Single cell transcriptomics in neuroscience: cell classification and beyond

Current Opinion in Neurobiology

Volumn 50, Issue , 2018, Pages 242-249

  Tasic, Bosiljka ^a  

^a ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL FUNCTION; CELL NUCLEUS; CELLS BY BODY ANATOMY; CLASSIFICATION; GENE EXPRESSION; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NEUROSCIENCE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SINGLE CELL ANALYSIS; TRANSCRIPTOMICS; ANIMAL; EVOLUTION; METABOLISM; NERVE CELL; PHYSIOLOGY; PROCEDURES;

TRANSCRIPTOME;

ANIMALS; BIOLOGICAL EVOLUTION; HUMANS; NEURONS; NEUROSCIENCES; SINGLE-CELL ANALYSIS; TRANSCRIPTOME;

EID: 85046784211     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2018.04.021     Document Type: Review

References (99)

1. Zeng, H., Sanes, J.R., Neuronal cell-type classification: challenges, opportunities and the path forward. Nat Rev Neurosci 18 (2017), 530–546.
2. DeFelipe, J., Lopez-Cruz, P.L., Benavides-Piccione, R., Bielza, C., Larranaga, P., Anderson, S., Burkhalter, A., Cauli, B., Fairen, A., Feldmeyer, D., et al. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 14 (2013), 202–216.
3. Rudy, B., Fishell, G., Lee, S., Hjerling-Leffler, J., Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 71 (2011), 45–61.
4. Tang, F., Barbacioru, C., Wang, Y., Nordman, E., Lee, C., Xu, N., Wang, X., Bodeau, J., Tuch, B.B., Siddiqui, A., et al. mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods 6 (2009), 377–382 The first single cell RNA-seq publication. Since then many alternative protocols have been developed and hundreds of thousands of cells sequenced in a single experiment.
5. Shendure, J., Ji, H., Next-generation DNA sequencing. Nat Biotechnol 26 (2008), 1135–1145.
6. Poulin, J.F., Tasic, B., Hjerling-Leffler, J., Trimarchi, J.M., Awatramani, R., Disentangling neural cell diversity using single-cell transcriptomics. Nat Neurosci 19 (2016), 1131–1141.
7. Tasic, B., Levi, B.P., Menon, V., Single-cell transcriptomic characterization of vertebrate brain composition, development, and function. Çelik, A., Wernet, M.F., (eds.) Decoding Neural Circuit Structure and Function: Cellular Dissection Using Genetic Model Organisms, 2017, Springer International Publishing, 437–468.
8. Haque, A., Engel, J., Teichmann, S.A., Lonnberg, T., A practical guide to single-cell RNA-sequencing for biomedical research and clinical applications. Genome Med, 9, 2017, 75.
9. Buenrostro, J.D., Wu, B., Litzenburger, U.M., Ruff, D., Gonzales, M.L., Snyder, M.P., Chang, H.Y., Greenleaf, W.J., Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523 (2015), 486–490.
10. Cusanovich, D.A., Daza, R., Adey, A., Pliner, H.A., Christiansen, L., Gunderson, K.L., Steemers, F.J., Trapnell, C., Shendure, J., Multiplex single cell profiling of chromatin accessibility by combinatorial cellular indexing. Science 348 (2015), 910–914.
11. Lake, B.B., Chen, S., Sos, B.C., Fan, J., Kaeser, G.E., Yung, Y.C., Duong, T.E., Gao, D., Chun, J., Kharchenko, P.V., et al. Integrative single-cell analysis of transcriptional and epigenetic states in the human adult brain. Nat Biotechnol 36 (2018), 70–80.
12. Preissl, S., Fang, R., Huang, H., Zhao, Y., Raviram, R., Gorkin, D.U., Zhang, Y., Sos, B.C., Afzal, V., Dickel, D.E., et al. Single-nucleus analysis of accessible chromatin in developing mouse forebrain reveals cell-type-specific transcriptional regulation. Nat Neurosci 21 (2018), 432–439.
