Abstract

Simultaneous, high-resolution imaging across a large number of synaptic and dendritic sites is critical for understanding how neurons receive and integrate signals. Yet, functional imaging that targets a large number of submicrometer-sized synaptic and dendritic locations poses significant technical challenges. We demonstrate a new parallelized approach to address such questions, increasing the signal-to-noise ratio by an order of magnitude compared to previous approaches. This selective access multifocal multiphoton microscopy uses a spatial light modulator to generate multifocal excitation in three dimensions (3D) and a Gaussian–Laguerre phase plate to simultaneously detect fluorescence from these spots throughout the volume. We test the performance of this system by simultaneously recording Ca2+ dynamics from cultured neurons at 98–118 locations distributed throughout a 3D volume. This is the first demonstration of 3D imaging in a “single shot” and permits synchronized monitoring of signal propagation across multiple different dendrites.

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

Full Article  |  PDF Article
OSA Recommended Articles
Spectral-resolved multifocal multiphoton microscopy with multianode photomultiplier tubes

Jae Won Cha, Dimitrios Tzeranis, Jaichandar Subramanian, Ioannis V. Yannas, Elly Nedivi, and Peter T. C. So
Opt. Express 22(18) 21368-21381 (2014)

Wide-field multiphoton imaging of cellular dynamics in thick tissue by temporal focusing and patterned illumination

O. D. Therrien, B. Aubé, S. Pagès, P. De Koninck, and D. Côté
Biomed. Opt. Express 2(3) 696-704 (2011)

High speed functional imaging with source localized multifocal two-photon microscopy

Peter Quicke, Stephanie Reynolds, Mark Neil, Thomas Knöpfel, Simon R. Schultz, and Amanda J. Foust
Biomed. Opt. Express 9(8) 3678-3693 (2018)

