Highly active insects and crabs depend on visual motion information for detecting and tracking mates, prey, or predators, for which they require directional control systems containing internal maps of visual space. A neural map formed by large, motion-sensitive neurons implicated in processing panoramic flow is known to exist in an optic ganglion of the fly. However, an equivalent map for processing spatial positions of single objects has not been hitherto identified in any arthropod. Crabs can escape directly away from a visual threat wherever the stimulus is located in the 360°field of view. When tested in a walking simulator, the crab Neohelice granulata immediately adjusts its running direction after changes in the position of the visual danger stimulus smaller than 1°. Combining mass and single-cell staining with in vivo intracellular recording, we show that a particular class of motion-sensitive neurons of the crab's lobula that project to the midbrain, the monostratified lobula giants type 1 (MLG1), form a system of 16 retinotopically organized elements that map the 360°a zimuthal space. The preference of these neurons for horizontally moving objects conforms the visual ecology of the crab's mudflat world. With a mean receptive field of 118°, MLG1s have a large superposition among neighboring elements. Our results suggest that the MLG1 system conveys information on object position as a population vector. Such computational code can enable the accurate directional control observed in the visually guided behaviors of crabs.

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 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, while 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.Most active animals became equipped with two eyes, which contributes to functions like depth perception, objects spatial location and motion processing, all used for guiding behaviors. In visually active arthropods, binocular neural processing of the panoramic optic flow generated during self-motion happens already in the optic neuropils. However, whether binocular processing of single object motion occurs in these neuropils remained unknown. We investigated this in a crab, where motion-sensitive neurons from the lobula can be recorded in the intact animal. Here we demonstrate that different classes of neurons from the lobula compute binocular information. Our results provide new insight into where and how the visual information acquired by the two eyes is first combined in the brain of an arthropod.

All animals need information about the direction of motion to be able to track the trajectory of a target (prey, predator, cospecific) or to control the course of navigation. This information is provided by direction selective (DS) neurons, which respond to images moving in a unique direction. DS neurons have been described in numerous species including many arthropods. In these animals, the majority of the studies have focused on DS neurons dedicated to processing the optic flow generated during navigation. In contrast, only a few studies were performed on DS neurons related to object motion processing. The crab Neohelice is an established experimental model for the study of neurons involved in visually-guided behaviors. Here, we describe in male crabs of this species a new group of DS neurons that are highly directionally selective to moving objects. The neurons were physiologically and morphologically characterized by intracellular recording and staining in the optic lobe of intact animals. Because of their arborization in the lobula complex, we called these cells lobula complex directional cells (LCDCs). LCDCs also arborize in a previously undescribed small neuropil of the lateral protocerebrum. LCDCs are responsive only to horizontal motion. This nicely fits in the behavioral adaptations of a crab inhabiting a flat, densely crowded environment, where most object motions are generated by neighboring crabs moving along the horizontal plane.