Abstract

We report a novel two-photon fluorescence microscope based on a fast-switching liquid crystal spatial light modulator and a pair of galvo-resonant scanners for large-scale recording of neural activity from the mammalian brain. The spatial light modulator is used to achieve fast switching between different imaging planes in multi-plane imaging and correct for intrinsic optical aberrations associated with this imaging scheme. The utilized imaging technique is capable of monitoring the neural activity from large populations of neurons with known coordinates spread across different layers of the neocortex in awake and behaving mice, regardless of the fluorescent labeling strategy. During each imaging session, all visual stimulus driven somatic activity could be recorded in the same behavior state. We observed heterogeneous response to different types of visual stimuli from $\sim$ 3,300 excitatory neurons reaching from layer II/III to V of the striate cortex.

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

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2019 (1)

S. Weisenburger, F. Tejera, J. Demas, B. Chen, J. Manley, F. T. Sparks, F. M. Traub, T. Daigle, H. Zeng, A. Losonczy, and A. Vaziri, “Volumetric ca2+ imaging in the mouse brain using hybrid multiplexed sculpted light microscopy,” Cell 177(4), 1050–1066.e14 (2019).
[Crossref]

2018 (2)

S. Weisenburger and A. Vaziri, “A guide to emerging technologies for large-scale and whole-brain optical imaging of neuronal activity,” Annu. Rev. Neurosci. 41(1), 431–452 (2018).
[Crossref]

S. E. de Vries, J. Lecoq, M. A. Buice, P. A. Groblewski, G. K. Ocker, M. Oliver, D. Feng, N. Cain, P. Ledochowitsch, and D. Millman, “A large-scale, standardized physiological survey reveals higher order coding throughout the mouse visual cortex,” bioRxiv 2, 359513 (2018).
[Crossref]

2017 (7)

W. J. Shain, N. A. Vickers, B. B. Goldberg, T. Bifano, and J. Mertz, “Extended depth-of-field microscopy with a high-speed deformable mirror,” Opt. Lett. 42(5), 995–998 (2017).
[Crossref]

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

W. Zong, R. Wu, M. Li, Y. Hu, Y. Li, J. Li, H. Rong, H. Wu, Y. Xu, Y. Lu, H. Jia, M. Fan, Z. Zhou, Y. Zhang, A. Wang, L. Chen, and H. Cheng, “Fast high-resolution miniature two-photon microscopy for brain imaging in freely behaving mice,” Nat. Methods 14(7), 713–719 (2017).
[Crossref]

M. Li, F. Liu, H. Jiang, T. S. Lee, and S. Tang, “Long-term two-photon imaging in awake macaque monkey,” Neuron 93(5), 1049–1057.e3 (2017).
[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. Orger, and J. Na, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20(4), 620–628 (2017).
[Crossref]

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of gcamp6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[Crossref]

J.-H. Park, L. Kong, Y. Zhou, and M. Cui, “Large-field-of-view imaging by multi-pupil adaptive optics,” Nat. Methods 14(6), 581–583 (2017).
[Crossref]

2016 (8)

E. A. Pnevmatikakis, D. Soudry, Y. Gao, T. A. Machado, J. Merel, D. Pfau, T. Reardon, Y. Mu, C. Lacefield, W. Yang, M. Ahrens, R. Bruno, T. Jessell, D. Peterka, R. Yuste, and L. Paninski, “Simultaneous denoising, deconvolution, and demixing of calcium imaging data,” Neuron 89(2), 285–299 (2016).
[Crossref]

M. Hawrylycz, C. Anastassiou, A. Arkhipov, J. Berg, M. Buice, N. Cain, N. W. Gouwens, S. Gratiy, R. Iyer, J. H. Lee, and M. team, “Inferring cortical function in the mouse visual system through large-scale systems neuroscience,” Proc. Natl. Acad. Sci. 113(27), 7337–7344 (2016).
[Crossref]

J. P. Nguyen, F. B. Shipley, A. N. Linder, G. S. Plummer, M. Liu, S. U. Setru, J. W. Shaevitz, and A. M. Leifer, “Whole-brain calcium imaging with cellular resolution in freely behaving caenorhabditis elegans,” Proc. Natl. Acad. Sci. 113(8), E1074–E1081 (2016).
[Crossref]

