• Chinese Journal of Lasers
  • Vol. 49, Issue 20, 2007301 (2022)
Lu Gao, Beibei Gao, and Fu Wang*
Author Affiliations
  • School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200240, China
  • show less
    DOI: 10.3788/CJL202249.2007301 Cite this Article Set citation alerts
    Lu Gao, Beibei Gao, Fu Wang. Applications of Super-Resolution Microscopy Techniques in Living Brain Imaging[J]. Chinese Journal of Lasers, 2022, 49(20): 2007301 Copy Citation Text show less
    References

    [1] Hama H, Kurokawa H, Kawano H et al. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain[J]. Nature Neuroscience, 14, 1481-1488(2011).

    [2] Li A N, Gong H, Zhang B et al. Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain[J]. Science, 330, 1404-1408(2010).

    [3] Denève S, Alemi A, Bourdoukan R. The brain as an efficient and robust adaptive learner[J]. Neuron, 94, 969-977(2017).

    [4] Balaram P, Kaas J H. Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity[J]. Frontiers in Neuroanatomy, 8, 81(2014).

    [5] Roberts P A[M]. Neuroanatomy(1992).

    [6] Kawakami R, Sawada K, Kusama Y et al. In vivo two-photon imaging of mouse hippocampal neurons in dentate gyrus using a light source based on a high-peak power gain-switched laser diode[J]. Biomedical Optics Express, 6, 891-901(2015).

    [7] Lodato S, Arlotta P. Generating neuronal diversity in the mammalian cerebral cortex[J]. Annual Review of Cell and Developmental Biology, 31, 699-720(2015).

    [8] Roland P E. Space-time dynamics of membrane currents evolve to shape excitation, spiking, and inhibition in the cortex at small and large scales[J]. Neuron, 94, 934-942(2017).

    [9] Zou C Y, Shi Y, Ohli J et al. Neuroinflammation impairs adaptive structural plasticity of dendritic spines in a preclinical model of Alzheimer’s disease[J]. Acta Neuropathologica, 131, 235-246(2016).

    [10] Dumoulin S O, Fracasso A, van der Zwaag W et al. Ultra-high field MRI: advancing systems neuroscience towards mesoscopic human brain function[J]. NeuroImage, 168, 345-357(2018).

    [11] Ritman E L. Molecular imaging in small animals: roles for micro-CT[J]. Journal of Cellular Biochemistry, 39, 116-124(2002).

    [12] Franc B L, Acton P D, Mari C et al. Small-animal SPECT and SPECT/CT: important tools for preclinical investigation[J]. Journal of Nuclear Medicine, 49, 1651-1663(2008).

    [13] Pan H C, Liao L D, Lo Y C et al. Neurovascular function recovery after focal ischemic stroke by enhancing cerebral collateral circulation via peripheral stimulation-mediated interarterial anastomosis[J]. Neurophotonics, 4, 035003(2017).

    [14] Mao D, Neumann A R, Sun J J et al. Hippocampus-dependent emergence of spatial sequence coding in retrosplenial cortex[J]. Proceedings of the National Academy of Sciences of the United States of America, 115, 8015-8018(2018).

    [15] Lecoq J, Orlova N, Grewe B F. Wide. fast. deep: recent advances in multiphoton microscopy of in vivo neuronal activity[J]. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 39, 9042-9052(2019).

    [16] Chen B C, Legant W R, Wang K et al. Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution[J]. Science, 346, 1257998(2014).

    [17] Theer P, Hasan M T, Denk W. Two-photon imaging to a depth of 1000 microm in living brains by use of a Ti∶Al2O3 regenerative amplifier[J]. Optics Letters, 28, 1022-1024(2003).

    [18] Helmchen F, Denk W. Deep tissue two-photon microscopy[J]. Nature Methods, 2, 932-940(2005).

    [19] Denk W, Strickler J H, Webb W W. Two-photon laser scanning fluorescence microscopy[J]. Science, 248, 73-76(1990).

    [20] Garaschuk O, Milos R I, Konnerth A. Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo[J]. Nature Protocols, 1, 380-386(2006).

    [21] Zhang H Q, Xie W S, Chen M et al. Aggregation-induced emission nanoparticles for in vivo three-photon fluorescence microscopic rat brain angiography[J]. Journal of Innovative Optical Health Sciences, 12, 1950012(2019).

    [22] Nimmerjahn A. Two-photon imaging of microglia in the mouse cortex in vivo[J]. Cold Spring Harbor Protocols, 2012, 069294(2012).

