Abstract

Adjusting the objective correction collar is a widely used approach to correct spherical aberrations (SA) in optical microscopy. In this work, we characterized and compared its performance with adaptive optics in the context of in vivo brain imaging with two-photon fluorescence microscopy. We found that the presence of sample tilt had a deleterious effect on the performance of SA-only correction. At large tilt angles, adjusting the correction collar even worsened image quality. In contrast, adaptive optical correction always recovered optimal imaging performance regardless of sample tilt. The extent of improvement with adaptive optics was dependent on object size, with smaller objects having larger relative gains in signal intensity and image sharpness. These observations translate into a superior performance of adaptive optics for structural and functional brain imaging applications in vivo, as we confirmed experimentally.

© 2017 Optical Society of America

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2017 (1)

N. Ji, “Adaptive optical fluorescence microscopy,” Nat. Methods 14(4), 374–380 (2017).
[Crossref] [PubMed]

2016 (1)

A. Courvoisier, M. J. Booth, and P. S. Salter, “Inscription of 3D waveguides in diamond using an ultrafast laser,” Appl. Phys. Lett. 109(3), 031109 (2016).
[Crossref]

2015 (3)

W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
[Crossref] [PubMed]

K. Wang, W. Sun, C. T. Richie, B. K. Harvey, E. Betzig, and N. Ji, “Direct wavefront sensing for high-resolution in vivo imaging in scattering tissue,” Nat. Commun. 6, 7276 (2015).
[Crossref] [PubMed]

N. Matsumoto, T. Inoue, A. Matsumoto, and S. Okazaki, “Correction of depth-induced spherical aberration for deep observation using two-photon excitation fluorescence microscopy with spatial light modulator,” Biomed. Opt. Express 6(7), 2575–2587 (2015).
[Crossref] [PubMed]

2014 (4)

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

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] [PubMed]

H. W. Yoo, M. E. van Royen, W. A. van Cappellen, A. B. Houtsmuller, M. Verhaegen, and G. Schitter, “Automated spherical aberration correction in scanning confocal microscopy,” Rev. Sci. Instrum. 85(12), 123706 (2014).
[Crossref] [PubMed]

L. Silvestri, L. Sacconi, and F. S. Pavone, “Correcting spherical aberrations in confocal light sheet microscopy: A theoretical study,” Microsc. Res. Tech. 77(7), 483–491 (2014).
[Crossref] [PubMed]

2013 (2)

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]

X. Tao, A. Norton, M. Kissel, O. Azucena, and J. Kubby, “Adaptive optical two-photon microscopy using autofluorescent guide stars,” Opt. Lett. 38(23), 5075–5078 (2013).
[Crossref] [PubMed]

2012 (1)

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
[Crossref] [PubMed]

2011 (2)

2010 (2)

2009 (3)

H. Itoh, N. Matsumoto, and T. Inoue, “Spherical aberration correction suitable for a wavefront controller,” Opt. Express 17(16), 14367–14373 (2009).
[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]

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

2008 (1)

P. A. Muriello and K. W. Dunn, “Improving signal levels in intravital multiphoton microscopy using an objective correction collar,” Opt. Commun. 281(7), 1806–1812 (2008).
[Crossref] [PubMed]

2007 (3)

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]

E. J. Botcherby, R. Juškaitis, M. J. Booth, and T. Wilson, “Aberration-free optical refocusing in high numerical aperture microscopy,” Opt. Lett. 32(14), 2007–2009 (2007).
[Crossref] [PubMed]

W. Göbel and F. Helmchen, “In vivo calcium imaging of neural network function,” Physiology (Bethesda) 22(6), 358–365 (2007).
[Crossref] [PubMed]

2004 (1)

R. Arimoto and J. M. Murray, “A common aberration with water-immersion objective lenses,” J. Microsc. 216(1), 49–51 (2004).
[Crossref] [PubMed]

2002 (3)

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[Crossref] [PubMed]

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[Crossref] [PubMed]

J. T. Trachtenberg, B. E. Chen, G. W. Knott, G. Feng, J. R. Sanes, E. Welker, and K. Svoboda, “Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex,” Nature 420(6917), 788–794 (2002).
[Crossref] [PubMed]

2000 (3)

