Active Intermixing of Indirect and Direct Neurons Builds the Striatal Mosaic

Overview

Journal Nat Commun

Specialty Biology

Date 2018 Nov 11

PMID 30413696

Citations 17

Authors

Andrea Tinterri

Fabien Menardy

Marco A Diana

Ludmilla Lokmane

Maryama Keita

Fanny Coulpier

Sophie Lemoine

Caroline Mailhes

Benjamin Mathieu

Paloma Merchan-Sala

Kenneth Campbell

Ildiko Gyory

Rudolf Grosschedl

Daniela Popa

Sonia Garel

Affiliations

Soon will be listed here.

Abstract

The striatum controls behaviors via the activity of direct and indirect pathway projection neurons (dSPN and iSPN) that are intermingled in all compartments. While such cellular mosaic ensures the balanced activity of the two pathways, its developmental origin and pattern remains largely unknown. Here, we show that both SPN populations are specified embryonically and intermix progressively through multidirectional iSPN migration. Using conditional mutant mice, we found that inactivation of the dSPN-specific transcription factor Ebf1 impairs selective dSPN properties, including axon pathfinding, while molecular and functional features of iSPN were preserved. Ebf1 mutation disrupted iSPN/dSPN intermixing, resulting in an uneven distribution. Such architectural defect was selective of the matrix compartment, highlighting that intermixing is a parallel process to compartment formation. Our study reveals while iSPN/dSPN specification is largely independent, their intermingling emerges from an active migration of iSPN, thereby providing a novel framework for the building of striatal architecture.

Citing Articles

Haploinsufficiency of in Striatal Indirect Pathway Neurons Alters Motor and Goal-Directed Behaviors in Mice.

Haetzel L, Iafrati J, Cording K, Farhan M, Noveir S, Rumbaugh G J Neurosci. 2024; 44(48).

PMID: 39358043 PMC: 11604145. DOI: 10.1523/JNEUROSCI.1264-23.2024.

Striatal projection neurons coexpressing dopamine D1 and D2 receptors modulate the motor function of D1- and D2-SPNs.

Bonnavion P, Varin C, Fakhfouri G, Martinez Olondo P, De Groote A, Cornil A Nat Neurosci. 2024; 27(9):1783-1793.

PMID: 38965445 DOI: 10.1038/s41593-024-01694-4.

Plasticity of thalamocortical axons is regulated by serotonin levels modulated by preterm birth.

Sinclair-Wilson A, Lawrence A, Ferezou I, Cartonnet H, Mailhes C, Garel S Proc Natl Acad Sci U S A. 2023; 120(33):e2301644120.

PMID: 37549297 PMC: 10438379. DOI: 10.1073/pnas.2301644120.

The transcription factor promotes the D1 MSN identity and represses the D2 MSN identity.

Shang Z, Yang L, Wang Z, Tian Y, Gao Y, Su Z Front Cell Dev Biol. 2022; 10:948331.

PMID: 36081908 PMC: 9445169. DOI: 10.3389/fcell.2022.948331.

Transcription factor Sp9 is a negative regulator of D1-type MSN development.

Li Z, Shang Z, Sun M, Jiang X, Tian Y, Yang L Cell Death Discov. 2022; 8(1):301.

PMID: 35773249 PMC: 9247084. DOI: 10.1038/s41420-022-01088-0.

References

Mega T, Lupia M, Amodio N, Horton S, Mesuraca M, Pelaggi D . Zinc finger protein 521 antagonizes early B-cell factor 1 and modulates the B-lymphoid differentiation of primary hematopoietic progenitors. Cell Cycle. 2011; 10(13):2129-39. DOI: 10.4161/cc.10.13.16045. View

Newman H, Liu F, Graybiel A . Dynamic ordering of early generated striatal cells destined to form the striosomal compartment of the striatum. J Comp Neurol. 2014; 523(6):943-62. PMC: 4329021. DOI: 10.1002/cne.23725. View

Lin H, Grosschedl R . Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature. 1995; 376(6537):263-7. DOI: 10.1038/376263a0. View

Ruest L, Hammer R, Yanagisawa M, Clouthier D . Dlx5/6-enhancer directed expression of Cre recombinase in the pharyngeal arches and brain. Genesis. 2003; 37(4):188-94. PMC: 2830754. DOI: 10.1002/gene.10247. View

