Spatial Learning by Using Non-Visual Geometry and a Visual 3D Landmark in Zebrafish (Danio rerio)

SIMPLE SUMMARY: Orienting in space requires building informative relationships based on environmental cues, which animals use to meet survival needs. During navigation, spatial geometries interact with featural information, thereby providing a cohesive representation where a variety of concurrent elements must be considered. When a conspicuous landmark marks a distinctive geometric space, the ability to use or even conjoin both is essential, most importantly, in conditions of visual deprivation. The present study investigated whether zebrafish (Danio rerio) reoriented, taking advantage of the transparent geometry of a bounded rectangular arena equipped with a blue-colored 3D landmark, for finding food and social rewards. Fish were required to reorient over time while varying the landmark’s position (i.e., proximal/distal; on the short/long arena’s side) in relation to a target corner. The repeated experience would have allowed fish to handle the two pieces of information which depend on different sensory pathways: the visual system, as regards the landmark; extra-visual systems (e.g., haptic and tactile-like), as regards geometry. Results revealed zebrafish’s reorientation behavior ability within the non-visual geometric framework and the use of the visual 3D landmarks, which are partially affected by proximity–length interactions. For the first time in zebrafish, we report the possible recruitment of different sensory channels (sight and touch, i.e., “wall-following” exploration of boundaries) for experiencing multi-factor life environments. ABSTRACT: Fish conjoin environmental geometry with conspicuous landmarks to reorient towards foraging sites and social stimuli. Zebrafish (Danio rerio) can merge a rectangular opaque arena with a 2D landmark (a blue-colored wall) but cannot merge a rectangular transparent arena with a 3D landmark (a blue cylinder) without training to “feel” the environment thanks to other-than-sight pathways. Thus, their success is linked to tasks differences (spontaneous vs. rewarded). This study explored the reorientation behavior of zebrafish within a rectangular transparent arena, with a blue cylinder outside, proximal to/distal from a target corner position, on the short/long side of the arena. Adult males were extensively trained to distinguish the correct corner from the rotational one, sharing an equivalent metric–sense relationship (short surface left, long surface right), to access food and companions. Results showed that zebrafish’s reorientation behavior was driven by both the non-visual geometry and the visual landmark, partially depending on the landmark’s proximity and surface length. Better accuracy was attained when the landmark was proximal to the target corner. When long-term experience was allowed, zebrafish handled non-visual and visual sensory stimulations over time for reorienting. We advance the possibility that multisensory processes affect fish’s reorientation behavior and spatial learning, providing a link through which to investigate animals’ exploratory strategies to face situations of visual deprivation or impairments.