Transcriptome Tomography for Brain Analysis in the Web-Accessible Anatomical Space
Publication Date
September 19, 2012
Journal
PLOS ONE
Authors
Yuko Okamura Oho, Kazuro Shimokawa, Satoko Takemoto, Asami Hirakiyama, et al
Volume
7
Issue
9
Pages
e45373
DOI
https://dx.plos.org/10.1371/journal.pone.0045373
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0045373
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23028969
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3446890
Europe PMC
http://europepmc.org/abstract/MED/23028969
Web of Science
000309388400080
Scopus
84866542711
Mendeley
http://www.mendeley.com/research/transcriptome-tomography-brain-analysis-webaccessible-anatomical-space
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Mendeley | Further Information

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Determination of gene expression-anatomy associations is crucial for this understanding. To elicit the association in the three-dimensional (3D) space, we introduce a novel technique for comprehensive mapping of endogenous gene expression into a web-accessible standard space: Transcriptome Tomography. The technique is based on conjugation of sequential tissue-block sectioning, all fractions of which are used for molecular measurements of gene expression densities, and the block- face imaging, which are used for 3D reconstruction of the fractions. To generate a 3D map, tissues are serially sectioned in each of three orthogonal planes and the expression density data are mapped using a tomographic technique. This rapid and unbiased mapping technique using a relatively small number of original data points allows researchers to create their own expression maps in the broad anatomical context of the space. In the first instance we generated a dataset of 36,000 maps, reconstructed from data of 61 fractions measured with microarray, covering the whole mouse brain (ViBrism: http://vibrism.riken.jp/3dviewer/ex/index.html) in one month. After computational estimation of the mapping accuracy we validated the dataset against existing data with respect to the expression location and density. To demonstrate the relevance of the framework, we showed disease related expression of Huntington's disease gene and Bdnf. Our tomographic approach is applicable to analysis of any biological molecules derived from frozen tissues, organs and whole embryos, and the maps are spatially isotropic and well suited to the analysis in the standard space (e.g. Waxholm Space for brain-atlas databases). This will facilitate research creating and using open-standards for a molecular-based understanding of complex structures; and will contribute to new insights into a broad range of biological and medical questions.", "link"=>"http://www.mendeley.com/research/transcriptome-tomography-brain-analysis-webaccessible-anatomical-space", "reader_count"=>27, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>1, "Student > Bachelor"=>5, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. 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Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/304271", "https://ndownloader.figshare.com/files/304330", "https://ndownloader.figshare.com/files/304346", "https://ndownloader.figshare.com/files/304369", "https://ndownloader.figshare.com/files/304394", "https://ndownloader.figshare.com/files/304488", "https://ndownloader.figshare.com/files/304548", "https://ndownloader.figshare.com/files/304802"], "description"=>"<div><p>Increased information on the encoded mammalian genome is expected to facilitate an integrated understanding of complex anatomical structure and function based on the knowledge of gene products. Determination of gene expression-anatomy associations is crucial for this understanding. To elicit the association in the three-dimensional (3D) space, we introduce a novel technique for comprehensive mapping of endogenous gene expression into a web-accessible standard space: Transcriptome Tomography. The technique is based on conjugation of sequential tissue-block sectioning, all fractions of which are used for molecular measurements of gene expression densities, and the block- face imaging, which are used for 3D reconstruction of the fractions. To generate a 3D map, tissues are serially sectioned in each of three orthogonal planes and the expression density data are mapped using a tomographic technique. This rapid and unbiased mapping technique using a relatively small number of original data points allows researchers to create their own expression maps in the broad anatomical context of the space. In the first instance we generated a dataset of 36,000 maps, reconstructed from data of 61 fractions