References

  • View by:
  • |
  • |
  • |

  1. M. P. Jadi, B. F. Behabadi, A. Poleg-Polsky, J. Schiller, and B. W. Mel, “An augmented two-layer model captures nonlinear analog spatial integration effects in pyramidal neuron dendrites,” Proc. IEEE 102, 782–798 (2014).
    [Crossref]
  2. G. J. Stuart and N. Spruston, “Dendritic integration: 60 years of progress,” Nat. Neurosci. 18, 1713–1721 (2015).
    [Crossref]
  3. W. Rall, “Core conductor theory and cable properties of neurons,” in Comprehensive Physiology (Wiley, 2011).
  4. R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yáñez, J. DeFelipe, and R. Yuste, “Dendritic size of pyramidal neurons differs among mouse cortical regions,” Cereb. Cortex 16, 990–1001 (2006).
    [Crossref]
  5. J. DeFelipe and I. Fariñas, “The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs,” Prog. Neurobiol. 39, 563–607 (1992).
    [Crossref]
  6. K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50, 823–839 (2006).
    [Crossref]
  7. F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2, 932–940 (2005).
    [Crossref]
  8. W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
    [Crossref]
  9. 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, 713–720 (2008).
    [Crossref]
  10. G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
    [Crossref]
  11. X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475, 501–505 (2011).
    [Crossref]
  12. K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
    [Crossref]
  13. M. Ducros, Y. Goulam Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. USA 110, 13138–13143 (2013).
    [Crossref]
  14. 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, 295–300 (2013).
    [Crossref]
  15. R. Yuste and W. Denk, “Dendritic spines as basic functional units of neuronal integration,” Nature 375, 682–684 (1995).
    [Crossref]
  16. P. T. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-photon excitation fluorescence microscopy,” Annu. Rev. Biomed. Eng. 2, 399–429 (2000).
    [Crossref]
  17. J. Bewersdorf, R. Pick, and S. W. Hell, “Multifocal multiphoton microscopy,” Opt. Lett. 23, 655–657 (1998).
    [Crossref]
  18. K. König, “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104 (2000).
    [Crossref]
  19. K. Bahlmann, P. T. So, M. Kirber, R. Reich, B. Kosicki, W. McGonagle, and K. Bellve, “Multifocal multiphoton microscopy (MMM) at a frame rate beyond 600  hz,” Opt. Express 15, 10991–10998 (2007).
    [Crossref]
  20. G. Zhu, J. van Howe, M. Durst, W. Zipfel, and C. Xu, “Simultaneous spatial and temporal focusing of femtosecond pulses,” Opt. Express 13, 2153–2159 (2005).
    [Crossref]
  21. E. Tal, D. Oron, and Y. Silberberg, “Improved depth resolution in video-rate line-scanning multiphoton microscopy using temporal focusing,” Opt. Lett. 30, 1686–1688 (2005).
    [Crossref]
  22. H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
    [Crossref]
  23. 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, 1021–1028 (2016).
    [Crossref]
  24. W. Yang, J.-E. K. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89, 269–284 (2016).
    [Crossref]
  25. 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, 139–142 (2011).
    [Crossref]
  26. L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
    [Crossref]
  27. R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
    [Crossref]
  28. E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
    [Crossref]
  29. V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
    [Crossref]
  30. J. Rosen and G. Brooker, “Non-scanning motionless fluorescence three-dimensional holographic microscopy,” Nat. Photonics 2, 190–195 (2008).
    [Crossref]
  31. 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]
  32. E. J. Botcherby, R. Juškaitis, and T. Wilson, “Scanning two photon fluorescence microscopy with extended depth of field,” Opt. Commun. 268, 253–260 (2006).
    [Crossref]
  33. 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, 620–628 (2017).
    [Crossref]
  34. H. Ren, H. Lin, X. Li, and M. Gu, “Three-dimensional parallel recording with a Debye diffraction-limited and aberration-free volumetric multifocal array,” Opt. Lett. 39, 1621–1624 (2014).
    [Crossref]
  35. S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
    [Crossref]
  36. L. Feng, T. Zhao, and J. Kim, “neutube 1.0: a new design for efficient neuron reconstruction software based on the SWC format,” eNeuro.2(1) (2015).
    [Crossref]
  37. Y. Xue, K. P. Berry, J. R. Boivin, D. Wadduwage, E. Nedivi, and P. T. C. So, “Scattering reduction by structured light illumination in line-scanning temporal focusing microscopy,” Biomed. Opt. Express 9, 5654–5666 (2018).
    [Crossref]
  38. A. Nagy, J. Wu, and K. M. Berland, “Characterizing observation volumes and the role of excitation saturation in one-photon fluorescence fluctuation spectroscopy,” J. Biomed. Opt. 10, 44015 (2005).
    [Crossref]
  39. B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
    [Crossref]
  40. G. Whyte and J. Courtial, “Experimental demonstration of holographic three-dimensional light shaping using a Gerchberg-Saxton algorithm,” New J. Phys. 7, 117 (2005).
    [Crossref]
  41. D. Débarre, E. J. Botcherby, T. Watanabe, S. Srinivas, M. J. Booth, and T. Wilson, “Image-based adaptive optics for two-photon microscopy,” Opt. Lett. 34, 2495–2497 (2009).
    [Crossref]

2018 (1)

2017 (2)

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, 620–628 (2017).
[Crossref]

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

2016 (3)

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, 1021–1028 (2016).
[Crossref]

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

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

2015 (1)

G. J. Stuart and N. Spruston, “Dendritic integration: 60 years of progress,” Nat. Neurosci. 18, 1713–1721 (2015).
[Crossref]

2014 (5)

M. P. Jadi, B. F. Behabadi, A. Poleg-Polsky, J. Schiller, and B. W. Mel, “An augmented two-layer model captures nonlinear analog spatial integration effects in pyramidal neuron dendrites,” Proc. IEEE 102, 782–798 (2014).
[Crossref]

H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
[Crossref]

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

H. Ren, H. Lin, X. Li, and M. Gu, “Three-dimensional parallel recording with a Debye diffraction-limited and aberration-free volumetric multifocal array,” Opt. Lett. 39, 1621–1624 (2014).
[Crossref]

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]

2013 (2)

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

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, 295–300 (2013).
[Crossref]

2012 (1)

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

2011 (2)

X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475, 501–505 (2011).
[Crossref]

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, 139–142 (2011).
[Crossref]

2010 (1)

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

2009 (2)

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

D. Débarre, E. J. Botcherby, T. Watanabe, S. Srinivas, M. J. Booth, and T. Wilson, “Image-based adaptive optics for two-photon microscopy,” Opt. Lett. 34, 2495–2497 (2009).
[Crossref]

2008 (3)

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
[Crossref]

J. Rosen and G. Brooker, “Non-scanning motionless fluorescence three-dimensional holographic microscopy,” Nat. Photonics 2, 190–195 (2008).
[Crossref]

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, 713–720 (2008).
[Crossref]

2007 (1)

2006 (3)