Hamasaki T, Goto S, Nishikawa S, Ushio Y . Neuronal cell migration for the developmental formation of the mammalian striatum. Brain Res Brain Res Rev. 2002; 41(1):1-12. DOI: 10.1016/s0165-0173(02)00216-3. View

Burguiere E, Monteiro P, Mallet L, Feng G, Graybiel A . Striatal circuits, habits, and implications for obsessive-compulsive disorder. Curr Opin Neurobiol. 2014; 30:59-65. PMC: 4293232. DOI: 10.1016/j.conb.2014.08.008. View

Lee S, Shen R, Cho H, Kwon R, Seo S, Lee J . STAT3 promotes motor neuron differentiation by collaborating with motor neuron-specific LIM complex. Proc Natl Acad Sci U S A. 2013; 110(28):11445-50. PMC: 3710787. DOI: 10.1073/pnas.1302676110. View

Long J, Swan C, Liang W, Cobos I, Potter G, Rubenstein J . Dlx1&2 and Mash1 transcription factors control striatal patterning and differentiation through parallel and overlapping pathways. J Comp Neurol. 2008; 512(4):556-72. PMC: 2761428. DOI: 10.1002/cne.21854. View

Gyory I, Boller S, Nechanitzky R, Mandel E, Pott S, Liu E . Transcription factor Ebf1 regulates differentiation stage-specific signaling, proliferation, and survival of B cells. Genes Dev. 2012; 26(7):668-82. PMC: 3323878. DOI: 10.1101/gad.187328.112. View

10.

Lobo M, Yeh C, Yang X . Pivotal role of early B-cell factor 1 in development of striatonigral medium spiny neurons in the matrix compartment. J Neurosci Res. 2008; 86(10):2134-46. DOI: 10.1002/jnr.21666. View

11.

Arlotta P, Molyneaux B, Jabaudon D, Yoshida Y, Macklis J . Ctip2 controls the differentiation of medium spiny neurons and the establishment of the cellular architecture of the striatum. J Neurosci. 2008; 28(3):622-32. PMC: 6670353. DOI: 10.1523/JNEUROSCI.2986-07.2008. View

12.

Gangarossa G, Espallergues J, Mailly P, De Bundel D, de Kerchove dExaerde A, Herve D . Spatial distribution of D1R- and D2R-expressing medium-sized spiny neurons differs along the rostro-caudal axis of the mouse dorsal striatum. Front Neural Circuits. 2013; 7:124. PMC: 3725430. DOI: 10.3389/fncir.2013.00124. View

13.

Nadarajah B, Parnavelas J . Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci. 2002; 3(6):423-32. DOI: 10.1038/nrn845. View

14.

GAREL S, Marin F, Grosschedl R, Charnay P . Ebf1 controls early cell differentiation in the embryonic striatum. Development. 1999; 126(23):5285-94. DOI: 10.1242/dev.126.23.5285. View

15.

Ding J, Oh W, Sabatini B, Gu C . Semaphorin 3E-Plexin-D1 signaling controls pathway-specific synapse formation in the striatum. Nat Neurosci. 2011; 15(2):215-23. PMC: 3267860. DOI: 10.1038/nn.3003. View

16.

Gong S, Zheng C, Doughty M, Losos K, Didkovsky N, Schambra U . A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature. 2003; 425(6961):917-25. DOI: 10.1038/nature02033. View

17.

Hagimoto K, Takami S, Murakami F, Tanabe Y . Distinct migratory behaviors of striosome and matrix cells underlying the mosaic formation in the developing striatum. J Comp Neurol. 2016; 525(4):794-817. DOI: 10.1002/cne.24096. View

18.

Zhang Z, Hao C, Li C, Zang D, Zhao J, Li X . Mutation of SLC35D3 causes metabolic syndrome by impairing dopamine signaling in striatal D1 neurons. PLoS Genet. 2014; 10(2):e1004124. PMC: 3923682. DOI: 10.1371/journal.pgen.1004124. View

19.

Xu Z, Liang Q, Song X, Zhang Z, Lindtner S, Li Z . SP8 and SP9 coordinately promote D2-type medium spiny neuron production by activating expression. Development. 2018; 145(14). PMC: 6078334. DOI: 10.1242/dev.165456. View

20.

Lu K, Evans S, Hirano S, Liu F . Dual role for Islet-1 in promoting striatonigral and repressing striatopallidal genetic programs to specify striatonigral cell identity. Proc Natl Acad Sci U S A. 2013; 111(1):E168-77. PMC: 3890800. DOI: 10.1073/pnas.1319138111. View