Abstract

Biological systems undergo dynamical changes continuously which span multiple spatial and temporal scales. To study these complex biological dynamics in vivo, high-speed volumetric imaging that can work at large imaging depth is highly desired. However, deep tissue imaging suffers from wavefront distortion, resulting in reduced Strehl ratio and image quality. Here we combine the two wavefront engineering methods developed in our lab, namely the optical phase-locked ultrasound lens based volumetric imaging and the iterative multiphoton adaptive compensation technique, and demonstrate in vivo volumetric imaging of microglial and mitochondrial dynamics at large depth in mouse brain cortex and lymph node, respectively.

© 2016 Optical Society of America

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References

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2015 (9)

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

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

B. Thomas, A. Wolstenholme, S. N. Chaudhari, E. T. Kipreos, and P. Kner, “Enhanced resolution through thick tissue with structured illumination and adaptive optics,” J. Biomed. Opt. 20(2), 026006 (2015).
[Crossref] [PubMed]

J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U.S.A. 112(30), 9236–9241 (2015).
[Crossref] [PubMed]

L. Kong and M. Cui, “In vivo neuroimaging through the highly scattering tissue via iterative multi-photon adaptive compensation technique,” Opt. Express 23(5), 6145–6150 (2015).
[Crossref] [PubMed]

T. W. Wu and M. Cui, “Numerical study of multi-conjugate large area wavefront correction for deep tissue microscopy,” Opt. Express 23(6), 7463–7470 (2015).
[Crossref] [PubMed]

J. Mertz, H. Paudel, and T. G. Bifano, “Field of view advantage of conjugate adaptive optics in microscopy applications,” Appl. Opt. 54(11), 3498–3506 (2015).
[Crossref] [PubMed]

I. M. Vellekoop, “Feedback-based wavefront shaping,” Opt. Express 23(9), 12189–12206 (2015).
[Crossref] [PubMed]

H. P. Paudel, J. Taranto, J. Mertz, and T. Bifano, “Axial range of conjugate adaptive optics in two-photon microscopy,” Opt. Express 23(16), 20849–20857 (2015).
[Crossref] [PubMed]

2014 (5)

M. Duocastella, G. Vicidomini, and A. Diaspro, “Simultaneous multiplane confocal microscopy using acoustic tunable lenses,” Opt. Express 22(16), 19293–19301 (2014).
[Crossref] [PubMed]

L. Kong and M. Cui, “In vivo fluorescence microscopy via iterative multi-photon adaptive compensation technique,” Opt. Express 22(20), 23786–23794 (2014).
[Crossref] [PubMed]

M. J. Booth, “Adaptive optical microscopy: the ongoing quest for a perfect image,” Light Sci. Appl. 3(4), e165 (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(7), 727–730 (2014).
[Crossref] [PubMed]

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] [PubMed]

2013 (6)

T. Schrödel, R. Prevedel, K. Aumayr, M. Zimmer, and A. Vaziri, “Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light,” Nat. Methods 10(10), 1013–1020 (2013).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

R. D. Simmonds and M. J. Booth, “Modelling of multi-conjugate adaptive optics for spatially variant aberrations in microscopy,” J. Opt. 15(9), 094010 (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] [PubMed]

X. Tao, Z. Dean, C. Chien, O. Azucena, D. Bodington, and J. Kubby, “Shack-Hartmann wavefront sensing using interferometric focusing of light onto guide-stars,” Opt. Express 21(25), 31282–31292 (2013).
[Crossref] [PubMed]

2012 (6)

R. Fiolka, K. Si, and M. Cui, “Complex wavefront corrections for deep tissue focusing using low coherence backscattered light,” Opt. Express 20(15), 16532–16543 (2012).
[Crossref]

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (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]

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]

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
[Crossref] [PubMed]

R. N. Germain, E. A. Robey, and M. D. Cahalan, “A Decade of Imaging Cellular Motility and Interaction Dynamics in the Immune System,” Science 336(6089), 1676–1681 (2012).
[Crossref] [PubMed]

2011 (2)

2010 (1)

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
[Crossref] [PubMed]

2009 (2)

2007 (2)

Z. Kam, P. Kner, D. Agard, and J. W. Sedat, “Modelling the application of adaptive optics to wide-field microscope live imaging,” J. Microsc. 226(1), 33–42 (2007).
[Crossref] [PubMed]

P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, “Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane,” Appl. Phys. Lett. 91(19), 191102 (2007).
[Crossref]

2006 (4)

Y. Zhang, S. Poonja, and A. Roorda, “MEMS-based adaptive optics scanning laser ophthalmoscopy,” Opt. Lett. 31(9), 1268–1270 (2006).
[Crossref] [PubMed]

