Mapping brain circuitry with a light microscope (original) (raw)

• Golgi, C. Sulla Struttura Della Sostanza Grigia del Cervello. Gazz. Med. Ital. (Lombardia) 33, 244–246 (1873).
  Google Scholar
• Ramón y Cajal, S. Textura del Sistema Nervioso del Hombre y de los Vertebrados. Vol. 2 (Moya, 1904).
• Felleman, D.J. & Van Essen, D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).
  CAS PubMed Google Scholar
• Rockland, K.S. & Pandya, D.N. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 179, 3–20 (1979).
  Article CAS PubMed Google Scholar
• Craddock, R.C. et al. Imaging human connectomes at the macroscale. Nat. Methods 10, 524–536 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Helmstaedter, M. Cellular-resolution connectomics: challenges of dense neural circuit reconstruction. Nat. Methods 10, 501–507 (2013).
  Article CAS PubMed Google Scholar
• Bohland, J.W. et al. A proposal for a coordinated effort for the determination of brainwide neuroanatomical connectivity in model organisms at a mesoscopic scale. PLoS Comput. Biol. 5, e1000334 (2009).This paper describes the rationale for mapping connectivity in the whole mouse brain at the mesoscale level by LM.
  Article CAS PubMed PubMed Central Google Scholar
• Odgaard, A., Andersen, K., Melsen, F. & Gundersen, H.J. A direct method for fast three-dimensional serial reconstruction. J. Microsc. 159, 335–342 (1990).
  Article CAS PubMed Google Scholar
• Ewald, A.J., McBride, H., Reddington, M., Fraser, S.E. & Kerschmann, R. Surface imaging microscopy, an automated method for visualizing whole embryo samples in three dimensions at high resolution. Dev. Dyn. 225, 369–375 (2002).
  Article PubMed Google Scholar
• Tsai, P.S. et al. All-optical histology using ultrashort laser pulses. Neuron 39, 27–41 (2003).This study pioneered the approach of serial imaging by two-photon microscopy and tissue sectioning for ex vivo collection of neuroanatomical data.
  Article CAS PubMed Google Scholar
• Sands, G.B. et al. Automated imaging of extended tissue volumes using confocal microscopy. Microsc. Res. Tech. 67, 227–239 (2005).
  Article PubMed Google Scholar
• Ragan, T. et al. High-resolution whole organ imaging using two-photon tissue cytometry. J. Biomed. Opt. 12, 014015 (2007).
  Article PubMed Google Scholar
• Mayerich, D., Abbott, L. & McCormick, B. Knife-edge scanning microscopy for imaging and reconstruction of three-dimensional anatomical structures of the mouse brain. J. Microsc. 231, 134–143 (2008).
  Article CAS PubMed Google Scholar
• Li, A. et al. Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain. Science 330, 1404–1408 (2010).
  Article CAS PubMed Google Scholar
• Ragan, T. et al. Serial two-photon tomography for automated ex vivo mouse brain imaging. Nat. Methods 9, 255–258 (2012).This study introduces the method of STP tomography and demonstrates its use for anterograde and retrograde tracing in the mouse brain.
  Article CAS PubMed PubMed Central Google Scholar
• Gong, H. et al. Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution. Neuroimage 74, 87–98, (2013).This study demonstrates the first long-range tracing of individual axons in the mouse brain by fMOST.
  Article PubMed Google Scholar
• Denk, W., Strickler, J.H. & Webb, W.W. Two-photon laser scanning fluorescence microscopy. Science 248, 73–76 (1990).
  Article CAS PubMed Google Scholar
• Huisken, J., Swoger, J., Del Bene, F., Wittbrodt, J. & Stelzer, E.H. Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305, 1007–1009 (2004).
  Article CAS PubMed Google Scholar
• Dodt, H.U. et al. Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain. Nat. Methods 4, 331–336 (2007).This study is the first to use LSFM for imaging the entire mouse brain.
