Estrogen involvement in social behavior in rodents: Rapid and long-term actions

• Published in: Hormones and behavior Vol. 74; pp. 53 - 76
• Main Authors: Ervin, Kelsy S.J., Lymer, Jennifer M., Matta, Richard, Clipperton-Allen, Amy E., Kavaliers, Martin, Choleris, Elena
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01-08-2015; Elsevier BV
• Subjects: Aggression; Animal behavior; Animals; Behavior, Animal - drug effects; Behavior, