Abstract

When imaging through tissue, the optical inhomogeneities of the sample generate aberrations that can prevent effective Stimulated Emission Depletion (STED) imaging. This is particularly problematic for 3D-enhanced STED. We present here an adaptive optics implementation that incorporates two adaptive optic elements to enable correction in all beam paths, allowing performance improvement in thick tissue samples. We use this to demonstrate 3D STED imaging of complex structures in Drosophila melanogaster brains.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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References

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    [Crossref] [PubMed]
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2015 (3)

M. Booth, D. Andrade, D. Burke, B. Patton, and M. Zurauskas, “Aberrations and adaptive optics in super-resolution microscopy,” Microscopy 64(4), 251–261 (2015).
[Crossref] [PubMed]

B. R. Patton, D. Burke, R. Vrees, and M. J. Booth, “Is phase-mask alignment aberrating your STED microscope?” Meth. Appl. Fluoresc. 3, 024002 (2015).
[Crossref]

D. Owald, J. Felsenberg, C. Talbot, G. Das, E. Perisse, W. Huetteroth, and S. Waddell, “Activity of defined mushroom body output neurons underlies learned olfactory behavior in drosophila,” Neuron 86, 417–427 (2015).
[Crossref] [PubMed]

2014 (2)

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

M. J. Booth, “Adaptive optical microscopy: the ongoing quest for a perfect image,” Light Sci. Appl. 3, 165 (2014).
[Crossref]

2013 (4)

F. Goettfert, C. A. Wurm, V. Mueller, S. Berning, V. C. Cordes, A. Honigmann, and S. W. Hell, “Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution,” Biophys. J. 105, L01–L03 (2013).
[Crossref]

N. Banterle, K. H. Bui, E. A. Lemke, and M. Beck, “Fourier ring correlation as a resolution criterion for super-resolution microscopy,” J. Struct. Biol. 183, 363–367 (2013).
[Crossref] [PubMed]

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grunwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Meth. 10, 557–562 (2013).
[Crossref]

T. J. Gould, E. B. Kromann, D. Burke, M. J. Booth, and J. Bewersdorf, “Auto-aligning stimulated emission depletion microscope using adaptive optics,” Opt. Lett. 38, 1860–1862 (2013).
[Crossref] [PubMed]

2012 (5)

A. Facomprez, E. Beaurepaire, and D. Débarre, “Accuracy of correction in modal sensorless adaptive optics,” Opt. Express 20, 2598–2612 (2012).
[Crossref] [PubMed]

S. Galiani, B. Harke, G. Vicidomini, G. Lignani, F. Benfenati, A. Diaspro, and P. Bianchini, “Strategies to maximize the performance of a STED microscope,” Opt. Express 20, 7362–7374 (2012).
[Crossref] [PubMed]

T. J. Gould, D. Burke, J. Bewersdorf, and M. J. Booth, “Adaptive optics enables 3D STED microscopy in aberrating specimens,” Opt. Express 20, 20998–21009 (2012).
[Crossref] [PubMed]

S. Berning, K. I. Willig, H. Steffens, P. Dibaj, and S. W. Hell, “Nanoscopy in a living mouse brain,” Science 335, 551 (2012).
[Crossref] [PubMed]

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

2011 (3)

N. Urban, K. Willig, S. Hell, and U. Naegerl, “STED nanoscopy of actin dynamics in synapses deep inside living brain slices,” Biophys. J. 101, 1277–1284 (2011).
[Crossref] [PubMed]

A. Thayil and M. Booth, “Self calibration of sensorless adaptive optical microscopes,” J. Euro. Opt. Soc. Rapid Publ. 6, 11045 (2011).
[Crossref]

D. A. Green, “A colour scheme for the display of astronomical intensity images,” Bull. Astronom. Soc. India 39, 289–295 (2011).