measured with microarray, covering the whole mouse brain (ViBrism: <a href=\"http://vibrism.riken.jp/3dviewer/ex/index.html\">http://vibrism.riken.jp/3dviewer/ex/index.html</a>) in one month. After computational estimation of the mapping accuracy we validated the dataset against existing data with respect to the expression location and density. To demonstrate the relevance of the framework, we showed disease related expression of Huntington’s disease gene and <em>Bdnf</em>. Our tomographic approach is applicable to analysis of any biological molecules derived from frozen tissues, organs and whole embryos, and the maps are spatially isotropic and well suited to the analysis in the standard space (e.g. Waxholm Space for brain-atlas databases). This will facilitate research creating and using open-standards for a molecular-based understanding of complex structures; and will contribute to new insights into a broad range of biological and medical questions.</p> </div>", "links"=>[], "tags"=>["transcriptome", "tomography", "web-accessible", "anatomical"], "article_id"=>120009, "categories"=>["Biological Sciences", "Neuroscience", "Information And Computing Sciences", "Mathematics", "Physiology", "Biotechnology", "Genetics"], "users"=>["Yuko Okamura-Oho", "Kazuro Shimokawa", "Satoko Takemoto", "Asami Hirakiyama", "Sakiko Nakamura", "Yuki Tsujimura", "Masaomi Nishimura", "Takeya Kasukawa", "Koh-hei Masumoto", "Itoshi Nikaido", "Yasufumi Shigeyoshi", "Hiroki R. Ueda", "Gang Song", "James Gee", "Ryutaro Himeno", "Hideo Yokota"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0045373.s001", "https://dx.doi.org/10.1371/journal.pone.0045373.s002", "https://dx.doi.org/10.1371/journal.pone.0045373.s003", "https://dx.doi.org/10.1371/journal.pone.0045373.s004", "https://dx.doi.org/10.1371/journal.pone.0045373.s005", "https://dx.doi.org/10.1371/journal.pone.0045373.s006", "https://dx.doi.org/10.1371/journal.pone.0045373.s007", "https://dx.doi.org/10.1371/journal.pone.0045373.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Transcriptome_Tomography_for_Brain_Analysis_in_the_Web_Accessible_Anatomical_Space/120009", "title"=>"Transcriptome Tomography for Brain Analysis in the Web-Accessible Anatomical Space", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-09-19 00:00:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/573988"], "description"=>"<p>(<b>A</b>) <b>A schematic illustrated using a model material.</b> Two types of data, material shape images (drawn with green lines) and gene expression densities (shown in red) of fractions (indicated with asterisks), are obtained with sectioning, conjugated with block-face imaging and expression density measurement, along three body axes (shown in parentheses). The three series of sectioning are named after orthogonal planes (C, S and H). The densities are assigned to the voxels (pixels on a regular grid in a 3D space) in the images (as shown with +) and subjected to tomographic reconstruction (indicated in purple). A series of the process from one direction needs one material; therefore, at least three genetically identical materials were required. (<b>B</b>) <b>An outline of the technique and the first dataset creation.</b> Two types of data, fraction templates, which are the material shape image (in green) and fraction data, which are gene expression densities measured with microarray (in dotted red), were acquired from the same fractions prepared with a sectioning machine 3D-ISM <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373-Yokota1\" target=\"_blank\">[12]</a>. The fractions were named “image fractions” for the former data and “material fractions” for the latter (the preparation process seen in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373.s007\" target=\"_blank\">Video S1</a>). Six fraction templates for the first dataset, two groups of three series sectioned in each of orthogonal and slightly oblique to the orthogonal planes: S/C/H and So/Co/Ho, composed of 9/13/6 and 10/16/7 fractions, respectively, (61 fractions in total as seen in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373.s001\" target=\"_blank\">Figure S1B</a>), are shown with fraction numbers in Template C: 13 fractions of 1 mm (5 µm×200 sections)-thickness. The pseudo-tomography technique of mapping in a single coordinate space (named ViBrism) including image registration, pseudo-back projection and tomographic reconstruction is shown in the flowchart (see details in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373.s001\" target=\"_blank\">Figure S1A</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373.s005\" target=\"_blank\">Text S1</a>). After volume rendering, 3D expression maps for genes (a sample: Slitrk6) are visualized as pseudo-colored expression densities and anatomical images with an 80% cutoff filter (also seen in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373.s008\" target=\"_blank\">Video S2</a>). Slitrk6 is known to be expressed mostly in the thalamus as shown in the Allen Brain Atlas and BrainStars databases: 2Dand 3D views displayed here are compatible to those data shown below in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone-0045373-g004\" target=\"_blank\">Figure 4A and B</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373.s008\" target=\"_blank\">VideoS2</a>.