M. J. Booth and T. Wilson, “Strategies for the compensation of specimen-induced spherical aberration in confocal microscopy of skin,” J. Microsc. 200(1), 68–74 (2000).
[Crossref] [PubMed]

M. Carandini and D. Ferster, “Membrane potential and firing rate in cat primary visual cortex,” J. Neurosci. 20(1), 470–484 (2000).
[PubMed]

D.-S. Wan, M. Rajadhyaksha, and R. H. Webb, “Analysis of spherical aberration of a water immersion objective: application to specimens with refractive indices 1.33-1.40,” J. Microsc. 197(3), 274–284 (2000).
[Crossref] [PubMed]

1998 (1)

M. J. Booth, M. A. A. Neil, and T. Wilson, “Aberration correction for confocal imaging in refractive-index-mismatched media,” J. Microsc. 192(2), 90–98 (1998).
[Crossref]

1997 (2)

Z. Kam, D. A. Agard, and J. W. Sedat, “Three-dimensional microscopy in thick biological samples: A fresh approach for adjusting focus and correcting spherical aberration,” Bioimaging 5(1), 40–49 (1997).
[Crossref]

P. Török, S. J. Hewlett, and P. Varga, “The role of specimen-induced spherical aberration in confocal microscopy,” J. Microsc. 188(2), 158–172 (1997).
[Crossref]

1994 (1)

1991 (2)

1979 (1)

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]

Agard, D. A.

Z. Kam, D. A. Agard, and J. W. Sedat, “Three-dimensional microscopy in thick biological samples: A fresh approach for adjusting focus and correcting spherical aberration,” Bioimaging 5(1), 40–49 (1997).
[Crossref]

Albert, O.

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[Crossref] [PubMed]

Andilla, J.

Arimoto, R.

R. Arimoto and J. M. Murray, “A common aberration with water-immersion objective lenses,” J. Microsc. 216(1), 49–51 (2004).
[Crossref] [PubMed]

Artigas, D.

Aviles-Espinosa, R.

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.

K. Wang, W. Sun, C. T. Richie, B. K. Harvey, E. Betzig, and N. Ji, “Direct wavefront sensing for high-resolution in vivo imaging in scattering tissue,” Nat. Commun. 6, 7276 (2015).
[Crossref] [PubMed]

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
[Crossref] [PubMed]

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]

Bonhoeffer, T.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Booth, M. J.

A. Courvoisier, M. J. Booth, and P. S. Salter, “Inscription of 3D waveguides in diamond using an ultrafast laser,” Appl. Phys. Lett. 109(3), 031109 (2016).
[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(16), 2495–2497 (2009).
[Crossref] [PubMed]

E. J. Botcherby, R. Juškaitis, M. J. Booth, and T. Wilson, “Aberration-free optical refocusing in high numerical aperture microscopy,” Opt. Lett. 32(14), 2007–2009 (2007).
[Crossref] [PubMed]

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[Crossref] [PubMed]

M. J. Booth and T. Wilson, “Strategies for the compensation of specimen-induced spherical aberration in confocal microscopy of skin,” J. Microsc. 200(1), 68–74 (2000).
[Crossref] [PubMed]

M. J. Booth, M. A. A. Neil, and T. Wilson, “Aberration correction for confocal imaging in refractive-index-mismatched media,” J. Microsc. 192(2), 90–98 (1998).
[Crossref]

Botcherby, E. J.

Brain, K.

Bronner, M. E.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

Cao, J.

Carandini, M.

M. Carandini and D. Ferster, “Membrane potential and firing rate in cat primary visual cortex,” J. Neurosci. 20(1), 470–484 (2000).
[PubMed]

Chen, B. E.

J. T. Trachtenberg, B. E. Chen, G. W. Knott, G. Feng, J. R. Sanes, E. Welker, and K. Svoboda, “Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex,” Nature 420(6917), 788–794 (2002).
[Crossref] [PubMed]

Chen, T.-W.

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] [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]

Chow, D. K.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Chuckowree, J.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Courvoisier, A.

A. Courvoisier, M. J. Booth, and P. S. Salter, “Inscription of 3D waveguides in diamond using an ultrafast laser,” Appl. Phys. Lett. 109(3), 031109 (2016).
[Crossref]

Crest, J.

De Paola, V.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Débarre, D.

Dillon, D.

Dunn, K. W.