2010 (2)

2008 (1)

2006 (3)

R. W. Daniels, C. A. Collins, K. Chen, M. V. Gelfand, D. E. Featherstone, and A. DiAntonio, “A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle,” Neuron 49, 11–16 (2006).
[Crossref] [PubMed]

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

A. Mahr and H. Aberle, “The expression pattern of the drosophila vesicular glutamate transporter: A marker protein for motoneurons and glutamatergic centers in the brain,” Gene Expression Patterns 6, 299–309 (2006).
[Crossref]

2005 (1)

M. van Heel and M. Schatz, “Fourier shell correlation threshold criteria,” J. Struct. Biol. 151, 250–262 (2005).
[Crossref] [PubMed]

2000 (2)

1998 (1)

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

1982 (1)

W. Saxton and W. Baumeister, “The correlation averaging of a regularly arranged bacterial cell envelope protein,” J. Microsc. 127, 127–138 (1982).
[Crossref] [PubMed]

Aberle, H.

A. Mahr and H. Aberle, “The expression pattern of the drosophila vesicular glutamate transporter: A marker protein for motoneurons and glutamatergic centers in the brain,” Gene Expression Patterns 6, 299–309 (2006).
[Crossref]

Andrade, D.

M. Booth, D. Andrade, D. Burke, B. Patton, and M. Zurauskas, “Aberrations and adaptive optics in super-resolution microscopy,” Microscopy 64(4), 251–261 (2015).
[Crossref] [PubMed]

Andrei, M. A.

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Arlt, J.

Arndt, H.-D.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Auksorius, E.

Banterle, N.

N. Banterle, K. H. Bui, E. A. Lemke, and M. Beck, “Fourier ring correlation as a resolution criterion for super-resolution microscopy,” J. Struct. Biol. 183, 363–367 (2013).
[Crossref] [PubMed]

Bates, M.

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grunwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Meth. 10, 557–562 (2013).
[Crossref]

Baumeister, W.

W. Saxton and W. Baumeister, “The correlation averaging of a regularly arranged bacterial cell envelope protein,” J. Microsc. 127, 127–138 (1982).
[Crossref] [PubMed]

Beaurepaire, E.

Beck, M.

N. Banterle, K. H. Bui, E. A. Lemke, and M. Beck, “Fourier ring correlation as a resolution criterion for super-resolution microscopy,” J. Struct. Biol. 183, 363–367 (2013).
[Crossref] [PubMed]

Benfenati, F.

Berning, S.

F. Goettfert, C. A. Wurm, V. Mueller, S. Berning, V. C. Cordes, A. Honigmann, and S. W. Hell, “Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution,” Biophys. J. 105, L01–L03 (2013).
[Crossref]

S. Berning, K. I. Willig, H. Steffens, P. Dibaj, and S. W. Hell, “Nanoscopy in a living mouse brain,” Science 335, 551 (2012).
[Crossref] [PubMed]

Bewersdorf, J.

Bianchini, P.

Blaukopf, C.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Booth, M.

M. Booth, D. Andrade, D. Burke, B. Patton, and M. Zurauskas, “Aberrations and adaptive optics in super-resolution microscopy,” Microscopy 64(4), 251–261 (2015).
[Crossref] [PubMed]

A. Thayil and M. Booth, “Self calibration of sensorless adaptive optical microscopes,” J. Euro. Opt. Soc. Rapid Publ. 6, 11045 (2011).
[Crossref]

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

Booth, M. J.

Boruah, B. R.

Bui, K. H.

N. Banterle, K. H. Bui, E. A. Lemke, and M. Beck, “Fourier ring correlation as a resolution criterion for super-resolution microscopy,” J. Struct. Biol. 183, 363–367 (2013).
[Crossref] [PubMed]

Burke, D.

B. R. Patton, D. Burke, R. Vrees, and M. J. Booth, “Is phase-mask alignment aberrating your STED microscope?” Meth. Appl. Fluoresc. 3, 024002 (2015).
[Crossref]

M. Booth, D. Andrade, D. Burke, B. Patton, and M. Zurauskas, “Aberrations and adaptive optics in super-resolution microscopy,” Microscopy 64(4), 251–261 (2015).
[Crossref] [PubMed]

T. J. Gould, E. B. Kromann, D. Burke, M. J. Booth, and J. Bewersdorf, “Auto-aligning stimulated emission depletion microscope using adaptive optics,” Opt. Lett. 38, 1860–1862 (2013).
[Crossref] [PubMed]

T. J. Gould, D. Burke, J. Bewersdorf, and M. J. Booth, “Adaptive optics enables 3D STED microscopy in aberrating specimens,” Opt. Express 20, 20998–21009 (2012).
[Crossref] [PubMed]

Chen, K.

