Abstract
Compared with connections between the retinae and primary visual centers, relatively less is known in both mammals and insects about the functional segregation of neural pathways connecting primary and higher centers of the visual processing cascade. Here, using the Drosophila visual system as a model, we demonstrate two levels of parallel computation in the pathways that connect primary visual centers of the optic lobe to computational circuits embedded within deeper centers in the central brain. We show that a seemingly simple achromatic behavior, namely phototaxis, is under the control of several independent pathways, each of which is responsible for navigation towards unique wavelengths. Silencing just one pathway is enough to disturb phototaxis towards one characteristic monochromatic source, whereas phototactic behavior towards white light is not affected. The response spectrum of each demonstrable pathway is different from that of individual photoreceptors, suggesting subtractive computations. A choice assay between two colors showed that these pathways are responsible for navigation towards, but not for the detection itself of, the monochromatic light. The present study provides novel insights about how visual information is separated and processed in parallel to achieve robust control of an innate behavior.
Highlights
In animals ranging from insects to mammals, visual information is processed in a highly parallel manner
Our analysis revealed that visual information required for proper phototaxis is mediated by multiple parallel pathways in a wavelength-specific manner and that phototactic responses towards ambient light and distant light source are handled differently
ARCHITECTURE OF THE PHOTOTAXIS-ASSOCIATED VISUAL PROJECTION NEURONS (VPNs) We examined the detailed architecture of the Lobula Tangential 11 neurons (LT11) and Medulla Columnar 61 neurons (MC61) pathways
Summary
In animals ranging from insects to mammals, visual information is processed in a highly parallel manner. In insects, projections from the compound eye to nested neuropils of the optic lobe show clear retinotopic patterns, with each columnar visual cartridge in the optic lobe neuropils having specific projection from the retinal cells oriented to a specific angle of view (Figure 1A). These retinotopic projections involve many different morphologically and functionally distinct neurons (Fischbach and Dittrich, 1989; Otsuna and Ito, 2006; Strausfeld et al, 2006; Strausfeld and Okamura, 2007), which encode specific visual information such as figure-ground discrimination, motion detection, spectral information, and stereopsis (Krapp and Hengstenberg, 1996; Wicklein and Strausfeld, 2000; Douglass and Strausfeld, 2003; Strausfeld et al, 2006). Relay interneurons connect the cartridges of different neuropils to mediate retinotopic signal transmission (Figure 1A)
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