Active intermixing of indirect and direct neurons builds the striatal mosaic

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 and Sonia Garel ()
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Andrea Tinterri: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris
Fabien Menardy: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris
Marco A. Diana: UPMC University Paris 06, UM119 Neuroscience Paris Seine (NPS), CNRS UMR8246, Inserm
Ludmilla Lokmane: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris
Maryama Keita: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris
Fanny Coulpier: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris
Sophie Lemoine: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris
Caroline Mailhes: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris
Benjamin Mathieu: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris
Paloma Merchan-Sala: Cincinnati Children’s Hospital Medical Center
Kenneth Campbell: Cincinnati Children’s Hospital Medical Center
Ildiko Gyory: Max Plank Institute of Immunobiology
Rudolf Grosschedl: Max Plank Institute of Immunobiology
Daniela Popa: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris
Sonia Garel: Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris

Nature Communications, 2018, vol. 9, issue 1, 1-13

Abstract: 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.

Date: 2018
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DOI: 10.1038/s41467-018-07171-4

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