Honeybees acquire a spatial memory by learning landmarks and visual patterns in parallel

Spatial memory is vital for central-place foragers that navigate the same habitat on a daily basis. Computational models suggest that insects remember panoramic snapshots to return to goal locations. To what extent these snapshots represent retinotopic images or whether salient landmarks are stored isolated from the panorama remains unclear. With a newly designed spatial-memory task, we show that honeybees employ two different strategies for learning visual cues. In essence, they learn visual patterns as panoramic snapshots and three-dimensional objects as single entities. Freely walking honeybees were challenged to locate a rewarded feeder in the presence of visual patterns or objects. Selectively perturbing the panorama degraded the orientation behaviour only when visual patterns were present but not when objects were available. Presenting visual patterns and objects simultaneously and setting these cues in conflict revealed that honeybees primarily rely on a landmark-based navigation strategy. Making the spatial information of the objects ambiguous did not induce disorientation because the honeybees then relied on the visual patterns for finding the feeder. Altogether, our results suggest two independent visual memories operating in parallel, one dedicated to local landmarks and a second one for visual patterns that could be interpreted as distal cues. Notably, in rats, the spatial tuning of some hippocampal cells has been shown to be either anchored to local or distal cues. Our results provide the first hints that a distinction between local and distal cues may also be present in the insect brain.