</p>", "links"=>[], "tags"=>["genetics and genomics", "physiology", "biotechnology", "Computational biology", "neuroscience", "computer science", "neurological disorders", "mathematics"], "article_id"=>244455, "categories"=>["Biological Sciences", "Neuroscience", "Information And Computing Sciences", "Mathematics", "Physiology", "Biotechnology", "Genetics"], "users"=>["Yuko Okamura-Oho", "Kazuro Shimokawa", "Satoko Takemoto", "Asami Hirakiyama", "Sakiko Nakamura", "Yuki Tsujimura", "Masaomi Nishimura", "Takeya Kasukawa", "Koh-hei Masumoto", "Itoshi Nikaido", "Yasufumi Shigeyoshi", "Hiroki R. Ueda", "Gang Song", "James Gee", "Ryutaro Himeno", "Hideo Yokota"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0045373.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transcriptome_Tomography_/244455", "title"=>"Transcriptome Tomography.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-19 01:14:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/574110"], "description"=>"<p>Gene expression that was evenly distributed in one of the test spheres located randomly in the virtual brain of ViBrism was computationally reconstructed (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373.s006\" target=\"_blank\">Text S2</a> for Supporting Methods). A histogram for the number of test spheres with true positive rates (% of TP: percentages of test sphere volumes overlapped with the reconstructed area) is shown. Maps of the reconstructed results (shown in yellow) with the test spheres (in red) are attached. In 2D maps, the 80% cutoff filter was applied to the results of left-upper S panels; otherwise, the reconstructed densities are shown in gray scales. 3D maps are shown with the filter. Approximately one fifth (20.4%) of the test spheres had more than 95% of TP, which is the mode in the histogram, and 94.7% in total had at least 5% of TP as indicated. One of the mode results, the median result (TP = 80%) and one of the poorly reconstructed results (TP<5%) are shown. Only 0.8% of the test spheres resulted in no TP, which was mainly due to the peripheral location of the test spheres in the virtual brain (data not shown).</p>", "links"=>[], "tags"=>["computational", "reconstruction"], "article_id"=>244582, "categories"=>["Biological Sciences", "Neuroscience", "Information And Computing Sciences", "Mathematics", "Physiology", "Biotechnology", "Genetics"], "users"=>["Yuko Okamura-Oho", "Kazuro Shimokawa", "Satoko Takemoto", "Asami Hirakiyama", "Sakiko Nakamura", "Yuki Tsujimura", "Masaomi Nishimura", "Takeya Kasukawa", "Koh-hei Masumoto", "Itoshi Nikaido", "Yasufumi Shigeyoshi", "Hiroki R. Ueda", "Gang Song", "James Gee", "Ryutaro Himeno", "Hideo Yokota"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0045373.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_for_the_computational_experiment_of_reconstruction_using_1_366_test_spheres_/244582", "title"=>"Results for the computational experiment of reconstruction using 1,366 test spheres.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-19 01:16:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/574293"], "description"=>"<p>(<b>A</b>) <b>B* areas mapped in the ViBrism space.</b> To compare datasets obtained from different anatomical contexts, areas selected for BrainStars analysis (B* areas; 500-µm-diameter spheres) were mapped onto the ViBrism space as shown in the website Video C (<a href=\"http://opensciences.brent-research.org/home/project-updates\" target=\"_blank\">http://opensciences.brent-research.org/home/project-updates</a>). (<b>B</b>) <b>Comparison of the expression datasets of ViBrism 3D mapped data and BrainStars data in B* areas in a scatter plot.</b> 3D mapped data re-calculated in the 46 areas for 17,155 gene probes were log-2 transformed and plotted against BrainStars expression intensity data. Despite two datasets were obtained from different anatomical contexts using different material preparation procedures and microarray platforms, good agreement was observed in a scatter plot (r = 0.73, p<1.0×10<sup>−12</sup>). (<b>C</b>) <b>Coefficient of variance (CV) of the 3D-mapped data for each quantile window of the corresponding expression intensity values in the BrainStars dataset.