Directional Selectivity in the Simple Eye of an Insect

Among other sensory modalities, flight stabilization in insects is performed with the aid of visual feedback from three simple eyes (ocelli). It is thought that each ocellus acts as a single wide-field sensor that detects changes in light intensity. We challenge this notion by providing evidence that, when light-adapted, the large retinal L-neurons in the median ocellus of the dragonfly respond in a directional way to upward moving bars and gratings. This ability is pronounced under UV illumination but weak or nonexistent in green light and is optimal at angular velocities of approximately 750 degrees s(-1). Using a reverse-correlation technique, we analyze the functional organization of the receptive fields of the L-neurons. Our results reveal that L-neurons alter the structure of their linear spatiotemporal receptive fields with changes in the illuminating wavelength, becoming more inseparable and directional in UV light than in green. For moving bars and gratings, the strength of directionality predicted from the receptive fields is consistent with the measured values. Our results strongly suggest that, during the day, the retinal circuitry of the dragonfly median ocellus performs an early linear stage of motion processing. The likely advantage of this computation is to enhance pitch control.