P. A. Muriello and K. W. Dunn, “Improving signal levels in intravital multiphoton microscopy using an objective correction collar,” Opt. Commun. 281(7), 1806–1812 (2008).
[Crossref] [PubMed]

Engerer, P.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

Feng, G.

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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).
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Kner, P.

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Matsumoto, A.

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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).
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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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N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
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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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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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Sheppard, C. J. R.

Sherman, L.

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
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L. Silvestri, L. Sacconi, and F. S. Pavone, “Correcting spherical aberrations in confocal light sheet microscopy: A theoretical study,” Microsc. Res. Tech. 77(7), 483–491 (2014).
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Sullivan, W.

Sun, W.

K. Wang, W. Sun, C. T. Richie, B. K. Harvey, E. Betzig, and N. Ji, “Direct wavefront sensing for high-resolution in vivo imaging in scattering tissue,” Nat. Commun. 6, 7276 (2015).
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W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
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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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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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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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Tan, Z.

W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
[Crossref] [PubMed]

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).
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P. Török, S. J. Hewlett, and P. Varga, “The role of specimen-induced spherical aberration in confocal microscopy,” J. Microsc. 188(2), 158–172 (1997).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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J. T. Trachtenberg, B. E. Chen, G. W. Knott, G. Feng, J. R. Sanes, E. Welker, and K. Svoboda, “Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex,” Nature 420(6917), 788–794 (2002).
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H. W. Yoo, M. E. van Royen, W. A. van Cappellen, A. B. Houtsmuller, M. Verhaegen, and G. Schitter, “Automated spherical aberration correction in scanning confocal microscopy,” Rev. Sci. Instrum. 85(12), 123706 (2014).
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H. W. Yoo, M. E. van Royen, W. A. van Cappellen, A. B. Houtsmuller, M. Verhaegen, and G. Schitter, “Automated spherical aberration correction in scanning confocal microscopy,” Rev. Sci. Instrum. 85(12), 123706 (2014).
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P. Török, S. J. Hewlett, and P. Varga, “The role of specimen-induced spherical aberration in confocal microscopy,” J. Microsc. 188(2), 158–172 (1997).
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H. W. Yoo, M. E. van Royen, W. A. van Cappellen, A. B. Houtsmuller, M. Verhaegen, and G. Schitter, “Automated spherical aberration correction in scanning confocal microscopy,” Rev. Sci. Instrum. 85(12), 123706 (2014).
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D.-S. Wan, M. Rajadhyaksha, and R. H. Webb, “Analysis of spherical aberration of a water immersion objective: application to specimens with refractive indices 1.33-1.40,” J. Microsc. 197(3), 274–284 (2000).
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Wang, C.

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] [PubMed]

Wang, K.

K. Wang, W. Sun, C. T. Richie, B. K. Harvey, E. Betzig, and N. Ji, “Direct wavefront sensing for high-resolution in vivo imaging in scattering tissue,” Nat. Commun. 6, 7276 (2015).
[Crossref] [PubMed]

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Watanabe, T.

Webb, R. H.

D.-S. Wan, M. Rajadhyaksha, and R. H. Webb, “Analysis of spherical aberration of a water immersion objective: application to specimens with refractive indices 1.33-1.40,” J. Microsc. 197(3), 274–284 (2000).
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Welker, E.

J. T. Trachtenberg, B. E. Chen, G. W. Knott, G. Feng, J. R. Sanes, E. Welker, and K. Svoboda, “Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex,” Nature 420(6917), 788–794 (2002).
[Crossref] [PubMed]

Wilbrecht, L.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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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(16), 2495–2497 (2009).
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E. J. Botcherby, R. Juškaitis, M. J. Booth, and T. Wilson, “Aberration-free optical refocusing in high numerical aperture microscopy,” Opt. Lett. 32(14), 2007–2009 (2007).
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M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[Crossref] [PubMed]

M. J. Booth and T. Wilson, “Strategies for the compensation of specimen-induced spherical aberration in confocal microscopy of skin,” J. Microsc. 200(1), 68–74 (2000).
[Crossref] [PubMed]

M. J. Booth, M. A. A. Neil, and T. Wilson, “Aberration correction for confocal imaging in refractive-index-mismatched media,” J. Microsc. 192(2), 90–98 (1998).
[Crossref]

C. J. R. Sheppard and T. Wilson, “Effect of spherical aberration on the imaging properties of scanning optical microscopes,” Appl. Opt. 18(7), 1058–1063 (1979).
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Ye, J. Y.

