Dragonfly Neurons Selectively Attend to Targets Within Natural Scenes

Aerial predators, such as the dragonfly, determine the position and movement of their prey even when both are moving through complex, natural scenes. This task is likely supported by a group of neurons in the optic lobe which respond to moving targets that subtend less than a few degrees. These Small Target Motion Detector (STMD) neurons are tuned to both target size and velocity, whilst also exhibiting facilitated responses to targets traveling along continuous trajectories. When presented with a pair of targets, some STMDs generate spiking activity that represent a competitive selection of one target, as if the alternative does not exist (i.e., selective attention). Here, we describe intracellular responses of CSTMD1 (an identified STMD) to the visual presentation of targets embedded within cluttered, natural scenes. We examine CSTMD1 response changes to target contrast, as well as a range of target and background velocities. We find that background motion affects CSTMD1 responses via the competitive selection between features within the natural scene. Here, robust discrimination of our artificially embedded “target” is limited to scenarios when its velocity is matched to, or greater than, the background velocity. Additionally, the background’s direction of motion affects discriminability, though not in the manner observed in STMDs of other flying insects. Our results highlight that CSTMD1’s competitive responses are to those features best matched to the neuron’s underlying spatiotemporal tuning, whether from the embedded target or other features in the background clutter. In many scenarios, CSTMD1 responds robustly to targets moving through cluttered scenes. However, whether this neuronal system could underlie the task of competitively selecting slow moving prey against fast-moving backgrounds remains an open question.Bernard John Essex Evans, David Charles O, Carroll, Joseph Mahandas Fabian, and Steven D. Wiederma

A target-detecting visual neuron in the dragonfly locks-on to selectively attended targets

The visual world projects a complex and rapidly changing image onto the retina of many animal species. This presents computational challenges for those animals reliant on visual processing to provide an accurate representation 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 selectively prioritize processing of some stimuli over others is known as 'selective attention'. We recently identified a dragonfly visual neuron called 'Centrifugal Small Target Motion Detector 1' (CSTMD1) that exhibits selective attention when presented with multiple, equally salient targets. Here we conducted in vivo, electrophysiological recordings from CSTMD1 in wild-caught male dragonflies (Hemicordulia tau), whilst presenting visual stimuli on an LCD monitor. To identify the target selected in any given trial, we uniquely modulated the intensity of the moving targets (frequency-tagging). We found that the frequency information of the selected target is preserved in the neuronal response, whilst the distracter is completely ignored. We also 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 than an abrupt, novel distracter. With this improved method for identifying and biasing target selection in CSTMD1, the dragonfly provides an ideal animal model system to probe the neuronal mechanisms underlying selective attention.Benjamin H. Lancer, Bernard J.E. Evans, Joseph M. Fabian, David C. O’Carroll, and Steven D. Wiederma

The visual neuroecology of anisoptera

Dragonflies belong to the oldest known lineage of flying animals, found across the globe around streams, ponds and forests. They are insect predators, specialising in ambush attack as aquatic larvae and rapid pursuit as adults. Dragonfly adults hunt amidst swarms in conditions that confuse many predatory species, and exhibit capture rates above 90%. Underlying the performance of such a remarkable predator is a finely tuned visual system capable of tracking targets amidst distractors and background clutter. The dragonfly performs a complex repertoire of flight behaviours, from near-motionless hovering to acute turns at high speeds. Here, we review the optical, neuronal, and behavioural adaptations that underlie the dragonflies’ ability to achieve such remarkable predatory success.Benjamin Horatio Lancer, Bernard John Essex Evans and Steven D Wiederma

Preattentive facilitation of target trajectories in a dragonfly visual neuron

The ability to pursue targets in visually cluttered and distraction-rich environments is critical for predators such as dragonflies. Previously, we identified Centrifugal Small-Target Motion Detector 1 (CSTMD1), a dragonfly visual neuron likely involved in such target-tracking behaviour. CSTMD1 exhibits facilitated responses to targets moving along a continuous trajectory. Moreover, CSTMD1 competitively selects a single target out of a pair. Here, we conducted in vivo, intracellular recordings from CSTMD1 to examine the interplay between facilitation and selection, in response to the presentation of paired targets. We find that neuronal responses to both individual trajectories of simultaneous, paired targets are facilitated, rather than being constrained to the single, selected target. Additionally, switches in selection elicit suppression which is likely an important attribute underlying target pursuit. However, binocular experiments reveal these results are constrained to paired targets within the same visual hemifield, while selection of a target in one visual hemifield establishes ocular dominance that prevents facilitation or response to contralaterally presented targets. These results reveal that the dragonfly brain preattentively represents more than one target trajectory, to balance between attentional flexibility and resistance against distraction.Benjamin H. Lancer, Bernard J. E. Evans, Joseph M. Fabian, David C. O, Carroll, Steven D. Wiederma