Wireless recordings from dragonfly target detecting neurons during prey interception flight

Abstract

Target interception is a complex sensorimotor behavior which requires fine tuning of the sensory system and its strategic coordination with the motor system. Despite various theories about how interception is achieved, its neural implementation remains unknown. We have previously shown that hunting dragonflies employ a balance of reactive and predictive control to intercept prey, using sophisticated model driven predictions to account for expected prey and self-motion. Here we explore the neural substrate of this interception system by investigating a well-known class of target-selective descending neurons (TSDNs). These cells have long been speculated to underlie interception steering but have never been studied in a behaving dragonfly. We combined detailed neuroanatomy, high-precision kinematics data and state-of-the-art neural telemetry to measure TSDN activity during flight. We found that TSDNs are exquisitely tuned to prey angular size and speed at ethological distances, and that they synapse directly onto neck and wing motoneurons in an unusual manner. However, we found that TSDNs were only weakly active during flight and are thus unlikely to provide the primary steering signal. Instead, they appear to drive the foveating head movements that stabilize prey on the eye before and likely throughout the interception flight. We suggest the TSDN population implements the reactive portion of the interception steering control system, coordinating head and wing movements to compensate for unexpected prey motion.