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

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 can also play an important role in conspecific interactions. Male hoverflies (Eristalis tenax), for example, vigorously defend their territories against conspecific intruders. Visual target detection is believed to be subserved by specialized target-tuned neurons that are found in a range of species, including cats, zebrafish, and insects. 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 the neurons have dorso-frontal receptive fields, with a preferred direction up and away from the visual midline. We next 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 compared the observed spike probability with the spike probability predicted from each neuron's receptive field and size tuning and found a correlation coefficient of 0.35. 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 a substantially larger proportion of the pursuits (up to a median of 23%). This large variation between neurons could be useful if different neurons control different parts of the behavioral output.Funding provided by: Australian Research CouncilCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100000923Award Number: DP180100144Funding provided by: Australian Research CouncilCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100000923Award Number: DP210100740Funding provided by: Australian Research CouncilCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100000923Award Number: FT180100289Funding provided by: Air Force Office of Scientific ResearchCrossref Funder Registry ID: http://dx.doi.org/10.13039/100000181Award Number: FA9550-19-1-0294This is described in detail in the README file as well as the methods of the paper