R. W. Daniels, C. A. Collins, K. Chen, M. V. Gelfand, D. E. Featherstone, and A. DiAntonio, “A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle,” Neuron 49, 11–16 (2006).
[Crossref] [PubMed]

Cheng, Y.

Collins, C. A.

R. W. Daniels, C. A. Collins, K. Chen, M. V. Gelfand, D. E. Featherstone, and A. DiAntonio, “A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle,” Neuron 49, 11–16 (2006).
[Crossref] [PubMed]

Cordes, V. C.

F. Goettfert, C. A. Wurm, V. Mueller, S. Berning, V. C. Cordes, A. Honigmann, and S. W. Hell, “Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution,” Biophys. J. 105, L01–L03 (2013).
[Crossref]

D’Este, E.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Daniels, R. W.

R. W. Daniels, C. A. Collins, K. Chen, M. V. Gelfand, D. E. Featherstone, and A. DiAntonio, “A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle,” Neuron 49, 11–16 (2006).
[Crossref] [PubMed]

Das, G.

D. Owald, J. Felsenberg, C. Talbot, G. Das, E. Perisse, W. Huetteroth, and S. Waddell, “Activity of defined mushroom body output neurons underlies learned olfactory behavior in drosophila,” Neuron 86, 417–427 (2015).
[Crossref] [PubMed]

Débarre, D.

Deng, S.

DiAntonio, A.

R. W. Daniels, C. A. Collins, K. Chen, M. V. Gelfand, D. E. Featherstone, and A. DiAntonio, “A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle,” Neuron 49, 11–16 (2006).
[Crossref] [PubMed]

Diaspro, A.

Dibaj, P.

S. Berning, K. I. Willig, H. Steffens, P. Dibaj, and S. W. Hell, “Nanoscopy in a living mouse brain,” Science 335, 551 (2012).
[Crossref] [PubMed]

Donnert, G.

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Dunsby, C.

Eggeling, C.

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Facomprez, A.

Featherstone, D. E.

R. W. Daniels, C. A. Collins, K. Chen, M. V. Gelfand, D. E. Featherstone, and A. DiAntonio, “A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle,” Neuron 49, 11–16 (2006).
[Crossref] [PubMed]

Felsenberg, J.

D. Owald, J. Felsenberg, C. Talbot, G. Das, E. Perisse, W. Huetteroth, and S. Waddell, “Activity of defined mushroom body output neurons underlies learned olfactory behavior in drosophila,” Neuron 86, 417–427 (2015).
[Crossref] [PubMed]

Fournier, M.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

French, P. M. W.

Galiani, S.

Gelfand, M. V.

R. W. Daniels, C. A. Collins, K. Chen, M. V. Gelfand, D. E. Featherstone, and A. DiAntonio, “A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle,” Neuron 49, 11–16 (2006).
[Crossref] [PubMed]

Gerlich, D. W.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Goettfert, F.

F. Goettfert, C. A. Wurm, V. Mueller, S. Berning, V. C. Cordes, A. Honigmann, and S. W. Hell, “Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution,” Biophys. J. 105, L01–L03 (2013).
[Crossref]

Gottfert, F.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Gould, T. J.

Green, D. A.

D. A. Green, “A colour scheme for the display of astronomical intensity images,” Bull. Astronom. Soc. India 39, 289–295 (2011).

Grunwald, D.

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grunwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Meth. 10, 557–562 (2013).
[Crossref]

Guther, A.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Hadden, J. P.

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Harke, B.

Hell, S.

N. Urban, K. Willig, S. Hell, and U. Naegerl, “STED nanoscopy of actin dynamics in synapses deep inside living brain slices,” Biophys. J. 101, 1277–1284 (2011).
[Crossref] [PubMed]

Hell, S. W.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

F. Goettfert, C. A. Wurm, V. Mueller, S. Berning, V. C. Cordes, A. Honigmann, and S. W. Hell, “Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution,” Biophys. J. 105, L01–L03 (2013).
[Crossref]

S. Berning, K. I. Willig, H. Steffens, P. Dibaj, and S. W. Hell, “Nanoscopy in a living mouse brain,” Science 335, 551 (2012).
[Crossref] [PubMed]

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Honigmann, A.

