Ultra-selective looming detection from radial motion opponency

Abstract

The discovery of a visual-looming-sensitive neuron, LPLC2, that provides input to the Drosophila escape pathway, and uses dendrites patterned to integrate directionally selective inputs to selectively encode outward motion. To detect the threat of a looming object, visual systems must integrate many motion cues across the whole visual field, and thus face the challenge of rejecting confounding stimuli, such as large passing objects. The neuronal computation behind this complex response is unknown. Gwyneth Card and colleagues have discovered a cross-shaped neuron in the Drosophila brain, LPLC2, whose dendrites align with the four cardinal directions of motion, as represented along the layers of elementary motion detector neurons T4 and T5 in the lobula plate. A balance of inhibitory and excitatory inputs then ensures that individual LPLC2 neurons respond to outward but not inward motion from the center of the neuron''s receptive field, making LPLC2 neurons non-responsive to related patterns of motion such as contraction, wide-field translation or luminance change. 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.