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Dynamic spatiotemporal coordination of neural stem cell fate decisions through local feedback in the adult vertebrate brain

Nicolas Dray, Laure Mancini, Udi Binshtok, Felix Cheysson, View ORCID ProfileWilly Supatto, Pierre Mahou, Sébastien Bedu, Sara Ortica, Monika Krecsmarik, Sébastien Herbert, View ORCID ProfileJean-Baptiste Masson, Jean-Yves Tinevez, Gabriel Lang, Emmanuel Beaurepaire, David Sprinzak, Laure Bally-Cuif
doi: https://doi.org/10.1101/2020.07.15.205021
Nicolas Dray
1Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, Team supported by the Ligue Nationale Contre le Cancer, Paris (75015), France
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  • For correspondence: laure.bally-cuif@pasteur.fr nicolas.dray@pasteur.fr davidsp@tauex.tau.ac.il
Laure Mancini
1Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, Team supported by the Ligue Nationale Contre le Cancer, Paris (75015), France
2Sorbonne Université, Collège doctoral, F-75005 Paris, France
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Udi Binshtok
3School of Neurobiology, Biochemistry, and Biophysics, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv (69978), Israel
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Felix Cheysson
4Université Paris-Saclay, AgroParisTech, INRAE, UMR MIA-Paris, Paris (75005), France
5Epidemiology and Modeling of bacterial Evasion to Antibacterials Unit (EMEA), Institut Pasteur, Paris (75015), France
6Anti-infective Evasion and Pharmacoepidemiology team, Centre for Epidemiology and Public Health (CESP), INSERM/UVSQ, France
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Willy Supatto
7Laboratory for Optics and Biosciences, Ecole Polytechnique, CNRS, INSERM, IP Paris, Palaiseau (91128), France
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  • ORCID record for Willy Supatto
Pierre Mahou
7Laboratory for Optics and Biosciences, Ecole Polytechnique, CNRS, INSERM, IP Paris, Palaiseau (91128), France
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Sébastien Bedu
1Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, Team supported by the Ligue Nationale Contre le Cancer, Paris (75015), France
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Sara Ortica
1Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, Team supported by the Ligue Nationale Contre le Cancer, Paris (75015), France
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Monika Krecsmarik
1Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, Team supported by the Ligue Nationale Contre le Cancer, Paris (75015), France
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Sébastien Herbert
8Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris (75015), France
9Image Analysis Hub, Institut Pasteur, Paris (75015), France
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Jean-Baptiste Masson
10Department of Neuroscience and Department of Computational Biology, Institut Pasteur, Paris (75015), France
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  • ORCID record for Jean-Baptiste Masson
Jean-Yves Tinevez
9Image Analysis Hub, Institut Pasteur, Paris (75015), France
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Gabriel Lang
4Université Paris-Saclay, AgroParisTech, INRAE, UMR MIA-Paris, Paris (75005), France
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Emmanuel Beaurepaire
7Laboratory for Optics and Biosciences, Ecole Polytechnique, CNRS, INSERM, IP Paris, Palaiseau (91128), France
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David Sprinzak
3School of Neurobiology, Biochemistry, and Biophysics, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv (69978), Israel
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  • For correspondence: laure.bally-cuif@pasteur.fr nicolas.dray@pasteur.fr davidsp@tauex.tau.ac.il
Laure Bally-Cuif
1Zebrafish Neurogenetics Unit, Institut Pasteur, UMR3738, CNRS, Team supported by the Ligue Nationale Contre le Cancer, Paris (75015), France
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  • For correspondence: laure.bally-cuif@pasteur.fr nicolas.dray@pasteur.fr davidsp@tauex.tau.ac.il
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SUMMARY

Neural stem cell (NSC) populations persist in the adult vertebrate brain over a life time, and their homeostasis is controlled at the population level. The nature and properties of these coordination mechanisms remain unknown. Here we combine dynamic imaging of entire NSC populations in their in vivo niche over weeks, pharmacological manipulations, mathematical modeling and spatial statistics, and demonstrate that NSCs use spatiotemporally resolved local feedbacks to coordinate their decision to divide. These involve a Notch-mediated inhibition from transient neural progenitors, and a dispersion effect from dividing NSCs themselves, exerted with a delay of 9-12 days. Simulations from a stochastic NSC lattice model capturing these interactions demonstrate that they are linked by lineage progression and control the spatiotemporal distribution of output neurons. These results highlight how local and temporally delayed interactions occurring between brain germinal cells generate self-propagating dynamics that maintain NSC population homeostasis with specific spatiotemporal correlations.

Competing Interest Statement

The authors have declared no competing interest.

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Posted July 16, 2020.
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Dynamic spatiotemporal coordination of neural stem cell fate decisions through local feedback in the adult vertebrate brain
Nicolas Dray, Laure Mancini, Udi Binshtok, Felix Cheysson, Willy Supatto, Pierre Mahou, Sébastien Bedu, Sara Ortica, Monika Krecsmarik, Sébastien Herbert, Jean-Baptiste Masson, Jean-Yves Tinevez, Gabriel Lang, Emmanuel Beaurepaire, David Sprinzak, Laure Bally-Cuif
bioRxiv 2020.07.15.205021; doi: https://doi.org/10.1101/2020.07.15.205021
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Dynamic spatiotemporal coordination of neural stem cell fate decisions through local feedback in the adult vertebrate brain
Nicolas Dray, Laure Mancini, Udi Binshtok, Felix Cheysson, Willy Supatto, Pierre Mahou, Sébastien Bedu, Sara Ortica, Monika Krecsmarik, Sébastien Herbert, Jean-Baptiste Masson, Jean-Yves Tinevez, Gabriel Lang, Emmanuel Beaurepaire, David Sprinzak, Laure Bally-Cuif
bioRxiv 2020.07.15.205021; doi: https://doi.org/10.1101/2020.07.15.205021

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