</b> For the each 0.02-quantile window of the BrainStars dataset, the CVs (standard deviation/mean of non-log transformed values) of the re-calculated 3D-mapped data were calculated and dotted.</p>", "links"=>[], "tags"=>["3d", "mapped"], "article_id"=>244765, "categories"=>["Biological Sciences", "Neuroscience", "Information And Computing Sciences", "Mathematics", "Physiology", "Biotechnology", "Genetics"], "users"=>["Yuko Okamura-Oho", "Kazuro Shimokawa", "Satoko Takemoto", "Asami Hirakiyama", "Sakiko Nakamura", "Yuki Tsujimura", "Masaomi Nishimura", "Takeya Kasukawa", "Koh-hei Masumoto", "Itoshi Nikaido", "Yasufumi Shigeyoshi", "Hiroki R. Ueda", "Gang Song", "James Gee", "Ryutaro Himeno", "Hideo Yokota"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0045373.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Validation_of_3D_mapped_data_/244765", "title"=>"Validation of 3D mapped data.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-19 01:19:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/574462"], "description"=>"<p>(<b>A</b>) <b>Comparison of 3D expression maps to B* area maps.</b> 3D expression maps of 40 regionally expressed genes were chosen (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373.s003\" target=\"_blank\">Table S2</a>). Corresponding B* area maps were overlaid on the expression maps and highlighted as 500 µm in diameters with VCAT. The names of the genes and the B* areas are shown at the top and the bottom of panels respectively. Spheres of the B* areas are indicated with arrows in the panels. If the gene expression areas indicated with yellow/orange/red colors are located in the B* areas, the colors are highlighted to be seen in the spheres (23 genes): otherwise, gray colors appear. In most latter cases, the gene expression areas were located close to the highlighted spheres, suggesting that the distances between the areas and the spheres were mainly caused by the resolution differences of two systems. All maps were viewed in the same angle to show the expression pattern differences. Color codes for are shown. (<b>B</b>) <b>Comparison of 3D Expression maps to ABA maps.</b> Among the 40 regionally expressed genes, 3D map data of 33 genes were available in ABA. Expression maps in ABA and our maps (ViBrism) were visualized with VCAT. The names of the gene and the B* area, in which the gene was selectively expressed, are shown at the top and the bottom of panels for ViBrism, respectively. B* areas are indicated with arrows in the maps of ViBrism in the same way as <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone-0045373-g004\" target=\"_blank\">Figure 4A</a> and are also indicated in the maps of ABA if the areas were visualized with high expression. Expression areas common in the two maps but outside the named B* areas are indicated with asterisks. All maps are shown in the same angle to show the expression pattern differences. Color codes for ABA and ViBrism are shown.</p>", "links"=>[], "tags"=>["3d"], "article_id"=>244928, "categories"=>["Biological Sciences", "Neuroscience", "Information And Computing Sciences", "Mathematics", "Physiology", "Biotechnology", "Genetics"], "users"=>["Yuko Okamura-Oho", "Kazuro Shimokawa", "Satoko Takemoto", "Asami Hirakiyama", "Sakiko Nakamura", "Yuki Tsujimura", "Masaomi Nishimura", "Takeya Kasukawa", "Koh-hei Masumoto", "Itoshi Nikaido", "Yasufumi Shigeyoshi", "Hiroki R. Ueda", "Gang Song", "James Gee", "Ryutaro Himeno", "Hideo Yokota"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0045373.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Validation_of_3D_expression_maps_/244928", "title"=>"Validation of 3D expression maps.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-19 01:22:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/574614"], "description"=>"<p><b>(A) Quantified expression variances of </b><b><i>Htt</i></b><b>, related to differential vulnerability in the disease.</b> 3D expression maps of <i>Htt</i> are highlighted in areas (with arrows) defined by the expression of area-marker genes (named at the bottom of the panels), which are known to be expressed in the anatomical regions or the cell types (named at the top). Percentages of <i>Htt</i> expression densities (100% in the motor CTX) and the vulnerability of the areas in Huntington’s disease are indicated below the panels. *: significantly lower compared to motor CTX (p = 10<sup>−5</sup>–10<sup>−41</sup>), **: selective cells are partly affected <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373-Oyanagi1\" target=\"_blank\">[21]</a><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373-Jeste1\" target=\"_blank\">[23]</a>. (<b>B</b>) <b>Expression variances of Bdnf related to the vulnerability of the disease.