Nanoscopy of living brain slices with low light levels
Open accessAbstract
Lens-based fluorescence microscopy, which has long been limited in resolution to about 200 nanometers by diffraction, is rapidly evolving into a nanoscale imaging technique. Here, we show that the superresolution fluorescence microscopy called RESOLFT enables comparatively fast and continuous imaging of sensitive, nanosized features in living brain tissue. Using low-intensity illumination to switch photochromic fluorescent proteins reversibly between a fluorescent and a nonfluorescent state, we increased the resolution more than 3-fold over that of confocal microscopy in all dimensions. Dendritic spines located 10-50 μm deep inside living organotypic hippocampal brain slices were recorded for hours without signs of degradation. Using a fast-switching protein increased the imaging speed 50-fold over reported RESOLFT schemes, which in turn enabled the recording of spontaneous and stimulated changes of dendritic actin filaments and spine morphology occurring on time scales from seconds to hours.
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RESOLFT requires orders of magnitude less light intensity and has been demonstrated on living brain slices.
“This approach requires orders of magnitude of less light intensity and has been demonstrated on living brain slices (Testa et al., 2012).”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Testa et al., 2012
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Two-photon laser scanning fluorescence microscopy
Denk, W., Strickler, J. H., & Webb, W. W. (1990) · Science · doi:10.1126/science.2321027 · Cited by 9,488 · see citing works
Imaging Intracellular Fluorescent Proteins at Nanometer Resolution
Betzig, E., Patterson, G. H., Sougrat, R., Lindwasser, O. W., Olenych, S. G., Bonifacino, J. S., Davidson, M. W., Lippincott‐Schwartz, J., & Hess, H. F. (2006) · Science · doi:10.1126/science.1127344 · Cited by 8,802 · see citing works
Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM)
Rust, M. J., Bates, M., & Zhuang, X. (2006) · Nature Methods · doi:10.1038/nmeth929 · Cited by 8,109 · see citing works
Hell, S. W., & Wichmann, J. (1994) · Optics Letters · doi:10.1364/ol.19.000780 · Cited by 6,068 · see citing works
Self-citationDeep tissue two-photon microscopy
Helmchen, F., & Denk, W. T. (2005) · Nature Methods · doi:10.1038/nmeth818 · Cited by 4,165 · see citing works
Hell, S. W. (2007) · Science · doi:10.1126/science.1137395 · Cited by 2,967 · see citing works
Self-citationBeiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung
Abbe, E. (1873) · Archiv für Mikroskopische Anatomie · doi:10.1007/bf02956173 · Cited by 2,747 · see citing works
Gustafsson, M. G. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406877102 · Cited by 2,239 · see citing works
Lifeact: a versatile marker to visualize F-actin
Riedl, J., Crevenna, A. H., Kessenbrock, K., Yu, J. H., Neukirchen, D., Bista, M., Bradke, F., Jenne, D., Holak, T. A., Werb, Z., et al. (2008) · Nature Methods · doi:10.1038/nmeth.1220 · Cited by 2,189 · see citing works
Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission
Klar, T. A., Jakobs, S., Dyba, M., Egner, A., & Hell, S. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.15.8206 · Cited by 1,869 · see citing works
Self-citationDendritic spine changes associated with hippocampal long-term synaptic plasticity
Engert, F., & Bonhoeffer, T. (1999) · Nature · doi:10.1038/19978 · Cited by 1,664 · see citing works
Morphological Changes in Dendritic Spines Associated with Long-Term Synaptic Plasticity
