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Object tracking in motion-blind flies

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Abstract

Different visual features of an object, such as its position and direction of motion, are important elements for animal orientation, but the neural circuits extracting them are generally not well understood. We analyzed this problem in Drosophila, focusing on two well-studied behaviors known as optomotor response and fixation response. In the neural circuit controlling the optomotor response, columnar T4 and T5 cells are thought to be crucial. We found that blocking T4 and T5 cells resulted in a complete loss of the optomotor response. Nevertheless, these flies were still able to fixate a black bar, although at a reduced performance level. Further analysis revealed that flies in which T4 and T5 cells were blocked possess an intact position circuit that is implemented in parallel to the motion circuit; the optomotor response is exclusively controlled by the motion circuit, whereas the fixation response is supported by both the position and the motion circuit.

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Figure 1: Optomotor response and fixation response of control and T4/T5 block flies.
Figure 2: Open-loop analysis of the fixation response.
Figure 3: Open-loop responses to an appearing and disappearing black bar.
Figure 4: Open-loop responses to local bar motion and to local luminance changes.
Figure 5: Closed-loop fixation response during open-loop background motion.
Figure 6: In vivo electrophysiological recordings from vertical system (VS) and horizontal system (HS) cells in the immobilized fly.
Figure 7: Model simulations of the fly's course control system.

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Acknowledgements

We wish to thank G. Rubin and A. Nern for providing the T4/T5 cell–specific driver line R42F06-Gal4 and V. Jayaraman for advice on setting up the locomotion recorder. We are also grateful to J. Haag, A. Mauss, A. Arenz and A. Leonhardt for many helpful discussions and critically reading the manuscript, S. Prech for help with the design of the Peltier temperature control system, C. Theile for fly work, and F. Foerstner for reconstructing the three horizontal system cells shown in Figure 1a. A. Bahl and A. Borst are members of the Bernstein Center for Computational Neuroscience and the Graduate School of Systemic Neurosciences.

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Contributions

A. Bahl set up the locomotion recorder and the stimulus display, and wrote the software for reading the behavioral output and displaying the stimulus. A. Bahl and T.S. performed all of the behavioral experiments and evaluated the data. G.A. performed the electrophysiological recordings and analyzed the data. A. Bahl and A. Borst designed the study. A. Borst carried out the modeling work. A. Borst and A. Bahl wrote the manuscript with the help of the other authors.

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Correspondence to Armin Bahl or Alexander Borst.

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Bahl, A., Ammer, G., Schilling, T. et al. Object tracking in motion-blind flies. Nat Neurosci 16, 730–738 (2013). https://doi.org/10.1038/nn.3386

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