    [23] Yang W J, Yuste R. In vivo imaging of neural activity[J]. Nature Methods, 14, 349-359(2017).

    [24] Akerboom J, Chen T W, Wardill T J et al. Optimization of a GCaMP calcium indicator for neural activity imaging[J]. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 32, 13819-13840(2012).

    [25] Endlich N, Simon O, Göpferich A et al. Two-photon microscopy reveals stationary podocytes in living zebrafish larvae[J]. Journal of the American Society of Nephrology: JASN, 25, 681-686(2014).

    [26] de Niz M, Nacer A, Frischknecht F. Intravital microscopy: imaging host-parasite interactions in the brain[J]. Cellular Microbiology, 21, e13024(2019).

    [27] Grewe B F, Voigt F F, van’t Hoff M et al. Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens[J]. Biomedical Optics Express, 2, 2035-2046(2011).

    [28] Kaplan A, Friedman N, Davidson N. Acousto-optic lens with very fast focus scanning[J]. Optics Letters, 26, 1078-1080(2001).

    [29] Chen X, Leischner U, Varga Z et al. LOTOS-based two-photon calcium imaging of dendritic spines in vivo[J]. Nature Protocols, 7, 1818-1829(2012).

    [30] Ding R, Liao X, Li J et al. Targeted patching and dendritic Ca2+ imaging in nonhuman primate brain in vivo[J]. Scientific Reports, 7, 2873(2017).

    [31] Yang W J, Miller J E K, Carrillo-Reid L et al. Simultaneous multi-plane imaging of neural circuits[J]. Neuron, 89, 269-284(2016).

    [32] Cheng A, Gonçalves J T, Golshani P et al. Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing[J]. Nature Methods, 8, 139-142(2011).

    [33] Amir W, Carriles R, Hoover E E et al. Simultaneous imaging of multiple focal planes using a two-photon scanning microscope[J]. Optics Letters, 32, 1731-1733(2007).

    [34] Stirman J N, Smith I T, Kudenov M W et al. Wide field-of-view, multi-region, two-photon imaging of neuronal activity in the mammalian brain[J]. Nature Biotechnology, 34, 857-862(2016).

    [35] Kobat D, Horton N G, Xu C. In vivo two-photon microscopy to 1.6-mm depth in mouse cortex[J]. Journal of Biomedical Optics, 16, 106014(2011).

    [36] Horton N G, Wang K, Kobat D et al. In vivo three-photon microscopy of subcortical structures within an intact mouse brain[J]. Nature Photonics, 7, 205-209(2013).

    [37] Klioutchnikov A, Wallace D J, Frosz M H et al. Three-photon head-mounted microscope for imaging deep cortical layers in freely moving rats[J]. Nature Methods, 17, 509-513(2020).

    [38] Olmedillas del Moral M, Asavapanumas N, Uzcátegui N L et al. Healthy brain aging modifies microglial calcium signaling in vivo[J]. International Journal of Molecular Sciences, 20, 589(2019).

    [39] Ohki K, Chung S, Ch’ng Y H et al. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex[J]. Nature, 433, 597-603(2005).

    [40] Ter Veer M J T, Pfeiffer T, Nägerl U V. Two-photon STED microscopy for nanoscale imaging of neural morphology in vivo[J]. Methods in Molecular Biology, 1663, 45-64(2017).

    [41] Huang S H, Irawati N, Chien Y F et al. Optical volumetric brain imaging: speed, depth, and resolution enhancement[J]. Journal of Physics D: Applied Physics, 54, 323002(2021).

    [42] Takasaki K, Sabatini B L. Super-resolution 2-photon microscopy reveals that the morphology of each dendritic spine correlates with diffusive but not synaptic properties[J]. Frontiers in Neuroanatomy, 8, 29(2014).

    [43] Sigal Y M, Zhou R B, Zhuang X W. Visualizing and discovering cellular structures with super-resolution microscopy[J]. Science, 361, 880-887(2018).

    [44] Schermelleh L, Ferrand A, Huser T et al. Super-resolution microscopy demystified[J]. Nature Cell Biology, 21, 72-84(2019).

    [45] Calovi S, Soria F N, Tønnesen J. Super-resolution STED microscopy in live brain tissue[J]. Neurobiology of Disease, 156, 105420(2021).

    [46] Gabor K A, Kim D, Kim C H et al. Nanoscale imaging of caveolin-1 membrane domains in vivo[J]. PLoS One, 10, e0117225(2015).