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[Crossref] [PubMed]

Yoo, H. W.

H. W. Yoo, M. E. van Royen, W. A. van Cappellen, A. B. Houtsmuller, M. Verhaegen, and G. Schitter, “Automated spherical aberration correction in scanning confocal microscopy,” Rev. Sci. Instrum. 85(12), 123706 (2014).
[Crossref] [PubMed]

Zhou, H.

Appl. Opt. (3)

Appl. Phys. Lett. (1)

A. Courvoisier, M. J. Booth, and P. S. Salter, “Inscription of 3D waveguides in diamond using an ultrafast laser,” Appl. Phys. Lett. 109(3), 031109 (2016).
[Crossref]

Bioimaging (1)

Z. Kam, D. A. Agard, and J. W. Sedat, “Three-dimensional microscopy in thick biological samples: A fresh approach for adjusting focus and correcting spherical aberration,” Bioimaging 5(1), 40–49 (1997).
[Crossref]

Biomed. Opt. Express (2)

J. Microsc. (7)

D.-S. Wan, M. Rajadhyaksha, and R. H. Webb, “Analysis of spherical aberration of a water immersion objective: application to specimens with refractive indices 1.33-1.40,” J. Microsc. 197(3), 274–284 (2000).
[Crossref] [PubMed]

R. Arimoto and J. M. Murray, “A common aberration with water-immersion objective lenses,” J. Microsc. 216(1), 49–51 (2004).
[Crossref] [PubMed]

P. Török, S. J. Hewlett, and P. Varga, “The role of specimen-induced spherical aberration in confocal microscopy,” J. Microsc. 188(2), 158–172 (1997).
[Crossref]

M. J. Booth, M. A. A. Neil, and T. Wilson, “Aberration correction for confocal imaging in refractive-index-mismatched media,” J. Microsc. 192(2), 90–98 (1998).
[Crossref]

M. J. Booth and T. Wilson, “Strategies for the compensation of specimen-induced spherical aberration in confocal microscopy of skin,” J. Microsc. 200(1), 68–74 (2000).
[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]

L. Sherman, J. Y. Ye, O. Albert, and T. B. Norris, “Adaptive correction of depth-induced aberrations in multiphoton scanning microscopy using a deformable mirror,” J. Microsc. 206(1), 65–71 (2002).
[Crossref] [PubMed]

J. Neurosci. (1)

M. Carandini and D. Ferster, “Membrane potential and firing rate in cat primary visual cortex,” J. Neurosci. 20(1), 470–484 (2000).
[PubMed]

J. Opt. Soc. Am. A (1)

Microsc. Res. Tech. (1)

L. Silvestri, L. Sacconi, and F. S. Pavone, “Correcting spherical aberrations in confocal light sheet microscopy: A theoretical study,” Microsc. Res. Tech. 77(7), 483–491 (2014).
[Crossref] [PubMed]

Nat. Commun. (1)

K. Wang, W. Sun, C. T. Richie, B. K. Harvey, E. Betzig, and N. Ji, “Direct wavefront sensing for high-resolution in vivo imaging in scattering tissue,” Nat. Commun. 6, 7276 (2015).
[Crossref] [PubMed]

Nat. Methods (4)

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

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]

N. Ji, “Adaptive optical fluorescence microscopy,” Nat. Methods 14(4), 374–380 (2017).
[Crossref] [PubMed]

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] [PubMed]

Nat. Neurosci. (1)

W. Sun, Z. Tan, B. D. Mensh, and N. Ji, “Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs,” Nat. Neurosci. 19(2), 308–315 (2015).
[Crossref] [PubMed]

Nat. Protoc. (1)

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W.-C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Nature (2)

J. T. Trachtenberg, B. E. Chen, G. W. Knott, G. Feng, J. R. Sanes, E. Welker, and K. Svoboda, “Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex,” Nature 420(6917), 788–794 (2002).
[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]

Opt. Commun. (1)

P. A. Muriello and K. W. Dunn, “Improving signal levels in intravital multiphoton microscopy using an objective correction collar,” Opt. Commun. 281(7), 1806–1812 (2008).
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Opt. Express (3)