13. Luo, C., Keown, C.L., Kurihara, L., Zhou, J., He, Y., Li, J., Castanon, R., Lucero, J., Nery, J.R., Sandoval, J.P., et al. Single-cell methylomes identify neuronal subtypes and regulatory elements in mammalian cortex. Science 357 (2017), 600–604.
14. Armananzas, R., Ascoli, G.A., Towards the automatic classification of neurons. Trends Neurosci 38 (2015), 307–318.
15. Cembrowski, M.S., Menon, V., Continuous variation within cell types of the nervous system. Trends Neurosci, 2018.
16. Hrvatin, S., Hochbaum, D.R., Nagy, M.A., Cicconet, M., Robertson, K., Cheadle, L., Zilionis, R., Ratner, A., Borges-Monroy, R., Klein, A.M., et al. Single-cell analysis of experience-dependent transcriptomic states in the mouse visual cortex. Nat Neurosci 21 (2018), 120–129.
17. Chevee, M., Robertson, J.J., Cannon, G.H., Brown, S.P., Goff, L.A., Variation in activity state, axonal projection, and position define the transcriptional identity of individual neocortical projection neurons. Cell Rep 22 (2018), 441–455.
18. Li, H., Horns, F., Wu, B., Xie, Q., Li, J., Li, T., Luginbuhl, D.J., Quake, S.R., Luo, L., Classifying Drosophila olfactory projection neuron subtypes by single-cell RNA sequencing. Cell, 171, 2017 1206-1220 e1222 A fascinating study showing that the differences among some neuronal types may be the highest at the time of synaptic partner matching during development.
19. ••], but for the mouse lateral geniculate nucleus.
20. ••], this paper described taxonomy of cells in adult mouse cortex, and it also included hippocampus.
21. ••], this paper described taxonomy of cells in adult mouse cortex.
22. Habib, N., Li, Y., Heidenreich, M., Swiech, L., Avraham-Davidi, I., Trombetta, J.J., Hession, C., Zhang, F., Regev, A., Div-Seq: single-nucleus RNA-Seq reveals dynamics of rare adult newborn neurons. Science 353 (2016), 925–928.
23. Lake, B.B., Ai, R., Kaeser, G.E., Salathia, N.S., Yung, Y.C., Liu, R., Wildberg, A., Gao, D., Fung, H.L., Chen, S., et al. Neuronal subtypes and diversity revealed by single-nucleus RNA sequencing of the human brain. Science 352 (2016), 1586–1590 This paper describes the first taxonomy of cells in adult human cortex guided by single-nucleus RNA-seq.
24. Habib, N., Avraham-Davidi, I., Basu, A., Burks, T., Shekhar, K., Hofree, M., Choudhury, S.R., Aguet, F., Gelfand, E., Ardlie, K., et al. Massively parallel single-nucleus RNA-seq with DroNc-seq. Nat Methods 14 (2017), 955–958.
25. Lacar, B., Linker, S.B., Jaeger, B.N., Krishnaswami, S., Barron, J., Kelder, M., Parylak, S., Paquola, A., Venepally, P., Novotny, M., et al. Nuclear RNA-seq of single neurons reveals molecular signatures of activation. Nat Commun, 7, 2016, 11022.
26. Wu, Y.E., Pan, L., Zuo, Y., Li, X., Hong, W., Detecting activated cell populations using single-cell RNA-Seq. Neuron, 96, 2017 313-329 e316.
27. Lake, B.B., Codeluppi, S., Yung, Y.C., Gao, D., Chun, J., Kharchenko, P.V., Linnarsson, S., Zhang, K., A comparative strategy for single-nucleus and single-cell transcriptomes confirms accuracy in predicted cell-type expression from nuclear RNA. Sci Rep, 7, 2017, 6031.
