide field-of-view, multi-region, two-photon imaging of neuronal activity in the mammalian brain,” Nat. Biotechnol. 34(8), 857–862 (2016).
[Crossref] [PubMed]

J. L. Chen, F. F. Voigt, M. Javadzadeh, R. Krueppel, and F. Helmchen, “Long-range population dynamics of anatomically defined neocortical networks,” eLife 5, e14679 (2016).
[Crossref] [PubMed]

2015 (2)

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]

B. Podor, Y. L. Hu, M. Ohkura, J. Nakai, R. Croll, and A. Fine, “Comparison of genetically encoded calcium indicators for monitoring action potentials in mammalian brain by two-photon excitation fluorescence microscopy,” Neurophotonics 2(2), 021014 (2015).
[Crossref] [PubMed]

2014 (1)

J. Lecoq, J. Savall, D. Vučinić, B. F. Grewe, H. Kim, J. Z. Li, L. J. Kitch, and M. J. Schnitzer, “Visualizing mammalian brain area interactions by dual-axis two-photon calcium imaging,” Nat. Neurosci. 17(12), 1825–1829 (2014).
[Crossref] [PubMed]

2013 (3)

E. D. Diebold, B. W. Buckley, D. R. Gossett, and B. Jalali, “Digitally synthesized beat frequency multiplexing for sub-millisecond fluorescence microscopy,” Nat. Photonics 7(10), 806–810 (2013).
[Crossref]

M. Ducros, Y. G. Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

S. S. Howard, A. Straub, N. Horton, D. Kobat, and C. Xu, “Frequency-multiplexed in vivo multiphoton phosphorescence lifetime microscopy,” Nat. Photonics 7(1), 33–37 (2013).
[Crossref] [PubMed]

2012 (1)

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)

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]

2008 (3)

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]

K. P. Lillis, A. Eng, J. A. White, and J. Mertz, “Two-photon imaging of spatially extended neuronal network dynamics with high temporal resolution,” J. Neurosci. Methods 172(2), 178–184 (2008).
[Crossref] [PubMed]

S. E. Bohndiek, A. Blue, A. T. Clark, M. L. Prydderch, R. Turchetta, G. J. Royle, and R. D. Speller, “Comparison of methods for estimating the conversion gain of CMOS active pixel sensors,” IEEE Sens. J. 8(10), 1734–1744 (2008).
[Crossref]

2007 (1)

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]

1990 (1)

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

Allende Motz, A. M.

J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
[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]

Baltuska, A.

R. Prevedel, A. J. Verhoef, A. J. Pernía-Andrade, S. Weisenburger, B. S. Huang, T. Nöbauer, A. Fernández, J. E. Delcour, P. Golshani, A. Baltuska, and A. Vaziri, “Fast volumetric calcium imaging across multiple cortical layers using sculpted light,” Nat. Methods 13(12), 1021–1028 (2016).
[Crossref] [PubMed]

Bartels, R. A.

J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
[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]

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]

Blue, A.

S. E. Bohndiek, A. Blue, A. T. Clark, M. L. Prydderch, R. Turchetta, G. J. Royle, and R. D. Speller, “Comparison of methods for estimating the conversion gain of CMOS active pixel sensors,” IEEE Sens. J. 8(10), 1734–1744 (2008).
[Crossref]

Bohndiek, S. E.

S. E. Bohndiek, A. Blue, A. T. Clark, M. L. Prydderch, R. Turchetta, G. J. Royle, and R. D. Speller, “Comparison of methods for estimating the conversion gain of CMOS active pixel sensors,” IEEE Sens. J. 8(10), 1734–1744 (2008).
[Crossref]

Bradley, J.

M. Ducros, Y. G. Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

Buckley, B. W.

E. D. Diebold, B. W. Buckley, D. R. Gossett, and B. Jalali, “Digitally synthesized beat frequency multiplexing for sub-millisecond fluorescence microscopy,” Nat. Photonics 7(10), 806–810 (2013).
[Crossref]

Charles, A. S.

