Mutual inhibition among postmitotic neurons regulates robustness of brain wiring in Drosophila
Brain connectivity maps display a delicate balance between individual variation and stereotypy, suggesting the existence of dedicated mechanisms that simultaneously permit and limit individual variation. We show that during the development of the Drosophila central nervous system, mutual inhibition...
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doaj-258d5181d118405eb0d694e1b6c5a3052021-05-04T21:29:15ZengeLife Sciences Publications LtdeLife2050-084X2013-03-01210.7554/eLife.00337Mutual inhibition among postmitotic neurons regulates robustness of brain wiring in DrosophilaMarion Langen0Marta Koch1Jiekun Yan2Natalie De Geest3Maria-Luise Erfurth4Barret D Pfeiffer5Dietmar Schmucker6Yves Moreau7Bassem A Hassan8Center for the Biology of Disease, VIB, Leuven, Belgium; Center for Human Genetics, University of Leuven School of Medicine, Leuven, Belgium; Doctoral Program in Molecular and Cognitive Neuroscience, Doctoral School of Biomedical Sciences, University of Leuven, Leuven, BelgiumCenter for the Biology of Disease, VIB, Leuven, Belgium; Center for Human Genetics, University of Leuven School of Medicine, Leuven, BelgiumCenter for the Biology of Disease, VIB, Leuven, Belgium; Center for Human Genetics, University of Leuven School of Medicine, Leuven, BelgiumCenter for the Biology of Disease, VIB, Leuven, Belgium; Center for Human Genetics, University of Leuven School of Medicine, Leuven, BelgiumVesalius Research Center, VIB, Leuven, Belgium; Department of Oncology, University of Leuven School of Medicine, Leuven, BelgiumJanelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesVesalius Research Center, VIB, Leuven, Belgium; Department of Oncology, University of Leuven School of Medicine, Leuven, BelgiumDepartment of Electrical Engineering, University of Leuven, Leuven, BelgiumCenter for the Biology of Disease, VIB, Leuven, Belgium; Center for Human Genetics, University of Leuven School of Medicine, Leuven, Belgium; Doctoral Program in Molecular and Cognitive Neuroscience, Doctoral School of Biomedical Sciences, University of Leuven, Leuven, Belgium; Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesBrain connectivity maps display a delicate balance between individual variation and stereotypy, suggesting the existence of dedicated mechanisms that simultaneously permit and limit individual variation. We show that during the development of the Drosophila central nervous system, mutual inhibition among groups of neighboring postmitotic neurons during development regulates the robustness of axon target choice in a nondeterministic neuronal circuit. Specifically, neighboring postmitotic neurons communicate through Notch signaling during axonal targeting, to ensure balanced alternative axon target choices without a corresponding change in cell fate. Loss of Notch in postmitotic neurons modulates an axon's target choice. However, because neighboring axons respond by choosing the complementary target, the stereotyped connectivity pattern is preserved. In contrast, loss of Notch in clones of neighboring postmitotic neurons results in erroneous coinnervation by multiple axons. Our observations establish mutual inhibition of axonal target choice as a robustness mechanism for brain wiring and unveil a novel cell fate independent function for canonical Notch signaling.https://elifesciences.org/articles/00337NeurobiologyNeural CircuitRobustnessVariabilityNotch SignalingAxonal targeting |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Marion Langen Marta Koch Jiekun Yan Natalie De Geest Maria-Luise Erfurth Barret D Pfeiffer Dietmar Schmucker Yves Moreau Bassem A Hassan |
spellingShingle |
Marion Langen Marta Koch Jiekun Yan Natalie De Geest Maria-Luise Erfurth Barret D Pfeiffer Dietmar Schmucker Yves Moreau Bassem A Hassan Mutual inhibition among postmitotic neurons regulates robustness of brain wiring in Drosophila eLife Neurobiology Neural Circuit Robustness Variability Notch Signaling Axonal targeting |
author_facet |
Marion Langen Marta Koch Jiekun Yan Natalie De Geest Maria-Luise Erfurth Barret D Pfeiffer Dietmar Schmucker Yves Moreau Bassem A Hassan |
author_sort |
Marion Langen |
title |
Mutual inhibition among postmitotic neurons regulates robustness of brain wiring in Drosophila |
title_short |
Mutual inhibition among postmitotic neurons regulates robustness of brain wiring in Drosophila |
title_full |
Mutual inhibition among postmitotic neurons regulates robustness of brain wiring in Drosophila |
title_fullStr |
Mutual inhibition among postmitotic neurons regulates robustness of brain wiring in Drosophila |
title_full_unstemmed |
Mutual inhibition among postmitotic neurons regulates robustness of brain wiring in Drosophila |
title_sort |
mutual inhibition among postmitotic neurons regulates robustness of brain wiring in drosophila |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2013-03-01 |
description |
Brain connectivity maps display a delicate balance between individual variation and stereotypy, suggesting the existence of dedicated mechanisms that simultaneously permit and limit individual variation. We show that during the development of the Drosophila central nervous system, mutual inhibition among groups of neighboring postmitotic neurons during development regulates the robustness of axon target choice in a nondeterministic neuronal circuit. Specifically, neighboring postmitotic neurons communicate through Notch signaling during axonal targeting, to ensure balanced alternative axon target choices without a corresponding change in cell fate. Loss of Notch in postmitotic neurons modulates an axon's target choice. However, because neighboring axons respond by choosing the complementary target, the stereotyped connectivity pattern is preserved. In contrast, loss of Notch in clones of neighboring postmitotic neurons results in erroneous coinnervation by multiple axons. Our observations establish mutual inhibition of axonal target choice as a robustness mechanism for brain wiring and unveil a novel cell fate independent function for canonical Notch signaling. |
topic |
Neurobiology Neural Circuit Robustness Variability Notch Signaling Axonal targeting |
url |
https://elifesciences.org/articles/00337 |
work_keys_str_mv |
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