Yuste, R., & Bonhoeffer, T. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1071 · Cited by 1,269 · see citing works
STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis
Willig, K. I., Rizzoli, S. O., Westphal, V., Jahn, R., & Hell, S. W. (2006) · Nature · doi:10.1038/nature04592 · Cited by 1,227 · see citing works
Self-citationStructure and function of dendritic spines
Nimchinsky, E. A., Sabatini, B. L., & Svoboda, K. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.081501.160008 · Cited by 1,208 · see citing works
Breaking the Diffraction Barrier: Super-Resolution Imaging of Cells
Huang, B., Babcock, H. P., & Zhuang, X. (2010) · Cell · doi:10.1016/j.cell.2010.12.002 · Cited by 1,159 · see citing works
Hell, S. W. (2003) · Nature Biotechnology · doi:10.1038/nbt895 · Cited by 1,006 · see citing works
Self-citationMicroscopy and its focal switch
Hell, S. W. (2008) · Nature Methods · doi:10.1038/nmeth.1291 · Cited by 993 · see citing works
Self-citationDendritic spines as basic functional units of neuronal integration
Yuste, R., & Denk, W. (1995) · Nature · doi:10.1038/375682a0 · Cited by 950 · see citing works
Organotypic slice cultures: a technique has come of age
Gähwiler, B. H. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01122-3 · Cited by 884 · see citing works
Hofmann, M., Eggeling, C., Jakobs, S., & Hell, S. W. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506010102 · Cited by 845 · see citing works
Self-citationRegulated Fast Nucleocytoplasmic Shuttling Observed by Reversible Protein Highlighting
Ando, R., Mizuno, H., & Miyawaki, A. (2004) · Science · doi:10.1126/science.1102506 · Cited by 844 · see citing works
Actin-based plasticity in dendritic spines
Matus, A. (2000) · Science · doi:10.1126/science.290.5492.754 · Cited by 815 · see citing works
Actin in dendritic spines: connecting dynamics to function
Hotulainen, P., & Hoogenraad, C. C. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201003008 · Cited by 815 · see citing works
Video-Rate Far-Field Optical Nanoscopy Dissects Synaptic Vesicle Movement
Westphal, V., Rizzoli, S. O., Lauterbach, M. A., Kamin, D., Jahn, R., & Hell, S. W. (2008) · Science · doi:10.1126/science.1154228 · Cited by 788 · see citing works
Self-citationFast, three-dimensional super-resolution imaging of live cells
Jones, S. A., Shim, S., He, J., & Zhuang, X. (2011) · Nature Methods · doi:10.1038/nmeth.1605 · Cited by 752 · see citing works
Superresolution Imaging of Chemical Synapses in the Brain
Dani, A., Huang, B., Bergan, J. F., Dulac, C. G., & Zhuang, X. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.021 · Cited by 718 · see citing works
Photon Upmanship: Why Multiphoton Imaging Is More than a Gimmick
Denk, W. T., & Svoboda, K. (1997) · Neuron · doi:10.1016/s0896-6273(00)81237-4 · Cited by 679 · see citing works
Saturated patterned excitation microscopy—a concept for optical resolution improvement
Heintzmann, R., Jovin, T. M., & Cremer, C. G. (2002) · Journal of the Optical Society of America A · doi:10.1364/josaa.19.001599 · Cited by 569 · see citing works
Diffraction-unlimited all-optical imaging and writing with a photochromic GFP
Grotjohann, T., Testa, I., Leutenegger, M., Bock, H., Urban, N. T., Lavoie-Cardinal, F., Willig, K. I., Eggeling, C., Jakobs, S., & Hell, S. W. (2011) · Nature · doi:10.1038/nature10497 · Cited by 501 · see citing works
Self-citationReversible single-molecule photoswitching in the GFP-like fluorescent protein Dronpa
Habuchi, S., Ando, R., Dedecker, P., Verheijen, W., Mizuno, H., Miyawaki, A., & Hofkens, J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500489102 · Cited by 486 · see citing works
