Literature DB >> 33149298

Neuronal diversity and convergence in a visual system developmental atlas.

Mehmet Neset Özel1, Félix Simon1, Shadi Jafari1,2, Isabel Holguera1, Yen-Chung Chen1, Najate Benhra3, Rana Naja El-Danaf3, Katarina Kapuralin3, Jennifer Amy Malin1, Nikolaos Konstantinides4, Claude Desplan5,6.   

Abstract

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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Year:  2020        PMID: 33149298      PMCID: PMC7790857          DOI: 10.1038/s41586-020-2879-3

Source DB:  PubMed          Journal:  Nature        ISSN: 0028-0836            Impact factor:   49.962


  51 in total

1.  Synaptic circuits and their variations within different columns in the visual system of Drosophila.

Authors:  Shin-ya Takemura; C Shan Xu; Zhiyuan Lu; Patricia K Rivlin; Toufiq Parag; Donald J Olbris; Stephen Plaza; Ting Zhao; William T Katz; Lowell Umayam; Charlotte Weaver; Harald F Hess; Jane Anne Horne; Juan Nunez-Iglesias; Roxanne Aniceto; Lei-Ann Chang; Shirley Lauchie; Ashley Nasca; Omotara Ogundeyi; Christopher Sigmund; Satoko Takemura; Julie Tran; Carlie Langille; Kelsey Le Lacheur; Sari McLin; Aya Shinomiya; Dmitri B Chklovskii; Ian A Meinertzhagen; Louis K Scheffer
Journal:  Proc Natl Acad Sci U S A       Date:  2015-10-19       Impact factor: 11.205

2.  Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways.

Authors:  Hideo Otsuna; Kei Ito
Journal:  J Comp Neurol       Date:  2006-08-20       Impact factor: 3.215

3.  Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system.

Authors:  Aljoscha Nern; Barret D Pfeiffer; Gerald M Rubin
Journal:  Proc Natl Acad Sci U S A       Date:  2015-05-11       Impact factor: 11.205

Review 4.  Heterogeneity within classical cell types is the rule: lessons from hippocampal pyramidal neurons.

Authors:  Mark S Cembrowski; Nelson Spruston
Journal:  Nat Rev Neurosci       Date:  2019-04       Impact factor: 34.870

5.  Neurons with cholinergic phenotype in the visual system of Drosophila.

Authors:  Shamprasad Varija Raghu; Dierk F Reiff; Alexander Borst
Journal:  J Comp Neurol       Date:  2011-01-01       Impact factor: 3.215

Review 6.  Generating neuronal diversity in the mammalian cerebral cortex.

Authors:  Simona Lodato; Paola Arlotta
Journal:  Annu Rev Cell Dev Biol       Date:  2015-09-11       Impact factor: 13.827

7.  Wiring economy and volume exclusion determine neuronal placement in the Drosophila brain.

Authors:  Marta Rivera-Alba; Shiv N Vitaladevuni; Yuriy Mishchenko; Yuriy Mischenko; Zhiyuan Lu; Shin-Ya Takemura; Lou Scheffer; Ian A Meinertzhagen; Dmitri B Chklovskii; Gonzalo G de Polavieja
Journal:  Curr Biol       Date:  2011-11-23       Impact factor: 10.834

8.  Candidate glutamatergic neurons in the visual system of Drosophila.

Authors:  Shamprasad Varija Raghu; Alexander Borst
Journal:  PLoS One       Date:  2011-05-05       Impact factor: 3.240

9.  Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain.

Authors:  Kazunori Shinomiya; Gary Huang; Zhiyuan Lu; Toufiq Parag; C Shan Xu; Roxanne Aniceto; Namra Ansari; Natasha Cheatham; Shirley Lauchie; Erika Neace; Omotara Ogundeyi; Christopher Ordish; David Peel; Aya Shinomiya; Claire Smith; Satoko Takemura; Iris Talebi; Patricia K Rivlin; Aljoscha Nern; Louis K Scheffer; Stephen M Plaza; Ian A Meinertzhagen
Journal:  Elife       Date:  2019-01-09       Impact factor: 8.140

10.  Automatic Segmentation of Drosophila Neural Compartments Using GAL4 Expression Data Reveals Novel Visual Pathways.

Authors:  Karin Panser; Laszlo Tirian; Florian Schulze; Santiago Villalba; Gregory S X E Jefferis; Katja Bühler; Andrew D Straw
Journal:  Curr Biol       Date:  2016-07-14       Impact factor: 10.834

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  34 in total

1.  Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila.

Authors:  Emil Kind; Kit D Longden; Aljoscha Nern; Arthur Zhao; Gizem Sancer; Miriam A Flynn; Connor W Laughland; Bruck Gezahegn; Henrique Df Ludwig; Alex G Thomson; Tessa Obrusnik; Paula G Alarcón; Heather Dionne; Davi D Bock; Gerald M Rubin; Michael B Reiser; Mathias F Wernet
Journal:  Elife       Date:  2021-12-16       Impact factor: 8.140

2.  Analysis of Single-Cell Transcriptome Data in Drosophila.

Authors:  Schayan Yousefian; Maria Jelena Musillo; Josephine Bageritz
Journal:  Methods Mol Biol       Date:  2022

3.  Neural mechanisms to exploit positional geometry for collision avoidance.

Authors:  Ryosuke Tanaka; Damon A Clark
Journal:  Curr Biol       Date:  2022-05-03       Impact factor: 10.900

Review 4.  The regulatory role of Pin1 in neuronal death.

