Interaction of "chromatic" and "achromatic" circuits in Drosophila color opponent processing.

Color vision is an important sensory capability of humans and many animals. It relies on color opponent processing in visual circuits that gradually compare the signals of photoreceptors with different spectral sensitivities. In Drosophila, this comparison begins already in the presynaptic terminals of UV-sensitive R7 and longer wavelength-sensitive R8 inner photoreceptors that inhibit each other in the medulla. How downstream neurons process their signals is unknown. Here, we report that the second order medulla interneuron Dm8 is inhibited when flies are stimulated with UV light and strongly excited in response to a broad range of longer wavelength (VIS) stimuli. Inhibition to UV light is mediated by histaminergic input from R7 and expression of the histamine receptor ort in Dm8, as previously suggested. However, two additional excitatory inputs antagonize the R7 input. First, activation of R8 leads to excitation of Dm8 by non-canonical photoreceptor signaling and cholinergic neurotransmission in the visual circuitry. Second, activation of outer photoreceptors R1-R6 with broad spectral sensitivity causes excitation in Dm8 through the cholinergic medulla interneuron Mi1, which is known for its major contribution to the detection of spatial luminance contrast and visual motion. In summary, Dm8 mediates a second step in UV/VIS color opponent processing in Drosophila by integrating input from all types of photoreceptors. Our results demonstrate novel insights into the circuit integration of R1-R6 into color opponent processing and reveal that chromatic and achromatic circuitries of the fly visual system interact more extensively than previously thought.

Selective processing of all rotational and translational optic flow directions in the zebrafish pretectum and tectum.

BACKGROUND: The processing of optic flow in the pretectum/accessory optic system allows animals to stabilize retinal images by executing compensatory optokinetic and optomotor behavior. The success of this behavior depends on the integration of information from both eyes to unequivocally identify all possible translational or rotational directions of motion. However, it is still unknown whether the precise direction of ego-motion is already identified in the zebrafish pretectum or later in downstream premotor areas. RESULTS: Here, we show that the zebrafish pretectum and tectum each contain four populations of motion-sensitive direction-selective (DS) neurons, with each population encoding a different preferred direction upon monocular stimulation. In contrast, binocular stimulation revealed the existence of pretectal and tectal neurons that are specifically tuned to only one of the many possible combinations of monocular motion, suggesting that further downstream sensory processing might not be needed to instruct appropriate optokinetic and optomotor behavior. CONCLUSION: Our results suggest that local, task-specific pretectal circuits process DS retinal inputs and carry out the binocular sensory computations necessary for optokinetic and optomotor behavior.

Color Processing in the Early Visual System of Drosophila.

Color vision extracts spectral information by comparing signals from photoreceptors with different visual pigments. Such comparisons are encoded by color-opponent neurons that are excited at one wavelength and inhibited at another. Here, we examine the circuit implementation of color-opponent processing in the Drosophila visual system by combining two-photon calcium imaging with genetic dissection of visual circuits. We report that color-opponent processing of UVshort/blue and UVlong/green is already implemented in R7/R8 inner photoreceptor terminals of "pale" and "yellow" ommatidia, respectively. R7 and R8 photoreceptors of the same type of ommatidia mutually inhibit each other directly via HisCl1 histamine receptors and receive additional feedback inhibition that requires the second histamine receptor Ort. Color-opponent processing at the first visual synapse represents an unexpected commonality between Drosophila and vertebrates; however, the differences in the molecular and cellular implementation suggest that the same principles evolved independently.

Optogenetic control of fly optomotor responses.

When confronted with a large-field stimulus rotating around the vertical body axis, flies display a following behavior called "optomotor response." As neural control elements, the large tangential horizontal system (HS) cells of the lobula plate have been prime candidates for long. Here, we applied optogenetic stimulation of HS cells to evaluate their behavioral role in Drosophila. To minimize interference of the optical activation of channelrhodopsin-2 with the visual perception of the flies, we used a bistable variant called ChR2-C128S. By applying pulses of blue and yellow light, we first demonstrate electrophysiologically that lobula plate tangential cells can be activated and deactivated repeatedly with no evident change in depolarization strength over trials. We next show that selective optogenetic activation of HS cells elicits robust yaw head movements and yaw turning responses in fixed and tethered flying flies, respectively.