Object-Detecting Neurons in Drosophila.

ABSTRACT

Many animals rely on vision to detect objects such as conspecifics, predators, and prey. Hypercomplex cells found in feline cortex and small target motion detectors found in dragonfly and hoverfly optic lobes demonstrate robust tuning for small objects, with weak or no response to larger objects or movement of the visual panorama [1-3]. However, the relationship among anatomical, molecular, and functional properties of object detection circuitry is not understood. Here we characterize a specialized object detector in Drosophila, the lobula columnar neuron LC11 [4]. By imaging calcium dynamics with two-photon excitation microscopy, we show that LC11 responds to the omni-directional movement of a small object darker than the background, with little or no responses to static flicker, vertically elongated bars, or panoramic gratings. LC11 dendrites innervate multiple layers of the lobula, and each dendrite spans enough columns to sample 75° of visual space, yet the area that evokes calcium responses is only 20° wide and shows robust responses to a 2.2° object spanning less than half of one facet of the compound eye. The dendrites of neighboring LC11s encode object motion retinotopically, but the axon terminals fuse into a glomerular structure in the central brain where retinotopy is lost. Blocking inhibitory ionic currents abolishes small object sensitivity and facilitates responses to elongated bars and gratings. Our results reveal high-acuity object motion detection in the Drosophila optic lobe.