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]

Charpak, S.

M. Ducros, Y. G. Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

Chen, J. L.

J. L. Chen, F. F. Voigt, M. Javadzadeh, R. Krueppel, and F. Helmchen, “Long-range population dynamics of anatomically defined neocortical networks,” eLife 5, e14679 (2016).
[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]

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]

Chiovini, 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]

Clark, A. T.

S. E. Bohndiek, A. Blue, A. T. Clark, M. L. Prydderch, R. Turchetta, G. J. Royle, and R. D. Speller, “Comparison of methods for estimating the conversion gain of CMOS active pixel sensors,” IEEE Sens. J. 8(10), 1734–1744 (2008).
[Crossref]

Croll, R.

B. Podor, Y. L. Hu, M. Ohkura, J. Nakai, R. Croll, and A. Fine, “Comparison of genetically encoded calcium indicators for monitoring action potentials in mammalian brain by two-photon excitation fluorescence microscopy,” Neurophotonics 2(2), 021014 (2015).
[Crossref] [PubMed]

Cui, M.

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]

de Sars, V.

M. Ducros, Y. G. Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

Delcour, J. E.

R. Prevedel, A. J. Verhoef, A. J. Pernía-Andrade, S. Weisenburger, B. S. Huang, T. Nöbauer, A. Fernández, J. E. Delcour, P. Golshani, A. Baltuska, and A. Vaziri, “Fast volumetric calcium imaging across multiple cortical layers using sculpted light,” Nat. Methods 13(12), 1021–1028 (2016).
[Crossref] [PubMed]

DeLuca, J. G.

J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
[Crossref] [PubMed]

DeLuca, K. F.

J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
[Crossref] [PubMed]

Denk, W.

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

Diebold, E. D.

E. D. Diebold, B. W. Buckley, D. R. Gossett, and B. Jalali, “Digitally synthesized beat frequency multiplexing for sub-millisecond fluorescence microscopy,” Nat. Photonics 7(10), 806–810 (2013).
[Crossref]

Domingue, S. R.

J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
[Crossref] [PubMed]

Ducros, M.

M. Ducros, Y. G. Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Eng, A.

K. P. Lillis, A. Eng, J. A. White, and J. Mertz, “Two-photon imaging of spatially extended neuronal network dynamics with high temporal resolution,” J. Neurosci. Methods 172(2), 178–184 (2008).
[Crossref] [PubMed]

Fernández, A.

R. Prevedel, A. J. Verhoef, A. J. Pernía-Andrade, S. Weisenburger, B. S. Huang, T. Nöbauer, A. Fernández, J. E. Delcour, P. Golshani, A. Baltuska, and A. Vaziri, “Fast volumetric calcium imaging across multiple cortical layers using sculpted light,” Nat. Methods 13(12), 1021–1028 (2016).
[Crossref] [PubMed]

Field, J. J.

J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
[Crossref] [PubMed]

Fine, A.

B. Podor, Y. L. Hu, M. Ohkura, J. Nakai, R. Croll, and A. Fine, “Comparison of genetically encoded calcium indicators for monitoring action potentials in mammalian brain by two-photon excitation fluorescence microscopy,” Neurophotonics 2(2), 021014 (2015).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Fitzpatrick, D.

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J. Lecoq, J. Savall, D. Vučinić, B. F. Grewe, H. Kim, J. Z. Li, L. J. Kitch, and M. J. Schnitzer, “Visualizing mammalian brain area interactions by dual-axis two-photon calcium imaging,” Nat. Neurosci. 17(12), 1825–1829 (2014).
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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]

Svoboda, K.

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]

Szalay, G.

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]

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).
[Crossref] [PubMed]

Tanimoto, M.

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]

Tank, D. 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]

Thiberge, S. Y.

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]

Tsyboulski, D.

Turchetta, R.

S. E. Bohndiek, A. Blue, A. T. Clark, M. L. Prydderch, R. Turchetta, G. J. Royle, and R. D. Speller, “Comparison of methods for estimating the conversion gain of CMOS active pixel sensors,” IEEE Sens. J. 8(10), 1734–1744 (2008).
[Crossref]

Vaziri, A.

