Abstract

Two-photon laser-scanning microscopy enables to record neuronal network activity in three-dimensional space while maintaining single-cellular resolution. One of the proposed approaches combines galvanometric x-y scanning with piezo-driven objective movements and employs hardware feedback signals for position monitoring. However, readily applicable methods to quantify the accuracy of those feedback signals are currently lacking. Here we provide techniques based on contact-free laser reflection and laser triangulation for the quantification of positioning accuracy of each spatial axis. We found that the lateral feedback signals are sufficiently accurate (defined as <2.5 µm) for a wide range of scan trajectories and frequencies. We further show that axial positioning accuracy does not only depend on objective acceleration and mass but also its geometry. We conclude that the introduced methods allow a reliable quantification of position feedback signals in a cost-efficient, easy-to-install manner and should be applicable for a wide range of two-photon laser scanning microscopes.

© 2015 Optical Society of America

Full Article  |  PDF Article
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References

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  1. W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
    [Crossref] [PubMed]
  2. W. Göbel, B. M. Kampa, and F. Helmchen, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
    [Crossref] [PubMed]
  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]
  4. 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]
  5. 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]
  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).
    [Crossref] [PubMed]
  7. G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
    [Crossref] [PubMed]
  8. 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]
  9. M. Dal Maschio, A. M. De Stasi, F. Benfenati, and T. Fellin, “Three-dimensional in vivo scanning microscopy with inertia-free focus control,” Opt. Lett. 36(17), 3503–3505 (2011).
    [Crossref] [PubMed]
  10. 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]
  11. M. Ducros, Y. 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]
  12. S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8(29), 29 (2014).
    [PubMed]
  13. S. Bovetti, C. Moretti, and T. Fellin, “Mapping brain circuit function in vivo using two-photon fluorescence microscopy,” Microsc. Res. Tech. 77(7), 492–501 (2014).
    [Crossref] [PubMed]
  14. 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]
  15. T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
    [Crossref] [PubMed]
  16. R. J. Cotton, E. Froudarakis, P. Storer, P. Saggau, and A. S. Tolias, “Three-dimensional mapping of microcircuit correlation structure,” Front. Neural Circuits 7(151), 151 (2013).
    [PubMed]
  17. B. M. Kampa, M. M. Roth, W. Göbel, and F. Helmchen, “Representation of visual scenes by local neuronal populations in layer 2/3 of mouse visual cortex,” Front. Neural Circuits 5(18), 18 (2011).
    [PubMed]
  18. P. A. Kirkby, K. M. Srinivas Nadella, and R. A. Silver, “A compact acousto-optic lens for 2D and 3D femtosecond based 2-photon microscopy,” Opt. Express 18(13), 13720–13745 (2010).
    [Crossref] [PubMed]
  19. A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
    [Crossref] [PubMed]
  20. K. Kirmse, M. Kummer, Y. Kovalchuk, O. W. Witte, O. Garaschuk, and K. Holthoff, “GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo,” Nat. Commun. 6, 7750 (2015).
    [Crossref] [PubMed]
  21. M. Paukert and D. E. Bergles, “Reduction of motion artifacts during in vivo two-photon imaging of brain through heartbeat triggered scanning,” J. Physiol. 590(13), 2955–2963 (2012).
    [Crossref] [PubMed]
  22. J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
    [Crossref] [PubMed]
  23. A. M. Kerlin, M. L. Andermann, V. K. Berezovskii, and R. C. Reid, “Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex,” Neuron 67(5), 858–871 (2010).
    [Crossref] [PubMed]

2015 (1)

K. Kirmse, M. Kummer, Y. Kovalchuk, O. W. Witte, O. Garaschuk, and K. Holthoff, “GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo,” Nat. Commun. 6, 7750 (2015).
[Crossref] [PubMed]

2014 (3)

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

S. Bovetti, C. Moretti, and T. Fellin, “Mapping brain circuit function in vivo using two-photon fluorescence microscopy,” Microsc. Res. Tech. 77(7), 492–501 (2014).
[Crossref] [PubMed]

T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
[Crossref] [PubMed]

2013 (3)

R. J. Cotton, E. Froudarakis, P. Storer, P. Saggau, and A. S. Tolias, “Three-dimensional mapping of microcircuit correlation structure,” Front. Neural Circuits 7(151), 151 (2013).
[PubMed]