  Article CAS PubMed Google Scholar
• Niedworok, C.J. et al. Charting monosynaptic connectivity maps by two-color light-sheet fluorescence microscopy. Cell Rep. 2, 1375–1386 (2012).
  Article CAS PubMed Google Scholar
• Chung, K. et al. Structural and molecular interrogation of intact biological systems. Nature 10.1038/nature12107 (2013).
• Chung, K. & Deisseroth, K. CLARITY for mapping the nervous system. Nat. Methods 10, 508–513 (2013).
  Article CAS PubMed Google Scholar
• Leischner, U., Zieglgansberger, W. & Dodt, H.U. Resolution of ultramicroscopy and field of view analysis. PLoS ONE 4, e5785 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Mertz, J. & Kim, J. Scanning light-sheet microscopy in the whole mouse brain with HiLo background rejection. J. Biomed. Opt. 15, 016027 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Kalchmair, S., Jahrling, N., Becker, K. & Dodt, H.U. Image contrast enhancement in confocal ultramicroscopy. Opt. Lett. 35, 79–81 (2010).
  Article PubMed Google Scholar
• Keller, P.J. et al. Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy. Nat. Methods 7, 637–642 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Wickersham, I.R., Finke, S., Conzelmann, K.K. & Callaway, E.M. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods 4, 47–49 (2007).
  Article CAS PubMed Google Scholar
• Wickersham, I.R. et al. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53, 639–647 (2007).This study describes a genetically modified rabies virus designed to specifically label direct presynaptic input onto a given cell population.
  Article CAS PubMed PubMed Central Google Scholar
• Ng, L. et al. An anatomic gene expression atlas of the adult mouse brain. Nat. Neurosci. 12, 356–362 (2009).
  Article CAS PubMed Google Scholar
• Jones, E.G., Stone, J.M. & Karten, H.J. High-resolution digital brain atlases: a Hubble telescope for the brain. Ann. NY Acad. Sci. 1225 (suppl. 1), E147–E159 (2011).
  Article PubMed Google Scholar
• Lein, E.S. et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168–176 (2007).This study pioneered large-scale LM-based mouse brain anatomy and introduced the Allen Mouse Brain Atlas and online data portal.
  Article CAS PubMed Google Scholar
• Dong, H.W. The Allen Reference Atlas: A Digital Color Brain Atlas of the C57Bl/6J Male Mouse (John Wiley & Sons Inc., 2008).
• Lanciego, J.L. & Wouterlood, F.G. A half century of experimental neuroanatomical tracing. J. Chem. Neuroanat. 42, 157–183 (2011).
  Article PubMed Google Scholar
• Glover, J.C., Petursdottir, G. & Jansen, J.K. Fluorescent dextran-amines used as axonal tracers in the nervous system of the chicken embryo. J. Neurosci. Methods 18, 243–254 (1986).
  Article CAS PubMed Google Scholar
• Llewellyn-Smith, I.J., Martin, C.L., Arnolda, L.F. & Minson, J.B. Tracer-toxins: cholera toxin B-saporin as a model. J. Neurosci. Methods 103, 83–90 (2000).
  Article CAS PubMed Google Scholar
• Grinevich, V., Brecht, M. & Osten, P. Monosynaptic pathway from rat vibrissa motor cortex to facial motor neurons revealed by lentivirus-based axonal tracing. J. Neurosci. 25, 8250–8258 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Atasoy, D., Aponte, Y., Su, H.H. & Sternson, S.M. A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 28, 7025–7030 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995–1013 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010).
  Article CAS PubMed Google Scholar
• Madisen, L. et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat. Neurosci. 15, 793–802 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Harris, J.A., Wook Oh, S. & Zeng, H. Adeno-associated viral vectors for anterograde axonal tracing with fluorescent proteins in nontransgenic and cre driver mice. Curr. Protoc. Neurosci. 1.20, 21–18 (2012).
