Adult mouse cortical cell taxonomy revealed by single cell transcriptomics (original) (raw)

• Lein, E.S. et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168–176 (2007).
  CAS PubMed Google Scholar
• Hawrylycz, M.J. et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489, 391–399 (2012).
  CAS PubMed PubMed Central Google Scholar
• Harris, K.D. & Shepherd, G.M. The neocortical circuit: themes and variations. Nat. Neurosci. 18, 170–181 (2015).
  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).
  CAS PubMed PubMed Central Google Scholar
• Sugino, K. et al. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat. Neurosci. 9, 99–107 (2006).
  CAS PubMed Google Scholar
• Rudy, B., Fishell, G., Lee, S. & Hjerling-Leffler, J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45–61 (2011).
  PubMed PubMed Central Google Scholar
• Sorensen, S.A. et al. Correlated gene expression and target specificity demonstrate excitatory projection neuron diversity. Cereb. Cortex 25, 433–449 (2015).
  PubMed Google Scholar
• Greig, L.C., Woodworth, M.B., Galazo, M.J., Padmanabhan, H. & Macklis, J.D. Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 14, 755–769 (2013).
  CAS PubMed Google Scholar
• Toledo-Rodriguez, M. et al. Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. Cereb. Cortex 14, 1310–1327 (2004).
  PubMed 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).
  CAS PubMed Google Scholar
• Belgard, T.G. et al. A transcriptomic atlas of mouse neocortical layers. Neuron 71, 605–616 (2011).
  CAS PubMed PubMed Central Google Scholar
• Cahoy, J.D. et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28, 264–278 (2008).
  CAS PubMed PubMed Central Google Scholar
• Zhang, Y. et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34, 11929–11947 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Pollen, A.A. et al. Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex. Nat. Biotechnol. 32, 1053–1058 (2014).
  CAS PubMed PubMed Central Google Scholar
• Usoskin, D. et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Neurosci. 18, 145–153 (2015).
  CAS PubMed Google Scholar
• Zeisel, A. et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347, 1138–1142 (2015).
  CAS PubMed Google Scholar
• Macosko, E.Z. et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161, 1202–1214 (2015).
  CAS PubMed PubMed Central Google Scholar
• Glickfeld, L.L., Reid, R.C. & Andermann, M.L. A mouse model of higher visual cortical function. Curr. Opin. Neurobiol. 24, 28–33 (2014).
  CAS PubMed Google Scholar
• Harris, J.A. et al. Anatomical characterization of Cre driver mice for neural circuit mapping and manipulation. Front. Neural Circuits 8, 76 (2014).
  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).
  CAS PubMed PubMed Central Google Scholar
• Olsen, S.R., Bortone, D.S., Adesnik, H. & Scanziani, M. Gain control by layer six in cortical circuits of vision. Nature 483, 47–52 (2012).
  CAS PubMed PubMed Central Google Scholar
• Huang, Z.J. Toward a genetic dissection of cortical circuits in the mouse. Neuron 83, 1284–1302 (2014).
  CAS PubMed PubMed Central Google Scholar
• Gonchar, Y., Wang, Q. & Burkhalter, A.H. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front. Neuroanat. 1, 3 (2008).
  PubMed PubMed Central Google Scholar
• Xu, X., Roby, K.D. & Callaway, E.M. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J. Comp. Neurol. 518, 389–404 (2010).
  PubMed PubMed Central Google Scholar
• Pfeffer, C.K., Xue, M., He, M., Huang, Z.J. & Scanziani, M. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16, 1068–1076 (2013).
  CAS PubMed PubMed Central Google Scholar
• Xu, X., Roby, K.D. & Callaway, E.M. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J. Comp. Neurol. 499, 144–160 (2006).
  CAS PubMed Google Scholar
• Oliva, A.A. Jr., Jiang, M., Lam, T., Smith, K.L. & Swann, J.W. Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J. Neurosci. 20, 3354–3368 (2000).
  CAS PubMed PubMed Central Google Scholar
• Seress, L., Abrahám, H., Hajnal, A., Lin, H. & Totterdell, S. NOS-positive local circuit neurons are exclusively axo-dendritic cells both in the neo- and archi-cortex of the rat brain. Brain Res. 1056, 183–190 (2005).
  CAS PubMed Google Scholar
• Lee, J.E. & Jeon, C.J. Immunocytochemical localization of nitric oxide synthase–containing neurons in mouse and rabbit visual cortex and co-localization with calcium-binding proteins. Mol. Cells 19, 408–417 (2005).
  CAS PubMed Google Scholar
• Tomioka, R. et al. Demonstration of long-range GABAergic connections distributed throughout the mouse neocortex. Eur. J. Neurosci. 21, 1587–1600 (2005).
