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.