R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yáñez, J. DeFelipe, and R. Yuste, “Dendritic size of pyramidal neurons differs among mouse cortical regions,” Cereb. Cortex 16, 990–1001 (2006).
[Crossref]

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50, 823–839 (2006).
[Crossref]

E. J. Botcherby, R. Juškaitis, and T. Wilson, “Scanning two photon fluorescence microscopy with extended depth of field,” Opt. Commun. 268, 253–260 (2006).
[Crossref]

2005 (5)

G. Whyte and J. Courtial, “Experimental demonstration of holographic three-dimensional light shaping using a Gerchberg-Saxton algorithm,” New J. Phys. 7, 117 (2005).
[Crossref]

A. Nagy, J. Wu, and K. M. Berland, “Characterizing observation volumes and the role of excitation saturation in one-photon fluorescence fluctuation spectroscopy,” J. Biomed. Opt. 10, 44015 (2005).
[Crossref]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2, 932–940 (2005).
[Crossref]

G. Zhu, J. van Howe, M. Durst, W. Zipfel, and C. Xu, “Simultaneous spatial and temporal focusing of femtosecond pulses,” Opt. Express 13, 2153–2159 (2005).
[Crossref]

E. Tal, D. Oron, and Y. Silberberg, “Improved depth resolution in video-rate line-scanning multiphoton microscopy using temporal focusing,” Opt. Lett. 30, 1686–1688 (2005).
[Crossref]

2004 (1)

B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
[Crossref]

2000 (2)

K. König, “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104 (2000).
[Crossref]

P. T. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-photon excitation fluorescence microscopy,” Annu. Rev. Biomed. Eng. 2, 399–429 (2000).
[Crossref]

1998 (1)

1995 (1)

R. Yuste and W. Denk, “Dendritic spines as basic functional units of neuronal integration,” Nature 375, 682–684 (1995).
[Crossref]

1994 (1)

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
[Crossref]

1992 (1)

J. DeFelipe and I. Fariñas, “The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs,” Prog. Neurobiol. 39, 563–607 (1992).
[Crossref]

Anselmi, F.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

Araya, R.

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
[Crossref]

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, 139–142 (2011).
[Crossref]

Bahlmann, K.

Bai, L.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

Ballesteros-Yáñez, I.

R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yáñez, J. DeFelipe, and R. Yuste, “Dendritic size of pyramidal neurons differs among mouse cortical regions,” Cereb. Cortex 16, 990–1001 (2006).
[Crossref]

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, 1021–1028 (2016).
[Crossref]

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, 295–300 (2013).
[Crossref]

Baragli, C.

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

Barry, N.

B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
[Crossref]

Bègue, A.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

Behabadi, B. F.

M. P. Jadi, B. F. Behabadi, A. Poleg-Polsky, J. Schiller, and B. W. Mel, “An augmented two-layer model captures nonlinear analog spatial integration effects in pyramidal neuron dendrites,” Proc. IEEE 102, 782–798 (2014).
[Crossref]

Bellve, K.

Benavides-Piccione, R.

R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yáñez, J. DeFelipe, and R. Yuste, “Dendritic size of pyramidal neurons differs among mouse cortical regions,” Cereb. Cortex 16, 990–1001 (2006).
[Crossref]

Berland, K. M.

A. Nagy, J. Wu, and K. M. Berland, “Characterizing observation volumes and the role of excitation saturation in one-photon fluorescence fluctuation spectroscopy,” J. Biomed. Opt. 10, 44015 (2005).
[Crossref]

P. T. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-photon excitation fluorescence microscopy,” Annu. Rev. Biomed. Eng. 2, 399–429 (2000).
[Crossref]

Berry, K. P.

Bewersdorf, J.

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, 620–628 (2017).
[Crossref]

Biteen, J. S.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Boivin, J. R.

Booth, M. J.

Botcherby, E. J.

D. Débarre, E. J. Botcherby, T. Watanabe, S. Srinivas, M. J. Booth, and T. Wilson, “Image-based adaptive optics for two-photon microscopy,” Opt. Lett. 34, 2495–2497 (2009).
[Crossref]

E. J. Botcherby, R. Juškaitis, and T. Wilson, “Scanning two photon fluorescence microscopy with extended depth of field,” Opt. Commun. 268, 253–260 (2006).
[Crossref]

Boyden, E. S.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Bradley, J.

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

Brooker, G.

