Rapid oestrogenic regulation of social and nonsocial learning

Abstract

Much research on oestrogens has focused on their long-term action, exerting behavioural effects within hours to days through gene transcription. Oestrogens also affect behaviour on a much shorter time scale. These rapid effects are assumed to occur through cell signalling and can elicit a behavioural effect as early as 15 min after treatment. These effects on behaviour have primarily been explored through the action of oestradiol at three well-known oestrogen receptors (ERs): ERα, ERβ and the more recently described G protein-coupled ER1 (GPER1). The rapid effects of oestradiol and ER agonists have been tested on both social and nonsocial learning paradigms. Social learning refers to a paradigm in which an animal acquires information and modifies its behaviour based on observation of another animal, commonly studied using the social transmission of food preferences paradigm. When administered shortly before testing, oestradiol rapidly improves social learning on this task, although no ER agonist has definitive, comparable improving effects. Some evidence points to GPER1, whereas ERα impairs, and ERβ activation has no effect on social learning. Conversely, ERα and GPER1 play a larger role than ERβ in the rapid improving effect of oestrogens on nonsocial learning, including social and object recognition. In addition, when administered immediately post-acquisition, oestrogens also rapidly improve memory consolidation in a variety of learning paradigms: object recognition, object placement, inhibitory avoidance and the Morris water maze, indicating that oestradiol affects the consolidation of multiple types of memory. Evidence suggests that these improvements are the result of oestrogens acting in the dorsal hippocampus where selective activation of all three ERs shows rapid improving effects on spatial learning comparable to oestradiol. However, the hippocampus is not necessary for rapid oestradiol improvements on social recognition. Although acute treatment with oestradiol enhances learning and memory on various social and nonsocial learning paradigms, the specific ERs play different roles in each type of learning. Future research should aim to further determine the roles of ERs with respect to the enhancing effects of oestradiol on learning and memory, and also determine where in the brain oestradiol acts to affect social and nonsocial learning. © 2013 British Society for Neuroendocrinology.