  PubMed Google Scholar
• Gerashchenko, D. et al. Identification of a population of sleep-active cerebral cortex neurons. Proc. Natl. Acad. Sci. USA 105, 10227–10232 (2008).
  CAS PubMed PubMed Central Google Scholar
• Taniguchi, H., Lu, J. & Huang, Z.J. The spatial and temporal origin of chandelier cells in mouse neocortex. Science 339, 70–74 (2013).
  CAS PubMed Google Scholar
• Dehorter, N. et al. Tuning of fast-spiking interneuron properties by an activity-dependent transcriptional switch. Science 349, 1216–1220 (2015).
  CAS PubMed PubMed Central Google Scholar
• von Engelhardt, J., Eliava, M., Meyer, A.H., Rozov, A. & Monyer, H. Functional characterization of intrinsic cholinergic interneurons in the cortex. J. Neurosci. 27, 5633–5642 (2007).
  CAS PubMed PubMed Central Google Scholar
• Molyneaux, B.J., Arlotta, P., Menezes, J.R. & Macklis, J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427–437 (2007).
  CAS PubMed Google Scholar
• Zeng, H. et al. Large-scale cellular-resolution gene profiling in human neocortex reveals species-specific molecular signatures. Cell 149, 483–496 (2012).
  CAS PubMed PubMed Central Google Scholar
• Sommer, B. et al. Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249, 1580–1585 (1990).
  CAS PubMed Google Scholar
• Vélez-Fort, M. et al. The stimulus selectivity and connectivity of layer six principal cells reveals cortical microcircuits underlying visual processing. Neuron 83, 1431–1443 (2014).
  PubMed PubMed Central Google Scholar
• Bortone, D.S., Olsen, S.R. & Scanziani, M. Translaminar inhibitory cells recruited by layer 6 corticothalamic neurons suppress visual cortex. Neuron 82, 474–485 (2014).
  CAS PubMed PubMed Central Google Scholar
• Kawaguchi, Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci. 15, 2638–2655 (1995).
  CAS PubMed PubMed Central Google Scholar
• Hestrin, S. & Armstrong, W.E. Morphology and physiology of cortical neurons in layer I. J. Neurosci. 16, 5290–5300 (1996).
  CAS PubMed PubMed Central Google Scholar
• Povysheva, N.V. et al. Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex. J. Neurophysiol. 97, 1030–1039 (2007).
  CAS PubMed Google Scholar
• Chu, Z., Galarreta, M. & Hestrin, S. Synaptic interactions of late-spiking neocortical neurons in layer 1. J. Neurosci. 23, 96–102 (2003).
  CAS PubMed PubMed Central Google Scholar
• Simon, A., Oláh, S., Molnár, G., Szabadics, J. & Tamás, G. Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J. Neurosci. 25, 6278–6285 (2005).
  CAS PubMed PubMed Central Google Scholar
• Karayannis, T. et al. Slow GABA transient and receptor desensitization shape synaptic responses evoked by hippocampal neurogliaform cells. J. Neurosci. 30, 9898–9909 (2010).
  CAS PubMed PubMed Central Google Scholar
• Kawaguchi, Y. & Kubota, Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476–486 (1997).
  CAS PubMed Google Scholar
• Muralidhar, S., Wang, Y. & Markram, H. Synaptic and cellular organization of layer 1 of the developing rat somatosensory cortex. Front. Neuroanat. 7, 52 (2013).
  PubMed Google Scholar
• Herculano-Houzel, S., Watson, C. & Paxinos, G. Distribution of neurons in functional areas of the mouse cerebral cortex reveals quantitatively different cortical zones. Front. Neuroanat. 7, 35 (2013).
  PubMed PubMed Central Google Scholar
• DeFelipe, J. Cortical interneurons: from Cajal to 2001. Prog. Brain Res. 136, 215–238 (2002).
  PubMed Google Scholar
• Jaitin, D.A. et al. Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types. Science 343, 776–779 (2014).
  CAS PubMed PubMed Central Google Scholar
• Rossi, J. et al. Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab. 13, 195–204 (2011).
  CAS PubMed PubMed Central Google Scholar
• Gerfen, C.R., Paletzki, R. & Heintz, N. GENSAT BAC cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits. Neuron 80, 1368–1383 (2013).
  CAS PubMed Google Scholar
• Franco, S.J. et al. Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 337, 746–749 (2012).
  CAS PubMed PubMed Central Google Scholar
• Dhillon, H. et al. Leptin directly activates SF1 neurons in the VMH, and this action by leptin is required for normal body-weight homeostasis. Neuron 49, 191–203 (2006).