J. Rosen and G. Brooker, “Non-scanning motionless fluorescence three-dimensional holographic microscopy,” Nat. Photonics 2, 190–195 (2008).
[Crossref]

Brosh, I.

H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
[Crossref]

Buehler, C.

B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
[Crossref]

Carrillo-Reid, L.

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

Chai, Y.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

Charpak, S.

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

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, 295–300 (2013).
[Crossref]

Chen, X.

X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475, 501–505 (2011).
[Crossref]

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, 139–142 (2011).
[Crossref]

Chiovini, B.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

Cong, L.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

Courtial, J.

G. Whyte and J. Courtial, “Experimental demonstration of holographic three-dimensional light shaping using a Gerchberg-Saxton algorithm,” New J. Phys. 7, 117 (2005).
[Crossref]

Dana, H.

H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
[Crossref]

de Sars, V.

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

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

Débarre, D.

DeFelipe, J.

R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yáñez, J. DeFelipe, and R. Yuste, “Dendritic size of pyramidal neurons differs among mouse cortical regions,” Cereb. Cortex 16, 990–1001 (2006).
[Crossref]

J. DeFelipe and I. Fariñas, “The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs,” Prog. Neurobiol. 39, 563–607 (1992).
[Crossref]

Delaney, K. R.

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
[Crossref]

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, 1021–1028 (2016).
[Crossref]

Denk, W.

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2, 932–940 (2005).
[Crossref]

R. Yuste and W. Denk, “Dendritic spines as basic functional units of neuronal integration,” Nature 375, 682–684 (1995).
[Crossref]

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
[Crossref]

Dong, C. Y.

P. T. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-photon excitation fluorescence microscopy,” Annu. Rev. Biomed. Eng. 2, 399–429 (2000).
[Crossref]

Du, J.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

Ducros, M.

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

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, 713–720 (2008).
[Crossref]

Durst, M.

Dvorkin, R.

H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
[Crossref]

Emiliani, V.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

Evans, G. J.

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

Fariñas, I.

J. DeFelipe and I. Fariñas, “The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs,” Prog. Neurobiol. 39, 563–607 (1992).
[Crossref]

Feng, L.

L. Feng, T. Zhao, and J. Kim, “neutube 1.0: a new design for efficient neuron reconstruction software based on the SWC format,” eNeuro.2(1) (2015).
[Crossref]

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, 1021–1028 (2016).
[Crossref]

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, 713–720 (2008).
[Crossref]

Fitzpatrick, D.

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, 620–628 (2017).
[Crossref]

Gelperin, A.

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
[Crossref]

Glückstad, J.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

Golshani, P.

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, 1021–1028 (2016).
[Crossref]

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, 139–142 (2011).
[Crossref]

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, 139–142 (2011).
[Crossref]

Goulam Houssen, Y.

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

Gratton, E.

B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
[Crossref]

Griffiths, V. A.

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

Gu, M.

Hamzei-Sichani, F.

R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yáñez, J. DeFelipe, and R. Yuste, “Dendritic size of pyramidal neurons differs among mouse cortical regions,” Cereb. Cortex 16, 990–1001 (2006).
[Crossref]

Hang, W.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

Hell, S. W.

Helmchen, F.

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2, 932–940 (2005).
[Crossref]

Hillier, D.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

Hoffmann, M.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Huang, B. S.

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, 1021–1028 (2016).
[Crossref]

Isacoff, E. Y.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

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).
[Crossref]

Jadi, M. P.

M. P. Jadi, B. F. Behabadi, A. Poleg-Polsky, J. Schiller, and B. W. Mel, “An augmented two-layer model captures nonlinear analog spatial integration effects in pyramidal neuron dendrites,” Proc. IEEE 102, 782–798 (2014).
[Crossref]

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, 295–300 (2013).
[Crossref]

Ji, N.

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, 620–628 (2017).
[Crossref]

Juškaitis, R.

E. J. Botcherby, R. Juškaitis, and T. Wilson, “Scanning two photon fluorescence microscopy with extended depth of field,” Opt. Commun. 268, 253–260 (2006).
[Crossref]

Kaszás, A.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

Kato, S.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Katona, G.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

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, 713–720 (2008).
[Crossref]

Kerlin, A.

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

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, 295–300 (2013).
[Crossref]

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, 295–300 (2013).
[Crossref]

Kim, J.

L. Feng, T. Zhao, and J. Kim, “neutube 1.0: a new design for efficient neuron reconstruction software based on the SWC format,” eNeuro.2(1) (2015).
[Crossref]

Kirber, M.

