Two Are Better Than One: Integrating Spatial Geometry with a Conspicuous Landmark in Zebrafish Reorientation Behavior

SIMPLE SUMMARY: Fish navigation is supported by noteworthy spatial memory and precision. The use of environmental information allows aquatic organisms to meet survival needs, such as searching for nourishment and social companions. Within natural ecosystems, handling different sources of spatial cues is crucial, most of all when such capacity requires the integrated use of this information. In this research, we studied zebrafish spatial reorientation behavior in a rectangular-shaped arena (“geometry”), which was equipped with a conspicuous landmark, a blue wall (“feature”). The aim was to explore the combined use of both information elements for goal-oriented purposes. Fish were trained over time, under operant conditioning, to distinguish a target corner position from its symmetric one (i.e., rotational), thanks to the simultaneous use of surface metrics (long/short, close/far; left-right sense) and a landmark (one surface different in color). Results revealed that zebrafish exhibit conjoining abilities over time and develop intelligent solutions in terms of exploration routines. ABSTRACT: Within bounded environments of a distinctive shape, zebrafish locate two geometrically equivalent corner positions, based on surface metrics and left-right directions. For instance, the corners with a short surface right/long surface left cannot be distinguished as unique spatial locations unless other cues break the symmetry. By conjoining geometry with a conspicuous landmark, such as a different-color surface, one of the two geometric twins will have a short different-colored surface right, becoming identifiable. Zebrafish spontaneously combine a rectangular white arena’s shape with a blue wall landmark, but only when this landmark is near the target corner; when far, that cue triggers a steady attractiveness bias. In this study, we trained zebrafish to use a blue wall landmark in conjunction with a rectangular-shaped arena, providing them rewards over time. We found that trained zebrafish learned to locate the target corner, regardless of the landmark’s length and distance, overcoming the attractiveness bias. Zebrafish preferred geometry after removing the landmark (geometric test), but not if put into conflict geometry and landmark (affine transformation). Analysis on movement patterns revealed wall-following exploration as a consistent strategy for approaching the target corner, with individual left-right direction. The capacity of zebrafish to handle different sources of information may be grounds for investigating how environmental changes affect fish spatial behavior in threatened ecosystems.