R. Prevedel, A. J. Verhoef, A. J. Pernía-Andrade, S. Weisenburger, B. S. Huang, T. Nöbauer, A. Fernández, J. E. Delcour, P. Golshani, A. Baltuska, and A. Vaziri, “Fast volumetric calcium imaging across multiple cortical layers using sculpted light,” Nat. Methods 13(12), 1021–1028 (2016).
[Crossref] [PubMed]

Veress, M.

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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R. Prevedel, A. J. Verhoef, A. J. Pernía-Andrade, S. Weisenburger, B. S. Huang, T. Nöbauer, A. Fernández, J. E. Delcour, P. Golshani, A. Baltuska, and A. Vaziri, “Fast volumetric calcium imaging across multiple cortical layers using sculpted light,” Nat. Methods 13(12), 1021–1028 (2016).
[Crossref] [PubMed]

Vizi, E. S.

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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J. L. Chen, F. F. Voigt, M. Javadzadeh, R. Krueppel, and F. Helmchen, “Long-range population dynamics of anatomically defined neocortical networks,” eLife 5, e14679 (2016).
[Crossref] [PubMed]

Vucinic, D.

J. Lecoq, J. Savall, D. Vučinić, B. F. Grewe, H. Kim, J. Z. Li, L. J. Kitch, and M. J. Schnitzer, “Visualizing mammalian brain area interactions by dual-axis two-photon calcium imaging,” Nat. Neurosci. 17(12), 1825–1829 (2014).
[Crossref] [PubMed]

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

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R. Prevedel, A. J. Verhoef, A. J. Pernía-Andrade, S. Weisenburger, B. S. Huang, T. Nöbauer, A. Fernández, J. E. Delcour, P. Golshani, A. Baltuska, and A. Vaziri, “Fast volumetric calcium imaging across multiple cortical layers using sculpted light,” Nat. Methods 13(12), 1021–1028 (2016).
[Crossref] [PubMed]

Wernsing, K. A.

J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
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K. P. Lillis, A. Eng, J. A. White, and J. Mertz, “Two-photon imaging of spatially extended neuronal network dynamics with high temporal resolution,” J. Neurosci. Methods 172(2), 178–184 (2008).
[Crossref] [PubMed]

Wilson, D. E.

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]

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).
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Xu, C.

S. S. Howard, A. Straub, N. Horton, D. Kobat, and C. Xu, “Frequency-multiplexed in vivo multiphoton phosphorescence lifetime microscopy,” Nat. Photonics 7(1), 33–37 (2013).
[Crossref] [PubMed]

Yang, W.

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

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J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
[Crossref] [PubMed]

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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).
[Crossref] [PubMed]

Yuste, R.

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

Zeng, S.

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).
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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]

eLife (2)

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]

J. L. Chen, F. F. Voigt, M. Javadzadeh, R. Krueppel, and F. Helmchen, “Long-range population dynamics of anatomically defined neocortical networks,” eLife 5, e14679 (2016).
[Crossref] [PubMed]

IEEE Sens. J. (1)

S. E. Bohndiek, A. Blue, A. T. Clark, M. L. Prydderch, R. Turchetta, G. J. Royle, and R. D. Speller, “Comparison of methods for estimating the conversion gain of CMOS active pixel sensors,” IEEE Sens. J. 8(10), 1734–1744 (2008).
[Crossref]

J. Biomed. Opt. (1)

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)

K. Podgorski and G. Ranganathan, “Brain heating induced by near-infrared lasers during multiphoton microscopy,” J. Neurophysiol. 116(3), 1012–1023 (2016).
[Crossref] [PubMed]

J. Neurosci. Methods (1)

K. P. Lillis, A. Eng, J. A. White, and J. Mertz, “Two-photon imaging of spatially extended neuronal network dynamics with high temporal resolution,” J. Neurosci. Methods 172(2), 178–184 (2008).
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Nat. Biotechnol. (1)

