On Optical Detection of Densely Labeled Synapses in Neuropil and Mapping Connectivity with Combinatorially Multiplexed Fluorescent Synaptic Markers
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{"title"=>"On optical detection of densely labeled synapses in neuropil and mapping connectivity with combinatorially multiplexed fluorescent synaptic markers", "type"=>"journal", "authors"=>[{"first_name"=>"Yuriy", "last_name"=>"Mishchenko", "scopus_author_id"=>"36903063500"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-77749309878", "sgr"=>"77749309878", "pui"=>"358412633", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"20107507", "doi"=>"10.1371/journal.pone.0008853"}, "id"=>"4dcdf63b-f6fa-384f-8f39-ea47917aad7d", "abstract"=>"We propose a new method for mapping neural connectivity optically, by utilizing Cre/Lox system Brainbow to tag synapses of different neurons with random mixtures of different fluorophores, such as GFP, YFP, etc., and then detecting patterns of fluorophores at different synapses using light microscopy (LM). Such patterns will immediately report the pre- and post-synaptic cells at each synaptic connection, without tracing neural projections from individual synapses to corresponding cell bodies. We simulate fluorescence from a population of densely labeled synapses in a block of hippocampal neuropil, completely reconstructed from electron microscopy data, and show that high-end LM is able to detect such patterns with over 95% accuracy. We conclude, therefore, that with the described approach neural connectivity in macroscopically large neural circuits can be mapped with great accuracy, in scalable manner, using fast optical tools, and straightforward image processing. Relying on an electron microscopy dataset, we also derive and explicitly enumerate the conditions that should be met to allow synaptic connectivity studies with high-resolution optical tools.", "link"=>"http://www.mendeley.com/research/optical-detection-densely-labeled-synapses-neuropil-mapping-connectivity-combinatorially-multiplexed", "reader_count"=>67, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>22, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>2, "Other"=>3, "Student > Master"=>5, "Student > Bachelor"=>5, "Professor"=>7}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>22, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>18, "Student > Postgraduate"=>2, "Other"=>3, "Student > Master"=>5, "Student > Bachelor"=>5, "Professor"=>7}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>43, "Medicine and Dentistry"=>3, "Neuroscience"=>9, "Physics and Astronomy"=>4, "Computer Science"=>1, "Immunology and Microbiology"=>1, "Linguistics"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>9}, "Physics and Astronomy"=>{"Physics and Astronomy"=>4}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>43}, "Computer Science"=>{"Computer Science"=>1}, "Linguistics"=>{"Linguistics"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>4, "Japan"=>1, "United Kingdom"=>1, "Portugal"=>1, "Germany"=>2}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/866843"], "description"=>"<p>A) The fraction of unresolved synapses in the model of “spherical” synapses. Solid black line is for isotropic LM resolution; and the range corresponding to different synaptic densities, from 1 µm<sup>−3</sup> to 2 µm<sup>−3</sup>, is also shown (grayed area). Dashed lines are for LM instruments with anisotropic resolution, in which case the X-axis specifies the <i>axial</i> resolution of the instrument. Legend in A is also for B. B) The fraction of unresolved synapses in the model of “disk-shaped” synapses. Also shown is the fraction of optically resolved synapses determined directly from our EM reconstruction (squares).</p>", "links"=>[], "tags"=>["estimation", "optically", "resolved", "synapses", "lm"], "article_id"=>537296, "categories"=>["Neuroscience", "Biophysics"], "users"=>["Yuriy Mishchenko"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008853.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Theoretical_estimation_of_the_fraction_of_directly_optically_resolved_synapses_for_different_LM_resolutions_/537296", "title"=>"Theoretical estimation of the fraction of directly optically resolved synapses for different LM resolutions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:00:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/867013"], "description"=>"<p>A) Error rate for synapse detection as the function of the fluorophore molecules concentration on the synaptic membrane. Shown are Structured Illumination Microscopy (SIM, solid line), diffraction-limited microscopy on 100 nm slices (IDLM, dashed line), high-end confocal microscopy (<i>d</i><sub>xy</sub> = 0.2 µm and <i>d</i><sub>z</sub> = 0.6 µm, dash-dotted line), and low-end confocal microscopy (<i>d</i><sub>xy</sub> = 0.4 µm and <i>d</i><sub>z</sub> = 1.25 µm, dotted line). The error rate decays towards the resolution-set limits at about 200–400 µm<sup>−2</sup>. Legend in A is also for B and C. B) Error rate for synapse detection as the function of the photon budget. The error rate decays towards the resolution-set limits at about 50–100 photons/fluorophore molecule. C) Error rate for synapse detection as the function of the background fluorophore pollution. The error rate monotonically grows with the background density. Although the impact of the background is substantially different for different instruments, a generally acceptable range is 1–10 µM.</p>", "links"=>[], "tags"=>["synapse", "detection", "imaging"], "article_id"=>537473, "categories"=>["Neuroscience", "Biophysics"], "users"=>["Yuriy Mishchenko"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008853.g006", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Best_quality_of_synapse_detection_using_the_threshold_method_for_different_imaging_conditions_/537473", "title"=>"Best quality of synapse detection using the threshold method, for different imaging conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:01:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/866678"], "description"=>"<p>A) Using a 130 µm<sup>3</sup> block of hippocampal neuropil imaged with high-resolution electron microscopy, we investigate the possibility of detecting individual synapses optically. This block was fully segmented by the author, and all synapses were explicitly labeled. For illustration purposes, here is shown the 3D model of the reconstruction of all neuronal processes in said block, colored according to process type – yellow for dendrites, green for axons, and blue for glial processes. B) An example of the manual markup of the synapses within one electron micrograph (red lines). C) Simulated fluorescence from marked synapses (here, for isotropic diffraction limited microscopy, IDLM). Red arrows indicate synapses located directly inside shown EM section (B).