A Target-Detecting Visual Neuron in the Dragonfly Locks on to Selectively Attended Targets

Abstract

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 1Ј (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.

Spike bursting in a dragonfly target-detecting neuron

“…Most published work on dragonfly STMDs comes from a particularly interesting neuron, the Centrifugal Small Target Motion Detector neuron (CSTMD1) 5 – 13 . This neuron possesses remarkably complex response properties including predictive gain modulation 6 , 7 , 10 , 11 and selective attention 8 , 12 , proposed to underlie their interception of prey even amidst a swarm. Like many other investigations of neuronal activity, previous descriptions of CSTMD1 quantify response strength by counting spike rates over a temporal window of interest.…”

Oscillations in the central brain of Drosophila are phase locked to attended visual features

“…frequencies (37). However, it is unknown how such selective neural processes are controlled in the insect brain or whether these neural measures are relevant to behavioral decision making.…”

“…Similarly, visual learning paradigms for Drosophila melanogaster have uncovered a capacity for context generalization, where flies perceived visual objects as the same despite changes in color ( 31 , 32 ), suggesting they were attending to the object shape feature and ignoring color cues. There is growing evidence for attention-like processes in insects, such as during visual fixation, decision making, and novelty detection in Drosophila flies ( 33 – 36 ), as well as multiple object tracking in dragonflies ( 37 ). The latter electrophysiological study uncovered motion-detecting neurons in dragonflies that selectively lock onto the timing or phase of salient objects, which was shown by “tagging” competing objects with distinct flicker frequencies ( 37 ).…”

“…There is growing evidence for attention-like processes in insects, such as during visual fixation, decision making, and novelty detection in Drosophila flies ( 33 – 36 ), as well as multiple object tracking in dragonflies ( 37 ). The latter electrophysiological study uncovered motion-detecting neurons in dragonflies that selectively lock onto the timing or phase of salient objects, which was shown by “tagging” competing objects with distinct flicker frequencies ( 37 ). However, it is unknown how such selective neural processes are controlled in the insect brain or whether these neural measures are relevant to behavioral decision making.…”

The complex optic lobe of dragonflies

“…Recordings obtained were during ongoing experiments aimed at classifying motion sensitive and feature selective neurons such as the small target motion detecting (STMD) neurons and lobula tangential cells (LTC's) described in our recent work [33,[39][40][41], from more than 300 dragonflies over a 4 year period. Upon establishing a healthy recording, all neurons were characterized using a range of stimuli presented on an LCD monitor (either an Eizo Foris FG2421 LCD at a frame rate of 120 Hz, or an Asus ROG Swift PG279Q IPS LCD at 165 Hz).…”