A developmental framework linking neurogenesis and circuit formation in the Drosophila CNS

The mechanisms specifying neuronal diversity are well characterized, yet it remains unclear how or if these mechanisms regulate neural circuit assembly. To address this, we mapped the developmental origin of 160 interneurons from seven bilateral neural progenitors (neuroblasts) and identify them in...

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Bibliographic Details
Published in:eLife 2021-05, Vol.10
Main Authors: Mark, Brandon, Lai, Sen-Lin, Zarin, Aref Arzan, Manning, Laurina, Pollington, Heather Q, Litwin-Kumar, Ashok, Cardona, Albert, Truman, James W, Doe, Chris Q
Format: Article
Language:English
Subjects:
Animals
cell lineage
Central nervous system
Central Nervous System - physiology
Developmental Biology
Drosophila
Drosophila melanogaster - physiology
Drosophila Proteins - physiology
hemilineage
Insects
Interneurons
Localization
Microscopy
Morphology
Nervous system
neural circuit
Neural circuitry
Neural networks
Neural stem cells
Neural Stem Cells - physiology
neuroblast
Neurogenesis
Neurogenesis - physiology
Neurons
Neuropil
Neuroscience
Notch
Synapses
temporal identity
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Summary:The mechanisms specifying neuronal diversity are well characterized, yet it remains unclear how or if these mechanisms regulate neural circuit assembly. To address this, we mapped the developmental origin of 160 interneurons from seven bilateral neural progenitors (neuroblasts) and identify them in a synapse-scale TEM reconstruction of the larval central nervous system. We find that lineages concurrently build the sensory and motor neuropils by generating sensory and motor hemilineages in a Notch-dependent manner. Neurons in a hemilineage share common synaptic targeting within the neuropil, which is further refined based on neuronal temporal identity. Connectome analysis shows that hemilineage-temporal cohorts share common connectivity. Finally, we show that proximity alone cannot explain the observed connectivity structure, suggesting hemilineage/temporal identity confers an added layer of specificity. Thus, we demonstrate that the mechanisms specifying neuronal diversity also govern circuit formation and function, and that these principles are broadly applicable throughout the nervous system.
ISSN:2050-084X
2050-084X
DOI:10.7554/eLife.67510