Adaptive aberration correction in a confocal microscope
Booth, M. J., Neil, M. A. A., Juskaitis, R., & Wilson, T. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.082544799 · Cited by 425 · see citing works
Live-cell imaging of dendritic spines by STED microscopy
Nägerl, U. V., Willig, K. I., Hein, B., Hell, S. W., & Bonhoeffer, T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810028105 · Cited by 412 · see citing works
Self-citationRego, E. H., Shao, L., Macklin, J. J., Winoto, L., Johansson, G. A., Kamps-Hughes, N., Davidson, M. W., & Gustafsson, M. G. L. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107547108 · Cited by 400 · see citing works
Glutamate induces de novo growth of functional spines in developing cortex
Kwon, H.-B., & Sabatini, B. L. (2011) · Nature · doi:10.1038/nature09986 · Cited by 368 · see citing works
Nanoscopy in a living mouse brain
Berning, S., Willig, K. I., Steffens, H., Dibaj, P., & Hell, S. W. (2012) · Science · doi:10.1126/science.1215369 · Cited by 363 · see citing works
Self-citationA reversibly photoswitchable GFP-like protein with fluorescence excitation decoupled from switching
Brakemann, T., Stiel, A. C., Weber, G., Andresen, M. A., Testa, I., Grotjohann, T., Leutenegger, M., Plessmann, U., Urlaub, H., Eggeling, C., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1952 · Cited by 300 · see citing works
Self-citationSTED Nanoscopy of Actin Dynamics in Synapses Deep Inside Living Brain Slices
Urban, N. T., Willig, K. I., Hell, S. W., & Nägerl, U. V. (2011) · Biophysical Journal · doi:10.1016/j.bpj.2011.07.027 · Cited by 295 · see citing works
Self-citationConcepts for nanoscale resolution in fluorescence microscopy
Hell, S. W., Dyba, M., & Jakobs, S. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.08.015 · Cited by 288 · see citing works
Self-citationStiel, A. C., Trowitzsch, S., Weber, G., Andresen, M. A., Eggeling, C., Hell, S. W., Jakobs, S., & Wahl, M. C. (2007) · Biochemical Journal · doi:10.1042/bj20061401 · Cited by 257 · see citing works
Self-citationHell, S. W., Jakobs, S., & Kastrup, L. (2003) · Applied Physics A · doi:10.1007/s00339-003-2292-4 · Cited by 202 · see citing works
Self-citationHosokawa, T., Rusakov, D., Bliss, T., & Fine, A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05560.1995 · Cited by 187 · see citing works
Ding, J. B., Takasaki, K. T., & Sabatini, B. L. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.011 · Cited by 177 · see citing works
Non-synaptic dendritic spines in neocortex
Arellano, J. I., Espinosa, A., Fairén, A. G., Yuste, R., & DeFelipe, J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.12.015 · Cited by 171 · see citing works
Izeddin, I., Specht, C. G., Lelek, M., Darzacq, X., Triller, A., Zimmer, C., & Dahan, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015611 · Cited by 139 · see citing works
Dedecker, P., Hotta, J., Flors, C., Sliwa, M., Uji‐i, H., Roeffaers, M. B. J., Ando, R., Mizuno, H., Miyawaki, A., & Hofkens, J. (2007) · Journal of the American Chemical Society · doi:10.1021/ja076128z · Cited by 135 · see citing works
Wide‐field subdiffraction RESOLFT microscopy using fluorescent protein photoswitching
Schwentker, M. A., Bock, H., Hofmann, M., Jakobs, S., Bewersdorf, J., Eggeling, C., & Hell, S. W. (2007) · Microscopy Research and Technique · doi:10.1002/jemt.20443 · Cited by 125 · see citing works
Self-citationRapid, High Level Protein Production Using DNA-based Semliki Forest Virus Vectors
DiCiommo, D. P., & Bremner, R. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.29.18060 · Cited by 123 · see citing works
