Abstract

Wiring a complex brain requires many neurons with intricate cell specificity, generated by a limited number of neural stem cells. Drosophila central brain lineages are a predetermined series of neurons, born in a specific order. To understand how lineage identity translates to neuron morphology, we mapped 18 Drosophila central brain lineages. While we found large aggregate differences between lineages, we also discovered shared patterns of morphological diversification. Lineage identity plus Notch-mediated sister fate govern primary neuron trajectories, whereas temporal fate diversifies terminal elaborations. Further, morphological neuron types may arise repeatedly, interspersed with other types. Despite the complexity, related lineages produce similar neuron types in comparable temporal patterns. Different stem cells even yield two identical series of dopaminergic neuron types, but with unrelated sister neurons. Together, these phenomena suggest that straightforward rules drive incredible neuronal complexity, and that large changes in morphology can result from relatively simple fating mechanisms.

Highlights

  • In order to understand how the genome encodes behavior, we need to study the developmental mechanisms that build and wire complex centers in the brain

  • In order to target a large subset of related neuronal lineages, we wanted to exploit a conserved patterning gene. Both anteroposterior and dorsoventral patterning of the CNS are remarkably conserved from insects to humans (Lichtneckert and Reichert, 2008; Urbach and Technau, 2008), including the tripartite organization of the brain

  • For each of the 18 Vnd lineages, we identified morphologically distinguishable neuron types and further determined their approximate birth sequence based on the recovery window of each neuron type (Figure 1—source data 1; Supplementary file 1)

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Summary

Introduction

In order to understand how the genome encodes behavior, we need to study the developmental mechanisms that build and wire complex centers in the brain. The relatively small, yet complex fly brain enables scientists to connect neurons into functional circuits, map neural lineages, and test the role of essentially any gene in neurodevelopment and/or behavior (Venken et al, 2011). The fly brain connectome is being constructed at the level of individual synapses (Takemura et al, 2017; Zheng et al, 2018). Both morphology and development of the Drosophila brain are trackable at the single-cell level. It is possible to resolve fly brain development from neural stem cells to the connectome and engineer the brain

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