28. Jaitin, D.A., Kenigsberg, E., Keren-Shaul, H., Elefant, N., Paul, F., Zaretsky, I., Mildner, A., Cohen, N., Jung, S., Tanay, A., et al. Massively parallel single-cell RNA-Seq for marker-free decomposition of tissues into cell types. Science 343 (2014), 776–779.
29. Gierahn, T.M., Wadsworth, M.H. 2nd, Hughes, T.K., Bryson, B.D., Butler, A., Satija, R., Fortune, S., Love, J.C., Shalek, A.K., Seq-Well: portable, low-cost RNA sequencing of single cells at high throughput. Nat Methods 14 (2017), 395–398.
30. Yuan, J., Sims, P.A., An automated microwell platform for large-scale single cell RNA-seq. Sci Rep, 6, 2016, 33883.
31. Pollen, A.A., Nowakowski, T.J., Chen, J., Retallack, H., Sandoval-Espinosa, C., Nicholas, C.R., Shuga, J., Liu, S.J., Oldham, M.C., Diaz, A., et al. Molecular identity of human outer radial glia during cortical development. Cell 163 (2015), 55–67 scRNA-seq helped molecularly identify outer radial glia, which are responsible for the expansion of cortical cell number in primates. Also see [7].
32. Mi, D., Li, Z., Lim, L., Li, M., Moissidis, M., Yang, Y., Gao, T., Hu, T.X., Pratt, T., Price, D.J., et al. Early emergence of cortical interneuron diversity in the mouse embryo. Science 360 (2018), 81–85.
33. Telley, L., Govindan, S., Prados, J., Stevant, I., Nef, S., Dermitzakis, E., Dayer, A., Jabaudon, D., Sequential transcriptional waves direct the differentiation of newborn neurons in the mouse neocortex. Science 351 (2016), 1443–1446.
34. ••] opened the way to more scalable approaches to scRNA-seq using droplets.
35. Campbell, J.N., Macosko, E.Z., Fenselau, H., Pers, T.H., Lyubetskaya, A., Tenen, D., Goldman, M., Verstegen, A.M., Resch, J.M., McCarroll, S.A., et al. A molecular census of arcuate hypothalamus and median eminence cell types. Nat Neurosci 20 (2017), 484–496 This paper showcases integration of scRNA-seq with GWAS studies to identify cell types relevant for human phenotypes or diseases.
36. Shekhar, K., Lapan, S.W., Whitney, I.E., Tran, N.M., Macosko, E.Z., Kowalczyk, M., Adiconis, X., Levin, J.Z., Nemesh, J., Goldman, M., et al. Comprehensive classification of retinal bipolar neurons by single-cell transcriptomics. Cell, 166, 2016 1308-1323 e1330.
37. ••] opened the way to more scalable approaches to scRNA-seq using droplets.
38. Mayer, C., Hafemeister, C., Bandler, R.C., Machold, R., Batista Brito, R., Jaglin, X., Allaway, K., Butler, A., Fishell, G., Satija, R., Developmental diversification of cortical inhibitory interneurons. Nature 555 (2018), 457–462.
39. Cao, J., Packer, J.S., Ramani, V., Cusanovich, D.A., Huynh, C., Daza, R., Qiu, X., Lee, C., Furlan, S.N., Steemers, F.J., et al. Comprehensive single-cell transcriptional profiling of a multicellular organism. Science 357 (2017), 661–667.
40. Rosenberg, A.B., Roco, C.M., Muscat, R.A., Kuchina, A., Sample, P., Yao, Z., Gray, L., Peeler, D.J., Mukherjee, S., Chen, W., et al. Single-cell profiling of the developing mouse brain and spinal cord with split-pool barcoding. Science, 2018.
41. Islam, S., Zeisel, A., Joost, S., La Manno, G., Zajac, P., Kasper, M., Lonnerberg, P., Linnarsson, S., Quantitative single-cell RNA-seq with unique molecular identifiers. Nat Methods 11 (2014), 163–166.
