Abstract

Simple SummaryGeometric navigation allows animals to efficiently move towards essential life-spaces by taking advantage of macrostructural information such as distance, angular magnitude, and length, in relation to left-right positional sense. In natural contexts, these cues can be referred to extensive three-dimensional surfaces such as a slope or a riverbed, thus becoming crucial to orient and find useful supplies. In controlled contexts, it is possible to set apart these components by handling the global shape of the experimental space (rectangular or square) as well, with the aim to specially probe the impact of each of them on navigation behavior of animals, including fishes. The present study aimed at investigating whether a well-known vertebrate, the zebrafish, could learn to encode and retain in memory such metric information (in terms of distances, corners, and lengths) in association with left–right directions, to gain rewards. Our results showed that zebrafish learned to use all these geometric attributes when repeatedly exposed to them, over a period of training, thereby giving strength to the ecological relevance of environmental geometry as a source of spatial knowledge. Generally, the engagement of zebrafish may consent to assess computations underlying large-scale-based navigation, also by drawing targeted comparisons, due to its behavioral, cognitive, and even emotional similarities with mammals.Zebrafish spontaneously use distance and directional relationships among three-dimensional extended surfaces to reorient within a rectangular arena. However, they fail to take advantage of either an array of freestanding corners or an array of unequal-length surfaces to search for a no-longer-present goal under a spontaneous cued memory procedure, being unable to use the information supplied by corners and length without some kind of rewarded training. The present study aimed to tease apart the geometric components characterizing a rectangular enclosure under a procedure recruiting the reference memory, thus training zebrafish in fragmented layouts that provided differences in surface distance, corners, and length. Results showed that fish, besides the distance, easily learned to use both corners and length if subjected to a rewarded exit task over time, suggesting that they can represent all the geometrically informative parts of a rectangular arena when consistently exposed to them. Altogether, these findings highlight crucially important issues apropos the employment of different behavioral protocols (spontaneous choice versus training over time) to assess spatial abilities of zebrafish, further paving the way to deepen the role of visual and nonvisual encodings of isolated geometric components in relation to macrostructural boundaries.

Highlights

  • In recent years, the growing interest in the engagement of fish species for neuroscientific purposes has allowed comparative psychologists to deeply investigate cognitive skills and related underlying neural mechanisms of this heterogeneous group of organisms [1,2].Since there is high variability among underwater ecosystems and habitats, fish naturally face spatial orientation challenges, further showing noteworthy navigation capacities such as the use of compasses [3,4], landmarks [5,6], and cognitive maps [7,8]

  • The apparatus was the same used by Sovrano and colleagues [23] to test both spontaneous and rewarded extra-visual encodings of pure geometry in three-eyed fishes, where we introduced some adaptations with the aim to replicate the experimental conditions by Lee and colleagues [17], but by employing a different behavioral protocol

  • In the case of the rewarded exit task, the behavioral protocol exerted a relevant part on spatial performances of fish: by consistently exposing them to a fragmented array of corners, de facto, zebrafish were able to infer the macrostructural morphology of the rectangular arena to efficiently reorient

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Summary

Introduction

Since there is high variability among underwater ecosystems and habitats, fish naturally face spatial orientation challenges, further showing noteworthy navigation capacities such as the use of compasses [3,4], landmarks [5,6], and cognitive maps [7,8] Besides these skills, fish have been experimentally observed in relation to the use of environmental geometric layouts to solve place-finding demands after induced disorientation [9,10,11,12,13,14,15,16,17,18,19,20,21,22,23]. Such a capacity has been demonstrated to be spread across species, both vertebrates [24,25,26,27,28] and invertebrates [29,30,31,32], highlighting the adaptive value of cognitive map and geometric representations over the phylogenetic history of animals

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