Parallel encoding of direction of wind, head, abdomen, and visual pattern movement by single interneurons in the dragonfly

Abstract

1. The self-movement detectors whose detailed properties are introduced here are among the largest interneurons in the ventral nerve cord of the dragonflyAnax junius. They combine information from a wide variety of sensory structures including the compound eyes, mechanosensory frontal hairs, antennae, neck proprioceptors, and wind sensitive hairs in the neck region (Fig. 6). They fall into 8 classes, each with a specific pattern of multimodal inputs (Fig. 1). 2. Their visual receptive fields are large, anteriorly weighted, and selective for animal rotation in a given direction (Figs. 1, 2). 3. They show directionally selective responses to air puffs delivered to the front of the head and to shifts in direction of a stream of air onto the head (Fig. 8). 4. They show directionally selective responses to air puffs from the sides, above, and below the animal into the neck region (Figs. 3, 4, 5). 5. They respond directionally to rotations of the head in still air in the dark (Figs. 3, 4, 11). The receptors mediating these proprioceptive responses are probably different from those mediating the responses to air puffs to the neck. 6. Four of the eight classes respond when the animal actively flexes its abdomen (Fig. 12). 7. Within each modality, they are inhibited by stimulation in the non-preferred direction. Pairwise presentations of stimuli to different inputs showed that each sensory channel is capable of inhibiting self-movement-detector responses to stimulation through any other channel (Figs. 13, 14). 8. For each class, the receptive fields of the various inputs are all aligned to detect rotation of the animal or the head within the same plane in space (Figs. 3, 4, 5). Two classes are aligned in the horizontal plane, and the other six in oblique planes (Fig. 1). 9. The precise alignment of directional selectivity of several input modalities within the same plane, combined with the finding that individual self-movement detectors drive adjustments in wing position (Olberg 1978) indicates that these interneurons are critical elements of a feedback control system for flight control.