Eight pairs of descending visual neurons in the dragonfly give wing motor centers accurate population vector of prey direction

Abstract

Intercepting a moving object requires prediction of its future location. This complex task has been solved by dragonflies, who intercept their prey in midair with a 95% success rate. In this study, we show that a group of 16 neurons, called target-selective descending neurons (TSDNs), code a population vector that reflects the direction of the target with high accuracy and reliability across 360°. The TSDN spatial (receptive field) and temporal (latency) properties matched the area of the retina where the prey is focused and the reaction time, respectively, during predatory flights. The directional tuning curves and morphological traits (3D tracings) for each TSDN type were consistent among animals, but spike rates were not. Our results emphasize that a successful neural circuit for target tracking and interception can be achieved with few neurons and that in dragonflies this information is relayed from the brain to the wing motor centers in population vector form.

Fig. 1.

Small moving targets rapidly activate TSDNs. View of a L. luctuosa head from behind (A) and side (B) where the gray cone symbolizes the visual field of the dorsal area. The eyes are false colored in red (dorsal eye) and green (rest of the eye). A target (flying insect) moving above the dragonfly from front to back crossing the left visual field (yellow area) in the direction indicated by the arrow, excites the TSDN MDT1. (C) Polar plot with the “God’s eye view” reference used to display target directions, i.e., the target movement shown in A and B is here shown as a vector pointing down to the blue zone. (D) Summary of the latencies. The latencies obtained for each TSDN type were not significantly different from each other (one-way ANOVA).

Fig. 2.

Each TSDN type shows a unique direction tuning curve and receptive field consistent across animals. (A) Contralateral and (B) ipsilateral TSDN receptive fields whose axons were in the right connective of the ventral nerve cord (VNC). The polar plots show the directional preference of each recorded TSDN (red dots) and their mean direction tuning distribution (black bars). The red arrow indicates mean preferred direction. The color-coded direction receptive field (DRF) maps show the mean direction preference at each pixel, which was calculated by averaging the direction peak, at each pixel, for all recordings of each TSDN type. In addition, spike-triggered average (STA) maps are shown for each TSDN type. Note that, because number of spikes was normalized before and after computing the average, the same scale applies to all STA maps.

Fig. 3.

TSDN sensitivity is matched to the predatory behavior. (A) The visual receptive fields of the TSDNs combine to create an area of increased sensitivity to target movement near midline. For more details on eye coordinates, see Fig. S6. (B) DIT1, DIT3, and MDT1 transmit motion information in the visual field contralateral to their axons in the VNC. MDT5, MDT3, DIT2, MDT2, and MDT4 transmit motion information in the visual field ipsilateral to their axons in the VNC. Together, all eight axons travel through the ventral connective and thoracic ganglia.

Fig. 4.

In the wing motor centers, all TSDNs share morphological features. (A) The mesothoracic, metathoracic, and first abdominal ganglia were imaged and warped to allow morphological comparison. (B) Unilateral DIT2 on the left and bilateral MDT1 on the right, injected in the same animal, target the same locations. (C) Traces within each TSDN type (grouped according to the electrophysiological results) are consistent, so the most complete fill from each TSDN type was used for comparison. TSDNs were categorized into “simple” or “complex” cells. A pairwise comparison (dorsal views) shows that unilateral simple cells, DIT1 (green), DIT2 (red), and MDT2 (magenta), are indistinguishable from each other (D, Upper), but the bilateral simple cells MDT1 (white) and MDT4 (yellow) display specific branching patterns (D, Lower). However, all simple TSDNs target the same location. In contrast, pairwise comparisons between the complex cells, DIT3 (red), MDT3 (green), and MDT5 (cyan) (E, all panels) are less informative because their additional intricate branching exhibits higher variability, particularly in the medial region of the ganglia (traces in C).

Fig. 5.

The TSDN population vector codes direction of the prey with high accuracy. (A) A target moving in the left side of the visual field activates the subset of TSDNs shown in the diagram. The population of TSDNs providing inputs to the left (nine cells) and right (seven cells) wings differ. (B) Graphical representation of a dragonfly TSDN population vector. Contributing TSDN vectors (green), stimulus direction (yellow), and population vector (red) are shown. (C and D) Population vectors for the left (C) and right (D) wings were calculated for all presented trajectories. (C, i and D, i) The population vectors, binned in 18°, are strongly correlated with the target direction. Left wing circular R = 0.9986 (P < 0.001) and right wing R = 0.9984 (P < 0.001). (C, ii and D, ii) The direction of the target and the direction of the population vector are not significantly different in any direction because the difference between these two parameters is close to zero (dotted values) and because zero is within the 95% confidence interval (white bars). Colors refer to the direction of the presented target. The data concern targets moving in the left side of the visual field, so targets that traveled toward the medial part of the animal correspond to the red section. (C, iii and D, iii) On average, removing two types of TSDN from the population (six cell types used) does not impact the accuracy of the population vector significantly. For the left wing, three TSDN types are, on average, sufficient to provide a population vector whose bias is within 10° of the presented target direction.