TY - JOUR
T1 - Neuronal diversity and convergence in a visual system developmental atlas
AU - Özel, Mehmet Neset
AU - Simon, Félix
AU - Jafari, Shadi
AU - Holguera, Isabel
AU - Chen, Yen Chung
AU - Benhra, Najate
AU - El-Danaf, Rana Naja
AU - Kapuralin, Katarina
AU - Malin, Jennifer Amy
AU - Konstantinides, Nikolaos
AU - Desplan, Claude
N1 - Funding Information:
Acknowledgements We thank all members of the Desplan laboratory, S.-y. Takemura and F. P. Davis for discussions; L. Luo, C. Doe, F. Pinto Teixeira, J. Slabbaert and S. Cordoba for critical reading of the manuscript; and I. Salecker and R. Hiesinger for reagents. The C.D. laboratory is supported by NYSTEM (DOH01-C32604GG), the National Eye Institute (R01 EY017916) and by ADHPG-CGSB1 to the CGSB of the NYU Abu Dhabi Research Institute. M.N.O. is a Leon Levy Neuroscience Fellow. F.S. and Y.-C.C. are supported by New York University (MacCracken Fellowship). S.J. is supported by the Swedish Research Council (Vetenskapsrådet VR grant 2016-06726). I.H. is supported by a Human Frontier Science Program postdoctoral fellowship (LT000757/2017). J.A.M is supported by the National Eye Institute (F32 F32EY028012). N.K. is supported by the National Eye Institute (K99 EY029356-01).
Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature Limited.
PY - 2021/1/7
Y1 - 2021/1/7
N2 - Deciphering how neuronal diversity is established and maintained requires a detailed knowledge of neuronal gene expression throughout development. In contrast to mammalian brains1,2, the large neuronal diversity of the Drosophila optic lobe3 and its connectome4–6 are almost completely characterized. However, a molecular characterization of this neuronal diversity, particularly during development, has been lacking. Here we present insights into brain development through a nearly complete description of the transcriptomic diversity of the optic lobes of Drosophila. We acquired the transcriptome of 275,000 single cells at adult and at five pupal stages, and built a machine-learning framework to assign them to almost 200 cell types at all time points during development. We discovered two large neuronal populations that wrap neuropils during development but die just before adulthood, as well as neuronal subtypes that partition dorsal and ventral visual circuits by differential Wnt signalling throughout development. Moreover, we show that the transcriptomes of neurons that are of the same type but are produced days apart become synchronized shortly after their production. During synaptogenesis we also resolved neuronal subtypes that, although differing greatly in morphology and connectivity, converge to indistinguishable transcriptomic profiles in adults. Our datasets almost completely account for the known neuronal diversity of the Drosophila optic lobes, and serve as a paradigm to understand brain development across species.
AB - Deciphering how neuronal diversity is established and maintained requires a detailed knowledge of neuronal gene expression throughout development. In contrast to mammalian brains1,2, the large neuronal diversity of the Drosophila optic lobe3 and its connectome4–6 are almost completely characterized. However, a molecular characterization of this neuronal diversity, particularly during development, has been lacking. Here we present insights into brain development through a nearly complete description of the transcriptomic diversity of the optic lobes of Drosophila. We acquired the transcriptome of 275,000 single cells at adult and at five pupal stages, and built a machine-learning framework to assign them to almost 200 cell types at all time points during development. We discovered two large neuronal populations that wrap neuropils during development but die just before adulthood, as well as neuronal subtypes that partition dorsal and ventral visual circuits by differential Wnt signalling throughout development. Moreover, we show that the transcriptomes of neurons that are of the same type but are produced days apart become synchronized shortly after their production. During synaptogenesis we also resolved neuronal subtypes that, although differing greatly in morphology and connectivity, converge to indistinguishable transcriptomic profiles in adults. Our datasets almost completely account for the known neuronal diversity of the Drosophila optic lobes, and serve as a paradigm to understand brain development across species.
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U2 - 10.1038/s41586-020-2879-3
DO - 10.1038/s41586-020-2879-3
M3 - Article
C2 - 33149298
AN - SCOPUS:85094969309
SN - 0028-0836
VL - 589
SP - 88
EP - 95
JO - Nature
JF - Nature
IS - 7840
ER -