J. N. Stirman, I. T. Smith, M. W. Kudenov, and S. L. Smith, “Wide field-of-view, multi-region, two-photon imaging of neuronal activity in the mammalian brain,” Nat. Biotechnol. 34(8), 857–862 (2016).
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Nat. Methods (6)

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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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]

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

R. Prevedel, A. J. Verhoef, A. J. Pernía-Andrade, S. Weisenburger, B. S. Huang, T. Nöbauer, A. Fernández, J. E. Delcour, P. Golshani, A. Baltuska, and A. Vaziri, “Fast volumetric calcium imaging across multiple cortical layers using sculpted light,” Nat. Methods 13(12), 1021–1028 (2016).
[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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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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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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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]

J. Lecoq, J. Savall, D. Vučinić, B. F. Grewe, H. Kim, J. Z. Li, L. J. Kitch, and M. J. Schnitzer, “Visualizing mammalian brain area interactions by dual-axis two-photon calcium imaging,” Nat. Neurosci. 17(12), 1825–1829 (2014).
[Crossref] [PubMed]

Nat. Photonics (2)

S. S. Howard, A. Straub, N. Horton, D. Kobat, and C. Xu, “Frequency-multiplexed in vivo multiphoton phosphorescence lifetime microscopy,” Nat. Photonics 7(1), 33–37 (2013).
[Crossref] [PubMed]

E. D. Diebold, B. W. Buckley, D. R. Gossett, and B. Jalali, “Digitally synthesized beat frequency multiplexing for sub-millisecond fluorescence microscopy,” Nat. Photonics 7(10), 806–810 (2013).
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Neurophotonics (1)

B. Podor, Y. L. Hu, M. Ohkura, J. Nakai, R. Croll, and A. Fine, “Comparison of genetically encoded calcium indicators for monitoring action potentials in mammalian brain by two-photon excitation fluorescence microscopy,” Neurophotonics 2(2), 021014 (2015).
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Opt. Express (1)

Proc. Natl. Acad. Sci. U.S.A. (2)

M. Ducros, Y. G. Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
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J. J. Field, K. A. Wernsing, S. R. Domingue, A. M. Allende Motz, K. F. DeLuca, D. H. Levi, J. G. DeLuca, M. D. Young, J. A. Squier, and R. A. Bartels, “Superresolved multiphoton microscopy with spatial frequency-modulated imaging,” Proc. Natl. Acad. Sci. U.S.A. 113(24), 6605–6610 (2016).
[Crossref] [PubMed]

Science (1)

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

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J. B. Pawley, “Fundamental limits in confocal microscopy,” in Handbook of Biological Confocal Microscopy (Springer, 2006).

J. R. Janesik, Photon transfer (SPIE, 2007).

R. Yang, T. D. Weber, E. D. Witkowski, I. G. Davison, and J. Mertz, “Neuronal imaging with ultrahigh dynamic range multiphoton microscopy,” Sci. Rep. 7, 5817–1–7 (2017).
[Crossref]

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Figures (9)

