Lineage Analysis of Drosophila Lateral Antennal Lobe Neurons Reveals Notch-Dependent Binary Temporal Fate Decisions

Suewei Lin,Chih-Fei Kao,Hung-Hsiang Yu,Yaling Huang,Tzumin Lee,Claude Desplan

doi:10.1371/journal.pbio.1001425

Abstract

Author SummaryThe Drosophila brain develops from a limited number of neural stem cells that produce a series of ganglion mother cells (GMCs) that divide once to produce a pair of neurons in a defined order, termed a neuronal lineage. Here, we provide a detailed lineage map for the neurons derived from the Drosophila lateral antennal lobe (lAL) neuroblast. The lAL lineage consists of two distinct hemilineages, generated through differential Notch signaling in the two GMC daughters, to produce one projection neuron (PN) paired with a local interneuron (LN). Both hemilineages yield distinct cell types in the same sequence, although the temporal identity (birth-order-dependent fate) changes are regulated independently between projection neurons and local interneurons, such that a series of analogous local interneurons may co-derive with different projection neurons and vice versa. We also find that Notch signaling can transform a class of nonantennal lobe projection neurons into antennal lobe projection neurons. These findings suggest that Notch signaling not only modulates temporal fate but itself plays a role in the distinction of antennal lobe versus nonantennal lobe neurons.

Highlights

The computing power of a brain is rooted in its complex neural network, composed of numerous types of neurons
The Drosophila brain develops from a limited number of neural stem cells that produce a series of ganglion mother cells (GMCs) that divide once to produce a pair of neurons in a defined order, termed a neuronal lineage
The lateral antennal lobe (lAL) lineage consists of two distinct hemilineages, generated through differential Notch signaling in the two GMC daughters, to produce one projection neuron (PN) paired with a local interneuron (LN)

Summary

Introduction

The computing power of a brain is rooted in its complex neural network, composed of numerous types of neurons. Drosophila melanogaster has a relatively tractable neural development, study of which has revealed multiple mechanisms that act in sequence to diversify neuron fates [1]. Each NB generates a lineage of neurons through multiple rounds of self-renewing asymmetric cell divisions. One NB deposits a ganglion mother cell (GMC) that divides once to produce two neurons [4,5]. (2) The specification of temporal identity within a given lineage underlies the orderly derivation of distinct neurons from a common progenitor [7,8]. (3) The binary cell fate decision distinguishes fate between sister neurons made by a single GMC [9,10,11,12,13,14] Three known mechanisms underlie neuronal diversification through the protracted process of neurogenesis. (1) The acquisition of lineage identity by each NB occurs during early spatial patterning and governs the neural types it produces [6]. (2) The specification of temporal identity within a given lineage underlies the orderly derivation of distinct neurons from a common progenitor [7,8]. (3) The binary cell fate decision distinguishes fate between sister neurons made by a single GMC [9,10,11,12,13,14]

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Conclusion