Kirkby, P. A.

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

Kleinfeld, D.

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
[Crossref]

Koimtzis, T.

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

König, K.

K. König, “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104 (2000).
[Crossref]

Konnerth, A.

X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475, 501–505 (2011).
[Crossref]

Konstantinou, G.

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

Kosicki, B.

Koyama, 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, 620–628 (2017).
[Crossref]

Leischner, U.

X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475, 501–505 (2011).
[Crossref]

Li, X.

Liang, Y.

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, 620–628 (2017).
[Crossref]

Lin, H.

Liu, N.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

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, 295–300 (2013).
[Crossref]

Lord, S. J.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Lu, R.

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, 620–628 (2017).
[Crossref]

Maák, P.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

Mantulin, W. W.

B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
[Crossref]

Marom, A.

H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
[Crossref]

Masters, B. R.

B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
[Crossref]

P. T. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-photon excitation fluorescence microscopy,” Annu. Rev. Biomed. Eng. 2, 399–429 (2000).
[Crossref]

McGonagle, W.

Mel, B. W.

M. P. Jadi, B. F. Behabadi, A. Poleg-Polsky, J. Schiller, and B. W. Mel, “An augmented two-layer model captures nonlinear analog spatial integration effects in pyramidal neuron dendrites,” Proc. IEEE 102, 782–798 (2014).
[Crossref]

Miller, J.-E. K.

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

Moerner, W. E.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Mohar, B.

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

Nadella, K. M. N. S.

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

Nagy, A.

A. Nagy, J. Wu, and K. M. Berland, “Characterizing observation volumes and the role of excitation saturation in one-photon fluorescence fluctuation spectroscopy,” J. Biomed. Opt. 10, 44015 (2005).
[Crossref]

Nedivi, E.

Nelken, I.

X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475, 501–505 (2011).
[Crossref]

Nikolenko, V.

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
[Crossref]

Nöbauer, T.

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, 1021–1028 (2016).
[Crossref]

Orger, M. B.

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

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, 295–300 (2013).
[Crossref]

Oron, D.

Pak, N.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Paluch, S.

H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
[Crossref]

Paninski, L.

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

Papagiakoumou, E.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

Pavani, S. R. P.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Pernía-Andrade, A. J.

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, 1021–1028 (2016).
[Crossref]

Peterka, D. S.

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

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]

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
[Crossref]

Pick, R.

Piestun, R.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Pnevmatikakis, E.

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

Poleg-Polsky, A.

M. P. Jadi, B. F. Behabadi, A. Poleg-Polsky, J. Schiller, and B. W. Mel, “An augmented two-layer model captures nonlinear analog spatial integration effects in pyramidal neuron dendrites,” Proc. IEEE 102, 782–798 (2014).
[Crossref]

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, 139–142 (2011).
[Crossref]

Prevedel, R.

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, 1021–1028 (2016).
[Crossref]

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

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, 295–300 (2013).
[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]

Rall, W.

W. Rall, “Core conductor theory and cable properties of neurons,” in Comprehensive Physiology (Wiley, 2011).

Raskar, R.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Reich, R.

Ren, H.

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, 295–300 (2013).
[Crossref]

Rochefort, N. L.

X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475, 501–505 (2011).
[Crossref]

Roš, H.

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

Rosen, J.

J. Rosen and G. Brooker, “Non-scanning motionless fluorescence three-dimensional holographic microscopy,” Nat. Photonics 2, 190–195 (2008).
[Crossref]

Roska, B.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

Rózsa, B.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

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, 713–720 (2008).
[Crossref]

Schiller, J.

M. P. Jadi, B. F. Behabadi, A. Poleg-Polsky, J. Schiller, and B. W. Mel, “An augmented two-layer model captures nonlinear analog spatial integration effects in pyramidal neuron dendrites,” Proc. IEEE 102, 782–798 (2014).
[Crossref]

Scholl, B.

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

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, 295–300 (2013).
[Crossref]

Schrödel, T.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Seelig, J. D.

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, 620–628 (2017).
[Crossref]

Shang, C.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

Shoham, S.

H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
[Crossref]

Silberberg, Y.

Silver, R. A.

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

So, P. T.

