Abstract
The paired box gene Pox neuro (Poxn) is expressed in two bilaterally symmetric neuronal clusters of the developing adult Drosophila brain, a protocerebral dorsal cluster (DC) and a deutocerebral ventral cluster (VC). We show that all cells that express Poxn in the developing brain are postmitotic neurons. During embryogenesis, the DC and VC consist of only 20 and 12 neurons that express Poxn, designated embryonic Poxn-neurons. The number of Poxn-neurons increases only during the third larval instar, when the DC and VC increase dramatically to about 242 and 109 Poxn-neurons, respectively, virtually all of which survive to the adult stage, while no new Poxn-neurons are added during metamorphosis. Although the vast majority of Poxn-neurons express Poxn only during third instar, about half of them are born by the end of embryogenesis, as demonstrated by the absence of BrdU incorporation during larval stages. At late third instar, embryonic Poxn-neurons, which begin to express Poxn during embryogenesis, can be easily distinguished from embryonic-born and larval-born Poxn-neurons, which begin to express Poxn only during third instar, (i) by the absence of Pros, (ii) their overt differentiation of axons and neurites, and (iii) the strikingly larger diameter of their cell bodies still apparent in the adult brain. The embryonic Poxn-neurons are primary neurons that lay out the pioneering tracts for the secondary Poxn-neurons, which differentiate projections and axons that follow those of the primary neurons during metamorphosis. The DC and the VC participate only in two neuropils of the adult brain. The DC forms most, if not all, of the neurons that connect the bulb (lateral triangle) with the ellipsoid body, a prominent neuropil of the central complex, while the VC forms most of the ventral projection neurons of the antennal lobe, which connect it ipsilaterally to the lateral horn, bypassing the mushroom bodies. In addition, Poxn-neurons of the VC are ventral local interneurons of the antennal lobe. In the absence of Poxn protein in the developing brain, embryonic Poxn-neurons stall their projections and cannot find their proper target neuropils, the bulb and ellipsoid body in the case of the DC, or the antennal lobe and lateral horn in the case of the VC, whereby the absence of the ellipsoid body neuropil is particularly striking. Poxn is thus crucial for pathfinding both in the DC and VC. Additional implications of our results are discussed.
Highlights
During metamorphosis, Drosophila melanogaster undergoes dramatic morphological changes, including extensive reorganization of the nervous system that transforms its control of larval behaviors into that of radically different and much more complex adult behaviors [1,2,3,4,5]
The tracts of the two antennal nerves deliver their information to the glomeruli of the antennal lobes (ALs), from where it is passed on to other glomeruli of the ALs by local interneurons (LNs) and to higher brain centers, either directly to the lateral horn (LH) by ventral projection neurons or indirectly via the mushroom bodies (MB) to the LH by anterodorsal and lateral projection neurons, adPNs and lPNs [15,16,17,18]
Expression of Pox neuro (Poxn) in brain cells begins during embryogenesis and third larval instar In the brain, Poxn protein initially appears bilaterally at stage 12 of embryogenesis [19] in a single cell of the deutocerebrum [41]
Summary
Drosophila melanogaster undergoes dramatic morphological changes, including extensive reorganization of the nervous system that transforms its control of larval behaviors into that of radically different and much more complex adult behaviors [1,2,3,4,5]. In Drosophila, these are (from anterior to posterior) the ellipsoid body (EB), the fan-shaped body (FB) with the paired noduli below it, and the protocerebral bridge [10]. Neurons participating in these neuropils are classified as columnar small-field neurons and tangential large-field neurons, which form tracts perpendicular to those of the small-field neurons [10,14]. The tracts of the two antennal nerves deliver their information to the glomeruli of the ALs, from where it is passed on to other glomeruli of the ALs by local interneurons (LNs) and to higher brain centers, either directly to the lateral horn (LH) by ventral projection neurons (vPNs) or indirectly via the mushroom bodies (MB) to the LH by anterodorsal and lateral projection neurons, adPNs and lPNs [15,16,17,18]
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