Dynamics of optomotor responses in Drosophila to perturbations in optic flow

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Abstract
SUMMARY: For a small flying insect, correcting unplanned course perturbations is essential for navigating through the world. Visual course control relies on estimating optic flow patterns which, in flies, are encoded by interneurons of the third optic ganglion. However, the rules that translate optic flow into flight motor commands remain poorly understood. Here, we measured the temporal dynamics of optomotor responses in tethered flies to optic flow fields about three cardinal axes. For each condition, we used white noise analysis to determine the optimal linear filters linking optic flow to the sum and difference of left and right wing beat amplitudes. The estimated filters indicate that flies react very quickly to perturbations of the motion field, with pure delays in the order of ~20 ms and time-to-peak of ~100 ms. By convolution the filters also predict responses to arbitrary stimulus sequences, accounting for over half the variance in 5 of our 6 stimulus types, demonstrating the approximate linearity of the system with respect to optic flow variables. In the remaining case of yaw optic flow we improved predictability by measuring individual flies, which also allowed us to analyze the variability of optomotor responses within a population. Finally, the linear filters at least partly explain the optomotor responses to superimposed and decomposed compound flow fields.