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[Crossref] [PubMed]

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

B. N. G. Giepmans, S. R. Adams, M. H. Ellisman, and R. Y. Tsien, “The fluorescent toolbox for assessing protein location and function,” Science 312(5771), 217–224 (2006).
[Crossref] [PubMed]

2005 (2)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

A. Nimmerjahn, F. Kirchhoff, and F. Helmchen, “Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo,” Science 308(5726), 1314–1318 (2005).
[Crossref] [PubMed]

2004 (1)

R. Yasuda, E. A. Nimchinsky, V. Scheuss, T. A. Pologruto, T. G. Oertner, B. L. Sabatini, and K. Svoboda, “Imaging calcium concentration dynamics in small neuronal compartments,” Sci. STKE 2004(219), pl5 (2004).
[PubMed]

2003 (2)

M. Karbowski and R. J. Youle, “Dynamics of mitochondrial morphology in healthy cells and during apoptosis,” Cell Death Differ. 10(8), 870–880 (2003).
[Crossref] [PubMed]

P. Marsh, D. Burns, and J. Girkin, “Practical implementation of adaptive optics in multiphoton microscopy,” Opt. Express 11(10), 1123–1130 (2003).
[Crossref] [PubMed]

2002 (1)

2000 (1)

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]

1974 (1)

Adams, S. R.

B. N. G. Giepmans, S. R. Adams, M. H. Ellisman, and R. Y. Tsien, “The fluorescent toolbox for assessing protein location and function,” Science 312(5771), 217–224 (2006).
[Crossref] [PubMed]

Adie, S. G.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Agard, D.

Z. Kam, P. Kner, D. Agard, and J. W. Sedat, “Modelling the application of adaptive optics to wide-field microscope live imaging,” J. Microsc. 226(1), 33–42 (2007).
[Crossref] [PubMed]

Ahmad, A.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Ahrens, M. B.

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).
[Crossref] [PubMed]

Albert, O.

Aumayr, K.

T. Schrödel, R. Prevedel, K. Aumayr, M. Zimmer, and A. Vaziri, “Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light,” Nat. Methods 10(10), 1013–1020 (2013).
[Crossref] [PubMed]

Azucena, O.

Baohan, A.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Betzig, E.

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
[Crossref] [PubMed]

Bierden, P.

Bifano, T.

Bifano, T. G.

Bodington, D.

Booth, M. J.

M. J. Booth, “Adaptive optical microscopy: the ongoing quest for a perfect image,” Light Sci. Appl. 3(4), e165 (2014).
[Crossref]

R. D. Simmonds and M. J. Booth, “Modelling of multi-conjugate adaptive optics for spatially variant aberrations in microscopy,” J. Opt. 15(9), 094010 (2013).
[Crossref]

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]

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(16), 2495–2497 (2009).
[Crossref] [PubMed]

Boppart, S. A.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (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]

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(16), 2495–2497 (2009).
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M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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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(7), 727–730 (2014).
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Bridges, W. B.

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

R. N. Germain, E. A. Robey, and M. D. Cahalan, “A Decade of Imaging Cellular Motility and Interaction Dynamics in the Immune System,” Science 336(6089), 1676–1681 (2012).
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P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, “Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane,” Appl. Phys. Lett. 91(19), 191102 (2007).
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S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
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B. Thomas, A. Wolstenholme, S. N. Chaudhari, E. T. Kipreos, and P. Kner, “Enhanced resolution through thick tissue with structured illumination and adaptive optics,” J. Biomed. Opt. 20(2), 026006 (2015).
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Chen, T.-W.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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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).
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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).
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J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U.S.A. 112(30), 9236–9241 (2015).
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L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12(8), 759–762 (2015).
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L. Kong and M. Cui, “In vivo neuroimaging through the highly scattering tissue via iterative multi-photon adaptive compensation technique,” Opt. Express 23(5), 6145–6150 (2015).
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T. W. Wu and M. Cui, “Numerical study of multi-conjugate large area wavefront correction for deep tissue microscopy,” Opt. Express 23(6), 7463–7470 (2015).
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L. Kong and M. Cui, “In vivo fluorescence microscopy via iterative multi-photon adaptive compensation technique,” Opt. Express 22(20), 23786–23794 (2014).
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R. Fiolka, K. Si, and M. Cui, “Complex wavefront corrections for deep tissue focusing using low coherence backscattered light,” Opt. Express 20(15), 16532–16543 (2012).
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J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
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M. Cui, “Parallel wavefront optimization method for focusing light through random scattering media,” Opt. Lett. 36(6), 870–872 (2011).
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T. W. Wu, J. Tang, B. Hajj, and M. Cui, “Phase resolved interferometric spectral modulation (PRISM) for ultrafast pulse measurement and compression,” Opt. Express 19(14), 12961–12968 (2011).
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L. Kong and M. Cui, “In vivo Deep Tissue Imaging via Iterative Multi-photon Adaptive Compensation Technique,” IEEE J. Sel. Top. Quantum Electron. (2015), in press.