Dual-Label STED Nanoscopy of Living Cells Using Photochromism
Willig, K. I., Stiel, A. C., Brakemann, T., Jakobs, S., & Hell, S. W. (2011) · Nano Letters · doi:10.1021/nl202290w · Cited by 68 · see citing works
Self-citationImaging Living Synapses at the Nanoscale by STED Microscopy
Nägerl, U. V., & Bonhoeffer, T. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0990-10.2010 · Cited by 54 · see citing works
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Hell, S. W., Sahl, S. J., Bates, M., Zhuang, X., Heintzmann, R., Booth, M. J., Bewersdorf, J., Shtengel, G. E., Hess, H. F., Tinnefeld, P., et al. (2015) · Journal of Physics D Applied Physics · doi:10.1088/0022-3727/48/44/443001 · Cited by 355 · see citing works
Self-citationSTED Nanoscopy Reveals the Ubiquity of Subcortical Cytoskeleton Periodicity in Living Neurons
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Self-citationFast reversibly photoswitching red fluorescent proteins for live-cell RESOLFT nanoscopy
Pennacchietti, F., Serebrovskaya, E. O., Faro, A. R., Shemiakina, I. I., Bozhanova, N. G., Kotlobay, A. A., Gurskaya, N. G., Bodén, A., Dreier, J., Chudakov, D. M., et al. (2018) · Nature Methods · doi:10.1038/s41592-018-0052-9 · Cited by 89 · see citing works
Self-citationOrganization and dynamics of the actin cytoskeleton during dendritic spine morphological remodeling
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Nevskyi, O., Sysoiev, D., Dreier, J., Stein, S. C., Oppermann, A., Lemken, F., Janke, T., Enderlein, J., Testa, I., Huhn, T., et al. (2018) · Small · doi:10.1002/smll.201703333 · Cited by 85 · see citing works
Self-citationImaging of molecular surface dynamics in brain slices using single-particle tracking
Biermann, B., Sokoll, S., Klueva, J., Missler, M., Wiegert, J. S., Sibarita, J., & Heine, M. (2014) · Nature Communications · doi:10.1038/ncomms4024 · Cited by 83 · see citing works
Smart scanning for low-illumination and fast RESOLFT nanoscopy in vivo
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Self-citationA super-resolution platform for correlative live single-molecule imaging and STED microscopy
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STED microscopy of living cells – new frontiers in membrane and neurobiology
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Self-citationVolumetric live cell imaging with three-dimensional parallelized RESOLFT microscopy
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Self-citationEnhanced photon collection enables four dimensional fluorescence nanoscopy of living systems
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Self-citationBarriers in the brain: resolving dendritic spine morphology and compartmentalization
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Impaired plasticity of cortical dendritic spines in P301S tau transgenic mice
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Sahl, S. J., Balzarotti, F., Keller‐Findeisen, J., Leutenegger, M., Westphal, V., Egner, A., Lavoie‐Cardinal, F., Chmyrov, A., Grotjohann, T., & Jakobs, S. (2016) · Science · doi:10.1126/science.aad7983 · Cited by 54 · see citing works
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Dual Channel RESOLFT Nanoscopy by Using Fluorescent State Kinetics
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Clausen, M. P., Galiani, S., de la Serna, J. B., Fritzsche, M., Chojnacki, J., Gehmlich, K., Lagerholm, B. C., & Eggeling, C. (2013) · NanoBioImaging · doi:10.2478/nbi-2013-0001 · Cited by 32 · see citing works