F. Goettfert, C. A. Wurm, V. Mueller, S. Berning, V. C. Cordes, A. Honigmann, and S. W. Hell, “Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution,” Biophys. J. 105, L01–L03 (2013).
[Crossref]

Huetteroth, W.

D. Owald, J. Felsenberg, C. Talbot, G. Das, E. Perisse, W. Huetteroth, and S. Waddell, “Activity of defined mushroom body output neurons underlies learned olfactory behavior in drosophila,” Neuron 86, 417–427 (2015).
[Crossref] [PubMed]

Jahn, R.

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Jesacher, A.

Johnsson, K.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Keller, J.

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Kennedy, G.

Knauer, S.

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Kromann, E. B.

Lanigan, P. M. P.

Lemke, E. A.

N. Banterle, K. H. Bui, E. A. Lemke, and M. Beck, “Fourier ring correlation as a resolution criterion for super-resolution microscopy,” J. Struct. Biol. 183, 363–367 (2013).
[Crossref] [PubMed]

Lhrmann, R.

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Li, R.

Lidke, K. A.

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grunwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Meth. 10, 557–562 (2013).
[Crossref]

Lignani, G.

Liu, L.

Lukinavicius, G.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Mahr, A.

A. Mahr and H. Aberle, “The expression pattern of the drosophila vesicular glutamate transporter: A marker protein for motoneurons and glutamatergic centers in the brain,” Gene Expression Patterns 6, 299–309 (2006).
[Crossref]

Marseglia, L.

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Masharina, A.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Medda, R.

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Mueller, V.

F. Goettfert, C. A. Wurm, V. Mueller, S. Berning, V. C. Cordes, A. Honigmann, and S. W. Hell, “Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution,” Biophys. J. 105, L01–L03 (2013).
[Crossref]

Naegerl, U.

N. Urban, K. Willig, S. Hell, and U. Naegerl, “STED nanoscopy of actin dynamics in synapses deep inside living brain slices,” Biophys. J. 101, 1277–1284 (2011).
[Crossref] [PubMed]

Neil, M.

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

Neil, M. A. A.

Nieuwenhuizen, R. P. J.

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grunwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Meth. 10, 557–562 (2013).
[Crossref]

O’Brien, J. L.

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Owald, D.

D. Owald, J. Felsenberg, C. Talbot, G. Das, E. Perisse, W. Huetteroth, and S. Waddell, “Activity of defined mushroom body output neurons underlies learned olfactory behavior in drosophila,” Neuron 86, 417–427 (2015).
[Crossref] [PubMed]

Padgett, M. J.

Patton, B.

M. Booth, D. Andrade, D. Burke, B. Patton, and M. Zurauskas, “Aberrations and adaptive optics in super-resolution microscopy,” Microscopy 64(4), 251–261 (2015).
[Crossref] [PubMed]

Patton, B. R.

B. R. Patton, D. Burke, R. Vrees, and M. J. Booth, “Is phase-mask alignment aberrating your STED microscope?” Meth. Appl. Fluoresc. 3, 024002 (2015).
[Crossref]

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Perisse, E.

D. Owald, J. Felsenberg, C. Talbot, G. Das, E. Perisse, W. Huetteroth, and S. Waddell, “Activity of defined mushroom body output neurons underlies learned olfactory behavior in drosophila,” Neuron 86, 417–427 (2015).
[Crossref] [PubMed]

Puig, D. L.

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grunwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Meth. 10, 557–562 (2013).
[Crossref]

Rarity, J. G.

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Reymond, L.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Rieger, B.

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grunwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Meth. 10, 557–562 (2013).
[Crossref]

Rizzo, S.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Rizzoli, S. O.

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Saxton, W.

W. Saxton and W. Baumeister, “The correlation averaging of a regularly arranged bacterial cell envelope protein,” J. Microsc. 127, 127–138 (1982).
[Crossref] [PubMed]

Schatz, M.

M. van Heel and M. Schatz, “Fourier shell correlation threshold criteria,” J. Struct. Biol. 151, 250–262 (2005).
[Crossref] [PubMed]

Schill, H.