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).
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Dean, Z.

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]

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(16), 2495–2497 (2009).
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Denk, W.

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
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F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
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W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
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Doble, N.

Duocastella, 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).
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B. N. G. Giepmans, S. R. Adams, M. H. Ellisman, and R. Y. Tsien, “The fluorescent toolbox for assessing protein location and function,” Science 312(5771), 217–224 (2006).
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Germain, R. N.

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

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
[Crossref] [PubMed]

R. N. Germain, E. A. Robey, and M. D. Cahalan, “A Decade of Imaging Cellular Motility and Interaction Dynamics in the Immune System,” Science 336(6089), 1676–1681 (2012).
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B. N. G. Giepmans, S. R. Adams, M. H. Ellisman, and R. Y. Tsien, “The fluorescent toolbox for assessing protein location and function,” Science 312(5771), 217–224 (2006).
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Girkin, J.

Graf, B. W.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
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B. F. Grewe and F. Helmchen, “Optical probing of neuronal ensemble activity,” Curr. Opin. Neurobiol. 19(5), 520–529 (2009).
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P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, “Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane,” Appl. Phys. Lett. 91(19), 191102 (2007).
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M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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Helmchen, F.

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F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
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A. Nimmerjahn, F. Kirchhoff, and F. Helmchen, “Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo,” Science 308(5726), 1314–1318 (2005).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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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(7), 727–730 (2014).
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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).
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T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
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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]

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Z. Kam, P. Kner, D. Agard, and J. W. Sedat, “Modelling the application of adaptive optics to wide-field microscope live imaging,” J. Microsc. 226(1), 33–42 (2007).
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P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, “Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane,” Appl. Phys. Lett. 91(19), 191102 (2007).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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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(7), 727–730 (2014).
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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).
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Keller, P. J.

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).
[Crossref] [PubMed]

Kerr, R. A.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Kim, D. S.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Kim, T. N.

P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, “Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane,” Appl. Phys. Lett. 91(19), 191102 (2007).
[Crossref]

Kipreos, E. T.

B. Thomas, A. Wolstenholme, S. N. Chaudhari, E. T. Kipreos, and P. Kner, “Enhanced resolution through thick tissue with structured illumination and adaptive optics,” J. Biomed. Opt. 20(2), 026006 (2015).
[Crossref] [PubMed]

Kirchhoff, F.

A. Nimmerjahn, F. Kirchhoff, and F. Helmchen, “Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo,” Science 308(5726), 1314–1318 (2005).
[Crossref] [PubMed]

Kleinfeld, D.

P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, “Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane,” Appl. Phys. Lett. 91(19), 191102 (2007).
[Crossref]

Kner, P.

B. Thomas, A. Wolstenholme, S. N. Chaudhari, E. T. Kipreos, and P. Kner, “Enhanced resolution through thick tissue with structured illumination and adaptive optics,” J. Biomed. Opt. 20(2), 026006 (2015).
[Crossref] [PubMed]

Z. Kam, P. Kner, D. Agard, and J. W. Sedat, “Modelling the application of adaptive optics to wide-field microscope live imaging,” J. Microsc. 226(1), 33–42 (2007).
[Crossref] [PubMed]

Kobat, D.

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] [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]

Kong, L.

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

L. Kong and M. Cui, “In vivo neuroimaging through the highly scattering tissue via iterative multi-photon adaptive compensation technique,” Opt. Express 23(5), 6145–6150 (2015).
[Crossref] [PubMed]

L. Kong and M. Cui, “In vivo fluorescence microscopy via iterative multi-photon adaptive compensation technique,” Opt. Express 22(20), 23786–23794 (2014).
[Crossref] [PubMed]

L. Kong and M. Cui, “In vivo Deep Tissue Imaging via Iterative Multi-photon Adaptive Compensation Technique,” IEEE J. Sel. Top. Quantum Electron. (2015), in press.

Kubby, J.

Lacefield, C.

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

Lämmermann, T.

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

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).
[Crossref] [PubMed]

Lin, C. P.

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

Little, J. P.

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

Looger, L. L.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

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]

Mack-Bucher, J. A.

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[Crossref] [PubMed]

Mann, R. S.