  Google Scholar
• Thompson, R.H. & Swanson, L.W. Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc. Natl. Acad. Sci. USA 107, 15235–15239 (2010).
  Article PubMed PubMed Central Google Scholar
• Gerfen, C.R. & Sawchenko, P.E. An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res. 290, 219–238 (1984).
  Article CAS PubMed PubMed Central Google Scholar
• Naumann, T., Hartig, W. & Frotscher, M. Retrograde tracing with Fluoro-Gold: different methods of tracer detection at the ultrastructural level and neurodegenerative changes of back-filled neurons in long-term studies. J. Neurosci. Methods 103, 11–21 (2000).
  Article CAS PubMed Google Scholar
• Reiner, A. et al. Pathway tracing using biotinylated dextran amines. J. Neurosci. Methods 103, 23–37 (2000).
  Article CAS PubMed Google Scholar
• Hintiryan, H. et al. Comprehensive connectivity of the mouse main olfactory bulb: analysis and online digital atlas. Front. Neuroanat. 6, 30 (2012).
  Article PubMed PubMed Central Google Scholar
• Conte, W.L., Kamishina, H. & Reep, R.L. Multiple neuroanatomical tract-tracing using fluorescent Alexa Fluor conjugates of cholera toxin subunit B in rats. Nat. Protoc. 4, 1157–1166 (2009).
  Article CAS PubMed Google Scholar
• Sunkin, S.M. et al. Allen Brain Atlas: an integrated spatio-temporal portal for exploring the central nervous system. Nucleic Acids Res. 41, D996–D1008 (2013).
  Article CAS PubMed Google Scholar
• Ugolini, G. Advances in viral transneuronal tracing. J. Neurosci. Methods 194, 2–20 (2010).
  Article PubMed Google Scholar
• Ekstrand, M.I., Enquist, L.W. & Pomeranz, L.E. The alpha-herpesviruses: molecular pathfinders in nervous system circuits. Trends Mol. Med. 14, 134–140 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Song, C.K., Enquist, L.W. & Bartness, T.J. New developments in tracing neural circuits with herpesviruses. Virus Res. 111, 235–249 (2005).
  Article CAS PubMed Google Scholar
• Callaway, E.M. Transneuronal circuit tracing with neurotropic viruses. Curr. Opin. Neurobiol. 18, 617–623 (2008).
  Article CAS PubMed Google Scholar
• Wickersham, I.R. & Feinberg, E.H. New technologies for imaging synaptic partners. Curr. Opin. Neurobiol. 22, 121–127 (2012).
  Article CAS PubMed Google Scholar
• Rancz, E.A. et al. Transfection via whole-cell recording in vivo: bridging single-cell physiology, genetics and connectomics. Nat. Neurosci. 14, 527–532 (2011).This study was the first to combine intracellular neuronal recording with DNA delivery. The authors use this method to map the synaptic function of a single cell in vivo and then target rabies-based retrograde labeling of the cells' synaptic input.
  Article CAS PubMed PubMed Central Google Scholar
• Miyamichi, K. et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 472, 191–196 (2011).
  Article CAS PubMed Google Scholar
• Marshel, J.H., Mori, T., Nielsen, K.J. & Callaway, E.M. Targeting single neuronal networks for gene expression and cell labeling in vivo. Neuron 67, 562–574 (2010).This paper describes an electroporation method for single-cell delivery of DNA for targeted infection of modified rabies virus.
  Article CAS PubMed PubMed Central Google Scholar
• Takatoh, J. et al. New modules are added to vibrissal premotor circuitry with the emergence of exploratory whisking. Neuron 77, 346–360 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Arenkiel, B.R. et al. Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS ONE 6, e29423 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Finke, S. & Conzelmann, K.K. Replication strategies of rabies virus. Virus Res. 111, 120–131 (2005).
