Conservation and Divergence of Related Neuronal Lineages in the Central Brain

Overview

Journal Elife

Specialty Biology

Date 2020 Apr 8

PMID 32255422

Citations 19

Authors

Ying-Jou Lee

Ching-Po Yang

Rosa L Miyares

Yu-Fen Huang

Yisheng He

Qingzhong Ren

Hui-Min Chen

Takashi Kawase

Masayoshi Ito

Hideo Otsuna

Ken Sugino

Yoshi Aso

Kei Ito

Tzumin Lee

Affiliations

Soon will be listed here.

Abstract

Wiring a complex brain requires many neurons with intricate cell specificity, generated by a limited number of neural stem cells. central brain lineages are a predetermined series of neurons, born in a specific order. To understand how lineage identity translates to neuron morphology, we mapped 18 central brain lineages. While we found large aggregate differences between lineages, we also discovered shared patterns of morphological diversification. Lineage identity plus Notch-mediated sister fate govern primary neuron trajectories, whereas temporal fate diversifies terminal elaborations. Further, morphological neuron types may arise repeatedly, interspersed with other types. Despite the complexity, related lineages produce similar neuron types in comparable temporal patterns. Different stem cells even yield two identical series of dopaminergic neuron types, but with unrelated sister neurons. Together, these phenomena suggest that straightforward rules drive incredible neuronal complexity, and that large changes in morphology can result from relatively simple fating mechanisms.

Citing Articles

Imp/IGF2BP and Syp/SYNCRIP temporal RNA interactomes uncover combinatorial networks of regulators of brain development.

Lee J, Huang N, Samuels T, Davis I Sci Adv. 2025; 11(6):eadr6682.

PMID: 39919181 PMC: 11804933. DOI: 10.1126/sciadv.adr6682.

Lineage Analysis at Single-Cell Resolution by Twin-Spot MARCM with Lineage-Restricted Drivers.

Previero A, Yang C, Lee T Methods Mol Biol. 2025; 2886:401-420.

PMID: 39745652 DOI: 10.1007/978-1-0716-4310-5_20.

Whole-brain annotation and multi-connectome cell typing of Drosophila.

Schlegel P, Yin Y, Bates A, Dorkenwald S, Eichler K, Brooks P Nature. 2024; 634(8032):139-152.

PMID: 39358521 PMC: 11446831. DOI: 10.1038/s41586-024-07686-5.

Indirect neurogenesis in space and time.

Thor S Nat Rev Neurosci. 2024; 25(8):519-534.

PMID: 38951687 DOI: 10.1038/s41583-024-00833-x.

Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster.

Eckstein N, Bates A, Champion A, Du M, Yin Y, Schlegel P Cell. 2024; 187(10):2574-2594.e23.

PMID: 38729112 PMC: 11106717. DOI: 10.1016/j.cell.2024.03.016.

References

Spana E, Doe C . Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron. 1996; 17(1):21-6. DOI: 10.1016/s0896-6273(00)80277-9. View

Shepherd D, Sahota V, Court R, Williams D, Truman J . Developmental organization of central neurons in the adult Drosophila ventral nervous system. J Comp Neurol. 2019; 527(15):2573-2598. DOI: 10.1002/cne.24690. View

Ito K, Shinomiya K, Ito M, Armstrong J, Boyan G, Hartenstein V . A systematic nomenclature for the insect brain. Neuron. 2014; 81(4):755-65. DOI: 10.1016/j.neuron.2013.12.017. View

Yu H, Awasaki T, Schroeder M, Long F, Yang J, He Y . Clonal development and organization of the adult Drosophila central brain. Curr Biol. 2013; 23(8):633-43. PMC: 3637848. DOI: 10.1016/j.cub.2013.02.057. View

Zheng Z, Lauritzen J, Perlman E, Robinson C, Nichols M, Milkie D . A Complete Electron Microscopy Volume of the Brain of Adult Drosophila melanogaster. Cell. 2018; 174(3):730-743.e22. PMC: 6063995. DOI: 10.1016/j.cell.2018.06.019. View

Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T . Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012; 9(7):676-82. PMC: 3855844. DOI: 10.1038/nmeth.2019. View

Li H, Horns F, Wu B, Xie Q, Li J, Li T . Classifying Drosophila Olfactory Projection Neuron Subtypes by Single-Cell RNA Sequencing. Cell. 2017; 171(5):1206-1220.e22. PMC: 6095479. DOI: 10.1016/j.cell.2017.10.019. View

Takemura S, Aso Y, Hige T, Wong A, Lu Z, Xu C . A connectome of a learning and memory center in the adult brain. Elife. 2017; 6. PMC: 5550281. DOI: 10.7554/eLife.26975. View

Zhu S, Lin S, Kao C, Awasaki T, Chiang A, Lee T . Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell. 2006; 127(2):409-22. DOI: 10.1016/j.cell.2006.08.045. View

10.

Rein K, Zockler M, Mader M, Grubel C, Heisenberg M . The Drosophila standard brain. Curr Biol. 2002; 12(3):227-31. DOI: 10.1016/s0960-9822(02)00656-5. View

11.

Awasaki T, Kao C, Lee Y, Yang C, Huang Y, Pfeiffer B . Making Drosophila lineage-restricted drivers via patterned recombination in neuroblasts. Nat Neurosci. 2014; 17(4):631-7. DOI: 10.1038/nn.3654. View

12.

Wan Y, Otsuna H, Chien C, Hansen C . An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research. IEEE Trans Vis Comput Graph. 2009; 15(6):1489-96. PMC: 2874972. DOI: 10.1109/TVCG.2009.118. View

13.

Huang Z . Toward a genetic dissection of cortical circuits in the mouse. Neuron. 2014; 83(6):1284-302. PMC: 4169123. DOI: 10.1016/j.neuron.2014.08.041. View

14.

Costa M, Manton J, Ostrovsky A, Prohaska S, Jefferis G . NBLAST: Rapid, Sensitive Comparison of Neuronal Structure and Construction of Neuron Family Databases. Neuron. 2016; 91(2):293-311. PMC: 4961245. DOI: 10.1016/j.neuron.2016.06.012. View

15.

Thurmond J, Goodman J, Strelets V, Attrill H, Gramates L, Marygold S . FlyBase 2.0: the next generation. Nucleic Acids Res. 2018; 47(D1):D759-D765. PMC: 6323960. DOI: 10.1093/nar/gky1003. View

16.

Yu H, Chen C, Shi L, Huang Y, Lee T . Twin-spot MARCM to reveal the developmental origin and identity of neurons. Nat Neurosci. 2009; 12(7):947-53. PMC: 2701974. DOI: 10.1038/nn.2345. View

17.

Lee T, Luo L . Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron. 1999; 22(3):451-61. DOI: 10.1016/s0896-6273(00)80701-1. View

18.

Yu H, Kao C, He Y, Ding P, Kao J, Lee T . A complete developmental sequence of a Drosophila neuronal lineage as revealed by twin-spot MARCM. PLoS Biol. 2010; 8(8). PMC: 2927434. DOI: 10.1371/journal.pbio.1000461. View

19.

Urbach R, Technau G . Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development. 2003; 130(16):3621-37. DOI: 10.1242/dev.00533. View

20.

Lichtneckert R, Reichert H . Anteroposterior regionalization of the brain: genetic and comparative aspects. Adv Exp Med Biol. 2008; 628:32-41. DOI: 10.1007/978-0-387-78261-4_2. View