42. Li, C.L., Li, K.C., Wu, D., Chen, Y., Luo, H., Zhao, J.R., Wang, S.S., Sun, M.M., Lu, Y.J., Zhong, Y.Q., et al. Somatosensory neuron types identified by high-coverage single-cell RNA-sequencing and functional heterogeneity. Cell Res 26 (2016), 83–102.
43. Darmanis, S., Sloan, S.A., Zhang, Y., Enge, M., Caneda, C., Shuer, L.M., Hayden Gephart, M.G., Barres, B.A., Quake, S.R., A survey of human brain transcriptome diversity at the single cell level. Proc Natl Acad Sci U S A 112 (2015), 7285–7290.
44. Picelli, S., Bjorklund, A.K., Faridani, O.R., Sagasser, S., Winberg, G., Sandberg, R., Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat Methods, 2013.
45. Camara, P.G., Methods and challenges in the analysis of single-cell RNA-sequencing data. Curr Opin Syst Biol 7 (2018), 47–53.
46. Usoskin, D., Furlan, A., Islam, S., Abdo, H., Lonnerberg, P., Lou, D., Hjerling-Leffler, J., Haeggstrom, J., Kharchenko, O., Kharchenko, P.V., et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat Neurosci, 2014.
47. van der Maaten, L., Hinton, G., Visualizing data using t-SNE. J Mach Learn Res, 2008, 9.
48. Regev, A., Teichmann, S.A., Lander, E.S., Amit, I., Benoist, C., Birney, E., Bodenmiller, B., Campbell, P., Carninci, P., Clatworthy, M., et al. The human cell atlas. Elife, 2017, 6.
49. Okaty, B.W., Freret, M.E., Rood, B.D., Brust, R.D., Hennessy, M.L., deBairos, D., Kim, J.C., Cook, M.N., Dymecki, S.M., Multi-scale molecular deconstruction of the serotonin neuron system. Neuron 88 (2015), 774–791.
50. Gokce, O., Stanley, G.M., Treutlein, B., Neff, N.F., Camp, J.G., Malenka, R.C., Rothwell, P.E., Fuccillo, M.V., Sudhof, T.C., Quake, S.R., Cellular taxonomy of the mouse striatum as revealed by single-cell RNA-Seq. Cell Rep 16 (2016), 1126–1137.
51. Chen, R., Wu, X., Jiang, L., Zhang, Y., Single-cell RNA-seq reveals hypothalamic cell diversity. Cell Rep 18 (2017), 3227–3241.
52. Romanov, R.A., Zeisel, A., Bakker, J., Girach, F., Hellysaz, A., Tomer, R., Alpar, A., Mulder, J., Clotman, F., Keimpema, E., et al. Molecular interrogation of hypothalamic organization reveals distinct dopamine neuronal subtypes. Nat Neurosci 20 (2017), 176–188.
53. La Manno, G., Gyllborg, D., Codeluppi, S., Nishimura, K., Salto, C., Zeisel, A., Borm, L.E., Stott, S.R., Toledo, E.M., Villaescusa, J.C., et al. Molecular diversity of midbrain development in mouse, human, and stem cells. Cell, 167, 2016 566-580 e519.
54. Hook, P.W., McClymont, S.A., Cannon, G.H., Law, W.D., Morton, A.J., Goff, L.A., McCallion, A.S., Single-cell RNA-Seq of mouse dopaminergic neurons informs candidate gene selection for sporadic Parkinson disease. Am J Hum Genet 102 (2018), 427–446.
55. Furlan, A., La Manno, G., Lubke, M., Haring, M., Abdo, H., Hochgerner, H., Kupari, J., Usoskin, D., Airaksinen, M.S., Oliver, G., et al. Visceral motor neuron diversity delineates a cellular basis for nipple- and pilo-erection muscle control. Nat Neurosci 19 (2016), 1331–1340.
