Elsevier

Hormones and Behavior

Volume 64, Issue 1, June 2013, Pages 122-135
Hormones and Behavior

Do hormonal changes that appear at the onset of puberty determine the strategies used by female rats when solving a navigation task?

https://doi.org/10.1016/j.yhbeh.2013.05.007Get rights and content

Highlights

  • The results show qualitative sex differences in spatial learning.

  • Male rats do not change their preferred strategy throughout their lifespan.

  • Females do change their preferred strategy throughout their lifespan.

  • Sexual maturation seems to be responsible for this change of strategy in female rats.

Abstract

The present set of experiments evaluated the possibility that the hormonal changes that appear at the onset of puberty might influence the strategies used by female rats to solve a spatial navigation task. In each experiment, rats were trained in a triangular shaped pool to find a hidden platform which maintained a constant relationship with two sources of information, one individual landmark and one corner of the pool with a distinctive geometry. Then, three test trials were conducted without the platform in counterbalanced order. In one, both the geometry and the landmark were simultaneously presented, although in different spatial positions, in order to measure the rats' preferences. In the remaining test trials what the rats had learned about the two sources of information was measured by presenting them individually. Experiment 1, with 60-day old rats, revealed a clear sex difference, thus replicating a previous finding (Rodríguez et al., 2010): females spent more time in an area of the pool that corresponded to the landmark, whereas males spent more time in the distinctive corner of the pool even though the remaining tests revealed that both sexes had learned about the two sources of information. In Experiment 2, 30-day old female rats, unlike adults, preferred to solve the task using the geometry information rather than the landmark (although juvenile males behaved in exactly the same way as adults). Experiment 3 directly compared the performance of 90- and 30-day old females and found that while the adult females preferred to solve the task using the landmark, the reverse was true in juvenile females. Experiment 4 compared ovariectomized and sham operated females and found that while sham operated females preferred to solve the task using the landmark, the reverse was true in ovariectomized females. Finally, Experiment 5 directly compared adult males and females, juvenile males and females, and ovariectomized females and found that adult males, juvenile males and females, and ovariectomized females did not differ among them in their preferred cue, but they all differed from adult females.

Introduction

There is considerable evidence that males and females may rely on different cues to solve spatial problems. For example, Williams et al. (1990) trained rats in a radial maze; after they had reached asymptotic performance, they were tested following various manipulations to the geometry of the room or to the landmarks. Provided the geometry of the room was unchanged, males' performance was unaffected by any change to the landmarks, but alteration of the geometry of the testing room disrupted their performance, even when the landmarks were still available for navigation. In contrast, females' performance was disrupted by rearrangement of the landmarks whether the geometry of the room was changed or not, although they were unaffected by the removal of the landmarks provided the geometry of the room was unchanged.

A more recent study by Rodríguez et al. (2010) employed a different procedure to demonstrate rather similar effects. Rats were trained in a triangular-shaped pool to find a hidden platform, whose location was defined in terms of two sources of information, a landmark outside the pool and a particular corner of the pool with a distinctive geometry. Subsequent test trials, without the platform pitted these two sources of information against one another. This test revealed a clear sex difference: females spent more time in an area of the pool next to the landmark, whereas males spent more time in the distinctive corner of the pool. Although further tests in which the two sources of information were presented individually revealed that both sexes had learned something about both cues, males performed significantly better on the geometry than the landmark test, while females performed equally well on both. The results imply that geometry is clearly more salient for males, and landmarks somewhat more salient for females. A subsequent study by Rodríguez et al. (2011b) used a cue competition design to confirm this conclusion. Employing the same apparatus and general procedure as Rodríguez et al. (2010), they showed that geometrical information overshadowed learning about the landmark in males, but not vice-versa, while in females the landmark overshadowed learning about geometry, but geometry did not overshadow the landmark.

Interestingly, some authors have claimed that the differences observed in the performance of males and females when solving spatial tasks do not appear at birth, but tend to emerge after puberty (in a water maze, see Kanit et al., 2000; in a symmetrical maze, see Krasnoff and Weston, 1976), and therefore that they are found more reliably in adults than in juveniles. Kanit et al. (2000), for example, trained four-month and three-week old male and female rats in a spatial navigation task in a Morris pool. The platform remained visible on most training days, but was hidden on one training session in four. After acquisition, a test trial was conducted where the platform was transferred to another quadrant, and the time the animal spent in the quadrant where the platform was during training and the time it took to reach the platform in the new place were measured.