Authors:  Shu-Chao Wang; Xi-Min Hu; Kun Xiong
Journal:  Neural Regen Res       Date:  2023-01       Impact factor: 6.058

5.  A global timing mechanism regulates cell-type-specific wiring programmes.

Authors:  Saumya Jain; Ying Lin; Yerbol Z Kurmangaliyev; Javier Valdes-Aleman; Samuel A LoCascio; Parmis Mirshahidi; Brianna Parrington; S Lawrence Zipursky
Journal:  Nature       Date:  2022-02-23       Impact factor: 69.504

6.  Fly Cell Atlas: A single-nucleus transcriptomic atlas of the adult fruit fly.

Authors:  Hongjie Li; Jasper Janssens; Maxime De Waegeneer; Sai Saroja Kolluru; Kristofer Davie; Vincent Gardeux; Wouter Saelens; Fabrice P A David; Maria Brbić; Katina Spanier; Jure Leskovec; Colleen N McLaughlin; Qijing Xie; Robert C Jones; Katja Brueckner; Jiwon Shim; Sudhir Gopal Tattikota; Frank Schnorrer; Katja Rust; Todd G Nystul; Zita Carvalho-Santos; Carlos Ribeiro; Soumitra Pal; Sharvani Mahadevaraju; Teresa M Przytycka; Aaron M Allen; Stephen F Goodwin; Cameron W Berry; Margaret T Fuller; Helen White-Cooper; Erika L Matunis; Stephen DiNardo; Anthony Galenza; Lucy Erin O'Brien; Julian A T Dow; Heinrich Jasper; Brian Oliver; Norbert Perrimon; Bart Deplancke; Stephen R Quake; Liqun Luo; Stein Aerts; Devika Agarwal; Yasir Ahmed-Braimah; Michelle Arbeitman; Majd M Ariss; Jordan Augsburger; Kumar Ayush; Catherine C Baker; Torsten Banisch; Katja Birker; Rolf Bodmer; Benjamin Bolival; Susanna E Brantley; Julie A Brill; Nora C Brown; Norene A Buehner; Xiaoyu Tracy Cai; Rita Cardoso-Figueiredo; Fernando Casares; Amy Chang; Thomas R Clandinin; Sheela Crasta; Claude Desplan; Angela M Detweiler; Darshan B Dhakan; Erika Donà; Stefanie Engert; Swann Floc'hlay; Nancy George; Amanda J González-Segarra; Andrew K Groves; Samantha Gumbin; Yanmeng Guo; Devon E Harris; Yael Heifetz; Stephen L Holtz; Felix Horns; Bruno Hudry; Ruei-Jiun Hung; Yuh Nung Jan; Jacob S Jaszczak; Gregory S X E Jefferis; Jim Karkanias; Timothy L Karr; Nadja Sandra Katheder; James Kezos; Anna A Kim; Seung K Kim; Lutz Kockel; Nikolaos Konstantinides; Thomas B Kornberg; Henry M Krause; Andrew Thomas Labott; Meghan Laturney; Ruth Lehmann; Sarah Leinwand; Jiefu Li; Joshua Shing Shun Li; Kai Li; Ke Li; Liying Li; Tun Li; Maria Litovchenko; Han-Hsuan Liu; Yifang Liu; Tzu-Chiao Lu; Jonathan Manning; Anjeli Mase; Mikaela Matera-Vatnick; Neuza Reis Matias; Caitlin E McDonough-Goldstein; Aaron McGeever; Alex D McLachlan; Paola Moreno-Roman; Norma Neff; Megan Neville; Sang Ngo; Tanja Nielsen; Caitlin E O'Brien; David Osumi-Sutherland; Mehmet Neset Özel; Irene Papatheodorou; Maja Petkovic; Clare Pilgrim; Angela Oliveira Pisco; Carolina Reisenman; Erin Nicole Sanders; Gilberto Dos Santos; Kristin Scott; Aparna Sherlekar; Philip Shiu; David Sims; Rene V Sit; Maija Slaidina; Harold E Smith; Gabriella Sterne; Yu-Han Su; Daniel Sutton; Marco Tamayo; Michelle Tan; Ibrahim Tastekin; Christoph Treiber; David Vacek; Georg Vogler; Scott Waddell; Wanpeng Wang; Rachel I Wilson; Mariana F Wolfner; Yiu-Cheung E Wong; Anthony Xie; Jun Xu; Shinya Yamamoto; Jia Yan; Zepeng Yao; Kazuki Yoda; Ruijun Zhu; Robert P Zinzen
Journal:  Science       Date:  2022-03-04       Impact factor: 63.714

7.  A discrete neuronal population coordinates brain-wide developmental activity.

Authors:  Bryce T Bajar; Nguyen T Phi; Jesse Isaacman-Beck; Jun Reichl; Harpreet Randhawa; Orkun Akin
Journal:  Nature       Date:  2022-02-09       Impact factor: 69.504

8.  Neural specification, targeting, and circuit formation during visual system assembly.

Authors:  Jennifer Malin; Claude Desplan
Journal:  Proc Natl Acad Sci U S A       Date:  2021-07-13       Impact factor: 11.205

9.  Profile of Claude Desplan.

Authors:  Jennifer Viegas
Journal:  Proc Natl Acad Sci U S A       Date:  2021-07-13       Impact factor: 11.205

10.  Single-cell transcriptomes of developing and adult olfactory receptor neurons in Drosophila.

Authors:  Colleen N McLaughlin; Maria Brbić; Qijing Xie; Tongchao Li; Felix Horns; Sai Saroja Kolluru; Justus M Kebschull; David Vacek; Anthony Xie; Jiefu Li; Robert C Jones; Jure Leskovec; Stephen R Quake; Liqun Luo; Hongjie Li
Journal:  Elife       Date:  2021-02-08       Impact factor: 8.140

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