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Schoenle, A.

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Smith, J. M.

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Sommer, C.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Stallinga, S.

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grunwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Meth. 10, 557–562 (2013).
[Crossref]

Steffens, H.

S. Berning, K. I. Willig, H. Steffens, P. Dibaj, and S. W. Hell, “Nanoscopy in a living mouse brain,” Science 335, 551 (2012).
[Crossref] [PubMed]

Ta, H.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Talbot, C.

D. Owald, J. Felsenberg, C. Talbot, G. Das, E. Perisse, W. Huetteroth, and S. Waddell, “Activity of defined mushroom body output neurons underlies learned olfactory behavior in drosophila,” Neuron 86, 417–427 (2015).
[Crossref] [PubMed]

Thayil, A.

A. Thayil and M. Booth, “Self calibration of sensorless adaptive optical microscopes,” J. Euro. Opt. Soc. Rapid Publ. 6, 11045 (2011).
[Crossref]

Urban, N.

N. Urban, K. Willig, S. Hell, and U. Naegerl, “STED nanoscopy of actin dynamics in synapses deep inside living brain slices,” Biophys. J. 101, 1277–1284 (2011).
[Crossref] [PubMed]

van Heel, M.

M. van Heel and M. Schatz, “Fourier shell correlation threshold criteria,” J. Struct. Biol. 151, 250–262 (2005).
[Crossref] [PubMed]

Vicidomini, G.

Vrees, R.

B. R. Patton, D. Burke, R. Vrees, and M. J. Booth, “Is phase-mask alignment aberrating your STED microscope?” Meth. Appl. Fluoresc. 3, 024002 (2015).
[Crossref]

Waddell, S.

D. Owald, J. Felsenberg, C. Talbot, G. Das, E. Perisse, W. Huetteroth, and S. Waddell, “Activity of defined mushroom body output neurons underlies learned olfactory behavior in drosophila,” Neuron 86, 417–427 (2015).
[Crossref] [PubMed]

Waldmann, H.

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

Wildanger, D.

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Willig, K.

N. Urban, K. Willig, S. Hell, and U. Naegerl, “STED nanoscopy of actin dynamics in synapses deep inside living brain slices,” Biophys. J. 101, 1277–1284 (2011).
[Crossref] [PubMed]

Willig, K. I.

S. Berning, K. I. Willig, H. Steffens, P. Dibaj, and S. W. Hell, “Nanoscopy in a living mouse brain,” Science 335, 551 (2012).
[Crossref] [PubMed]

Wilson, T.

M. A. A. Neil, M. J. Booth, and T. Wilson, “New modal wave-front sensor: a theoretical analysis,” J. Opt. Soc. Am. A 17, 1098–1107 (2000).
[Crossref]

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

Wurm, C. A.

F. Goettfert, C. A. Wurm, V. Mueller, S. Berning, V. C. Cordes, A. Honigmann, and S. W. Hell, “Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution,” Biophys. J. 105, L01–L03 (2013).
[Crossref]

Xu, Z.

Zurauskas, M.

M. Booth, D. Andrade, D. Burke, B. Patton, and M. Zurauskas, “Aberrations and adaptive optics in super-resolution microscopy,” Microscopy 64(4), 251–261 (2015).
[Crossref] [PubMed]

Adv. Mater. (1)

D. Wildanger, B. R. Patton, H. Schill, L. Marseglia, J. P. Hadden, S. Knauer, A. Schoenle, J. G. Rarity, J. L. O’Brien, S. W. Hell, and J. M. Smith, “Solid immersion facilitates fluorescence microscopy with nanometer resolution and sub-angstrom emitter localization,” Adv. Mater. 24, OP309–OP313 (2012).
[Crossref] [PubMed]

Biophys. J. (2)

N. Urban, K. Willig, S. Hell, and U. Naegerl, “STED nanoscopy of actin dynamics in synapses deep inside living brain slices,” Biophys. J. 101, 1277–1284 (2011).
[Crossref] [PubMed]

F. Goettfert, C. A. Wurm, V. Mueller, S. Berning, V. C. Cordes, A. Honigmann, and S. W. Hell, “Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution,” Biophys. J. 105, L01–L03 (2013).
[Crossref]

Bull. Astronom. Soc. India (1)

D. A. Green, “A colour scheme for the display of astronomical intensity images,” Bull. Astronom. Soc. India 39, 289–295 (2011).