J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[Crossref] [PubMed]

M. Ducros, Y. 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]

2012 (3)

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]

M. Paukert and D. E. Bergles, “Reduction of motion artifacts during in vivo two-photon imaging of brain through heartbeat triggered scanning,” J. Physiol. 590(13), 2955–2963 (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 (5)

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]

G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
[Crossref] [PubMed]

B. M. Kampa, M. M. Roth, W. Göbel, and F. Helmchen, “Representation of visual scenes by local neuronal populations in layer 2/3 of mouse visual cortex,” Front. Neural Circuits 5(18), 18 (2011).
[PubMed]

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]

M. Dal Maschio, A. M. De Stasi, F. Benfenati, and T. Fellin, “Three-dimensional in vivo scanning microscopy with inertia-free focus control,” Opt. Lett. 36(17), 3503–3505 (2011).
[Crossref] [PubMed]

2010 (3)

A. M. Kerlin, M. L. Andermann, V. K. Berezovskii, and R. C. Reid, “Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex,” Neuron 67(5), 858–871 (2010).
[Crossref] [PubMed]

P. A. Kirkby, K. M. Srinivas Nadella, and R. A. Silver, “A compact acousto-optic lens for 2D and 3D femtosecond based 2-photon microscopy,” Opt. Express 18(13), 13720–13745 (2010).
[Crossref] [PubMed]

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

2008 (2)

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]

2007 (1)

W. Göbel, B. M. Kampa, and F. Helmchen, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
[Crossref] [PubMed]

2005 (1)

A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
[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]

Andermann, M. L.

A. M. Kerlin, M. L. Andermann, V. K. Berezovskii, and R. C. Reid, “Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex,” Neuron 67(5), 858–871 (2010).
[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]

Benfenati, F.

Berezovskii, V. K.

A. M. Kerlin, M. L. Andermann, V. K. Berezovskii, and R. C. Reid, “Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex,” Neuron 67(5), 858–871 (2010).
[Crossref] [PubMed]

Bergles, D. E.

M. Paukert and D. E. Bergles, “Reduction of motion artifacts during in vivo two-photon imaging of brain through heartbeat triggered scanning,” J. Physiol. 590(13), 2955–2963 (2012).
[Crossref] [PubMed]

Booth, M. 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]

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]

Bovetti, S.

S. Bovetti, C. Moretti, and T. Fellin, “Mapping brain circuit function in vivo using two-photon fluorescence microscopy,” Microsc. Res. Tech. 77(7), 492–501 (2014).
[Crossref] [PubMed]

Bradley, J.

M. Ducros, Y. 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]

Charpak, S.

M. Ducros, Y. 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, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[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]

Chirico, G.

A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
[Crossref] [PubMed]

Collini, M.

A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
[Crossref] [PubMed]

Cotton, R. J.

R. J. Cotton, E. Froudarakis, P. Storer, P. Saggau, and A. S. Tolias, “Three-dimensional mapping of microcircuit correlation structure,” Front. Neural Circuits 7(151), 151 (2013).
[PubMed]

Dal Maschio, M.

de Sars, V.

M. Ducros, Y. 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]

De Stasi, A. M.

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]

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]

Diaspro, A.

A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
[Crossref] [PubMed]

Ducros, M.

M. Ducros, Y. 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]

Fellin, T.

S. Bovetti, C. Moretti, and T. Fellin, “Mapping brain circuit function in vivo using two-photon fluorescence microscopy,” Microsc. Res. Tech. 77(7), 492–501 (2014).
[Crossref] [PubMed]

M. Dal Maschio, A. M. De Stasi, F. Benfenati, and T. Fellin, “Three-dimensional in vivo scanning microscopy with inertia-free focus control,” Opt. Lett. 36(17), 3503–3505 (2011).
[Crossref] [PubMed]

Fernández-Alfonso, T.

T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
[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]

Froudarakis, E.

R. J. Cotton, E. Froudarakis, P. Storer, P. Saggau, and A. S. Tolias, “Three-dimensional mapping of microcircuit correlation structure,” Front. Neural Circuits 7(151), 151 (2013).
[PubMed]

Garaschuk, O.

