Abstract

Brain function emerges from the coordinated activity, over time, of large neuronal populations placed in different brain regions. Understanding the relationships of these specific areas and disentangling the contributions of individual neurons to overall function remain central goals for neuroscience. In this scenario, fluorescence microscopy has been proved as the tool of choice for in vivo recording of brain activity. Optical advances combined with genetically encoded indicators allow a large flexibility in terms of spatiotemporal resolution and field of view while keeping invasiveness in living animals to a minimum. Here we describe the latest advancements in the field of linear and nonlinear optical microscopy with special attention to the exploration of brain functionality of model animals. The present review aims to guide the reader through the main optical systems in the field toward future directions for in vivo microscopy applications.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (8)

M. A. Taylor, T. Nöbauer, A. Pernia-Andrade, F. Schlumm, and A. Vaziri, “Brain-wide 3D light-field imaging of neuronal activity with speckle-enhanced resolution,” Optica 5, 345–353 (2018).
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2017 (12)

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y. T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GcamP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14, 388–390 (2017).
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M. Kondo, K. Kobayashi, M. Ohkura, J. Nakai, and M. Matsuzaki, “Two-photon calcium imaging of the medial prefrontal cortex and hippocampus without cortical invasion,” Elife 6, e26839 (2017).
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O. A. Shemesh, D. Tanese, V. Zampini, C. Linghu, K. Piatkevich, E. Ronzitti, E. Papagiakoumou, E. S. Boyden, and V. Emiliani, “Temporally precise single-cell-resolution optogenetics,” Nat. Neurosci. 20, 1796–1806 (2017).
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N. Ji, “Adaptive optical fluorescence microscopy,” Nat. Methods 14, 374–380 (2017).
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A. Song, A. S. Charles, S. A. Koay, J. L. Gauthier, S. Y. Thiberge, J. W. Pillow, and D. W. Tank, “Volumetric two-photon imaging of neurons using stereoscopy (vTwINS),” Nat. Methods 14, 420–426 (2017).
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T. Nöbauer, O. Skocek, A. J. Pernía-Andrade, L. Weilguny, F. Martínez Traub, M. I. Molodtsov, and A. Vaziri, “Video rate volumetric Ca2+ imaging across cortex using seeded iterative demixing (SID) microscopy,” Nat. Methods 14, 811–818 (2017).
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Y. Hayashi, S. Yawata, K. Funabiki, and T. Hikida, “In vivo calcium imaging from dentate granule cells with wide-field fluorescence microscopy,” PLoS One 12, e0180452 (2017).
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2016 (16)

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W. Yang, J. K. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89, 269–284 (2016).
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2015 (10)

D. Oron and Y. Silberberg, “Temporal focusing microscopy,” Cold Spring Harbor Protocols 2015, 145–151 (2015).
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A. Attardo, J. E. Fitzgerald, and M. J. Schnitzer, “Impermanence of dendritic spines in live adult CA1 hippocampus,” Nature 523, 592–596 (2015).
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M. E. J. Sheffield and D. A. Dombeck, “Calcium transient prevalence across the dendritic arbour predicts place field properties,” Nature 517, 200–204 (2015).
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M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9, 113–119 (2015).
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2014 (7)

M. P. Vanni and T. H. Murphy, “Mesoscale transcranial spontaneous activity mapping in GCaMP3 transgenic mice reveals extensive reciprocal connections between areas of somatomotor cortex,” J. Neurosci. 34, 15931–15946 (2014).
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R. J. Low, Y. Gu, and D. W. Tank, “Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex,” Proc. Natl. Acad. Sci. USA 111, 18739–18744 (2014).
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J. G. Heys, K. V. Rangarajan, and D. A. Dombeck, “The functional micro-organization of grid cells revealed by cellular-resolution imaging,” Neuron 84, 1079–1090 (2014).
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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, 625–628 (2014).
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T. Schrödel, R. Prevedel, K. Aumayr, M. Zimmer, and A. Vaziri, “Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light,” Nat. Methods 10, 1013–1020 (2013).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7, 205–209 (2013).
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M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10, 413–420 (2013).
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T. Panier, S. A. Romano, R. Olive, T. Pietri, G. Sumbre, R. Candelier, and G. Debrégeas, “Fast functional imaging of multiple brain regions in intact zebrafish larvae using selective plane illumination microscopy,” Front. Neural Circuits 7, 65 (2013).
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M. H. Mohajerani, A. W. Chan, M. Mohsenvand, J. Ledue, R. Liu, D. A. McVea, J. D. Boyd, Y. T. Wang, M. Reimers, and T. H. Murphy, “Spontaneous cortical activity alternates between motifs defined by regional axonal projections,” Nat. Neurosci. 16, 1426–1435 (2013).
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R. P. J. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med. 17, 223–228 (2011).
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Figures (4)

Fig. 1.
Fig. 1. Human, mouse, and zebrafish larvae brains. Comparison of spatial extent and number of neurons of human and vertebrate animal models.
Fig. 2.
Fig. 2. Linear imaging of neuronal activity. (a) General scheme of epifluorescence wide-field imaging. Epifluorescence imaging of zebrafish brain, adapted by permission [9]. (b) General scheme of light-sheet fluorescence microscopy. Light-sheet imaging of zebrafish brain, adapted by permission from Springer Nature [13]. (c) General scheme of light field microscopy; application of this scheme for whole-brain functional imaging in a zebrafish larva. Adapted by permission from Springer Nature [24].
Fig. 3.
Fig. 3. (a) Optical layout of a two-photon laser-scanning microscope. (b) Large-FOV microscope, adapted with permission [37]. (c) Systems for beam scanning: galvo mirrors, polygonal mirrors, and acousto-optic deflectors. (d) Axial scanning: (top) linear stage system, (bottom) ETL-focus shifting. (e) AOD random-access imaging of selected neurons.
Fig. 4.
Fig. 4. Deep brain imaging. (a) Left: scheme of microprism implantation. Right: Simultaneous imaging of all cortical layers though invasive microprism, adapted by permission from American Physiologial Society [60], scale bar 200 μm. (b) Left: GRIN lens optical scheme; right: deep brain imaging of freely behaving mouse via a GRIN lens miniaturized microscope, adapted from [67]. (c) Left: schematic of wavefront correction of the signal coming from a deep region of the scattering sample; brain imaging adapted by permission from Springer Nature [77]. (d) Three-photon microscopy through the skull of a mouse, adapted by permission from Springer Nature [91].