The results of the test trial showed a clear interaction between sex and age. Adult female rats searched for the platform in the new quadrant; but adult males searched for the platform in its old location, as did both male and female juvenile rats. Thus, adult female rats solved the task differently than both adult male rats and juvenile rats whether male or female.

The implication of these results is that sex differences in spatial navigation tasks only appear in adult females. Given that the experiments carried out by Rodríguez et al., 2010, Rodríguez et al., 2011a were performed with adult rats, it is reasonable to think that their results might have been different if the rats had been younger.

The main purpose of the present set of experiments was to assess whether the rats' age would influence or determine the preferred strategy of males and females when solving a spatial navigation task where clear sex differences in adult rats have been found. Experiments 1 and 2 compared the performance of male and female rats on the same task as used by Rodríguez et al. (2010), Experiment 1 with adult rats, 60 days old, Experiment 2 with juvenile, 30-day-old rats. Experiments 3 and 4 were conducted only with female rats. Experiment 3 directly compared the performance of 90- and 30-day old females, while Experiment 4 was conducted to determine if ovariectomized 60-day rats solved the task using a different strategy than sham operated females of the same age. Finally, Experiment 5 directly compared adult males and females, juvenile males and females, and ovariectomized females.

Importantly, we should mention that in previous studies (Rodríguez et al., 2010, Experiment 2; Rodríguez et al., 2011a, Experiments 1 and 2a) where the procedure, experimental room, triangular-shaped pool and landmark were the same as those used in the present set of experiments, we examined the possibility that the estrus cycle of females could influence their performance. Before the experiments began, the rats were examined for 8 days to establish the estrus cycle by a daily collection of vaginal smear. During the experiments, they continued to be examined every day, and on test days, they were examined both before and after the experimental session to ensure that they did not change over to the next estrus cycle phase during testing. An ANOVA conducted on the female test data that included the variables of estrus cycle (i.e., high and low level of estradiol) and landmark versus shape revealed no significant effect of estrus cycle on preference for landmark or geometry in any of the experiments (for the same results with a related task see Rodríguez et al., 2011a). Given these null results, we did not measure the rats' estrus cycle in the present experiments in order to avoid unnecessarily stressing them.

Section snippets

Experiment 1

Experiment 1 was conducted with male and female rats, aged 60 days, using the same procedure as that of Experiment 2 in the study by Rodríguez et al. (2010), with the exception that all three test trials were counterbalanced for a better experimental control. Although the rats used by Rodriguez et al. were 4–5 months old rather than 60 days old, on the assumption that the critical variable is whether the rats are pre- or post-pubertal (the onset of puberty in rats is 40–45 days), we predicted that

Experiment 2

Experiment 2 was conducted with male and female rats, aged 30 days, and the procedure was the same as used in Experiment 1. If age has any effect on rats' preferred strategy, it is an open question whether 30-day-old males and females will solve the task as adult animals do.

Experiment 3

The results of Experiments 2a and 2b showed that, unlike adult female rats of Experiment 1, juvenile 30-day-old females preferred the information provided by the geometric shape of the pool. The aim of Experiment 3 was to provide a direct comparison between two groups of females: adult rats (approximately 90 days old) and juvenile rats (30 days old).

Experiment 4

The results of the previous experiments showed a clear “age effect” in the strategies used by female rats to solve the present navigation task. Specifically, while adult females preferred to use the information provided by the landmark to locate the hidden platform, juvenile females, preferred the information provided by the geometric shape of the pool.

The obvious explanation is that the hormonal changes that appear at the onset of puberty (which occurs around the 42nd day after birth, Spear,

Experiment 5

The purpose of Experiment 5 was to provide a direct comparison of the performance of all the groups tested in the previous experiments: adult and juvenile male and female rats, as well as ovariectomized adult females. In line with the results of the previous experiments, it was expected that adult female rats would differ from adult males, juvenile males and females, and ovariectomized adult females, which would all behave similarly. More specifically, adult female rats would rely more on the

General discussion

In the present series of experiments, rats were trained in a triangular shaped pool to find a hidden platform, whose location was defined by two sources of information: the platform was always in one particular corner of the pool, and a salient landmark was positioned immediately above it. After the rats had learned, they were given test trials without the platform. On one test trial (a preference test) these two sources of information were put into opposition (the landmark was positioned above

Acknowledgments

This research was supported by a grant from the Spanish ‘Ministerio de Ciencia e Innovación’ (Ref. no. PSI2010-20424) to V.D. Chamizo. The authors are very grateful to Josep Marimón for demonstrating the ovariectomy procedure to the first author and to Marta Torres and to Ariadna Arbat for excellent help to run the subjects.

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