K. Kirmse, M. Kummer, Y. Kovalchuk, O. W. Witte, O. Garaschuk, and K. Holthoff, “GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo,” Nat. Commun. 6, 7750 (2015).
[Crossref] [PubMed]

Göbel, W.

B. M. Kampa, M. M. Roth, W. Göbel, and F. Helmchen, “Representation of visual scenes by local neuronal populations in layer 2/3 of mouse visual cortex,” Front. Neural Circuits 5(18), 18 (2011).
[PubMed]

W. Göbel, B. M. Kampa, and F. Helmchen, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

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).
[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]

Hájos, N.

G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
[Crossref] [PubMed]

Helmchen, F.

J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[Crossref] [PubMed]

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]

B. M. Kampa, M. M. Roth, W. Göbel, and F. Helmchen, “Representation of visual scenes by local neuronal populations in layer 2/3 of mouse visual cortex,” Front. Neural Circuits 5(18), 18 (2011).
[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]

W. Göbel, B. M. Kampa, and F. Helmchen, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
[Crossref] [PubMed]

Hillier, D.

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]

Holthoff, K.

K. Kirmse, M. Kummer, Y. Kovalchuk, O. W. Witte, O. Garaschuk, and K. Holthoff, “GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo,” Nat. Commun. 6, 7750 (2015).
[Crossref] [PubMed]

Houssen, Y.

M. Ducros, Y. 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]

Iacaruso, M. F.

T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
[Crossref] [PubMed]

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), 29 (2014).
[PubMed]

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).
[Crossref] [PubMed]

Kampa, B. M.

B. M. Kampa, M. M. Roth, W. Göbel, and F. Helmchen, “Representation of visual scenes by local neuronal populations in layer 2/3 of mouse visual cortex,” Front. Neural Circuits 5(18), 18 (2011).
[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]

W. Göbel, B. M. Kampa, and F. Helmchen, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
[Crossref] [PubMed]

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]

Kaszás, A.

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]

G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
[Crossref] [PubMed]

Katona, 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]

G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
[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]

Kerlin, A. M.

A. M. Kerlin, M. L. Andermann, V. K. Berezovskii, and R. C. Reid, “Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex,” Neuron 67(5), 858–871 (2010).
[Crossref] [PubMed]

Kirkby, P. A.

T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
[Crossref] [PubMed]

P. A. Kirkby, K. M. Srinivas Nadella, and R. A. Silver, “A compact acousto-optic lens for 2D and 3D femtosecond based 2-photon microscopy,” Opt. Express 18(13), 13720–13745 (2010).
[Crossref] [PubMed]

Kirmse, K.

K. Kirmse, M. Kummer, Y. Kovalchuk, O. W. Witte, O. Garaschuk, and K. Holthoff, “GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo,” Nat. Commun. 6, 7750 (2015).
[Crossref] [PubMed]

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]

Kovalchuk, Y.

K. Kirmse, M. Kummer, Y. Kovalchuk, O. W. Witte, O. Garaschuk, and K. Holthoff, “GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo,” Nat. Commun. 6, 7750 (2015).
[Crossref] [PubMed]

Kummer, M.

K. Kirmse, M. Kummer, Y. Kovalchuk, O. W. Witte, O. Garaschuk, and K. Holthoff, “GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo,” Nat. Commun. 6, 7750 (2015).
[Crossref] [PubMed]

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]

Lillis, K. P.

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]

Maák, P.

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]

Margolis, D. J.

J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[Crossref] [PubMed]

Mertz, J.

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]

Moretti, C.

S. Bovetti, C. Moretti, and T. Fellin, “Mapping brain circuit function in vivo using two-photon fluorescence microscopy,” Microsc. Res. Tech. 77(7), 492–501 (2014).
[Crossref] [PubMed]

Nadella, K. M.

T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
[Crossref] [PubMed]

Paukert, M.

M. Paukert and D. E. Bergles, “Reduction of motion artifacts during in vivo two-photon imaging of brain through heartbeat triggered scanning,” J. Physiol. 590(13), 2955–2963 (2012).
[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.

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

Pfäffli, O. A.

J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[Crossref] [PubMed]

Pichler, B.

T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
[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]

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), 29 (2014).
[PubMed]

Reid, R. C.