</b> 3D expression maps of <i>Bdnf</i> in the areas defined by the expression of area maker genes as indicated are shown along with the vulnerability of the areas. (<b>C</b>) <b>Expression maps of </b><b><i>Htt</i></b><b> in brain areas defined by </b><b><i>Bdnf</i></b><b> expression.</b> The maps, a percentage of <i>Htt</i> expression densities and the vulnerability of the areas are visualized in the same way as in A. An Arrow indicates high expression of <i>Htt</i>, and <i>Bdnf</i> in the posterior cerebrum. Abbreviations for neural cell types: GABA: GABAergic, Ach: Acetyl-cholinergic, DA: dopaminergic, 5HT: serotonergic, NAd: noradrenalinergic. Abbreviations for brain regions: CA: Ammon’s Horn, CB: cerebellum, CPu: caudate putamen, CTX: cerebral cortex, Hipp: hippocampus, DG: dentate gyrus, SN: substantia nigra, VTA: ventral tegmental area, Tg: dorsal tegmental nucleus.</p>", "links"=>[], "tags"=>["densities", "genes", "areas", "defined", "area-marker"], "article_id"=>245082, "categories"=>["Biological Sciences", "Neuroscience", "Information And Computing Sciences", "Mathematics", "Physiology", "Biotechnology", "Genetics"], "users"=>["Yuko Okamura-Oho", "Kazuro Shimokawa", "Satoko Takemoto", "Asami Hirakiyama", "Sakiko Nakamura", "Yuki Tsujimura", "Masaomi Nishimura", "Takeya Kasukawa", "Koh-hei Masumoto", "Itoshi Nikaido", "Yasufumi Shigeyoshi", "Hiroki R. Ueda", "Gang Song", "James Gee", "Ryutaro Himeno", "Hideo Yokota"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0045373.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_densities_of_Huntington_8217_s_disease_related_genes_in_the_brain_areas_defined_by_area_marker_gene_expression_/245082", "title"=>"Expression densities of Huntington’s disease related genes in the brain areas defined by area-marker gene expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-19 01:24:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/574747"], "description"=>"<p>(<b>A</b>) <b>A schematic for the integration.</b> E80, the brain volume common to all expression maps in the ViBrism space, (colored in green) was transformed (shown with an arrow) into the brain volume in the Waxholm Space (WHS in gray). (<b>B–D</b>) <b>Integration of Huntington’s disease-related maps.</b> Areas defined by the gene expression of a pathogenetic combination deduced from the previous knowledge, Htt(+)/Bdnf(−), are colored with the Htt expression density in the ViBrism space (a right small panel in B). After the transformation into WHS, the areas are highlighted and colored with anatomical labels based on MRI data <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373-Johnson1\" target=\"_blank\">[26]</a> (a large panel in B). The areas contain vulnerable regions in this disease as follows: Label 1; Cerebral cortex (anterior rather than posterior, 22% of the volume with label 1), 9; Ventral thalamic nuclei (100%) <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373-Dom1\" target=\"_blank\">[28]</a>, 15; Globus pallidus (100%) <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373-Han1\" target=\"_blank\">[17]</a> shown in the panel D, 23; CPu (99%) also seen in the panel C, 24; hippocampus (77%), 37; cerebellum (21%). <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045373#pone.0045373.s004\" target=\"_blank\">Table S3</a> shows % of volumes overlapped with the Htt(+)Bdnf(−) areas in each of 37 anatomical regions labeled in WHS. The MRI T1 and T2* atlases are shown in the rectangular vertical and horizontal planes, respectively.</p>", "links"=>[], "tags"=>["3d", "maps", "whs", "mri"], "article_id"=>245216, "categories"=>["Biological Sciences", "Neuroscience", "Information And Computing Sciences", "Mathematics", "Physiology", "Biotechnology", "Genetics"], "users"=>["Yuko Okamura-Oho", "Kazuro Shimokawa", "Satoko Takemoto", "Asami Hirakiyama", "Sakiko Nakamura", "Yuki Tsujimura", "Masaomi Nishimura", "Takeya Kasukawa", "Koh-hei Masumoto", "Itoshi Nikaido", "Yasufumi Shigeyoshi", "Hiroki R. Ueda", "Gang Song", "James Gee", "Ryutaro Himeno", "Hideo Yokota"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0045373.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spatial_integration_of_3D_expression_maps_into_the_WHS_MRI_digital_atlas_/245216", "title"=>"Spatial integration of 3D expression maps into the WHS MRI digital atlas.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-19 01:26:56"}

PMC Usage Stats | Further Information

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