  CAS PubMed Google Scholar
• Madisen, L. et al. Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance. Neuron 85, 942–958 (2015).
  CAS PubMed PubMed Central Google Scholar
• Hippenmeyer, S. et al. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3, e159 (2005).
  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).
  CAS PubMed Google Scholar
• Vong, L. et al. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71, 142–154 (2011).
  CAS PubMed PubMed Central Google Scholar
• Tong, Q., Ye, C.P., Jones, J.E., Elmquist, J.K. & Lowell, B.B. Synaptic release of GABA by AgRP neurons is required for normal regulation of energy balance. Nat. Neurosci. 11, 998–1000 (2008).
  CAS PubMed PubMed Central Google Scholar
• Raymond, C.S. & Soriano, P. High-efficiency FLP and PhiC31 site-specific recombination in mammalian cells. PLoS One 2, e162 (2007).
  PubMed PubMed Central Google Scholar
• Sando, R. III et al. Inducible control of gene expression with destabilized Cre. Nat. Methods 10, 1085–1088 (2013).
  CAS PubMed PubMed Central Google Scholar
• Hnasko, T.S. et al. Cre recombinase-mediated restoration of nigrostriatal dopamine in dopamine-deficient mice reverses hypophagia and bradykinesia. Proc. Natl. Acad. Sci. USA 103, 8858–8863 (2006).
  CAS PubMed PubMed Central Google Scholar
• Harris, J.A., Oh, S.W. & Zeng, H. Adeno-associated viral vectors for anterograde axonal tracing with fluorescent proteins in nontransgenic and cre driver mice. Curr. Protoc. Neurosci. Chapter 1, Unit 1.20.1–18 (2012).
• Franklin, K.B.J.P.G. Mouse Brain in Stereotaxic Coordinates (Academic Press, 2008).
• Hempel, C.M., Sugino, K. & Nelson, S.B. A manual method for the purification of fluorescently labeled neurons from the mammalian brain. Nat. Protoc. 2, 2924–2929 (2007).
  CAS PubMed Google Scholar
• Ramsköld, D. et al. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat. Biotechnol. 30, 777–782 (2012).
  PubMed PubMed Central Google Scholar
• Shalek, A.K. et al. Single-cell RNA-seq reveals dynamic paracrine control of cellular variation. Nature 510, 363–369 (2014).
  CAS PubMed PubMed Central Google Scholar
• Treutlein, B. et al. Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature 509, 371–375 (2014).
  CAS PubMed PubMed Central Google Scholar
• Li, B. & Dewey, C.N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011).
  CAS PubMed PubMed Central Google Scholar
• Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
  PubMed PubMed Central Google Scholar
• Brennecke, P. et al. Accounting for technical noise in single-cell RNA-seq experiments. Nat. Methods 10, 1093–1095 (2013).
  CAS PubMed Google Scholar
• Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
  CAS PubMed PubMed Central Google Scholar
• Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9, 559 (2008).
  PubMed PubMed Central Google Scholar
• Ritchie, M.E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
  PubMed PubMed Central Google Scholar
• Katz, Y., Wang, E.T., Airoldi, E.M. & Burge, C.B. Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nat. Methods 7, 1009–1015 (2010).
  CAS PubMed PubMed Central Google Scholar
• Thompson, C.L. et al. Genomic anatomy of the hippocampus. Neuron 60, 1010–1021 (2008).
  CAS PubMed Google Scholar
• Peng, H., Ruan, Z., Long, F., Simpson, J.H. & Myers, E.W. V3D enables real-time 3D visualization and quantitative analysis of large-scale biological image data sets. Nat. Biotechnol. 28, 348–353 (2010).
  CAS PubMed PubMed Central Google Scholar
• Hu, H., Cavendish, J.Z. & Agmon, A. Not all that glitters is gold: off-target recombination in the somatostatin-IRES-Cre mouse line labels a subset of fast-spiking interneurons. Front. Neural Circuits 7, 195 (2013).
  PubMed PubMed Central Google Scholar
• Rossier, J. et al. Cortical fast-spiking parvalbumin interneurons enwrapped in the perineuronal net express the metallopeptidases Adamts8, Adamts15 and Neprilysin. Mol. Psychiatry 20, 154–161 (2015).
  CAS PubMed Google Scholar
• Nikkari, S.T., Järveläinen, H.T., Wight, T.N., Ferguson, M. & Clowes, A.W. Smooth muscle cell expression of extracellular matrix genes after arterial injury. Am. J. Pathol. 144, 1348–1356 (1994).
  CAS PubMed PubMed Central Google Scholar
• Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer, 2009).