Target-detecting neurons in the dragonfly lock on to selectively attended targets

Abstract

The visual world projects a complex and rapidly changing image on to the retina, presenting a computational challenge for any animal relying on vision for an accurate view of the world. One such challenge is parsing a visual scene for the most salient targets, such as the selection of prey amidst a swarm. The ability to selectivity prioritize processing of some stimuli over others is known as 'selective attention'. Previously, we identified a dragonfly visual neuron called 'Centrifugal Small Target Motion Detector 1' (CSTMD1) that exhibits selective attention when presented with multiple, equally salient features. Here we conducted electrophysiological recordings from CSTMD1 neurons in vivo, whilst presenting visual stimuli on a monitor display. To identify the target selected in any given trial, we modulated the intensity of moving targets, each with a unique frequency (frequency-tagging). We find that the frequency information of the selected stimulus is preserved in the neuronal response, whilst the distracter is completely ignored. We show that the competitive system that underlies selection in this neuron can be biased by the presentation of a preceding target on the same trajectory, even when it is of lower contrast to the distracter. With an improved method of identifying and biasing target selection in CSTMD1, the dragonfly provides an effective animal model system to probe the mechanisms underlying neuronal selective attention.Significance Statement: This is a novel application of frequency tagging at the intracellular level, demonstrating that frequency information of a flickering stimulus is preserved in the response of an individual neuron. Using this technique, we show that the selective attention mechanism in an individual dragonfly visual neuron is able to lock on to the selected stimuli, in the presence of distracters, even those of abrupt onset or higher contrast. Conversely, unidentified factors allow selection to occasionally switch mid-trial to the other target. We therefore show that this neuronal network underlying selective attention is more complex than the traditionally modelled winner-takes-all framework.