    [47] Yang J Y, Dong H, Xing F L et al. Single-molecule localization super-resolution microscopy and its applications[J]. Laser & Optoelectronics Progress, 58, 1200001(2021).

    [48] Hell S W, Sahl S J, Bates M et al. The 2015 super-resolution microscopy roadmap[J]. Journal of Physics D: Applied Physics, 48, 443001(2015).

    [49] Rankin B R, Moneron G, Wurm C A et al. Nanoscopy in a living multicellular organism expressing GFP[J]. Biophysical Journal, 100, L63-L65(2011).

    [50] Berning S, Willig K I, Steffens H et al. Nanoscopy in a living mouse brain[J]. Science, 335, 551(2012).

    [51] Willig K I, Steffens H, Gregor C et al. Nanoscopy of filamentous actin in cortical dendrites of a living mouse[J]. Biophysical Journal, 106, L01-L03(2014).

    [52] Wegner W, Ilgen P, Gregor C et al. In vivo mouse and live cell STED microscopy of neuronal actin plasticity using far-red emitting fluorescent proteins[J]. Scientific Reports, 7, 11781(2017).

    [53] Wegner W, Mott A C, Grant S G N et al. In vivo STED microscopy visualizes PSD95 sub-structures and morphological changes over several hours in the mouse visual cortex[J]. Scientific Reports, 8, 219(2018).

    [54] Masch J M, Steffens H, Fischer J et al. Robust nanoscopy of a synaptic protein in living mice by organic-fluorophore labeling[J]. Proceedings of the National Academy of Sciences of the United States of America, 115, E8047-E8056(2018).

    [55] Willig K I, Wegner W, Müller A et al. Multi-label in vivo STED microscopy by parallelized switching of reversibly switchable fluorescent proteins[J]. Cell Reports, 35, 109192(2021).

    [56] Steffens H, Mott A C, Li S Y et al. Stable but not rigid: chronic in vivo STED nanoscopy reveals extensive remodeling of spines, indicating multiple drivers of plasticity[J]. Science Advances, 7, eabf2806(2021).

    [57] Pfeiffer T, Poll S, Bancelin S et al. Chronic 2P-STED imaging reveals high turnover of dendritic spines in the hippocampus in vivo[J]. eLife, 7, e34700(2018).

    [58] Velasco M G M, Zhang M Y, Antonello J et al. 3D super-resolution deep-tissue imaging in living mice[J]. Optica, 8, 442-450(2021).

    [59] Turcotte R, Liang Y J, Tanimoto M et al. Dynamic super-resolution structured illumination imaging in the living brain[J]. Proceedings of the National Academy of Sciences of the United States of America, 116, 9586-9591(2019).

    [60] Urban B E, Xiao L, Chen S Y et al. In vivo superresolution imaging of neuronal structure in the mouse brain[J]. IEEE Transactions on Bio-Medical Engineering, 65, 232-238(2018).

    [61] Chitnis A, Dalle Nogare D. Time-lapse imaging beyond the diffraction limit[J]. Methods, 150, 32-41(2018).

    [62] Jing Y Y, Zhang C S, Yu B et al. Super-resolution microscopy: shedding new light on in vivo imaging[J]. Frontiers in Chemistry, 9, 746900(2021).

    [63] Testa I, Urban N T, Jakobs S et al. Nanoscopy of living brain slices with low light levels[J]. Neuron, 75, 992-1000(2012).

    [64] Dreier J, Castello M, Coceano G et al. Smart scanning for low-illumination and fast RESOLFT nanoscopy in vivo[J]. Nature Communications, 10, 556(2019).

    [65] Steffens H, Wegner W, Willig K I. In vivo STED microscopy: a roadmap to nanoscale imaging in the living mouse[J]. Methods, 174, 42-48(2020).

    [66] Harke B, Keller J, Ullal C K et al. Resolution scaling in STED microscopy[J]. Optics Express, 16, 4154-4162(2008).

    [67] Hernández I C, Buttafava M, Boso G et al. Gated STED microscopy with time-gated single-photon avalanche diode[J]. Biomedical Optics Express, 6, 2258-2267(2015).

    [68] Yang X, Yang Z, Wu Z et al. Mitochondrial dynamics quantitatively revealed by STED nanoscopy with an enhanced squaraine variant probe[J]. Nature Communications, 11, 3699(2020).

    [69] Liu Y, Lu Y, Yang X et al. Amplified stimulated emission in upconversion nanoparticles for super-resolution nanoscopy[J]. Nature, 543, 229-233(2017).

    [70] Gustafsson M G L. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy[J]. Journal of Microscopy, 198, 82-87(2000).

