Dual receptive fields underlying target and motion sensitivity in looming sensitive descending neurons

When an animal is pursuing a target, such as a bird pursuing prey, the retinal projection of the target is initially very small. However, prior to successful capture, as the pursuer nears the target, the image becomes a rapidly expanding object. This suggests that different neural pathways underlie these two behavioural stages: one tuned to small retinal objects, and one to larger, looming stimuli. Indeed, in zebrafish, two different optic brain regions support the initial visualization of prey and the final stages of prey capture. The pursuit of small targets is not limited to vertebrates, with many invertebrates also utilizing these capabilities for prey capture, territorial defences, or courtship. Male Eristalis tenax hoverflies, which are highly territorial, have target tuned neurons that likely underlie the initial stages of target detection and pursuit. However, the underlying neuronal control of the final stages of prey capture is currently unknown. We here show a class of descending neurons with dual sensitivity, separated into two distinct receptive fields. The dorsal receptive field shows sensitivity to small targets whereas the ventral receptive field responds to larger objects and looming stimuli. We show that the two receptive fields have different pre-synaptic input, where the inputs are not linearly summed. This novel and unique arrangement could thus support the different stages of target pursuit behavior, where targets are initially detected in the dorsal receptive field, whilst the ventral receptive field is used during the final stages of pursuit and eventual capture.