  Article CAS PubMed Google Scholar
• Ugolini, G. Specificity of rabies virus as a transneuronal tracer of motor networks: transfer from hypoglossal motoneurons to connected second-order and higher order central nervous system cell groups. J. Comp. Neurol. 356, 457–480 (1995).
  Article CAS PubMed Google Scholar
• Federspiel, M.J., Bates, P., Young, J.A., Varmus, H.E. & Hughes, S.H. A system for tissue-specific gene targeting: transgenic mice susceptible to subgroup A avian leukosis virus-based retroviral vectors. Proc. Natl. Acad. Sci. USA 91, 11241–11245 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Young, J.A., Bates, P. & Varmus, H.E. Isolation of a chicken gene that confers susceptibility to infection by subgroup A avian leukosis and sarcoma viruses. J. Virol. 67, 1811–1816 (1993).
  CAS PubMed PubMed Central Google Scholar
• Wall, N.R., Wickersham, I.R., Cetin, A., De La Parra, M. & Callaway, E.M. Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus. Proc. Natl. Acad. Sci. USA 107, 21848–21853 (2010).
  Article PubMed PubMed Central Google Scholar
• Etessami, R. et al. Spread and pathogenic characteristics of a G-deficient rabies virus recombinant: an in vitro and in vivo study. J. Gen. Virol. 81, 2147–2153 (2000).
  Article CAS PubMed Google Scholar
• Lo, L. & Anderson, D.J.A. Cre-dependent, anterograde transsynaptic viral tracer for mapping output pathways of genetically marked neurons. Neuron 72, 938–950 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Beier, K.T. et al. Anterograde or retrograde transsynaptic labeling of CNS neurons with vesicular stomatitis virus vectors. Proc. Natl. Acad. Sci. USA 108, 15414–15419 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Hawrylycz, M. et al. Digital atlasing and standardization in the mouse brain. PLoS Comput. Biol. 7, e1001065 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Paxinos, G. & Franklin, K.B. The Mouse Brain in Stereotaxic Coordinates (Gulf Professional Publishing, 2004).
• Swanson, L.W. & Bota, M. Foundational model of structural connectivity in the nervous system with a schema for wiring diagrams, connectome, and basic plan architecture. Proc. Natl. Acad. Sci. USA 107, 20610–20617 (2010).
  Article PubMed PubMed Central Google Scholar
• Moene, I.A., Subramaniam, S., Darin, D., Leergaard, T.B. & Bjaalie, J.G. Toward a workbench for rodent brain image data: systems architecture and design. Neuroinformatics 5, 35–58 (2007).
  Article PubMed Google Scholar
• Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53–57 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• O'Rourke, N.A., Weiler, N.C., Micheva, K.D. & Smith, S.J. Deep molecular diversity of mammalian synapses: why it matters and how to measure it. Nat. Rev. Neurosci. 13, 365–379 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• DeFelipe, J. et al. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14, 202–216 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Emes, R.D. & Grant, S.G. Evolution of synapse complexity and diversity. Annu. Rev. Neurosci. 35, 111–131 (2012).
  Article CAS PubMed Google Scholar
• Micheva, K.D., Busse, B., Weiler, N.C., O'Rourke, N. & Smith, S.J. Single-synapse analysis of a diverse synapse population: proteomic imaging methods and markers. Neuron 68, 639–653 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Micheva, K.D. & Smith, S.J. Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55, 25–36 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Tsai, P.S. et al. Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels. J. Neurosci. 29, 14553–14570 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Oberlaender, M. et al. Cell type-specific three-dimensional structure of thalamocortical circuits in a column of rat vibrissal cortex. Cereb. Cortex 22, 2375–2391 (2012).
  Article PubMed Google Scholar
• Meyer, H.S. et al. Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A. Proc. Natl. Acad. Sci. USA 108, 16807–16812 (2011).
  Article PubMed PubMed Central Google Scholar
• Meyer, H.S. et al. Number and laminar distribution of neurons in a thalamocortical projection column of rat vibrissal cortex. Cereb. Cortex 20, 2277–2286 (2010).
