Dragonfly Neurons Selectively Attend to Targets Within Natural Scenes

Abstract

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.

Visual versus visual-inertial guidance in hawks pursuing terrestrial targets

“…Tectal neuron responses are best known from pigeons, which do not engage in prey pursuit, but neurons with similar responses have also been found in many predatory insects. These include small target motion detectors (STMDs) [ 41 , 42 ] which synapse with target sensitive descending neurons (TSDNs) whose output commands thoracic muscle activity [ 43 ]. The STMD responses of hover flies (Diptera: Syrphidae) and dragonflies are unaffected by background motion [ 41 , 42 ], but the TSDN responses of hover flies and robber flies are strongly affected, appearing to depend specifically upon the motion of the target relative to its background [ 44 , 45 ].…”

“…These include small target motion detectors (STMDs) [ 41 , 42 ] which synapse with target sensitive descending neurons (TSDNs) whose output commands thoracic muscle activity [ 43 ]. The STMD responses of hover flies (Diptera: Syrphidae) and dragonflies are unaffected by background motion [ 41 , 42 ], but the TSDN responses of hover flies and robber flies are strongly affected, appearing to depend specifically upon the motion of the target relative to its background [ 44 , 45 ]. Indeed, TSDN response is suppressed completely when the target and the background are moving at the same apparent velocity [ 45 ], and this inhibition persists even when the region of syndirectional optic flow is confined to the small area of the frontal visual field where tracked targets are positioned on the retina [ 44 ].…”

Visual versus visual-inertial guidance in hawks pursuing terrestrial targets

“…Tectal neuron responses are best known from pigeons, which do not engage in prey pursuit, but neurons with similar responses have also been found in many predatory insects. These include small target motion detectors (STMDs) ( Nordström et al, 2006 ; Evans et al, 2022 ) which synapse with target sensitive descending neurons (TS-DNs) whose output commands thoracic muscle activity ( Namiki et al, 2018 ). The STMD responses of hover flies (Diptera: Syrphidae) and dragonflies are unaffected by background motion ( Nordström et al, 2006 ; Evans et al, 2022 ), but the TSDN responses of hover flies and robber flies are strongly affected, appearing to depend specifically upon the motion of the target relative to its background ( Nicholas et al, 2018 ; Nicholas and Nordström, 2021 ).…”

“…These include small target motion detectors (STMDs) ( Nordström et al, 2006 ; Evans et al, 2022 ) which synapse with target sensitive descending neurons (TS-DNs) whose output commands thoracic muscle activity ( Namiki et al, 2018 ). The STMD responses of hover flies (Diptera: Syrphidae) and dragonflies are unaffected by background motion ( Nordström et al, 2006 ; Evans et al, 2022 ), but the TSDN responses of hover flies and robber flies are strongly affected, appearing to depend specifically upon the motion of the target relative to its background ( Nicholas et al, 2018 ; Nicholas and Nordström, 2021 ). Indeed, TSDN response is suppressed completely when the target and the background are moving at the same apparent velocity ( Nicholas et al, 2018 ), and this inhibition persists even when the region of syndirectional optic flow is confined to the small area of the frontal visual field where tracked targets are positioned on the retina ( Nicholas and Nordström, 2021 ).…”

Sparse spike trains and the limitation of rate codes underlying rapid behaviours

“…However, this assumption requires evidence that a large homogeneous cell population exists, which is not always present. For example, higher-order neurons in the dragonfly target-detecting pathway appear to be heterogeneous in terms of receptive field location, direction tuning and spiking statistics [7][8][9][10][11]. In such a system, pooling across a population of neurons may occur, but many repetitions from a single neuron will produce a false estimate of real-time population activity.…”