Opt. Lett. (3)

Physiology (Bethesda) (1)

W. Göbel and F. Helmchen, “In vivo calcium imaging of neural network function,” Physiology (Bethesda) 22(6), 358–365 (2007).
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Proc. Natl. Acad. Sci. U.S.A. (2)

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[Crossref] [PubMed]

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
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Rev. Sci. Instrum. (1)

H. W. Yoo, M. E. van Royen, W. A. van Cappellen, A. B. Houtsmuller, M. Verhaegen, and G. Schitter, “Automated spherical aberration correction in scanning confocal microscopy,” Rev. Sci. Instrum. 85(12), 123706 (2014).
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Other (2)

RStudio Team, “RStudio: Integrated Development for R,” RStudio, Inc., Boston, MA (2016).

W. G. Hartley, The Light Microscope: its Use and Development (Senecio Publishing Company, 1993).

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Figures (5)

Fig. 1
Fig. 1

Adaptive optical versus spherical aberration corrections of optical aberrations introduced by a 5° tilted coverglass above a 1-µm-diameter bead. (a) Schematic of the optical system. (b-e) Axial-lateral images of the bead obtained with: (b, syscor) system correction only, (c, AO) system correction and adaptive optics, (d, CC) system correction and objective correction collar adjustment, and (e, CC + AO) system correction, objective correction collar adjustment, and adaptive optics. All images were individually normalized. z: axial; x: lateral. The calibration bars provide absolute intensity information. Scale bar: 2 µm. The wavefront aberrations for (f) AO and (g) CC + AO were reconstructed from the Zernike mode amplitudes (h and i, respectively) calculated from the patterns on the Shack-Hartmann wavefront sensor.

Fig. 2
Fig. 2

Performance of different aberration correction methods as a function of sample tilt. The (a) lateral FWHM, (b) axial FWHM, and (c) normalized intensity (to syscor) for 1 µm beads under a single ~170-µm-thick coverglass were evaluated for tilt angles 0°, 2°, 5°, and 10°. Black dots represent individual bead measurements. Colored dots and error bars are the mean and standard deviation, respectively. (d) The measured magnitudes for selected aberration modes are presented.

Fig. 3
Fig. 3

Effects on image size and brightness of different aberration correction methods as a function of bead size. The (a) normalized lateral FWHM, (b) normalized axial FWHM, and (c) normalized intensity for beads of different diameters (0.2, 0.5, 1, and 2 µm) under a single ~170-µm-thick coverglass with a tilt angle of 5°. Black dots represent individual bead measurements. Colored dots and error bars are the mean and standard deviation, respectively. Normalization was performed with respect to values obtained with syscor.

Fig. 4
Fig. 4

In vivo TPEF structural imaging with spherical aberration or full adaptive optical correction in the brain of a Thy1-GFP line M mouse. The cranial window was tilted by 3.5° (a-f) or 5° (g-h). Maximum intensity projections over 20 µm in z at a central depth of 25 µm of images recorded with (a,g) CC and (b,h) CC + AO. Scale bar: 20 µm. Maximum intensity projection along the y-axis for the images recorded with (c) CC and (d) CC + AO. Scale bar: 20 µm. Axial-lateral images of a spine at a depth of 25 µm measured with (c) CC and (d) CC + AO. Scale bar: 1 µm. (a) and (b), (c) and (d), (e) and (f), and (g) and (h) are plotted on the same intensity scale, respectively. z: axial; x and y: lateral.

Fig. 5
Fig. 5

In vivo TPEF functional imaging of neurites expressing calcium indicator GCaMP6s in the mouse primary visual cortex with spherical aberration or full adaptive optical correction. (a) Awake mouse was presented with drifting-grating visual stimulation. Average intensity TPEF images of visual stimulation experiments at a depth of 50 µm with (d) syscor, (b,e) CC, and (c,f) CC + AO. Scale bar: 20 µm. (g,h) Cumulative distributions of the maximal calcium transients ΔF/F to visual stimulation of all axonal boutons. Median values are indicated by colored dots. (i,j) Proportion of axonal boutons in three categories of responses to visual stimulation: non-responsive, responsive but non-orientation selective, and responsive and orientation selective. The tilt angle was (d-f,g,i) 3.5° and (b,c,h,j) 5°.

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