Characterization of spatial performance in male and female Long-Evans rats by means of the Morris water task and the ziggurat task

Abstract

Sex differences are prominent influences on spatial performance. One of the most common tasks to assess sex differences in spatial navigation in rodents is the Morris water task (MWT). In this task rats swim in a pool of water to locate a hidden platform employing the topographical relationships among the distal visual cues, pool wall, and goal location. Some evidence suggests that male rats display superior performance relative to females in the MWT. It is unknown, however, to what extent the sex difference in rats is task-dependent. This study compared the performance of male and female Long-Evans rats in the wet-land MWT versus the dry-land ziggurat task (ZT). The ZT represents a new dry-land task in which rats explore an arena with 16 ziggurat pyramids to locate food rewards. Several behavioural parameters, including latency, path length, path speed, probe trial performance, errors, and the number of returns were used as indices of spatial learning and memory. While males and females did not display significant differences in the traditional measures of spatial navigation within MWT, they displayed a robust sex difference in all measures of the ZT. These results indicate task-specific sex differences in spatial performance. Our findings suggest that males and females may employ different learning strategies in the MWT and ZT and that the latter task provides a more favourable task for assessing sex differences in rats.

Introduction

Spatial performance is generally based on the ability to encode, store and retrieve mainly visual information regarding route navigation and object locations [35]. Sex is a major variable that appears to be a source of individual differences in spatial function. Studies investigating sex differences in spatial function have provided some of the most reliable findings in psychological research. Substantial evidence in human studies suggests that men outperform women in spatial navigation tasks [41], [42], [12]. Furthermore, Astur et al. showed that male and female humans display robust and reliable differences in spatial performance within a virtual Morris water task (vMWT) [2].

In animal research, sex differences in spatial tasks are not displayed consistently. Generally, spatial performance in rodents such as rats is assessed in MWT [31] and radial arm maze (RAM) [33]. The MWT, as originally described, consists of a circular swimming pool filled with opaque water in which a small platform is hidden. The rats use the topographical relationship between distal cues and pool wall in order to locate the hidden platform and escape from water. Although some studies employing MWT show superior performance by male rats compared to females [34], [40], [43], no sex differences were found in others [8], [46]. Similarly, inconsistent findings concerning sex differences have been reported in the RAM ([13], [23], [45]; see also [3], [5]). Generally, sex differences in spatial performance stem, at least in part, from organizational effects of sex hormones [9], age [8], diet type [14], rearing conditions [23], and task-dependent procedures and parameters [40], [37]. In MWT, specifically, it has been shown that tank size [32] and rats’ strain [25] may influence spatial performance.

The present study aims to expand previous studies on sexual dimorphism in spatial function by comparing performance in the MWT and the new ziggurat task (ZT) [15]. The MWT can be regarded as a simple open field with minimal within-maze cues, while the ZT represents a task with abundant within-maze cues. Structural differences (e.g., physical features, and task demands and procedures) between water-based and dry-land tasks [21] can be potential reasons for sex differences in spatial behaviour in the MWT and ZT. For instance, although search-to-platform area determines the degree of reliance on spatial versus non-spatial strategies in both arenas, MWT requires rats to swim toward a submerged escape platform in an open field with minimum landmarks. In the ZT, however, rats are required to navigate from start locations of a dry open arena to locate a baited ziggurat. Compared to MWT, the ZT is an environment with more landmarks and complex route system. In humans, it has been previously shown that male superiority in spatial function (for example, on a map) may be attributable to sexually dimorphic route description [29]. Accordingly, we predicted that males outperform females on the ZT due to sex differences in route learning and the complex route system of the ZT.

The purpose of the present study was to investigate if structural and parametric features of the MWT and ZT differentially affect spatial performance in male and female rats. This study compares the task-dependent nature of sexually dimorphic spatial behaviour in terms of differences between MWT and ZT. The results in the present study indicate that males outperform females only in ZT testing. Males’ superiority in spatial behaviour in the ZT, not MWT reflects the effect of task-dependent demands and procedures on spatial performance.