    [71] Zhao T Y, Wang Z J, Feng K et al. High-speed structured illumination microscopy and its applications[J]. Laser & Optoelectronics Progress, 57, 240001(2020).

    [72] Li Z W, Zhang Q R, Chou S W et al. Fast widefield imaging of neuronal structure and function with optical sectioning in vivo[J]. Science Advances, 6, eaaz3870(2020).

    [73] Gustafsson M G L. Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution[J]. Proceedings of the National Academy of Sciences of the United States of America, 102, 13081-13086(2005).

    [74] Li D, Shao L, Chen B C et al. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics[J]. Science, 349, aab3500(2015).

    [75] Wang X, Tu S J, Liu X et al. Advance and prospect for three-dimensional super-resolution microscopy[J]. Laser & Optoelectronics Progress, 58, 2200001(2021).

    [76] Westphal V, Rizzoli S O, Lauterbach M A et al. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement[J]. Science, 320, 246-249(2008).

    [77] Yang B, Przybilla F, Mestre M et al. Large parallelization of STED nanoscopy using optical lattices[J]. Optics Express, 22, 5581-5589(2014).

    [78] Bergermann F, Alber L, Sahl S J et al. 2000-fold parallelized dual-color STED fluorescence nanoscopy[J]. Optics Express, 23, 211-223(2015).

    [79] Fan J, Suo J, Wu J et al. Video-rate imaging of biological dynamics at centimetre scale and micrometre resolution[J]. Nature Photonics, 13, 809-816(2019).

    [80] Ji N. The practical and fundamental limits of optical imaging in mammalian brains[J]. Neuron, 83, 1242-1245(2014).

    [81] Ghosh K K, Burns L D, Cocker E D et al. Miniaturized integration of a fluorescence microscope[J]. Nature Methods, 8, 871-878(2011).

    [82] Yanny K, Antipa N, Liberti W et al. Miniscope3D: optimized single-shot miniature 3D fluorescence microscopy[J]. Light: Science & Applications, 9, 171(2020).

    [83] Bocarsly M E, Jiang W C, Wang C et al. Minimally invasive microendoscopy system for in vivo functional imaging of deep nuclei in the mouse brain[J]. Biomedical Optics Express, 6, 4546-4556(2015).

    [84] Kim J K, Choi J W, Yun S H A. 350-μm side-view optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus[J]. Journal of Biomedical Optics, 18, 050502(2013).

    [85] Ratz M, Testa I, Hell S W et al. CRISPR/Cas9-mediated endogenous protein tagging for RESOLFT super-resolution microscopy of living human cells[J]. Scientific Reports, 5, 9592(2015).

    [86] Hamel E J O, Grewe B F, Parker J G et al. Cellular level brain imaging in behaving mammals: an engineering approach[J]. Neuron, 86, 140-159(2015).

    [87] Li D Y, Zhang H Q, Streich L L et al. AIE-nanoparticle assisted ultra-deep three-photon microscopy in the in vivo mouse brain under 1300 nm excitation[J]. Materials Chemistry Frontiers, 5, 3201-3208(2021).

    [88] Kong L J, Cui M. In vivo fluorescence microscopy via iterative multi-photon adaptive compensation technique[J]. Optics Express, 22, 23786-23794(2014).

    [89] Binding J, Arous J B, Léger J F et al. Brain refractive index measured in vivo with high-NA defocus-corrected full-field OCT and consequences for two-photon microscopy[J]. Optics Express, 19, 4833-4847(2011).

    [90] Dombeck D A, Khabbaz A N, Collman F et al. Imaging large-scale neural activity with cellular resolution in awake, mobile mice[J]. Neuron, 56, 43-57(2007).

    [91] Zong W, Wu R, Li M et al. Fast high-resolution miniature two-photon microscopy for brain imaging in freely behaving mice[J]. Nature Methods, 14, 713-719(2017).

    [92] Park J H, Sun W, Cui M. High-resolution in vivo imaging of mouse brain through the intact skull[J]. Proceedings of the National Academy of Sciences of the United States of America, 112, 9236-9241(2015).

    [93] Zhao W, Zhao S, Li L et al. Sparse deconvolution improves the resolution of live-cell super-resolution fluorescence microscopy[J]. Nature Biotechnology, 1-12(2021).

    Lu Gao, Beibei Gao, Fu Wang. Applications of Super-Resolution Microscopy Techniques in Living Brain Imaging[J]. Chinese Journal of Lasers, 2022, 49(20): 2007301
    Download Citation