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Bui, A. D., Kim, H. K., Maroso, M., & Soltész, I. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a022855 · Cited by 31 · see citing works
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Willig, K. I., & Barrantes, F. J. (2014) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2014.03.021 · Cited by 31 · see citing works
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Bin, J. M., & Lyons, D. A. (2016) · Brain Plasticity · doi:10.3233/bpl-160029 · Cited by 31 · see citing works
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Chmyrov, A., Leutenegger, M., Grotjohann, T., Schönle, A., Keller‐Findeisen, J., Kastrup, L., Jakobs, S., Donnert, G., Sahl, S. J., & Hell, S. W. (2017) · Scientific Reports · doi:10.1038/srep44619 · Cited by 31 · see citing works
Self-citationLabeling Cytosolic Targets in Live Cells with Blinking Probes
Xu, J., Chang, J., Yan, Q., Dertinger, T., Bruchez, M. P., & Weiss, S. (2013) · The Journal of Physical Chemistry Letters · doi:10.1021/jz400682m · Cited by 27 · see citing works
Advanced Methods in Fluorescence Microscopy
Fritzky, L., & Lagunoff, D. (2013) · Analytical Cellular Pathology · doi:10.1155/2013/569326 · Cited by 27 · see citing works
Li, C., Le, V., Wang, X., Hao, X., Liu, X., & Kuang, C. (2020) · Laser & Photonics Review · doi:10.1002/lpor.201900084 · Cited by 24 · see citing works
Rational design of enhanced photoresistance in a photoswitchable fluorescent protein
Duan, C., Byrdin, M., Khatib, M. E., Henry, X., Adam, V., & Bourgeois, D. (2015) · Methods and Applications in Fluorescence · doi:10.1088/2050-6120/3/1/014004 · Cited by 24 · see citing works
Advanced optical imaging techniques for neurodevelopment
Wu, Y., Christensen, R. P., Colón‐Ramos, D. A., & Shroff, H. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.06.008 · Cited by 24 · see citing works
Color centers in wide-bandgap semiconductors for subdiffraction imaging: a review
Castelletto, S., & Boretti, A. A. (2021) · Advanced Photonics · doi:10.1117/1.ap.3.5.054001 · Cited by 22 · see citing works
Reversibly Switchable Fluorescent Proteins for RESOLFT Nanoscopy
Jensen, N. A., Jansen, I., Kamper, M., & Jakobs, S. (2020) · Topics in applied physics · doi:10.1007/978-3-030-34413-9_9 · Cited by 22 · see citing works
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Gupta, A. K., Nishchal, N. K., & Banerjee, P. P. (2020) · OSA Continuum · doi:10.1364/osac.383527 · Cited by 21 · see citing works
Bonilla-Quintana, M., Wörgötter, F., D’Este, E., Tetzlaff, C., & Fauth, M. J. (2021) · Scientific Reports · doi:10.1038/s41598-021-83331-9 · Cited by 16 · see citing works
Light Sheet Illumination for 3D Single-Molecule Super-Resolution Imaging of Neuronal Synapses
Gagliano, G., Nelson, T., Saliba, N., Vargas-Hernández, S., & Gustavsson, A. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.761530 · Cited by 19 · see citing works
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Hensel, M., Klingauf, J., & Piehler, J. (2013) · Biological Chemistry · doi:10.1515/hsz-2012-0324 · Cited by 19 · see citing works
Okabe, S. (2020) · Microscopy · doi:10.1093/jmicro/dfaa016 · Cited by 17 · see citing works
In Vivo Superresolution Imaging of Neuronal Structure in the Mouse Brain
Urban, B. E., Xiao, L., Chen, S., Yang, H., Dong, B., Kozorovitskiy, Y., & Zhang, H. F. (2017) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2017.2773540 · Cited by 18 · see citing works
Optical control and study of biological processes at the single-cell level in a live organism
