Polarization-Sensitive and Light-Sensitive Neurons in Two Parallel Pathways Passing Through the Anterior Optic Tubercle in the Locust Brain

Abstract

Many migrating animals use a sun compass for long-range navigation. One of the guiding cues used by insects is the polarization pattern of the blue sky. In the desert locust Schistocerca gregaria, neurons of the central complex, a neuropil in the center of the brain, are sensitive to polarized light and might serve a key role in compass navigation. Visual pathways to the central complex include signal processing in the upper and lower units of the anterior optic tubercle. To determine whether these pathways carry polarization-vision signals, we have recorded the responses of interneurons of the optic tubercle of the locust to visual stimuli including polarized light. All neurons of the lower unit but only one of five recorded neurons of the upper unit of the tubercle were sensitive to linearly polarized light presented in the dorsal visual field. These neurons showed polarization opponency, or a sinusoidal modulation of activity, during stimulation through a rotating polarizer. Two types of bilateral interneurons preferred particular e-vector orientations, reflecting the presence of bilateral pairs of these neurons in the brain. We show here for the first time neurons with projections to the lateral accessory lobe that are suited to provide polarization input to the central complex. All neurons of the tubercle, furthermore, responded to unpolarized light, mostly with tonic activity changes. These responses strongly depended on stimulus position and might reflect navigation-relevant signals such as direct sunlight or visual landmarks that are integrated with polarization responses in neurons of the lower unit.