A. M. Kerlin, M. L. Andermann, V. K. Berezovskii, and R. C. Reid, “Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex,” Neuron 67(5), 858–871 (2010).
[Crossref] [PubMed]

Roš, H.

T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
[Crossref] [PubMed]

Roska, B.

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

Roth, M. M.

B. M. Kampa, M. M. Roth, W. Göbel, and F. Helmchen, “Representation of visual scenes by local neuronal populations in layer 2/3 of mouse visual cortex,” Front. Neural Circuits 5(18), 18 (2011).
[PubMed]

Rózsa, B.

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

G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
[Crossref] [PubMed]

Saggau, P.

R. J. Cotton, E. Froudarakis, P. Storer, P. Saggau, and A. S. Tolias, “Three-dimensional mapping of microcircuit correlation structure,” Front. Neural Circuits 7(151), 151 (2013).
[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]

Silver, R. A.

T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
[Crossref] [PubMed]

P. A. Kirkby, K. M. Srinivas Nadella, and R. A. Silver, “A compact acousto-optic lens for 2D and 3D femtosecond based 2-photon microscopy,” Opt. Express 18(13), 13720–13745 (2010).
[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]

Srinivas Nadella, K. M.

Storer, P.

R. J. Cotton, E. Froudarakis, P. Storer, P. Saggau, and A. S. Tolias, “Three-dimensional mapping of microcircuit correlation structure,” Front. Neural Circuits 7(151), 151 (2013).
[PubMed]

Strickler, J. H.

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

Tamás, G.

G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
[Crossref] [PubMed]

Tolias, A. S.

R. J. Cotton, E. Froudarakis, P. Storer, P. Saggau, and A. S. Tolias, “Three-dimensional mapping of microcircuit correlation structure,” Front. Neural Circuits 7(151), 151 (2013).
[PubMed]

Turi, G. F.

G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
[Crossref] [PubMed]

van ’t Hoff, M.

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]

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]

G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
[Crossref] [PubMed]

Voigt, F. F.

J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[Crossref] [PubMed]

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]

Webb, W. W.

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

White, J. 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]

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]

Witte, O. W.

K. Kirmse, M. Kummer, Y. Kovalchuk, O. W. Witte, O. Garaschuk, and K. Holthoff, “GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo,” Nat. Commun. 6, 7750 (2015).
[Crossref] [PubMed]

Yuste, R.

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

Biomed. Opt. Express (1)

Front. Neural Circuits (3)

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

R. J. Cotton, E. Froudarakis, P. Storer, P. Saggau, and A. S. Tolias, “Three-dimensional mapping of microcircuit correlation structure,” Front. Neural Circuits 7(151), 151 (2013).
[PubMed]

B. M. Kampa, M. M. Roth, W. Göbel, and F. Helmchen, “Representation of visual scenes by local neuronal populations in layer 2/3 of mouse visual cortex,” Front. Neural Circuits 5(18), 18 (2011).
[PubMed]

J. Neurosci. Methods (2)

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]

T. Fernández-Alfonso, K. M. Nadella, M. F. Iacaruso, B. Pichler, H. Roš, P. A. Kirkby, and R. A. Silver, “Monitoring synaptic and neuronal activity in 3D with synthetic and genetic indicators using a compact acousto-optic lens two-photon microscope,” J. Neurosci. Methods 222, 69–81 (2014).
[Crossref] [PubMed]

J. Physiol. (2)

M. Paukert and D. E. Bergles, “Reduction of motion artifacts during in vivo two-photon imaging of brain through heartbeat triggered scanning,” J. Physiol. 590(13), 2955–2963 (2012).
[Crossref] [PubMed]

J. L. Chen, O. A. Pfäffli, F. F. Voigt, D. J. Margolis, and F. Helmchen, “Online correction of licking-induced brain motion during two-photon imaging with a tunable lens,” J. Physiol. 591(19), 4689–4698 (2013).
[Crossref] [PubMed]

Microsc. Res. Tech. (1)

S. Bovetti, C. Moretti, and T. Fellin, “Mapping brain circuit function in vivo using two-photon fluorescence microscopy,” Microsc. Res. Tech. 77(7), 492–501 (2014).
[Crossref] [PubMed]

Nat. Commun. (1)

