Spatio-temporal pattern of neuronal differentiation in the Drosophila visual system: A user’s guide to the dynamic morphology of the developing optic lobe

Abstract

Visual information processing in animals with large image forming eyes is carried out in highly structured retinotopically ordered neuropils. Visual neuropils in Drosophila form the optic lobe, which consists of four serially arranged major subdivisions; the lamina, medulla, lobula and lobula plate; the latter three of these are further subdivided into multiple layers. The visual neuropils are formed by more than 100 different cell types, distributed and interconnected in an invariant highly regular pattern. This pattern relies on a protracted sequence of developmental steps, whereby different cell types are born at specific time points and nerve connections are formed in a tightly controlled sequence that has to be coordinated among the different visual neuropils. The developing fly visual system has become a highly regarded and widely studied paradigm to investigate the genetic mechanisms that control the formation of neural circuits. However, these studies are often made difficult by the complex and shifting patterns in which different types of neurons and their connections are distributed throughout development. In the present paper we have reconstructed the three-dimensional architecture of the Drosophila optic lobe from the early larva to the adult. Based on specific markers, we were able to distinguish the populations of progenitors of the four optic neuropils and map the neurons and their connections. Our paper presents sets of annotated confocal z-projections and animated 3D digital models of these structures for representative stages. The data reveal the temporally coordinated growth of the optic neuropils, and clarify how the position and orientation of the neuropils and interconnecting tracts (inner and outer optic chiasm) changes over time. Finally, we have analyzed the emergence of the discrete layers of the medulla and lobula complex using the same markers (DN-cadherin, Brp) employed to systematically explore the structure and development of the central brain neuropil. Our work will facilitate experimental studies of the molecular mechanisms regulating neuronal fate and connectivity in the fly visual system, which bears many fundamental similarities with the retina of vertebrates.

Sobremesa L-type Amino Acid Transporter Expressed in Glia Is Essential for Proper Timing of Development and Brain Growth

“…This difference in growth rate is further maintained though time (96 and 102 hAEL), and while Repo > SbmRNAi larvae spend almost 24 extra hours eating and growing (120 hAEL), their brain never reaches the final control size ( Figures 3 C and S6 A). Observations of the anatomical features ( Dearborn and Kunes, 2004 , Ngo et al., 2017 ) of the brain of the Sbm-knockdown larvae through these time points show that brain development is delayed compared to controls ( Figure 4 A). This is also highlighted by the differences in the number of dividing cells.…”

Modality-specific circuits for skylight orientation in the fly visual system

“…pausing at the distal border of the medulla, sending thin filopodia exploring prospective layer M3 After 47% pupation, DRA.R8 cell growth cone in non-DRA R8 recipient layer began to thicken, while simultaneously growing towards the deeper R7 recipient layer. Such behavior was never observed in non-DRA R8 cells, which still elongated after reaching the non-DRA R8 recipient layer, most likely via a passive process as the medulla thickens 42,51,52 . The speed and dynamics of the thickened DRA.R8 process descending towards M6 suggest it results from an active process.…”

Coordination between stochastic and deterministic specification in the Drosophila visual system

“…A proneuronal wave sequentially converts single rows of neuroepithelial cells into neuroblasts, the Drosophila neural stem cells, until the entire OPC is consumed (Egger et al, 2007). The medulla is thus sequentially produced, similarly and concomitantly to the retina where single rows of ommatidia are sequentially added in the eye disc at the morphogenetic furrow (Hofbauer and Campos-Ortega, 1990;Ngo et al, 2017;Ready et al, 1976). Once specified, medulla neuroblasts sequentially express a series of transcription factors that will command the fate of the neurons produced during each temporal window (Holguera and Desplan, 2018;Li et al, 2013;Suzuki et al, 2013).…”