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

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] [PubMed]

Marsh, P.

Mendes, C. S.

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

Mertz, J.

Migliori, B.

P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, “Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane,” Appl. Phys. Lett. 91(19), 191102 (2007).
[Crossref]

Milkie, D. E.

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
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Nimchinsky, E. A.

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A. Nimmerjahn, F. Kirchhoff, and F. Helmchen, “Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo,” Science 308(5726), 1314–1318 (2005).
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Norris, T. B.

Nussmeier, T. A.

O’Meara, T. R.

Oertner, T. G.

R. Yasuda, E. A. Nimchinsky, V. Scheuss, T. A. Pologruto, T. G. Oertner, B. L. Sabatini, and K. Svoboda, “Imaging calcium concentration dynamics in small neuronal compartments,” Sci. STKE 2004(219), pl5 (2004).
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Olivier, S.

Orger, M. B.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

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(7), 727–730 (2014).
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Appl. Opt. (2)

Appl. Phys. Lett. (1)

P. S. Tsai, B. Migliori, K. Campbell, T. N. Kim, Z. Kam, A. Groisman, and D. Kleinfeld, “Spherical aberration correction in nonlinear microscopy and optical ablation using a transparent deformable membrane,” Appl. Phys. Lett. 91(19), 191102 (2007).
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M. Karbowski and R. J. Youle, “Dynamics of mitochondrial morphology in healthy cells and during apoptosis,” Cell Death Differ. 10(8), 870–880 (2003).
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B. Thomas, A. Wolstenholme, S. N. Chaudhari, E. T. Kipreos, and P. Kner, “Enhanced resolution through thick tissue with structured illumination and adaptive optics,” J. Biomed. Opt. 20(2), 026006 (2015).
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Nat. Photonics (2)

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
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Nature (1)

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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Neuron (1)

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
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L. Kong and M. Cui, “In vivo neuroimaging through the highly scattering tissue via iterative multi-photon adaptive compensation technique,” Opt. Express 23(5), 6145–6150 (2015).
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T. W. Wu, J. Tang, B. Hajj, and M. Cui, “Phase resolved interferometric spectral modulation (PRISM) for ultrafast pulse measurement and compression,” Opt. Express 19(14), 12961–12968 (2011).
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Proc. Natl. Acad. Sci. U.S.A. (5)

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
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Supplementary Material (3)

NameDescription
» Visualization 1: MP4 (748 KB)      The imaging of microglia at depth 405-413 µm, with full correction and system correction respectively
» Visualization 2: MP4 (5092 KB)      Transient morphologies of the microglia
» Visualization 3: MP4 (810 KB)      Transient morphologies of the mitochondria in lymphocytes

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Figures (3)

Fig. 1
Fig. 1 Diagram of the experimental setup. DBS: dichroic beam splitter, PBS: polarization beam splitter, QWP: quarter wave plate, UL: ultrasound lens, RL: relay lens, M: mirror, PLL: phase-lock loop, PD: photodetector, DM: deformable mirror, L: lens, PMT: photomultiplier tube. The inset: phase pattern for correcting the system aberration.
Fig. 2
Fig. 2 Volumetric imaging of transient morphology of microglia in mouse brain cortex. (a) The phase pattern for full correction of both system and tissue induced wavefront distortions. (b, c) The maximum intensity projections of the microglia at depth 405-413 µm, with full correction and system correction respectively (Visualization 1). Scale bar: 10 µm. Power: 36 mW at 935 nm. (d) The signal intensity along the dashed line labeled in (c). (e-g) The transient morphologies of the microglia (Visualization 2) at depth 380-420 µm under the dura. Volume size: 98 × 49 × 40 µm3. The dashed circle in (f) labels a GFP-expressing cell patrolling around the brain cortex through a blood vessel. Laser power: 108 mW at 935 nm.
Fig. 3
Fig. 3 Volumetric imaging of the dynamics of mitochondrial network in lymphocytes of mouse lymph node. (a) The phase pattern for full correction of both system and tissue induced wavefront distortions. (b, c) The volume views of mitochondria in lymphocytes, with full correction and system correction respectively. The volume is 17.6 × 17.6 × 18 µm3, at the depth of 340-364 µm under the surface. Laser power: 55 mW at 935 nm. (d, e) The images acquired at 348 µm depth, with full correction and system correction respectively. Scale bar: 5 µm. (f) The signal intensity along the dashed line labeled in (e). (g-i) The transient morphologies of the mitochondria in lymphocytes (Visualization 3). Volume size: 12 × 9 × 18 µm3. Laser power: 90 mW at 935 nm.

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