K. Bahlmann, P. T. So, M. Kirber, R. Reich, B. Kosicki, W. McGonagle, and K. Bellve, “Multifocal multiphoton microscopy (MMM) at a frame rate beyond 600  hz,” Opt. Express 15, 10991–10998 (2007).
[Crossref]

P. T. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-photon excitation fluorescence microscopy,” Annu. Rev. Biomed. Eng. 2, 399–429 (2000).
[Crossref]

So, P. T. C.

Y. Xue, K. P. Berry, J. R. Boivin, D. Wadduwage, E. Nedivi, and P. T. C. So, “Scattering reduction by structured light illumination in line-scanning temporal focusing microscopy,” Biomed. Opt. Express 9, 5654–5666 (2018).
[Crossref]

B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
[Crossref]

Spruston, N.

G. J. Stuart and N. Spruston, “Dendritic integration: 60 years of progress,” Nat. Neurosci. 18, 1713–1721 (2015).
[Crossref]

Srinivas, S.

Strowbridge, B. W.

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
[Crossref]

Stuart, G. J.

G. J. Stuart and N. Spruston, “Dendritic integration: 60 years of progress,” Nat. Neurosci. 18, 1713–1721 (2015).
[Crossref]

Sun, W.

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, 620–628 (2017).
[Crossref]

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, 295–300 (2013).
[Crossref]

Sutin, J. D.

B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
[Crossref]

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, 295–300 (2013).
[Crossref]

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50, 823–839 (2006).
[Crossref]

Sylvester Vizi, E.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

Szalay, G.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

Tal, E.

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, 620–628 (2017).
[Crossref]

Tank, D. W.

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
[Crossref]

Thompson, M. A.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Twieg, R. J.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

van Howe, J.

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, 1021–1028 (2016).
[Crossref]

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Veress, M.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

Verhoef, A. J.

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, 1021–1028 (2016).
[Crossref]

Wadduwage, D.

Wang, K.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

Wang, Z.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

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, 295–300 (2013).
[Crossref]

Watanabe, T.

Watson, B. O.

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
[Crossref]

Weisenburger, S.

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, 1021–1028 (2016).
[Crossref]

Wen, Q.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

Wetzstein, G.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Whyte, G.

G. Whyte and J. Courtial, “Experimental demonstration of holographic three-dimensional light shaping using a Gerchberg-Saxton algorithm,” New J. Phys. 7, 117 (2005).
[Crossref]

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, 620–628 (2017).
[Crossref]

Wilson, T.

D. Débarre, E. J. Botcherby, T. Watanabe, S. Srinivas, M. J. Booth, and T. Wilson, “Image-based adaptive optics for two-photon microscopy,” Opt. Lett. 34, 2495–2497 (2009).
[Crossref]

E. J. Botcherby, R. Juškaitis, and T. Wilson, “Scanning two photon fluorescence microscopy with extended depth of field,” Opt. Commun. 268, 253–260 (2006).
[Crossref]

Woodruff, A.

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
[Crossref]

Wu, J.

A. Nagy, J. Wu, and K. M. Berland, “Characterizing observation volumes and the role of excitation saturation in one-photon fluorescence fluctuation spectroscopy,” J. Biomed. Opt. 10, 44015 (2005).
[Crossref]

Xu, C.

Xue, Y.

Yang, W.

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

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

Yasuda, R.

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50, 823–839 (2006).
[Crossref]

Yoon, Y.-G.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Yuste, R.

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

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]

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
[Crossref]

R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yáñez, J. DeFelipe, and R. Yuste, “Dendritic size of pyramidal neurons differs among mouse cortical regions,” Cereb. Cortex 16, 990–1001 (2006).
[Crossref]

R. Yuste and W. Denk, “Dendritic spines as basic functional units of neuronal integration,” Nature 375, 682–684 (1995).
[Crossref]

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
[Crossref]

Zhao, T.

L. Feng, T. Zhao, and J. Kim, “neutube 1.0: a new design for efficient neuron reconstruction software based on the SWC format,” eNeuro.2(1) (2015).
[Crossref]

Zhu, G.

Zimmer, M.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

Zipfel, W.

