Superresolution imaging for neuroscience

The advent of superresolution fluorescence microscopy beyond the classic diffraction barrier of optical microscopy is poised to transform cell-biological research. A series of proof-of-principle studies have demonstrated its vast potential for a wide range of applications in neuroscience, including nanoscale imaging of neuronal morphology, cellular organelles, protein distributions and protein trafficking. This review introduces the main incarnations of these new methodologies, including STED, PALM/STORM and SIM, covering basic theoretical and practical aspects concerning their optical principles, technical implementation, scope and limitations. In addition, it highlights several discoveries relating to synapse biology that have been made using these novel approaches to illustrate their appeal for neuroscience research.

[1]  Jianyong Tang,et al.  Three-Dimensional Super-resolution Imaging of Thick Biological Samples , 2009, Microscopy and Microanalysis.

[2]  S. Hell Far-Field Optical Nanoscopy , 2007, Science.

[3]  Christophe Zimmer,et al.  Super-Resolution Dynamic Imaging of Dendritic Spines Using a Low-Affinity Photoconvertible Actin Probe , 2011, PloS one.

[4]  James A Galbraith,et al.  Super-resolution microscopy at a glance , 2011, Journal of Cell Science.

[5]  E. Abbe Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung , 1873 .

[6]  Christian Eggeling,et al.  Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Gustafsson Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Bryant B. Chhun,et al.  Super-Resolution Video Microscopy of Live Cells by Structured Illumination , 2009, Nature Methods.

[9]  Rainer Heintzmann,et al.  Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating , 1999, European Conference on Biomedical Optics.

[10]  J. Lippincott-Schwartz,et al.  Imaging Intracellular Fluorescent Proteins at Nanometer Resolution , 2006, Science.

[11]  S. B. Kater,et al.  Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. , 1994, Annual review of neuroscience.

[12]  U Valentin Nägerl,et al.  STED nanoscopy of actin dynamics in synapses deep inside living brain slices. , 2011, Biophysical journal.

[13]  S.W. HELL,et al.  A compact STED microscope providing 3D nanoscale resolution , 2009, Journal of microscopy.

[14]  K. Chou,et al.  Subdiffraction-limit two-photon fluorescence microscopy for GFP-tagged cell imaging. , 2009, Biophysical journal.

[15]  Michael D. Mason,et al.  Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. , 2006, Biophysical journal.

[16]  M. Gustafsson,et al.  Subdiffraction Multicolor Imaging of the Nuclear Periphery with 3D Structured Illumination Microscopy , 2008, Science.

[17]  Mark Bates,et al.  Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging , 2011, Nature Methods.

[18]  S. Hell,et al.  STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis , 2006, Nature.

[19]  S. Hell,et al.  Dual-label STED nanoscopy of living cells using photochromism. , 2011, Nano letters.

[20]  George H. Patterson,et al.  A Photoactivatable GFP for Selective Photolabeling of Proteins and Cells , 2002, Science.

[21]  K. Harris,et al.  Ultrastructural Analysis of Hippocampal Neuropil from the Connectomics Perspective , 2010, Neuron.

[22]  Michael J Rust,et al.  Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) , 2006, Nature Methods.

[23]  Christian Eggeling,et al.  STED microscopy reveals crystal colour centres with nanometric resolution. , 2009 .

[24]  Christian Eggeling,et al.  Diffraction-unlimited all-optical imaging and writing with a photochromic GFP , 2011, Nature.

[25]  S. Hell,et al.  Endosomal sorting of readily releasable synaptic vesicles , 2010, Proceedings of the National Academy of Sciences.

[26]  X. Zhuang,et al.  Superresolution Imaging of Chemical Synapses in the Brain , 2010, Neuron.

[27]  S. Hell,et al.  Simultaneous multi-lifetime multi-color STED imaging for colocalization analyses. , 2011, Optics express.

[28]  Mark Bates,et al.  Three-Dimensional Super-Resolution Imaging by Stochastic Optical Reconstruction Microscopy , 2008, Science.

[29]  E. Kandel,et al.  Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Hell,et al.  Two-color far-field fluorescence nanoscopy. , 2007, Biophysical journal.

