Temperature modulates the tuning properties of small target motion detector neurons in the dragonfly visual system.

Dragonflies are poikilothermic animals with limited thermoregulation; therefore, their entire bodies, including the brain, experience a range of temperatures during their daily activities.1,2 These flying insects exhibit hunting prowess, pursuing prey or conspecifics whether in direct sunlight or under the cover of cloud.3,4 Likely to underlie these aerobatic feats are the small target motion detector (STMD) neurons.5 These visual neurons are sensitive to target contrast and tuned to the target's size and velocity, with some neurons exhibiting complex predictive and selective properties, well suited for prey interception and feeding amid swarms.3,4,6,7,8,9 Increased temperature can modulate the biochemical processes underlying neuronal processing, increasing sensitivity and quickening the responsiveness of insect photoreceptors and downstream optic flow neurons,10,11,12 while in other neuronal pathways, compensatory processes have been shown to account for temperature changes.13,14 We determined the ethological range of temperatures experienced by the dragonfly, Hemicordulia tau, in its natural environment. Across this behaviorally relevant range, we showed increased temperatures having a large 8.7-fold increase in the contrast sensitivity of STMD neurons. However, suppression of responses to larger targets was unaltered. STMD tuning for target velocities was changed remarkably, not only increasing the optimum but extending the fastest velocities encoded by an order of magnitude. These results caution against interpreting functionality underlying spike rates at constrained, experimental temperatures. Moreover, they raise intriguing new questions about how information is represented within the brain of these flying insects, given the relationship between visual stimulus parameters and neuronal activity varies so dramatically depending on current environmental conditions.

Localized and Long-Lasting Adaptation in Dragonfly Target-Detecting Neurons.

Some visual neurons in the dragonfly (Hemicordulia tau) optic lobe respond to small, moving targets, likely underlying their fast pursuit of prey and conspecifics. In response to repetitive targets presented at short intervals, the spiking activity of these "small target motion detector" (STMD) neurons diminishes over time. Previous experiments limited this adaptation by including intertrial rest periods of varying durations. However, the characteristics of this effect have never been quantified. Here, using extracellular recording techniques lasting for several hours, we quantified both the spatial and temporal properties of STMD adaptation. We found that the time course of adaptation was variable across STMD units. In any one STMD, a repeated series led to more rapid adaptation, a minor accumulative effect more akin to habituation. Following an adapting stimulus, responses recovered quickly, though the rate of recovery decreased nonlinearly over time. We found that the region of adaptation is highly localized, with targets displaced by ∼2.5° eliciting a naive response. Higher frequencies of target stimulation converged to lower levels of sustained response activity. We determined that adaptation itself is a target-tuned property, not elicited by moving bars or luminance flicker. As STMD adaptation is a localized phenomenon, dependent on recent history, it is likely to play an important role in closed-loop behavior where a target is foveated in a localized region for extended periods of the pursuit duration.

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.

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.

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.