Binocular neuronal processing of object motion in an arthropod

Abstract

Animals use binocular information to guide many behaviors. In highly visual arthropods, complex binocular computations involved in processing panoramic optic flow generated during self-motion occur in the optic neuropils. However, the extent to which binocular processing of object motion occurs in these neuropils remains unknown. We investigated this in a crab, where the distance between the eyes and the extensive overlapping of their visual fields advocate for the use of binocular processing. By performing in vivo intracellular recordings from the lobula (third optic neuropil) of male crabs, we assessed responses of object-motion-sensitive neurons to ipsilateral or contralateral moving objects under binocular and monocular conditions. Most recorded neurons responded to stimuli seen independently with either eye, proving that each lobula receives profuse visual information from both eyes. The contribution of each eye to the binocular response varies among neurons, from those receiving comparable inputs from both eyes to those with mainly ipsilateral or contralateral components, some including contralateral inhibition. Electrophysiological profiles indicated that a similar number of neurons were recorded from their input or their output side. In monocular conditions, the first group showed shorter response delays to ipsilateral than to contralateral stimulation, whereas the second group showed the opposite. These results fit well with neurons conveying centripetal and centrifugal information from and toward the lobula, respectively. Intracellular and massive stainings provided anatomical support for this and for direct connections between the two lobulae, but simultaneous recordings failed to reveal such connections. Simplified model circuits of interocular connections are discussed.