Descending neurons of the hoverfly respond to pursuits of artificial targets

Many animals use motion vision information to control dynamic behaviors. Predatory animals, for example, show an exquisite ability to detect rapidly moving prey, followed by pursuit and capture. Such target detection is not only used by predators but is also important in conspecific interactions, such as for male hoverflies defending their territories against conspecific intruders. Visual target detection is believed to be subserved by specialized target-tuned neurons found in a range of species, including vertebrates and arthropods. However, how these target-tuned neurons respond to actual pursuit trajectories is currently not well understood. To redress this, we recorded extracellularly from target-selective descending neurons (TSDNs) in male Eristalis tenax hoverflies. We show that they have dorso-frontal receptive fields with a preferred direction up and away from the visual midline. We reconstructed visual flow fields as experienced during pursuits of artificial targets (black beads). We recorded TSDN responses to six reconstructed pursuits and found that each neuron responded consistently at remarkably specific time points but that these time points differed between neurons. We found that the observed spike probability was correlated with the spike probability predicted from each neuron's receptive field and size tuning. Interestingly, however, the overall response rate was low, with individual neurons responding to only a small part of each reconstructed pursuit. In contrast, the TSDN population responded to substantially larger proportions of the pursuits but with lower probability. This large variation between neurons could be useful if different neurons control different parts of the behavioral output.