Nervous systems combine lower-level sensory signals to detect higher-order stimulus features critical to survival1,2,3, such as the visual looming motion created by an imminent collision or approaching predator4. Looming-sensitive neurons have been identified in diverse animal species5,6,7,8,9. Different large-scale visual features such as looming often share local cues, which means loom-detecting neurons face the challenge of rejecting confounding stimuli. Here we report the discovery of an ultra-selective looming detecting neuron, lobula plate/lobula columnar, type II (LPLC2)10 in Drosophila, and show how its selectivity is established by radial motion opponency. In the fly visual system, directionally selective small-field neurons called T4 and T5 form a spatial map in the lobula plate, where they each terminate in one of four retinotopic layers, such that each layer responds to motion in a different cardinal direction11,12,13. Single-cell anatomical analysis reveals that each arm of the LPLC2 cross-shaped primary dendrites ramifies in one of these layers and extends along that layer’s preferred motion direction. In vivo calcium imaging demonstrates that, as their shape predicts, individual LPLC2 neurons respond strongly to outward motion emanating from the centre of the neuron’s receptive field. Each dendritic arm also receives local inhibitory inputs directionally selective for inward motion opposing the excitation. This radial motion opponency generates a balance of excitation and inhibition that makes LPLC2 non-responsive to related patterns of motion such as contraction, wide-field rotation or luminance change. As a population, LPLC2 neurons densely cover visual space and terminate onto the giant fibre descending neurons, which drive the jump muscle motor neuron to trigger an escape take off. Our findings provide a mechanistic description of the selective feature detection that flies use to discern and escape looming threats.
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We thank the Janelia FlyLight Project Team for help with brain dissections, histology, and confocal imaging, Janelia Scientific Computing for image processing and data analysis tools, the Janelia FlyLight Project Team, M. Wu, and T. Ngo for help with split-GAL4 screening, H. Dionne for split-GAL4 molecular biology, and E. Gruntman for feedback on stimulus design. We thank Janelia Instrument Design and Fabrication and Vidrio Technologies for advice and help with the two-photon microscope setup. We thank S. Namiki and the Janelia Descending Interneuron Project for the empty split-GAL4 line. We also thank K. Svoboda, A. Chuong, and members of the Card and Reiser laboratories for discussions and comments on the manuscript. This work was supported by the Howard Hughes Medical Institute.
Extended data figures
Rotating view of a single LPLC2 neuron showing branching pattern (same cell as Fig. 1d,e) on reference neuropil (grey, anti-Brp). Dendrites in each lobula plate layer are colored differently.