Fig. 1
Fig. 1 A diagram of the custom Mach-Zehnder interferometric setup to create multiple amplitude-modulated femtosecond laser beams, coupled to the custom-built TPLSM system. BE is beam expander, UBB is 50:50 ultrafast beam splitter, AOD is acousto-optical deflector, HWP is half-wave plate, D is delay line, P is periscopic mirror, PBS is polarizing beam splitter, ν is optical frequency, f and fi are acoustic frequencies, SL is scan lens, TL is tube lens, DM is dichroic mirror. The inserted image shows 2 and 5 amplitude-modulated beams at the interferometer output visualized with a NIR detector card.
Fig. 2
Fig. 2 (a) Computer-generated waveforms from 1 and 10 simultaneous channels, amplitude-modulated at 7 MHz and 1 – 19 MHz. Average intensity in each channel is 0.5 photons/sample. (b) DFT spectra of the simulated waveform (blue trace in (a)) computed from 160 and 8,000 time samples. Note, the red plot is multiplied by 50. (c) Average DFT amplitudes at 7 MHz and 21 MHz computed from 400 simulated waveforms, representing comparison of signal and background. The corresponding waveform example is shown in (a) as the blue trace. Theoretical predictions from Eqs. (9) and (10) are shown as solid lines.
Fig. 3
Fig. 3 (a) Simulated frequency-multiplexed images from 1 to 10 active channels. False color intensity scale represents photons/pulse. (b) Conventional TPLSM images generated with different pixel dwell times. (c) Average and standard deviation of pixel intensity values computed from images in (a) and (b). (d) A comparison of theoretical estimates from Eqs. (9) and (10), and the data from (c) plotted as DFT amplitudes.
Fig. 4
Fig. 4 (a) Temporal profiles of simulated signals from all 10 channels. (b,c,d) Comparison of demultiplexed signals from channels 1, 4, 8 (f = 1,7,15 MHz), and conventional TPLSM signals. (e,f,g) Residuals in simulated 2P-FDM and TPLSM calcium signal traces computed from data in (b,c,d).
Fig. 5
Fig. 5 (a) Conventional two-photon image of a brain slice recorded while scanning the sample with 3 excitation beams, modulated at 7 MHz, 1 MHz, and 5 MHz. The image area shown contains 400 × 150 pixels along the vertical and horizontal axis, respectively. (b) A waveform section of a single scan line across the neuron on the left. The part shown in red represents 1,000 samples corresponding to 1 pixel in (a). (c) Waveform with 1,000 samples from (b) showing a fluorescence signal modulated at 7 MHz.
Fig. 6
Fig. 6 Demultiplexed images corresponding to different modulation frequencies and different number of samples/pixel as indicated. The scale bar is 30 µm.
Fig. 7
Fig. 7 (a) Phase images computed from pixels within selected ROIs in Fig. 5(a) outlining cell bodies. (b) Cross-section plots from vertical lines in (a), indicated by arrows.
Fig. 8
Fig. 8 (a) Averaged DFT spectra of [M1 + M2 + M3] and [M1 + M2] data sets computed with different number of samples/pixel. (b) DFT spectra of phase-aligned and concatenated waveforms from same data sets as in (a). (c) Signal at 5 MHz and average background computed from frequencies in the range of 3.5-4.5 MHz as a function of overall waveform length. (d) SBR plot computed from data in (c).
Fig. 9
Fig. 9 (a) Examples of PMT output showing individual photon events at different fluorescence intensities of a fluorescein solution. (b) Fluctuations in detected number of photons within a 10 µs temporal window, recorded at different excitation power levels. (c) Mean-variance plot of signals from (b). (d) Calibration plot showing average pixel intensity in TPLSM images as function of average number of detected photons. (e,f) Averaged in vivo images of mouse V1 layers 1 and 4 recorded at 75 μm and 375 μm depth. Intensity scale in units of photons/pixel. (g) Examples of calcium transients from selected ROIs in (e,f), recorded at ~18 Hz frame rate.

Equations (11)

Equations on this page are rendered with MathJax. Learn more.

F i (t)= S 0 + R i (t) ; F(t) = S 0 ; R(t) = 0 an d S 0 =Var(R(t))= R (t) 2 ,i.
S(t) =Var(R(t))= R (t) 2 .
I(t)= I 0 cos(2πft)+1 2 ,
S(t)=A[ 1+ 4 3 cos(2πft)+ 1 3 cos(4πft) ],
i=0 N s 1 R i (t) 2 = 1 N s k=0 N s 1 | R k ˜ (f) | 2 = P ˜ ,
A N s = P ˜ .
N s j=1 N ch A j = j=1 N ch P j ˜ ,
| R k ˜ (f) | = π 4 | R k ˜ (f) | 2 .
| R k ˜ (f) | = π 4 N s j=1 N ch A j .
S ˜ (f) = 2 3 A N s
SBR= 4 3 A N s π j=1 N ch A j .

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