56. Hanchate, N.K., Kondoh, K., Lu, Z., Kuang, D., Ye, X., Qiu, X., Pachter, L., Trapnell, C., Buck, L.B., Single-cell transcriptomics reveals receptor transformations during olfactory neurogenesis. Science 350 (2015), 1251–1255.
57. Shin, J., Berg, D.A., Zhu, Y., Shin, J.Y., Song, J., Bonaguidi, M.A., Enikolopov, G., Nauen, D.W., Christian, K.M., Ming, G.L., et al. Single-cell RNA-Seq with waterfall reveals molecular cascades underlying adult neurogenesis. Cell Stem Cell 17 (2015), 360–372.
58. Luo, Y., Coskun, V., Liang, A., Yu, J., Cheng, L., Ge, W., Shi, Z., Zhang, K., Li, C., Cui, Y., et al. Single-cell transcriptome analyses reveal signals to activate dormant neural stem cells. Cell 161 (2015), 1175–1186.
59. Llorens-Bobadilla, E., Zhao, S., Baser, A., Saiz-Castro, G., Zwadlo, K., Martin-Villalba, A., Single-cell transcriptomics reveals a population of dormant neural stem cells that become activated upon brain injury. Cell Stem Cell 17 (2015), 329–340.
60. Artegiani, B., Lyubimova, A., Muraro, M., van Es, J.H., van Oudenaarden, A., Clevers, H., A single-cell RNA sequencing study reveals cellular and molecular dynamics of the hippocampal neurogenic niche. Cell Rep 21 (2017), 3271–3284.
61. Marques, S., Zeisel, A., Codeluppi, S., van Bruggen, D., Mendanha Falcao, A., Xiao, L., Li, H., Haring, M., Hochgerner, H., Romanov, R.A., et al. Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science 352 (2016), 1326–1329.
62. Matcovitch-Natan, O., Winter, D.R., Giladi, A., Vargas Aguilar, S., Spinrad, A., Sarrazin, S., Ben-Yehuda, H., David, E., Zelada Gonzalez, F., Perrin, P., et al. Microglia development follows a stepwise program to regulate brain homeostasis. Science, 353, 2016, aad8670.
63. Frazer, S., Prados, J., Niquille, M., Cadilhac, C., Markopoulos, F., Gomez, L., Tomasello, U., Telley, L., Holtmaat, A., Jabaudon, D., et al. Transcriptomic and anatomic parcellation of 5-HT3AR expressing cortical interneuron subtypes revealed by single-cell RNA sequencing. Nat Commun, 8, 2017, 14219.
64. Butler, A., Hoffman, P., Smibert, P., Papalexi, E., Satija, R., Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nature Biotechnol, 2018.
65. Crow, M., Paul, A., Ballouz, S., Huang, Z.J., Gillis, J., Characterizing the replicability of cell types defined by single cell RNA-sequencing data using MetaNeighbor. Nature Commun, 9, 2018, 884.
66. Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N.J., Livak, K.J., Mikkelsen, T.S., Rinn, J.L., The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat Biotechnol 32 (2014), 381–386.
67. Qiu, X., Mao, Q., Tang, Y., Wang, L., Chawla, R., Pliner, H.A., Trapnell, C., Reversed graph embedding resolves complex single-cell trajectories. Nature Methods, 14, 2017, 979.
68. Haghverdi, L., Buttner, M., Wolf, F.A., Buettner, F., Theis, F.J., Diffusion pseudotime robustly reconstructs lineage branching. Nat Methods 13 (2016), 845–848.
69. Setty, M., Tadmor, M.D., Reich-Zeliger, S., Angel, O., Salame, T.M., Kathail, P., Choi, K., Bendall, S., Friedman, N., Pe'er, D., Wishbone identifies bifurcating developmental trajectories from single-cell data. Nat Biotechnol 34 (2016), 637–645.
