A Unique Class of Neural Progenitors in the Drosophila Optic Lobe Generates Both Migrating Neurons and Glia

Abstract

SUMMARY How neuronal and glial fates are specified from neural precursor cells is an important question for developmental neurobiologists. We address this question in the Drosophila optic lobe, composed of the lamina, medulla, and lobula complex. We show that two gliogenic regions posterior to the prospective lamina also produce lamina wide-field (Lawf) neurons, which share common progenitors with lamina glia. These progenitors express neither canonical neuroblast nor lamina precursor cell markers. They bifurcate into two sub-lineages in response to Notch signaling, generating lamina glia or Lawf neurons, respectively. The newly born glia and Lawfs then migrate tangentially over substantial distances to reach their target tissue. Thus, Lawf neurogenesis, which includes a common origin with glia, as well as neuronal migration, resembles several aspects of vertebrate neurogenesis.

Integration of temporal and spatial patterning generates neural diversity

“…The pOPC compartment can be further subdivided by the expression of the wingless and dpp signaling genes (Fig.1e) 30 . Cells in the wingless domain behave in a very distinct manner from the rest of the OPC, and have been described elsewhere 31,32 .…”

Lineage-guided Notch-dependent gliogenesis byDrosophilamulti-potent progenitors

“…Although the molecular mechanisms specific to type II lineage gliogenesis are poorly understood (Awasaki et al, 2008;Viktorin et al, 2011), gliogenesis has been widely studied in Drosophila and vertebrate nervous systems (Jones, 2005;Rowitch and Kriegstein, 2010). It has been shown that Notch signaling could either promote or repress gliogenesis, depending on the specific developmental context (Cattenoz and Giangrande, 2013;Chen et al, 2016;Gaiano and Fishell, 2002;Gho et al, 1999;Morrison et al, 2000;Udolph et al, 2001;Umesono et al, 2002;Van De Bor and Giangrande, 2001).…”

“…In vertebrate gliogenesis, Notch promotes the generation of Müller glia, astrocytes and Schwann cells, but represses oligodendrocyte differentiation (Kato et al, 2015;Morrison et al, 2000;Pierfelice et al, 2011). Similarly, Notch can either promote glial fate in specific lineages of the fly central nervous system (Chen et al, 2016;Udolph et al, 2001;Umesono et al, 2002) or inhibit gliogenesis in the sensory organ precursors of the Drosophila periphery nervous system (Gho et al, 1999;Van De Bor and Giangrande, 2001). In Drosophila, Notch regulates the expression of gcm, which is both necessary and sufficient to specify glial cells (Udolph et al, 2001;Umesono et al, 2002;Van De Bor and Giangrande, 2001).…”

Generation and Evolution of Neural Cell Types and Circuits: Insights from the Drosophila Visual System

“…Lat (lamina-tangential) neurons, according to their structure and arborizations, seem to be involved in relaying feedback to the lamina from the circadian circuit (136). Finally, Lawf1 and Lawf2 (lamina wide-field) neurons provide broad field feedback from the medulla (23, 136). These seven neural types are derived from different sources than the LMCs and emerge from the medulla part of the OPC, the inner proliferation center (IPC), or neuroblasts in the central brain, making the lamina a composite of cells that arise from spatially independent precursors.…”