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.

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 amid 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), while 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, while 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.SIGNIFICANCE STATEMENT We present the first application of frequency tagging to intracellular neuronal recordings, demonstrating that the frequency component of a stimulus is encoded in the spiking response of an individual neuron. Using this technique as an identifier, we demonstrate that CSTMD1 'locks on' to a selected target and encodes the absolute strength of this target, even in the presence of abruptly appearing, high-contrast distracters. The underlying mechanism also permits the selection mechanism to switch between targets mid-trial, even among equivalent targets. Together, these results demonstrate greater complexity in this selective attention system than would be expected in a winner-takes-all network. These results are in contrast to typical findings in the primate and avian brain, but display intriguing resemblance to observations in human psychophysics.

Differential Tuning to Visual Motion Allows Robust Encoding of Optic Flow in the Dragonfly.

Visual cues provide an important means for aerial creatures to ascertain their self-motion through the environment. In many insects, including flies, moths, and bees, wide-field motion-sensitive neurons in the third optic ganglion are thought to underlie such motion encoding; however, these neurons can only respond robustly over limited speed ranges. The task is more complicated for some species of dragonflies that switch between extended periods of hovering flight and fast-moving pursuit of prey and conspecifics, requiring motion detection over a broad range of velocities. Since little is known about motion processing in these insects, we performed intracellular recordings from hawking, emerald dragonflies (Hemicordulia spp.) and identified a diverse group of motion-sensitive neurons that we named lobula tangential cells (LTCs). Following prolonged visual stimulation with drifting gratings, we observed significant differences in both temporal and spatial tuning of LTCs. Cluster analysis of these changes confirmed several groups of LTCs with distinctive spatiotemporal tuning. These differences were associated with variation in velocity tuning in response to translated, natural scenes. LTCs with differences in velocity tuning ranges and optima may underlie how a broad range of motion velocities are encoded. In the hawking dragonfly, changes in LTC tuning over time are therefore likely to support their extensive range of behaviors, from hovering to fast-speed pursuits.SIGNIFICANCE STATEMENT Understanding how animals navigate the world is an inherently difficult and interesting problem. Insects are useful models for understanding neuronal mechanisms underlying these activities, with neurons that encode wide-field motion previously identified in insects, such as flies, hawkmoths, and butterflies. Like some Dipteran flies, dragonflies exhibit complex aerobatic behaviors, such as hovering, patrolling, and aerial combat. However, dragonflies lack halteres that support such diverse behavior in flies. To understand how dragonflies might address this problem using only visual cues, we recorded from their wide-field motion-sensitive neurons. We found these differ strongly in the ways they respond to sustained motion, allowing them collectively to encode the very broad range of velocities experienced during diverse behavior.