70. Bendall, S.C., Davis, K.L., Amir el, A.D., Tadmor, M.D., Simonds, E.F., Chen, T.J., Shenfeld, D.K., Nolan, G.P., Pe'er, D., Single-cell trajectory detection uncovers progression and regulatory coordination in human B cell development. Cell 157 (2014), 714–725.
71. Raj, B., Wagner, D.E., McKenna, A., Pandey, S., Klein, A.M., Shendure, J., Gagnon, J.A., Schier, A.F., Simultaneous single-cell profiling of lineages and cell types in the vertebrate brain. Nat Biotechnol, 2018.
72. Pollen, A.A., Nowakowski, T.J., Shuga, J., Wang, X., Leyrat, A.A., Lui, J.H., Li, N., Szpankowski, L., Fowler, B., Chen, P., et al. Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex. Nat Biotechnol 32 (2014), 1053–1058.
73. Nowakowski, T.J., Bhaduri, A., Pollen, A.A., Alvarado, B., Mostajo-Radji, M.A., Di Lullo, E., Haeussler, M., Sandoval-Espinosa, C., Liu, S.J., Velmeshev, D., et al. Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex. Science 358 (2017), 1318–1323.
74. Telley, L., Jabaudon, D., A mixed model of neuronal diversity. Nature 555 (2018), 452–454.
75. •].
76. Johnson, M.B., Wang, P.P., Atabay, K.D., Murphy, E.A., Doan, R.N., Hecht, J.L., Walsh, C.A., Single-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex. Nat Neurosci 18 (2015), 637–646.
77. Berdnik, D., Chihara, T., Couto, A., Luo, L., Wiring stability of the adult Drosophila olfactory circuit after lesion. J Neurosci 26 (2006), 3367–3376.
78. Chung, S., Weber, F., Zhong, P., Tan, C.L., Nguyen, T.N., Beier, K.T., Hormann, N., Chang, W.C., Zhang, Z., Do, J.P., et al. Identification of preoptic sleep neurons using retrograde labelling and gene profiling. Nature 545 (2017), 477–481.
79. Lein, E., Borm, L.E., Linnarsson, S., The promise of spatial transcriptomics for neuroscience in the era of molecular cell typing. Science 358 (2017), 64–69.
80. Moffitt, J.R., Hao, J., Bambah-Mukku, D., Lu, T., Dulac, C., Zhuang, X., High-performance multiplexed fluorescence in situ hybridization in culture and tissue with matrix imprinting and clearing. Proc Natl Acad Sci U S A 113 (2016), 14456–14461.
81. Shah, S., Lubeck, E., Zhou, W., Cai, L., In situ transcription profiling of single cells reveals spatial organization of cells in the mouse hippocampus. Neuron 92 (2016), 342–357.
82. Paul, A., Crow, M., Raudales, R., He, M., Gillis, J., Huang, Z.J., Transcriptional architecture of synaptic communication delineates GABAergic neuron identity. Cell, 2017.
83. •] paved the way to Patch-seq, a method for single cell bi-modal or tri-modal data acquisition (electrophysiology, morphology, and scRNA-seq).
84. •] paved the way to Patch-seq, a method for single cell bi-modal or tri-modal data acquisition (electrophysiology, morphology and scRNA-seq).
85. Foldy, C., Darmanis, S., Aoto, J., Malenka, R.C., Quake, S.R., Sudhof, T.C., Single-cell RNAseq reveals cell adhesion molecule profiles in electrophysiologically defined neurons. Proc Natl Acad Sci U S A 113 (2016), E5222–E5231.
86. Angermueller, C., Clark, S.J., Lee, H.J., Macaulay, I.C., Teng, M.J., Hu, T.X., Krueger, F., Smallwood, S., Ponting, C.P., Voet, T., et al. Parallel single-cell sequencing links transcriptional and epigenetic heterogeneity. Nat Methods 13 (2016), 229–232.
