Our current study focuses on the determination of the identify and function of the second/third-order interneurons, which synapse with R7 (UV ultraviolet channel), R8 photoreceptors (green/blue channel), or lamina neurons (achromatic channel, via R1-6). Using the promoter of the histamine-gated chloride channels, we have identified three synaptic partners of R7 and R8. These include two types of projection neurons, Tm5 and Tm9 neurons, which receive direct synaptic inputs from R7 and R8, respectively, as well as the L3 lamina neurons. These projection neurons likely serve as color opponent neurons and relay spectral information to higher visual center, the lobula. In addition, we found an amacrine neuron type, Dm8, which receives input from multiple R7 inputs and relays them to Tm5. These synaptic connections have been further confirmed by serial Electron-microscopic reconstruction. The core color-vision circuit, thus constitutes the photoreceptors, one lamina neuron type, two projection neuron types and one amacrine neuron type. The overall architecture of the core color-vision circuit in Drosophila resembles that of vertebrates. To determine the function of specific subtypes of the first-order interneurons, we selectively inactivated or restored the synaptic function of distinct neuron subtypes and examined the behavioral consequences. This approach requires expressing transgenes specifically in single neuron subtypes. To do so, we developed a new combinatorial gene expression system called split-LexA, which operates in parallel to the existing split-Gal4 system. Using these two systems, we were able to manipulate the activity of distinct neuron subtypes and test whether a specific neuron subtype is required or sufficient for a certain visual function. We found that inactivating the synaptic activity of the amacrine neuron Dm8 disrupted UV-preference in color-discriminating behavior tests but not motion detection, suggesting Dm8s are specifically required for color vision. Conversely, inactivating both L1 and L2 lamina neurons abolished the animals'ability to respond to motion stimuli but their color-discrimination ability remains intact, indicating that the lamina neurons L1 and L2 are specifically required for motion detection. Similarly, rescuing the expression of the histamine chloride channel Ort in Dm8s in ort mutant background completely restored UV preference, indicating that the synaptic path from R7 to Dm8, then to Tm5 is sufficient for detecting dim UV light. Rescuing the expression of the histamine chloride channel Ort in either L1 or L2 in ort mutant background completely restored motion detection but not color-discrimination, indicating L1 and L2 function redundantly in motion detection. In summary, our study reveals that specific visual functions can be assigned to distinct neuron subtypes and that color and motion pathways are segregated in the early visual pathways.
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