W.-C. A. Lee, V. Bonin, M. Reed, B. J. Graham, G. Hood, K. Glattfelder, and R. C. Reid, “Anatomy and function of an excitatory network in the visual cortex,” Nature 532(7599), 370–374 (2016).
[Crossref]

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

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

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(2), 269–284 (2016).
[Crossref]

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

2015 (5)

C. M. Niell, “Cell types, circuits, and receptive fields in the mouse visual cortex,” Annu. Rev. Neurosci. 38(1), 413–431 (2015).
[Crossref]

W. C. Lemon, S. R. Pulver, B. Höckendorf, K. McDole, K. Branson, J. Freeman, and P. J. Keller, “Whole-central nervous system functional imaging in larval drosophila,” Nat. Commun. 6(1), 7924 (2015).
[Crossref]

L. Madisen, A. R. Garner, D. Shimaoka, A. S. Chuong, N. C. Klapoetke, L. Li, A. van der Bourg, Y. Niino, L. Egolf, C. Monetti, H. Gu, M. Mills, A. Cheng, T. Tasic Bosiljka, T. Ngugen, S. Sunkin, A. Benucci, A. Nagy, M. Atsushi, F. Helmchen, R. Empson, T. Knopfel, E. Boyden, C. Reid, M. Carandini, and H. Zeng, “Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance,” Neuron 85(5), 942–958 (2015).
[Crossref]

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

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. Hillman, “Swept confocally-aligned planar excitation (scape) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

2014 (2)

R. Liu, D. E. Milkie, A. Kerlin, B. MacLennan, and N. Ji, “Direct phase measurement in zonal wavefront reconstruction using multidither coherent optical adaptive technique,” Opt. Express 22(2), 1619–1628 (2014).
[Crossref]

C. Wang, R. Liu, D. E. Milkie, W. Sun, Z. Tan, A. Kerlin, T.-W. Chen, D. S. Kim, and N. Ji, “Multiplexed aberration measurement for deep tissue imaging in vivo,” Nat. Methods 11(10), 1037–1040 (2014).
[Crossref]

2013 (4)

G. Thalhammer, R. W. Bowman, G. D. Love, M. J. Padgett, and M. Ritsch-Marte, “Speeding up liquid crystal slms using overdrive with phase change reduction,” Opt. Express 21(2), 1779–1797 (2013).
[Crossref]

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[Crossref]

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,” The J. physiology 591(19), 4689–4698 (2013).
[Crossref]

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
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2012 (2)

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Supplementary Material (4)

NameDescription
» Visualization 1       Image stack of neuronal structures in a living mouse brain (Nr5a1-Cre-Ai14 line) from an imaging depth of 193 $\mu$m to 241 $\mu$m with a separation of 1 $\mu$m.
» Visualization 2       Calcium imaging movie from 6 different imaging planes spread from 250 um to 500 um, with a separation of 50 um between planes
» Visualization 3       Calcium imaging movie from 2 different axial imaging planes with a separation of 204 um between the planes
» Visualization 4       Calcium imaging movie from 5 imaging planes arranged close to each other, with a separation of 24 um between planes

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Figures (14)