Gene Expression Patterns (1)

A. Mahr and H. Aberle, “The expression pattern of the drosophila vesicular glutamate transporter: A marker protein for motoneurons and glutamatergic centers in the brain,” Gene Expression Patterns 6, 299–309 (2006).
[Crossref]

J. Euro. Opt. Soc. Rapid Publ. (1)

A. Thayil and M. Booth, “Self calibration of sensorless adaptive optical microscopes,” J. Euro. Opt. Soc. Rapid Publ. 6, 11045 (2011).
[Crossref]

J. Microsc. (2)

W. Saxton and W. Baumeister, “The correlation averaging of a regularly arranged bacterial cell envelope protein,” J. Microsc. 127, 127–138 (1982).
[Crossref] [PubMed]

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

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

J. Struct. Biol. (2)

M. van Heel and M. Schatz, “Fourier shell correlation threshold criteria,” J. Struct. Biol. 151, 250–262 (2005).
[Crossref] [PubMed]

N. Banterle, K. H. Bui, E. A. Lemke, and M. Beck, “Fourier ring correlation as a resolution criterion for super-resolution microscopy,” J. Struct. Biol. 183, 363–367 (2013).
[Crossref] [PubMed]

Light Sci. Appl. (1)

M. J. Booth, “Adaptive optical microscopy: the ongoing quest for a perfect image,” Light Sci. Appl. 3, 165 (2014).
[Crossref]

Meth. Appl. Fluoresc. (1)

B. R. Patton, D. Burke, R. Vrees, and M. J. Booth, “Is phase-mask alignment aberrating your STED microscope?” Meth. Appl. Fluoresc. 3, 024002 (2015).
[Crossref]

Microscopy (1)

M. Booth, D. Andrade, D. Burke, B. Patton, and M. Zurauskas, “Aberrations and adaptive optics in super-resolution microscopy,” Microscopy 64(4), 251–261 (2015).
[Crossref] [PubMed]

Nat. Meth. (2)

G. Lukinavicius, L. Reymond, E. D’Este, A. Masharina, F. Gottfert, H. Ta, A. Guther, M. Fournier, S. Rizzo, H. Waldmann, C. Blaukopf, C. Sommer, D. W. Gerlich, H.-D. Arndt, S. W. Hell, and K. Johnsson, “Fluorogenic probes for live-cell imaging of the cytoskeleton,” Nat. Meth. 11, 731–733 (2014).
[Crossref]

R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grunwald, S. Stallinga, and B. Rieger, “Measuring image resolution in optical nanoscopy,” Nat. Meth. 10, 557–562 (2013).
[Crossref]

Neuron (2)

D. Owald, J. Felsenberg, C. Talbot, G. Das, E. Perisse, W. Huetteroth, and S. Waddell, “Activity of defined mushroom body output neurons underlies learned olfactory behavior in drosophila,” Neuron 86, 417–427 (2015).
[Crossref] [PubMed]

R. W. Daniels, C. A. Collins, K. Chen, M. V. Gelfand, D. E. Featherstone, and A. DiAntonio, “A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle,” Neuron 49, 11–16 (2006).
[Crossref] [PubMed]

Opt. Express (5)

Opt. Lett. (3)

Proc. Nat. Acad. Sci. U.S.A. (1)

G. Donnert, J. Keller, R. Medda, M. A. Andrei, S. O. Rizzoli, R. Lhrmann, R. Jahn, C. Eggeling, and S. W. Hell, “Macromolecular-scale resolution in biological fluorescence microscopy,” Proc. Nat. Acad. Sci. U.S.A. 103, 11440–11445 (2006).
[Crossref] [PubMed]

Science (1)

S. Berning, K. I. Willig, H. Steffens, P. Dibaj, and S. W. Hell, “Nanoscopy in a living mouse brain,” Science 335, 551 (2012).
[Crossref] [PubMed]

Other (1)