K. Kirmse, M. Kummer, Y. Kovalchuk, O. W. Witte, O. Garaschuk, and K. Holthoff, “GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo,” Nat. Commun. 6, 7750 (2015).
[Crossref] [PubMed]

Nat. Methods (4)

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

W. Göbel, B. M. Kampa, and F. Helmchen, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
[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]

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]

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]

Neuron (1)

A. M. Kerlin, M. L. Andermann, V. K. Berezovskii, and R. C. Reid, “Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex,” Neuron 67(5), 858–871 (2010).
[Crossref] [PubMed]

Opt. Express (1)

Opt. Lett. (1)

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

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]

M. Ducros, Y. 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]

G. Katona, A. Kaszás, G. F. Turi, N. Hájos, G. Tamás, E. S. Vizi, and B. Rózsa, “Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons,” Proc. Natl. Acad. Sci. U.S.A. 108(5), 2148–2153 (2011).
[Crossref] [PubMed]

Q. Rev. Biophys. (1)

A. Diaspro, G. Chirico, and M. Collini, “Two-photon fluorescence excitation and related techniques in biological microscopy,” Q. Rev. Biophys. 38(2), 97–166 (2005).
[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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Figures (9)

Fig. 1
Fig. 1

Principle of measuring lateral positioning accuracy. (A) Experimental arrangement. Laser focus is dynamically deflected by one of two galvanometers and projected on a reflective grid of lines (distance: 10 ± 0.2 µm). Focus position at a specific time point depends on applied galvanometer command voltage uCx(t) (or uCy(t)). Position feedback signal uFx(t) (or uFy(t)) is continuously measured. Reflected laser beam intensity is simultaneously measured by a PMT and converted into voltage uPMT(t). Inset shows relation between absolute focus position and grid tick marks. (B) Exemplified x-axis measurement. Top: Traces of uCx(t), uFx(t) and uPMT(t). Gray box is scaled up and displayed below. Note that there is a significant phase shift between command signal uC(t) and resulting mirror movement (uF(t)). Peak detection indicates identified reflection maxima in uPMT(t). Absolute positions pRx (or pRy) are calculated by discrete 10 µm distances of detected peaks. Note that calibrated position reverses after a change of galvanometer motion direction (gray highlighted, position 470 µm). Dashed lines indicate zero points (0 V). The dashed dotted line indicates position turning point.

Fig. 2
Fig. 2

Principle of measuring axial positioning accuracy. (A) Experimental arrangement. Absolute position of objective dummy ’20x’ is simultaneously measured via capacitive piezo actuator feedback signal uFz(t) and laser triangulation pRz(t). Dummy position at a specific time point depends on applied command voltage uCz(t). ∆z – dummy elongation induced by the applied command voltage. CMOS – Complementary metal-oxide-semiconductor (resolution: 0.1 µm). µC – Microcontroller. (B) Exemplified measurement. Top: Traces of uCz(t), uFz(t) and pRz(t). Gray box is scaled up and displayed below. Note significant time lag between command and position signals (tFz and tRz). Dashed lines indicate base line levels (0 V).

Fig. 3
Fig. 3

Change of bead intersection length as a measure of three-dimensional scan instability. (A) Three-dimensional projection of z-stack data (maximum intensity projections of z-stack intensities in XY, XZ and YZ plane) and spiral scan trajectory (white dashed line). Positions of intersected fluorescent beads, shown in B, are indicated by numbers (1 – 5). Cube dimensions: 500 × 500 × 200 µm3 (XYZ). (B) Examples of bead intensity profiles at different positions in spiral trajectory, scanned over 10 minutes. 10 pixels ≙ 10 µm. (C) Change of intersection length plotted versus time. The dotted line indicates no detected change. Note that no change in length not necessarily indicates position stability as the intersection of a sphere (bead) is not defined uniquely.