Annu. Rev. Biomed. Eng. (1)

P. T. So, C. Y. Dong, B. R. Masters, and K. M. Berland, “Two-photon excitation fluorescence microscopy,” Annu. Rev. Biomed. Eng. 2, 399–429 (2000).
[Crossref]

Biomed. Opt. Express (1)

Cereb. Cortex (1)

R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yáñez, J. DeFelipe, and R. Yuste, “Dendritic size of pyramidal neurons differs among mouse cortical regions,” Cereb. Cortex 16, 990–1001 (2006).
[Crossref]

Elife (1)

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (danio rerio),” Elife 6, e28158 (2017).
[Crossref]

Front. Neural Circuits (2)

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
[Crossref]

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]

J. Biomed. Opt. (2)

A. Nagy, J. Wu, and K. M. Berland, “Characterizing observation volumes and the role of excitation saturation in one-photon fluorescence fluctuation spectroscopy,” J. Biomed. Opt. 10, 44015 (2005).
[Crossref]

B. R. Masters, P. T. C. So, C. Buehler, N. Barry, J. D. Sutin, W. W. Mantulin, and E. Gratton, “Mitigating thermal mechanical damage potential during two-photon dermal imaging,” J. Biomed. Opt. 9, 1265–1270 (2004).
[Crossref]

J. Microsc. (1)

K. König, “Multiphoton microscopy in life sciences,” J. Microsc. 200, 83–104 (2000).
[Crossref]

J. Neurosci. Methods (1)

W. Denk, K. R. Delaney, A. Gelperin, D. Kleinfeld, B. W. Strowbridge, D. W. Tank, and R. Yuste, “Anatomical and functional imaging of neurons using 2-photon laser scanning microscopy,” J. Neurosci. Methods 54, 151–162 (1994).
[Crossref]

Nat. Commun. (1)

H. Dana, A. Marom, S. Paluch, R. Dvorkin, I. Brosh, and S. Shoham, “Hybrid multiphoton volumetric functional imaging of large-scale bioengineered neuronal networks,” Nat. Commun. 5, 3997 (2014).
[Crossref]

Nat. Methods (7)

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, 1021–1028 (2016).
[Crossref]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2, 932–940 (2005).
[Crossref]

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, 139–142 (2011).
[Crossref]

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11, 727–730 (2014).
[Crossref]

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. Sylvester 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, 201–208 (2012).
[Crossref]

K. M. N. S. Nadella, H. Roš, C. Baragli, V. A. Griffiths, G. Konstantinou, T. Koimtzis, G. J. Evans, P. A. Kirkby, and R. A. Silver, “Random-access scanning microscopy for 3D imaging in awake behaving animals,” Nat. Methods 13, 1001–1004 (2016).
[Crossref]

Nat. Neurosci. (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, 713–720 (2008).
[Crossref]

G. J. Stuart and N. Spruston, “Dendritic integration: 60 years of progress,” Nat. Neurosci. 18, 1713–1721 (2015).
[Crossref]

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, 620–628 (2017).
[Crossref]

Nat. Photonics (1)

J. Rosen and G. Brooker, “Non-scanning motionless fluorescence three-dimensional holographic microscopy,” Nat. Photonics 2, 190–195 (2008).
[Crossref]

Nature (3)

X. Chen, U. Leischner, N. L. Rochefort, I. Nelken, and A. Konnerth, “Functional mapping of single spines in cortical neurons in vivo,” Nature 475, 501–505 (2011).
[Crossref]

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, 295–300 (2013).
[Crossref]

R. Yuste and W. Denk, “Dendritic spines as basic functional units of neuronal integration,” Nature 375, 682–684 (1995).
[Crossref]

Neuron (2)

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50, 823–839 (2006).
[Crossref]

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

New J. Phys. (1)

G. Whyte and J. Courtial, “Experimental demonstration of holographic three-dimensional light shaping using a Gerchberg-Saxton algorithm,” New J. Phys. 7, 117 (2005).
[Crossref]

Opt. Commun. (1)

E. J. Botcherby, R. Juškaitis, and T. Wilson, “Scanning two photon fluorescence microscopy with extended depth of field,” Opt. Commun. 268, 253–260 (2006).
[Crossref]

Opt. Express (2)

Opt. Lett. (4)

Proc. IEEE (1)

M. P. Jadi, B. F. Behabadi, A. Poleg-Polsky, J. Schiller, and B. W. Mel, “An augmented two-layer model captures nonlinear analog spatial integration effects in pyramidal neuron dendrites,” Proc. IEEE 102, 782–798 (2014).
[Crossref]

Proc. Natl. Acad. Sci. USA (2)

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

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. USA 106, 2995–2999 (2009).
[Crossref]

Prog. Neurobiol. (1)

J. DeFelipe and I. Fariñas, “The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs,” Prog. Neurobiol. 39, 563–607 (1992).
[Crossref]

Other (2)

W. Rall, “Core conductor theory and cable properties of neurons,” in Comprehensive Physiology (Wiley, 2011).

L. Feng, T. Zhao, and J. Kim, “neutube 1.0: a new design for efficient neuron reconstruction software based on the SWC format,” eNeuro.2(1) (2015).
[Crossref]

Supplementary Material (1)

NameDescription
» Supplement 1       Supplemental document

Cited By

OSA participates in Crossref's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.