Fig. 1.
Fig. 1. (a) Schematic diagram of our microscope system. M, mirror; L1$-$L10, lens; SLM: liquid crystal spatial light modulator; Dichr: dichroic mirror; Obj: microscope objective; PMT: photomultiplier; S: Sample; X resonant: resonant scanner in x direction; X, Y galvo: galvo scanner in x, y direction. (b) 3D CAD model for the microscope design. (c) Experimental setup for our multi-plane imaging system
Fig. 2.
Fig. 2. (a) FWHM of the axial profile of z stack images of 2 $\mu$m fluorescent beads does not degrade significantly over an axial range of 400 $\mu$ms with an effective excitation NA of 0.45. (b) Axial profile of z stack images of 2 $\mu$m fluorescent beads with different axial shifts using the SLM defocusing mechanism with an effective excitation NA of 0.65. Upper: with adaptive optics; Bottom: without adaptive optics. Scale bar: 3 $\mu$m. (c) Axial signal profile at different focal plane of 23 $\mu$m; 46 $\mu$m; -23 $\mu$m; -46 $\mu$m. (d) Axial shifts of focal planes from its nominal position are practically linear with the Zernike defocus coefficients with an effective excitation NA of 0.45.
Fig. 3.
Fig. 3. Image stack of neuronal structures in a living mouse brain (Nr5a1-Cre-Ai14 line) from an imaging depth of 193 $\mu$m to 241 $\mu$m with a separation of 6 $\mu$m. See Visualization 1 for the same imaging stack with a separation of 1 $\mu$m. Scale bar: 100 $\mu$m
Fig. 4.
Fig. 4. (a) Multi-plane imaging of 6 planes separated by 50 $\mu$m each; (b) Multiplane imaging of two axial planes separated by 204 $\mu$m (c) Volumetric imaging of 5 imaging planes separated by 23 $\mu$m each. The neural circuit diagram is adapted from [10]
Fig. 5.
Fig. 5. (a) Maximum intensity projection of the calcium imaging movie at different depths of 500 $\mu$m, 450 $\mu$m, 400 $\mu$m, 350 $\mu$m, 300 $\mu$m, and 250 $\mu$m, with an effective excitation NA of 0.45 (see Visualization 2); (b) Segmented somata identified by Suite2P at different depths. Scale bar: 50 $\mu$m
Fig. 6.
Fig. 6. (a) $\Delta$F/F for neural activity traces extracted from different imaging depths; (b) Signal to noise ratio for neural activity traces extracted from different imaging depths
Fig. 7.
Fig. 7. (a) Illustration of selected ROIs in the imaging plane at a depth of 400 $\mu$m; (b) Neural activity traces extracted from (a); (c) Visual stimulus composed of drifting grating (DG), natural movie 1 (NM1), natural movie 2 (NM2), and grey screen for recording spontaneous activity; (d) Running speed recorded during the imaging session. The neural circuit diagram in (a) is adapted from [10]
Fig. 8.
Fig. 8. Tuning curves of selected neurons, the radial magnitude is in units of $\Delta$F/F
Fig. 9.
Fig. 9. Histogram of the orientation selectivity index for all segmented somata at different imaging depths
Fig. 10.
Fig. 10. Maximum intensity projection of calcium imaging movies at two different focal planes with 204 $\mu$m separation, at imaging depths of 393 $\mu$m and 177 $\mu$m. The effective excitation NA is 0.45. (see Visualization 3). Scale bar: 50 $\mu$m
Fig. 11.
Fig. 11. Maximum intensity projection of calcium imaging movies at five different axial planes with 23 $\mu$m separation, at imaging depths of 321 $\mu$m, 298 $\mu$m, 275 $\mu$m, 252 $\mu$m, and 229 $\mu$m. (see Visualization 4). Adaptive optics correction was applied for each focal plane, with an effective NA of 0.65. Scale bar: 50 $\mu$m
Fig. 12.
Fig. 12. Z stack of 2 $\mu$m fluorescent beads from 4 different corners (i.e., (250 $\mu$m, 0 $\mu$m), (-250 $\mu$m, 0 $\mu$m), (0 $\mu$m, 250 $\mu$m), and (0 $\mu$m, -250 $\mu$m)) and the central spot (i.e., (0 $\mu$m, 0 $\mu$m)) of the field of view at different focal planes from the nominal focal location. (a) 0 $\mu$ m; (b) - 200 $\mu$m; (c) 200 $\mu$m. (d) FWHM of axial signal profile from 2 $\mu$m fluorescent beads at different lateral positions for different focal planes (Upper: 0 $\mu$m, Middle: 200 $\mu$m, Bottom: -200 $\mu$m). Scale bar: 5 $\mu$m
Fig. 13.
Fig. 13. Images of 100 $\mu$m fluorescent grid structures at different focal planes, which are -46 $\mu$m, -23 $\mu$m, 0 $\mu$m, 23 $\mu$m, and 46 $\mu$m from the nominal focal location, respectively. Scale bar: 50 $\mu$m
Fig. 14.
Fig. 14. (a) Maximum intensity projection of the calcium imaging movie acquired at a depth of 550 $\mu$m. (b) Segmentation of the calcium imaging movie acquired at a depth of 550 $\mu$m using Suite2P. Scale bar: 50 $\mu$m

Equations (1)

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F r a m e R a t e = 1000 ( m s ) ( I ( m s ) + O ( m s ) ) × N

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