J. A. Kubby, ed., Adaptive Optics for Biological Imaging (CRC, 2013).
[Crossref]

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Figures (6)

Fig. 1
Fig. 1

The effect of correcting all three beams for an oil immersion lens imaging into glycerol. a) (b)) Calculated PSF at a depth of 15 µm. Upper row: 3D (2D) confocal (colour image) and overlaid depletion (contours at 15%, 35%, 55%, 75%, 95%) for uncorrected (left) and depletion-only corrected (right) cases. Lower row: Corresponding effective STED PSFs. Colour scale maximum, IMax, given relative to unaberrated confocal maximum, I0. c-e) Calculated plots for focal-depth dependence of confocal, 2D and 3D STED with depletion beam only correction (“Depl Only Corr”) and for no correction. c) Maximum intensity throughout calculated volume (to account for focal plane shifts). d) Full-width half-maximum (FWHM) of PSF in plane parallel to focal plane at depth corresponding to maximum intensity in volume. e) FWHM through maximum along the light propagation direction.

Fig. 2
Fig. 2

Schematic of the adaptive optics STED microscope. A TiSapph oscillator provided both the STED pulses and, after passing through a supercontinuum-generating fibre, the fluorescence excitation pulses. A SLM generated the phase mask used for the structured depletion focus. The deformable mirror allowed correction of sample induced aberrations in all optical paths. A choice of detectors allowed either confocal imaging through a pinhole or wide area imaging to observe the full extent of the foci by scattering off gold beads. The SLM, DM, galvo mirrors and objective back aperture are all in conjugate planes, with the appropriate imaging performed by (non-identical) lens pairs L1, L2 and L3

Fig. 3
Fig. 3

Confocal and 3D STED images of Atto647N labelled vesicular glutamate transporter in synaptic boutons in intact Drosophila brains. Confocal sections are shown in xy (a), yz (b) and xz (c) planes. The imaging depth was 10 µm beneath the surface of the brain. Figures (d,e,f) show corresponding 3D STED images. The arrows indicate direction and are all 1 µm in length. The colour scale ranges from 0-IMax, given as a ratio of the maximum intensity in each image, to the maximum intensity, I0, of the confocal xy image.

Fig. 4
Fig. 4

Upper: The phase correction required on the deformable mirror to acquire the images in Fig. 3. This phase corresponds to an RMS wavefront error of 1.05 radians and a Strehl number of 0.33. Lower: The corresponding decomposition into Zernike polynomials. Note the strong contribution from coma (mode 8), trefoil (mode 9) and 1st order astigmatism (mode 11).

Fig. 5
Fig. 5

a–c) Effect of the phase aberration in Fig. 4 on the 3D STED focus. d) intensity slices through the peak intensity in the focal plane x-direction for the 3D STED (solid line) and excitation (dashed line) showing both the filling in of the central zero-intensity region in the STED focus and the 100 nm misalignment of the excitation peak intensity with the STED minimum intensity. e–f) Effect of the phase aberration in Fig. 4 on the excitation focus. The bars are 1 µm and indicate the axes, while all colour scales are logarithmic over two orders of magnitude.

Fig. 6
Fig. 6

The effect of dual-AO correction on STED imaging. All images are xz slices from the same region of a Drosophila brain at a depth of 15 µm. Scale bars are 1 µm. For a-e) the colour scale ranges from 0-IMax, given as a scaling to the corrected maximum intensity, I0. a) Confocal imaging with only the instrument flat applied. b) Confocal imaging after correcting for aberrations with the DM. c) 3D STED imaging with only the instrument flat applied to both the DM and SLM. d) 3D STED imaging with the correction from b) applied to the DM. e) 3D STED imaging with the correction from b) on the DM and an additional round of AO correction performed on the SLM. f-j) The right half of a-e) with constant IMax=I0 for all colour scales

Equations (4)

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B = x , y I ( x , y )
B S q u a r e d = x , y | I ( x , y ) | 2
M = S + σ β B [ 1 1 + e k ( S S T ) ]
F R C ( q ) = q c i r c l e f 1 ^ ( q ) f 2 ^ ( q ) * q c i r c l e | f 1 ^ ( q ) | 2 q c i r c l e | f 2 ^ ( q ) | 2

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