Predictive saccades and decision making in the beetle-predating saffron robber fly.

Internal predictions about the sensory consequences of self-motion, encoded by corollary discharge, are ubiquitous in the animal kingdom, including for fruit flies, dragonflies, and humans. In contrast, predicting the future location of an independently moving external target requires an internal model. With the use of internal models for predictive gaze control, vertebrate predatory species compensate for their sluggish visual systems and long sensorimotor latencies. This ability is crucial for the timely and accurate decisions that underpin a successful attack. Here, we directly demonstrate that the robber fly Laphria saffrana, a specialized beetle predator, also uses predictive gaze control when head tracking potential prey. Laphria uses this predictive ability to perform the difficult categorization and perceptual decision task of differentiating a beetle from other flying insects with a low spatial resolution retina. Specifically, we show that (1) this predictive behavior is part of a saccade-and-fixate strategy, (2) the relative target angular position and velocity, acquired during fixation, inform the subsequent predictive saccade, and (3) the predictive saccade provides Laphria with additional fixation time to sample the frequency of the prey's specular wing reflections. We also demonstrate that Laphria uses such wing reflections as a proxy for the wingbeat frequency of the potential prey and that consecutively flashing LEDs to produce apparent motion elicits attacks when the LED flicker frequency matches that of the beetle's wingbeat cycle.

Binocular Encoding in the Damselfly Pre-motor Target Tracking System.

Akin to all damselflies, Calopteryx (family Calopterygidae), commonly known as jewel wings or demoiselles, possess dichoptic (separated) eyes with overlapping visual fields of view. In contrast, many dragonfly species possess holoptic (dorsally fused) eyes with limited binocular overlap. We have here compared the neuronal correlates of target tracking between damselfly and dragonfly sister lineages and linked these changes in visual overlap to pre-motor neural adaptations. Although dragonflies attack prey dorsally, we show that demoiselles attack prey frontally. We identify demoiselle target-selective descending neurons (TSDNs) with matching frontal visual receptive fields, anatomically and functionally homologous to the dorsally positioned dragonfly TSDNs. By manipulating visual input using eyepatches and prisms, we show that moving target information at the pre-motor level depends on binocular summation in demoiselles. Consequently, demoiselles encode directional information in a binocularly fused frame of reference such that information of a target moving toward the midline in the left eye is fused with information of the target moving away from the midline in the right eye. This contrasts with dragonfly TSDNs, where receptive fields possess a sharp midline boundary, confining responses to a single visual hemifield in a sagittal frame of reference (i.e., relative to the midline). Our results indicate that, although TSDNs are conserved across Odonata, their neural inputs, and thus the upstream organization of the target tracking system, differ significantly and match divergence in eye design and predatory strategies. VIDEO ABSTRACT.