</p>", "links"=>[], "tags"=>["microscopy", "reconstruction"], "article_id"=>537138, "categories"=>["Neuroscience", "Biophysics"], "users"=>["Yuriy Mishchenko"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008853.g001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Electron_Microscopy_reconstruction_data_/537138", "title"=>"Electron Microscopy reconstruction data.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 02:59:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/866955"], "description"=>"<p>Normalized histogram (gray) and respective cumulative distribution function (black line) are shown. The mean size is shown with dashed line. As can be seen here, distribution of synapse sizes is similar to the exponential distribution, with the majority of synapses measuring only up to 0.05 µm<sup>2</sup>.</p>", "links"=>[], "tags"=>["synapse", "sizes", "em"], "article_id"=>537414, "categories"=>["Neuroscience", "Biophysics"], "users"=>["Yuriy Mishchenko"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008853.g005", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_synapse_sizes_measured_from_our_EM_reconstruction_/537414", "title"=>"Distribution of synapse sizes measured from our EM reconstruction.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:01:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/866895"], "description"=>"<p><i>R</i> is the distance between centers of two synapses in the microscope's focal plane (lateral distance), and <i>Z</i> is the distance along the optical axis (axial distance). <i>θ</i> and <i>θ′</i> are the orientations of two synapses relative to the microscope's optical axis. Two synapses are said to not be resolved if there are any two points on their surfaces, <b>A</b> and <b>B</b>, that are closer together than the microscope's resolution limit. This condition can be expressed as a quadratic program, which should be solved numerically for each (<i>R</i>,<i>Z</i>,<i>θ</i>,<i>θ′</i>).</p>", "links"=>[], "tags"=>["setup", "unresolved", "synapses"], "article_id"=>537352, "categories"=>["Neuroscience", "Biophysics"], "users"=>["Yuriy Mishchenko"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008853.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Geometry_setup_for_calculating_the_fraction_of_unresolved_synapses_at_a_relative_position_R_Z_/537352", "title"=>"Geometry setup for calculating the fraction of unresolved synapses at a relative position (<i>R</i>,<i>Z</i>).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:01:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/866772"], "description"=>"<p>A) Schematic diagram of the synaptic Brainbow, with a red fluorophore on the pre-synaptic side and a green fluorophore on the post-synaptic side of a synaptic cleft. Spatial correlation of the fluorescence from the pre- and post-synaptic fluorophores, occurring due to their proximity across synaptic cleft, allows detecting synapses optically without explicitly resolving them. Due to absence of the fluorophores in the bulk of the axonal and dendritic cytoplasm, nearby processes do not interfere with the detection process even when all neurons are labeled, unlike in regular Brainbow. B) Due to close spatial co-localization of the pre- and post-synaptic fluorophores across the synaptic cleft, their fluorescence intensity is closely correlated near labeled synapses. In this figure we show a simulated scatter plot of the fluorescence intensity in IDLM. Blue dots represent voxels far away from one labeled synapse (further than ≈200 nm), and red dots represent voxels closer than ≈200 nm. One can threshold this diagram with certain thresholds, T<sub>1</sub> for the pre-synaptic marker and T<sub>2</sub> for the post-synaptic marker (dashed lines), in order to separate the proximal (red) from distant (blue) voxels, and thus detect presence of a synapse. C) Using correlations in the fluorescence from the pre- and post-synaptic markers, synapses may be detected even when they cannot be explicitly resolved into isolated puncta. Illustrated here are three “synapses”, fluorescence from which individually is shown with thin blue, magenta and brown lines. These are observed using two fluorescent markers, green and red. First synapse is tagged only with “green” marker, second synapse is tagged with “green” and “red” markers, and third synapse is tagged with “red” marker. Combined fluorescence from these synapses is shown with thick red and green lines, for the two markers respectively. Even though none of synapses can be seen separately in either green or red channels, by thresholding fluorescence with appropriate thresholds, T<sub>1</sub> and T<sub>2</sub>, three different supra-threshold fluorescence patterns (black dots) indicate presence of three synapses.</p>", "links"=>[], "tags"=>["synapse", "detection", "co-localization", "fluorescence", "pre-", "post-synaptic"], "article_id"=>537227, "categories"=>["Neuroscience", "Biophysics"], "users"=>["Yuriy Mishchenko"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008853.g002", "stats"=>{"downloads"=>1, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_explanation_of_synapse_detection_using_co_localization_of_fluorescence_from_different_pre_and_post_synaptic_markers_/537227", "title"=>"Schematic explanation of synapse detection using co-localization of fluorescence from different pre- and post-synaptic markers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:00:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/867076"], "description"=>"<p>For comparison also shown: the fraction of optically resolvable synapses in theoretical model of “spherical” synapses (dashed gray line), the fraction (solid gray line) and the range (grayed area, for different synaptic densities from 1 µm<sup>−3</sup> to 2 µm<sup>−3</sup>) of optically resolvable synapses in theoretical model with “disk-shaped” synapses, and the empirical fraction of optically resolvable synapses determined from our EM reconstruction data (squares).</p>", "links"=>[], "tags"=>["synapse", "detection", "lm"], "article_id"=>537534, "categories"=>["Neuroscience", "Biophysics"], "users"=>["Yuriy Mishchenko"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008853.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Best_quality_of_synapse_detection_using_the_threshold_method_for_different_LM_resolutions_/537534", "title"=>"Best quality of synapse detection using the threshold method, for different LM resolutions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:02:15"}

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