Learning strategy is influenced by trait anxiety and early rearing conditions in prepubertal male, but not prepubertal female rats

Rodents solve dual-solution tasks that require navigation to a goal by adopting either a hippocampus-dependent place strategy or a striatum-dependent stimulus–response strategy. A variety of factors, including biological sex and emotional status, influence the choice of learning strategy. In these experiments, we investigated the relationship between learning strategy and anxiety level in male and female rats prior to the onset of puberty, before the activational effects of gonadal hormones influence these processes. In the first experiment, prepubertal male rats categorized as high in trait anxiety at 26 days of age exhibited a bias toward stimulus–response strategy at 28 days of age, whereas age-matched females exhibited no preference in strategy regardless of anxiety level. In the second experiment, male and female rats were separated from their dams for either 15 or 180 min per day during the first 2 weeks of life and tested on a battery of anxiety and cognitive tasks between 25 and 29 days of age. Prolonged maternal separations for 180 min were associated with impaired spatial memory on a Y-maze task in both prepubertal males and females. Furthermore, prolonged maternal separations were linked to elevated anxiety and a bias for stimulus–response strategy in prepubertal males but not females. Alternatively, brief separations from dams for 15 min were associated with intact spatial memory, lower levels of anxiety, and no preference for either learning strategy in both sexes. These results provide evidence of sex-specific effects of trait anxiety and early maternal separation on the choice of learning strategy used by prepubertal rodents.

► Anxiety biases prepubertal male, but not female rats, toward a stimulus–response strategy.
► Long maternal separations elevate anxiety in prepubertal male, but not female rats.
► Long maternal separations bias prepubertal males toward a stimulus–response strategy.
► Long maternal separations do not bias learning strategy in prepubertal female rats.