Feng, Z., Zhang, W., Xu, J., Gauron, C., Ducos, B., Vriz, S., Volovitch, M., Jullien, L., Weiss, S., & Bensimon, D. (2013) · Reports on Progress in Physics · doi:10.1088/0034-4885/76/7/072601 · Cited by 17 · see citing works
Interrogating Synaptic Architecture: Approaches for Labeling Organelles and Cytoskeleton Components
Reshetniak, S., & Rizzoli, S. O. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00023 · Cited by 17 · see citing works
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Loew, L. M., & Hell, S. W. (2013) · Biophysical Journal · doi:10.1016/j.bpj.2013.01.011 · Cited by 15 · see citing works
Self-citationAutomated analysis of spine dynamics on live CA1 pyramidal cells
Blumer, C., Vivien, C., Genoud, C., Pérez‐Alvarez, A., Wiegert, J. S., Vetter, T. R., & Oertner, T. G. (2014) · Medical Image Analysis · doi:10.1016/j.media.2014.09.004 · Cited by 15 · see citing works
Visualizing Viral Infection In Vivo by Multi-Photon Intravital Microscopy
Sewald, X. (2018) · Viruses · doi:10.3390/v10060337 · Cited by 15 · see citing works
Abe, M., Fukuyama, H., & Mima, T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320223111 · Cited by 13 · see citing works
Moreno, X. C., Silva, M. M., Roos, J., Pennacchietti, F., Norlin, N., & Testa, I. (2023) · HardwareX · doi:10.1016/j.ohx.2023.e00400 · Cited by 13 · see citing works
Self-citationSuper-resolution imaging of the neuronal cytoskeleton
Butler-Hallissey, C., & Leterrier, C. (2024) · npj Imaging · doi:10.1038/s44303-024-00054-y · Cited by 13 · see citing works
Saturated Excitation Microscopy with Optimized Excitation Modulation
Yonemaru, Y., Yamanaka, M., Smith, N. I., Kawata, S., & Fujita, K. (2014) · ChemPhysChem · doi:10.1002/cphc.201300879 · Cited by 13 · see citing works
Low-light phase imaging using in-line digital holography and the transport of intensity equation
Gupta, A. K., & Nishchal, N. K. (2021) · Journal of Optics · doi:10.1088/2040-8986/abe18a · Cited by 12 · see citing works
Eggeling, C., & Hell, S. W. (2014) · Springer series on fluorescence · doi:10.1007/4243_2014_75 · Cited by 12 · see citing works
Self-citationSubdiffractive microscopy: techniques, applications, and challenges
Long, B., Robinson, D. C., & Zhong, H. (2014) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1259 · Cited by 11 · see citing works
Three-dimensional live microscopy beyond the diffraction limit
Fiolka, R. P. (2013) · Journal of Optics · doi:10.1088/2040-8978/15/9/094002 · Cited by 10 · see citing works
The Principles of Super-Resolution Fluorescence Microscopy (Review)
Klementieva, N. V., Вадимовна, З. Е., Lukyanov, K. A., & Mishin, A. S. (2016) · Современные технологии в медицине · doi:10.17691/stm2016.8.2.17 · Cited by 10 · see citing works
RESOLFT Nanoscopy of Fixed Cells Using a Z-Domain Based Fusion Protein for Labelling
Ilgen, P., Grotjohann, T., Jans, D. C., Kilisch, M., Hell, S. W., & Jakobs, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0136233 · Cited by 10 · see citing works
Self-citationAdvances in three-dimensional super-resolution nanoscopy
Zeng, Z., & Xi, P. (2016) · Microscopy Research and Technique · doi:10.1002/jemt.22719 · Cited by 9 · see citing works
Urban, B. E., Xiao, L., Dong, B., Chen, S., Kozorovitskiy, Y., & Zhang, H. F. (2017) · Journal of Biophotonics · doi:10.1002/jbio.201700171 · Cited by 9 · see citing works
Fluorescence Microscopy with Nanometer Resolution
Sahl, S. J., Schönle, A., & Hell, S. W. (2019) · Springer handbooks · doi:10.1007/978-3-030-00069-1_22 · Cited by 9 · see citing works
Self-citationIn vivo super-resolution of the brain – How to visualize the hidden nanoplasticity?