87. Clark, S.J., Argelaguet, R., Kapourani, C.A., Stubbs, T.M., Lee, H.J., Alda-Catalinas, C., Krueger, F., Sanguinetti, G., Kelsey, G., Marioni, J.C., et al. scNMT-seq enables joint profiling of chromatin accessibility DNA methylation and transcription in single cells. Nat Commun, 9, 2018, 781.
88. Alemany, A., Florescu, M., Baron, C.S., Peterson-Maduro, J., van Oudenaarden, A., Whole-organism clone tracing using single-cell sequencing. Nature, 556, 2018, 108.
89. Nowakowski, T.J., Pollen, A.A., Di Lullo, E., Sandoval-Espinosa, C., Bershteyn, M., Kriegstein, A.R., Expression analysis highlights AXL as a candidate Zika virus entry receptor in neural stem cells. Cell Stem Cell 18 (2016), 591–596.
90. Camp, J.G., Badsha, F., Florio, M., Kanton, S., Gerber, T., Wilsch-Bräuninger, M., Lewitus, E., Sykes, A., Hevers, W., Lancaster, M., et al. Human cerebral organoids recapitulate gene expression programs of fetal neocortex development. Proc Natl Acad Sci U S A 112 (2015), 15672–15677.
91. Bershteyn, M., Nowakowski, T.J., Pollen, A.A., Di Lullo, E., Nene, A., Wynshaw-Boris, A., Kriegstein, A.R., Human iPSC-derived cerebral organoids model cellular features of lissencephaly and reveal prolonged mitosis of outer radial glia. Cell Stem Cell, 20, 2017 435-449 e434.
92. Yao, Z., Mich, J.K., Ku, S., Menon, V., Krostag, A.-R., Martinez, R.A., Furchtgott, L., Mulholland, H., Bort, S., Fuqua, M.A., et al. A single-cell roadmap of lineage bifurcation in human ESC models of embryonic brain development. Cell Stem Cell 20 (2017), 120–134.
93. Close, J.L., Yao, Z., Levi, B.P., Miller, J.A., Bakken, T.E., Menon, V., Ting, J.T., Wall, A., Krostag, A.R., Thomsen, E.R., et al. Single-cell profiling of an in vitro model of human interneuron development reveals temporal dynamics of cell type production and maturation. Neuron, 93, 2017 1035-1048 e1035.
94. He, M., Tucciarone, J., Lee, S., Nigro, M.J., Kim, Y., Levine, J.M., Kelly, S.M., Krugikov, I., Wu, P., Chen, Y., et al. Strategies and tools for combinatorial targeting of GABAergic neurons in mouse cerebral cortex. Neuron, 92, 2016, 555.
95. Madisen, L., Garner Aleena, R., Shimaoka, D., Chuong Amy, S., Klapoetke Nathan, C., Li, L., van der Bourg, A., Niino, Y., Egolf, L., Monetti, C., et al. Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance. Neuron 85 (2015), 942–958.
96. Ecker, J.R., Geschwind, D.H., Kriegstein, A.R., Ngai, J., Osten, P., Polioudakis, D., Regev, A., Sestan, N., Wickersham, I.R., Zeng, H., The brain initiative cell census consortium: lessons learned toward generating a comprehensive brain cell atlas. Neuron 96 (2017), 542–557.
97. Marioni, J.C., Arendt, D., How single-cell genomics is changing evolutionary and developmental biology. Annu Rev Cell Dev Biol 33 (2017), 537–553.
98. Tanay, A., Regev, A., Scaling single-cell genomics from phenomenology to mechanism. Nature 541 (2017), 331–338.
99. Yuzwa, S.A., Borrett, M.J., Innes, B.T., Voronova, A., Ketela, T., Kaplan, D.R., Bader, G.D., Miller, F.D., Developmental emergence of adult neural stem cells as revealed by single-cell transcriptional profiling. Cell Rep 21 (2017), 3970–3986.