Figures (4)

Fig. 1.
Fig. 1. Outline of experimental flow for saMMM and comparison with other methods. (a) Comparison of similar state-of-the-art methods. (a1) Outline of RAS; (a2) outline of Bessel beam or big Gaussian spot scanning; (a3) outline of saMMM, emphasizing the differences from (a1) and (a2); (b) experimental flow of saMMM; (b1) neuronal structure z stack is first captured using line-scan TF; (b2) manual or automated structural tracing is used to compute the SLM phase mask for targeting the ROI by calculating the 3D phase on an Ewald sphere using the Gerchberg–Saxton algorithm and projecting it onto 2D phase mask. (b3) 3D simultaneous excitation; (b4) 3D simultaneous detection within the DoF; GL phase plate elongates the DoF compared to Gaussian PSF. (b5) Camera captures one image per plane; without GL phase plate, only spots in focus are clearly detected, with out-of-focus locations appearing as blurs (DoF 1.8μm); with GL phase plate, all spots in the slab (DoF 15μm) are detected.
Fig. 2.
Fig. 2. saMMM setup (with additional line-scan TF multiphoton microscopy) and GL phase plate modulated PSF. (a) System diagram. L1, L2, to collimate beam; HWP, half-wave plate; PBS, polarizing beam splitter; SLM, spatial light modulator; SM, scan mirror; CL, cylindrical lens; DM, dichroic mirror; L4, L5, tube lenses; GL, Gaussian–Laguerre phase plate; L6, L7, relay lenses to generate Fourier plane for GL phase plate; (b) image of a fluorescent nanoparticle (FluoSphere carboxylate, 0.04 μm, yellow-green (505/515), Life Technologies, California) viewed in 3D volume. Scale bar, 5 μm. (c) Double helix PSF modulated by the GL phase plate [measured with a fluorescent nanoparticle, same as (b)], where each small image on the right side shows the cross section at the corresponding white dashed line position on the left 3D PSF. The distance between each dashed line is about 3 μm. Scale bar, 5 μm. The intensity is normalized so that the color scale of each image is [0,1], corresponding to the gray scale. (d) Axial Gaussian PSF of the system is about 1.1 μm. (e) Lateral Gaussian PSF of the system is about 0.43 μm. (f) Total intensity of GL PSF (red) and Gaussian PSF (blue) along z axis. (summing area: 16×16μm in each z position); (g) total intensity ratio between GL PSF and Gaussian PSF along z axis; (h) encoding relation between axial difference and rotation angle (°) of GL PSF.
Fig. 3.
Fig. 3. Monitoring spontaneous Ca2+ dynamics from 113 foci “at once” on cultured neurons expressing jRGECO1 using 2D saMMM. (a) Superposition of line-scan TF structural image (magenta) with saMMM functional image (green). Scale bar, 50 μm. (b) The ΔF/F traces of every other spot on the three branches shown in (a), sorted by their distances to the soma. The ΔF/F of each dendrite is normalized to the global maximum.
Fig. 4.
Fig. 4. Monitoring spontaneous Ca2+ dynamics from around one hundred GL spots in 3D simultaneously. (a) Overlay of line-scan TF in focus image with the 3D targeted foci on a single plane. The foci are effectively in different planes of the line-scan TF in focus plane. (a1), (a2) 98 Gaussian and GL spots at ΔZ=0; (a3), (a4) 118 Gaussian and GL foci at ΔZ=3μm; and (a5), (a6) 99 Gaussian and GL foci at ΔZ=6μm. Scale bar, 50 μm. (b) Ca2+ activities from representative saMMM targeted foci; figure number corresponding to the figure number in (a). The ΔF/F traces are from foci pointed by the yellow arrows in (a). Blue line is calcium signal from the Gaussian spot, and red line is from the GL spot; (c) SNR comparison of ΔF/F traces between Gaussian foci and GL foci in different axial planes corresponding to (a).

Tables (1)

Tables Icon

Table 1. Comparison of saMMM with Other Methods