[31]  U Valentin Nägerl,et al.  Two-color STED microscopy of living synapses using a single laser-beam pair. , 2011, Biophysical journal.

[32]  X. Zhuang,et al.  Fast three-dimensional super-resolution imaging of live cells , 2011, Nature Methods.

[33]  S. Hell,et al.  Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Lars Kastrup,et al.  Limited Intermixing of Synaptic Vesicle Components upon Vesicle Recycling , 2010, Traffic.

[35]  G. Ellis‐Davies,et al.  Structural basis of long-term potentiation in single dendritic spines , 2004, Nature.

[36]  Lars Meyer,et al.  Dual-color STED microscopy at 30-nm focal-plane resolution. , 2008, Small.

[37]  Ji Yu,et al.  Investigating Sub-Spine Actin Dynamics in Rat Hippocampal Neurons with Super-Resolution Optical Imaging , 2009, PloS one.

[38]  Gael Moneron,et al.  Two-photon excitation STED microscopy. , 2009, Optics express.

[39]  S. Hell,et al.  High- and low-mobility stages in the synaptic vesicle cycle. , 2010, Biophysical journal.

[40]  S. Hell,et al.  Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. , 1994, Optics letters.

[41]  M. Gustafsson Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy , 2000, Journal of microscopy.

[42]  J. Lippincott-Schwartz,et al.  High-density mapping of single-molecule trajectories with photoactivated localization microscopy , 2008, Nature Methods.

[43]  X. Zhuang,et al.  Breaking the Diffraction Barrier: Super-Resolution Imaging of Cells , 2010, Cell.

[44]  Bernardo L. Sabatini,et al.  Supraresolution Imaging in Brain Slices using Stimulated-Emission Depletion Two-Photon Laser Scanning Microscopy , 2009, Neuron.

[45]  Stefan W. Hell,et al.  Nanoscopy in a Living Mouse Brain , 2012, Science.

[46]  Stephan J. Sigrist,et al.  Bruchpilot Promotes Active Zone Assembly, Ca2+ Channel Clustering, and Vesicle Release , 2006, Science.

[47]  Hari Shroff,et al.  Single-Molecule Discrimination of Discrete Perisynaptic and Distributed Sites of Actin Filament Assembly within Dendritic Spines , 2010, Neuron.

[48]  D. Toomre,et al.  A new wave of cellular imaging. , 2010, Annual review of cell and developmental biology.

[49]  Stefan W. Hell,et al.  Supporting Online Material Materials and Methods Figs. S1 to S9 Tables S1 and S2 References Video-rate Far-field Optical Nanoscopy Dissects Synaptic Vesicle Movement , 2022 .

[50]  T. Svitkina,et al.  Molecular Architecture of Synaptic Actin Cytoskeleton in Hippocampal Neurons Reveals a Mechanism of Dendritic Spine Morphogenesis , 2010, Molecular biology of the cell.

[51]  Mark Bates,et al.  Multicolor Super-Resolution Imaging with Photo-Switchable Fluorescent Probes , 2007, Science.

[52]  Max Born,et al.  Principles of optics - electromagnetic theory of propagation, interference and diffraction of light (7. ed.) , 1999 .

[53]  D. Owald,et al.  Maturation of active zone assembly by Drosophila Bruchpilot , 2009, The Journal of cell biology.

[54]  R. Heintzmann,et al.  Saturated patterned excitation microscopy--a concept for optical resolution improvement. , 2002, Journal of the Optical Society of America. A, Optics, image science, and vision.

[55]  T. Bonhoeffer,et al.  Live-cell imaging of dendritic spines by STED microscopy , 2008, Proceedings of the National Academy of Sciences.

[56]  K. Harris,et al.  Three-Dimensional Relationships between Hippocampal Synapses and Astrocytes , 1999, The Journal of Neuroscience.

[57]  Rafael Yuste,et al.  Dendritic Spines and Distributed Circuits , 2011, Neuron.

[58]  S. Hell,et al.  Wide‐field subdiffraction RESOLFT microscopy using fluorescent protein photoswitching , 2007, Microscopy research and technique.