Sensory Systems/Insects/Vision

= The Visual System of Drosophila = The visual system gives animals the ability to perceive their environment. This fast sensing of food sources or danger is important across species. The fruit fly Drosophila melanogaster (see Fig. 1) belongs to the invertebrates and constitutes an important model organism for this group. Drosophila shares the ability to see with vertebrates, like humans. Comparing the visual system of invertebrates (Fig. 2) with vertebrates reveals many similarities in the general structure and architecture but also differences. The exact molecular mechanisms are not yet completely understood, but there seem to be conserved mechanisms between the species.



Two papers (S. Hakeda-Suzuki, T. Suzuki (2014) and Zipursky (2010)) that focus on the Drosophila visual system will be discussed to gain information about the general structure, as well as differences and similarities to the retina of vertebrates. The different steps of specific targeting of the photoreceptor cells will be explained with the example of the photoreceptor cells R7 and R8.

Retina
Drosophila belongs to the invertebrates and possesses a compound eye, that consists of about 750 ommatidia (Fig. 3). One ommatidium comprises eight photoreceptor cells (R1 – R8), that differ in the rhodopsin, they express, and thereby in their functioning. The photoreceptor cells R1 – R6 perceive information about motion. They express rhodopsin Rh1, which responds to a broad spectrum of visible light. Colour vision is performed by R7 and R8. R7 expresses the UV-sensitive rhodopsin Rh3/ Rh4, while R8 expresses Rh5/ Rh6. Each of the 750 ommatidia contains all eight photoreceptor cells, arranged in a highly specific way. R1 – R6 surround the centred R7 and R8 photoreceptor cells. Incoming information that activates the photoreceptor cells is forwarded to the optic lobe, which consists of four distinct parts: lamina, medulla, lobula and lobula plate.

Lamina
The lamina is organized into radially distinct areas, called cartridges. The curvature of the compound eye causes the outer photoreceptor cells R1 - R6 to perceive information about different spatial locations. To account for this phenomenon and to increase sensitivity, the photoreceptor cells R1 - R6 from different, neighbouring ommatidia are guided to the same one cartridge within the lamina. This allows to maintain retinotopy. This process is called neural superposition. R7 and R8 do not share the problem of retinotopy, as they are located in the centre of the ommatidium. The photoreceptor cells R1 – R6 terminate in the lamina and connect to the lamina neurons by formation of synapses. Those lamina neurons forward the information into the medulla. R7 and R8 do not form synapses in the lamina and further project into the medulla.

Medulla
The medulla consists of ten distinct layers M1 – M10 and is radially differentiated into columns. R7 projects specifically into the layer M6, whereas R8 projects into M3. R7 and R8 from the same ommatidium (Retina) target the same column in the Medulla as lamina neurons from the same cartridge (Lamina). The lamina neurons also show stereotypic connection patterns. Lamina neurons, as well as the photoreceptor cells R7 and R8 form synapses to neurons that guide the visual information out of the medulla into the lobula and lobula plate. By passing of the information through the lamina, medulla, lobula and lobula plat, the information is computed and allows visual perception of the environment.

Comparison invertebrate and vertebrate retina
In general, there are major similarities between the visual systems of vertebrates and invertebrates. The most important one is the general structuring into layers and radial columns. The photoreceptor cells in the vertebrate visual system are called rods and cones. Rods are responsible for light sensation and motion. They share their functioning with the photoreceptor cells R1 – R6 in the invertebrate visual system. Cones are necessary for colour sensation. This role refers to the R7 and R8 photoreceptor cells.

One major difference is the presence of synapses in the retina of vertebrates. As already stated, Drosophila contains no synapses in the retina. All synaptic connections of the photoreceptor cells are located in the lamina (R1 – R6) or the medulla (R7 – R8). The vertebrate visual system also shows different cell types in the retina. It contains not only photoreceptor cells, but also horizontal cells, bipolar cells, amacrine cells and ganglion cells. This leads to a huge connectivity between the cell types and results in the development of five distinct layers that can be distinguished by whether they contain cell bodies or synapses. A development of horizontal layers in the retina of the fly visual system cannot be observed. In vertebrates, most visual computation takes place in the retina, whereas the computation of visual input in invertebrates is divided between retina, lamina and medulla.

Development: stepwise targeting of R7 and R8
The development of the insect visual system is illustrated with the example of the stepwise targeting of the photoreceptor cells R7 and R8. All photoreceptor cells target in a highly specific way in the lamina, in case of R1 – R6, or the medulla, in case of R7 and R8. The specific steps involved in targeting are herein described for R7 and R8. R7 targets the medulla layer M6, whereas R8 finally targets the medulla layer M3. In the larval instar, the starting point of the developing compound eye is called eye-disc. The photoreceptor cells in the retina start to differentiate but the lamina and medulla are not innervated by axons at the beginning of the larval instar. Throughout the larval instar the photoreceptors start differentiating form the posterior to the anterior tip. The first photoreceptor that differentiates is R8. R8 induces differentiation of the remaining photoreceptor cells in a specific order. The axon of R8 constitutes a pioneer axon, so the axons of R1 – R7 from the same ommatidium can orientate themselves to reach the lamina. R1 – R6 undergo synaptogenesis to connect to lamina neurons. Specific targeting underlies the principle of neural superposition, as described before. By growing towards the lamina, the axons build a connection between the eye and the brain. The positioning of the photoreceptor cells with respect to each other is maintained throughout growing to account for proper perception of the environment. Topography is thereby maintained. R7 and R8 continue growing until they reach the medulla. R8 photoreceptor cells pause at the apical surface of the developing medulla, which is called R8 temporary layer. R7 photoreceptor cells that follow the R8 pioneer axon continue growing until they reach the R7 temporary layer that is located basally with respect to the R8 temporary layer. Lamina neurons follow by extending axons towards the medulla. When they reach the medulla, they start to branch radially and horizontally. They establish distinct layers between the R8 temporary layer and the R7 temporary layer and, thereby, increase the distance between them. Only after all lamina neurons did innervate the medulla, R7 and R8 start growing again. They extend until they reach their final target layer by sending out thin processes, called filopodia. In their final target layer, R7 and R8 undergo synaptogenesis. Many different molecular cues are involved in the targeting steps and in the specific targeting of one distinct medulla layer, but they are not yet fully understood.