  Article PubMed PubMed Central Google Scholar
• Ascoli, G.A. et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557–568 (2008).
  Article CAS PubMed Google Scholar
• Margrie, T.W. et al. Targeted whole-cell recordings in the mammalian brain in vivo. Neuron 39, 911–918 (2003).
  Article CAS PubMed Google Scholar
• Kitamura, K., Judkewitz, B., Kano, M., Denk, W. & Hausser, M. Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat. Methods 5, 61–67 (2008).
  Article CAS PubMed Google Scholar
• Angelo, K. et al. A biophysical signature of network affiliation and sensory processing in mitral cells. Nature 488, 375–378 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Reid, R.C. From functional architecture to functional connectomics. Neuron 75, 209–217 (2012).
  Article CAS PubMed Google Scholar
• Briggman, K.L., Helmstaedter, M. & Denk, W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183–188 (2011).
  Article CAS PubMed Google Scholar
• Bock, D.D. et al. Network anatomy and in vivo physiology of visual cortical neurons. Nature 471, 177–182 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Wallace, D.J. et al. Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor. Nat. Methods 5, 797–804 (2008).
  Article CAS PubMed Google Scholar
• Akerboom, J. et al. Optimization of a GCaMP calcium indicator for neural activity imaging. J. Neurosci. 32, 13819–13840 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Mank, M. et al. A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat. Methods 5, 805–811 (2008).
  Article CAS PubMed Google Scholar
• Ko, H. et al. Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87–91 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Holmgren, C., Harkany, T., Svennenfors, B. & Zilberter, Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J. Physiol. 551, 139–153 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Thomson, A.M., West, D.C., Wang, Y. & Bannister, A.P. Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2–5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb. Cortex 12, 936–953 (2002).
  Article PubMed Google Scholar
• Song, S., Sjostrom, P.J., Reigl, M., Nelson, S. & Chklovskii, D.B. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 3, e68 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Harvey, C.D., Collman, F., Dombeck, D.A. & Tank, D.W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941–946 (2009).This study introduced the method of physiological recording in head-restrained mice on a spherical treadmill while the mice performed spatial tasks in a virtual environment.
  Article CAS PubMed PubMed Central Google Scholar
• Harvey, C.D., Coen, P. & Tank, D.W. Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 484, 62–68 (2012).
  CAS PubMed PubMed Central Google Scholar
• Huber, D. et al. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484, 473–478 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Fenno, L., Yizhar, O. & Deisseroth, K. The development and application of optogenetics. Annu. Rev. Neurosci. 34, 389–412 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Koch, C. & Reid, R.C. Neuroscience: observatories of the mind. Nature 483, 397–398 (2012).
  Article CAS PubMed Google Scholar
• Alivisatos, A.P. et al. Neuroscience. The brain activity map. Science 339, 1284–1285 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Ahrens, M.B., Orger, M.B., Robson, D.N., Li, J.M. & Keller, P.J. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 10, 413–420 (2013).
  Article CAS PubMed Google Scholar
• Ahrens, M.B. et al. Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485, 471–477 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Herrera, D.G. & Robertson, H.A. Activation of c-fos in the brain. Prog. Neurobiol. 50, 83–107 (1996).
  Article CAS PubMed Google Scholar
• Barth, A.L., Gerkin, R.C. & Dean, K.L. Alteration of neuronal firing properties after in vivo experience in a FosGFP transgenic mouse. J. Neurosci. 24, 6466–6475 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Grinevich, V. et al. Fluorescent Arc/Arg3.1 indicator mice: a versatile tool to study brain activity changes in vitro and in vivo. J. Neurosci. Methods 184, 25–36 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Reijmers, L.G., Perkins, B.L., Matsuo, N. & Mayford, M. Localization of a stable neural correlate of associative memory. Science 317, 1230–1233 (2007).
  Article CAS PubMed Google Scholar