Willig, K. I. (2022) · iScience · doi:10.1016/j.isci.2022.104961 · Cited by 8 · see citing works
Self-citationDiaspro, A., Bianchini, P., Zanacchi, F. C., Lanzanò, L. L., Vicidomini, G., Oneto, M., Pesce, L., & Cainero, I. (2019) · Springer handbooks · doi:10.1007/978-3-030-00069-1_21 · Cited by 9 · see citing works
Fluorescence microscopy at the molecular scale
Alvelid, J., & Testa, I. (2019) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2019.09.009 · Cited by 8 · see citing works
Self-citationMinehart, J. A., & Speer, C. M. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.615059 · Cited by 8 · see citing works
Imaging of spine synapses using super-resolution microscopy
Kashiwagi, Y., & Okabe, S. (2021) · Anatomical Science International · doi:10.1007/s12565-021-00603-0 · Cited by 9 · see citing works
Super-resolution microscopy heads towards 3D dynamics
Weißhart, K., Dertinger, T., Kalkbrenner, T., Kleppe, I. C., & Kempe, M. (2013) · Advanced Optical Technologies · doi:10.1515/aot-2013-0015 · Cited by 8 · see citing works
Lighting Up Live Cells with Smart Genetically Encoded Fluorescence Probes from GMars Family
Wang, S., Yao, S., Sun, C., Xue, B., Hou, Y., Su, X., & Sun, Y. (2018) · ACS Sensors · doi:10.1021/acssensors.8b00449 · Cited by 8 · see citing works
Molecular contribution function in RESOLFT nanoscopy
Frahm, L., Keller‐Findeisen, J., Alt, P., Schnorrenberg, S., Ruiz, M. D. Á., Aspelmeier, T., Munk, A., Jakobs, S., & Hell, S. W. (2019) · Optics Express · doi:10.1364/oe.27.021956 · Cited by 7 · see citing works
Self-citationMulti‐foci parallelised RESOLFT nanoscopy in an extended field‐of‐view
Moreno, X. C., Pennacchietti, F., Minet, G., Damenti, M., Ollech, D., Barabas, F. M., & Testa, I. (2022) · Journal of Microscopy · doi:10.1111/jmi.13157 · Cited by 7 · see citing works
Self-citationHogstrom, L. J., Guo, S.-M., Murugadoss, K., & Bathe, M. (2015) · Interface Focus · doi:10.1098/rsfs.2015.0081 · Cited by 7 · see citing works
Castro, J. B., & Gould, T. J. (2015) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155415610169 · Cited by 6 · see citing works
Super-resolution Fluorescence Microscopy
Mondal, P. P., & Diaspro, A. (2013) · Springer eBooks · doi:10.1007/978-94-007-7545-9_9 · Cited by 6 · see citing works
Nanoscopy at low light intensities shows its potential
Gould, T. J., & Bewersdorf, J. (2012) · eLife · doi:10.7554/elife.00475 · Cited by 6 · see citing works
Predicting resolution and image quality in RESOLFT and other point scanning microscopes [Invited]
Bodén, A., Moreno, X. C., Cooper, B. K., York, A. G., & Testa, I. (2020) · Biomedical Optics Express · doi:10.1364/boe.389911 · Cited by 6 · see citing works
Self-citation
- Authors
- Testa, I., Urban, N. T., Jakobs, S., Eggeling, C., Willig, K. I., & Hell, S. W.
- Affiliations
- Max Planck Institute for Biophysical Chemistry (DE)
- Max Planck Society (DE)
- Corresponding author
- Hell, Stefan W.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2012-09
- Volume
- 75
- Issue
- 6
- Pages
- 992-1000
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2054093040
- Cited by
- 131
- References
- 49
- Citations by year
- 2026: 4 · 2024: 2 · 2023: 3 · 2022: 7 · 2021: 13 · 2020: 7 · 2019: 7 · 2018: 11 · 2017: 8 · 2016: 12 · 2015: 15 · 2014: 19 · 2013: 21 · 2012: 2
- FWCI
- 8.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- GRO (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- OPUS (Augsburg University) (submittedVersion, cc-by-nc-nd)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Advanced Fluorescence Microscopy Techniques
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Physical Sciences › Materials Science › Materials Chemistry › Photochromic and Fluorescence Chemistry
- Keywords
- RESOLFT, super-resolution fluorescence microscopy, dendritic spines, organotypic hippocampal slices, low-light conditions, diffraction-limited resolution
- MeSH terms
- Animals, Animals, Newborn, Electric Stimulation, Hippocampus, Image Processing, Computer-Assisted, Light, Luminescent Proteins, Mice, Inbred C57BL, Neurons, Organ Culture Techniques, Time Factors, Transfection, Long-Term Potentiation, Patch-Clamp Techniques, Microscopy, Confocal, Nanotechnology, Dendritic Spines, Mice
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