Fig. 4
Fig. 4

Hardware time lag of measured position signals (tRx – x-axis reference, tFx – x-axis feedback, tRy – y-axis reference, tFy – y-axis feedback, tRz – z-axis reference, tFz – z-axis feedback) compared to command signals. (A) Lateral measurements. Data are pooled from sinusoidal movements (amplitude range: 62 – 248 µm, frequency range: 1 – 2000 Hz). x- and y-axis display different lag characteristics (Mann-Whitney U test: tRx – tRy, P < 0.001, n = 11 scan trials). Note additional constant lag between feedback and reference measurements (Wilcoxon signed rank tests: tRx – tFx and tRy – tFy, P < 0.001, n = 11 scan trials). (B) Axial measurements. Data is pooled from sinusoidal movements (command signal amplitude ûCz: 0.625 – 5 V, frequency: 1 – 20 Hz). Note additional constant lag between feedback and reference measurements (two-sided students t-Test: tRz – tFz, P < 0.001, n = 20 scan trials). Each symbol represents lag derived from a single scan trial. *** P < 0.001.

Fig. 5
Fig. 5

Position feedback calibration. Left: Calibration of feedback signals to reference positions (linear fit). Dashed lines indicate ideal fit. Insets: Magnification. Right: Deviations of feedback signals to reference position on the basis of linear fitted values. Dashed lines indicate zero deviation. Dotted lines indicate deviation threshold of ±2.5 µm. (A), (B) Discrete lateral position calibration (A: x-axis, B: y-axis). Each symbol represents a single analyzed discrete tick mark position. Note that data points are overlapping. (C) Continuous axial position calibration (z-axis). Right: Gray points represent single data points. Black curve represents moving average of data points (window size: 250 samples).

Fig. 6
Fig. 6

Positioning accuracy of x-axis scan pattern is smaller than ±2.5 µm. (A) Examples of two different scan trials. Left: Triangular scan, 248 µm scan amplitude, 10 Hz scan frequency. Right: Damped sinusoidal scan, 248 µm scan amplitude, 10 Hz scan frequency. Note that the maximal absolute deviation of each scan trial was used for the threshold criteria in B (indicators 1 and 2). Dashed lines indicate zero deviation. Each symbol represents one analyzed discrete position. (B) Summarized results for each scan type. Each symbol represents maximal absolute deviation of a single scan trial. Numbers 1 and 2 represent examples from A. Note that data points are overlapping. Dotted lines indicate deviation threshold of ±2.5 µm.

Fig. 7
Fig. 7

Positioning accuracy of y-axis scan pattern is smaller than ±2.5 µm. (A) Examples of two different scan trials. Left: Triangular scan, 248 µm scan amplitude, 20 Hz scan frequency. Right: Damped sinusoidal scan, 248 µm scan amplitude, 5 Hz scan frequency. Note that the maximal absolute deviation of each scan trial was used for the threshold criteria in B (indicators 1 and 2). Dashed lines indicate zero deviation. Each symbol represents one analyzed discrete position. (B) Summarized results for each scan type. Each symbol represents maximal absolute deviation of a single scan trial. Numbers 1 and 2 represent examples from A. Note that data points are overlapping. Dotted lines indicate deviation threshold of ±2.5 µm.

Fig. 8
Fig. 8

Axial positioning accuracy depends on scan parameters and objective properties. (A) Position deviations of three single trials at different scan frequencies, but the same scan amplitude of 200 µm sinusoidal motion using regular objective dummy. A hysteresis occurs at a scan frequency of 20 Hz, whereas at 1 Hz and 5 Hz deviations for both motion directions are similar. Dashed lines indicate zero deviation. (B) Maximal absolute deviation of four different objective dummies at different scan amplitudes and frequencies (n = 13 trials). Dotted lines indicate deviation threshold of ±2.5 µm.

Fig. 9
Fig. 9

Maximal absolute deviation of all four objective dummies at 20 Hz scan frequency and 200 µm scan amplitude sinusoidal motion. Each symbol represents a single scan trial. Maximal absolute deviation is dependent on objective mass and length (ANOVA: P < 0.001, n = 13 scan trials, post hoc Bonferroni pairwise comparisons: regular – none: P < 0.001; regular – short: P < 0.001; regular – long: P < 0.001). *** P < 0.001.

Equations (5)

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s C j (t)=sin(ωt+ω t Lag )
t Lag (k)=k t Res
SSE( t Lag )= i=0 N [ s R j (i) s C j (i, t Lag ) ] 2
u F j (i)= β 0 j + β 1 j p R j (i),
d j (i)= β 1 j 1 [ u F j (i) β 0 j ] p R j (i)

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