Ultra-selective looming detection from radial motion opponency

Nervous systems combine lower-level sensory signals to detect higher order stimulus features critical to survival(1–3), such as the visual looming motion created by an imminent collision or approaching predator(4). Looming-sensitive neurons have been identified in diverse animal species(5–9). 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, 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 direction(11–13). Single cell anatomical analysis reveals that each arm of LPLC2’s 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 center 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 translation, or luminance change. As a population, LPLC2 neurons densely cover visual space and terminate onto the giant fiber descending neurons, which drive the jump muscle motoneuron to trigger an escape takeoff. Our findings provide a mechanistic description of the selective feature detection that flies use to discern and escape looming threats.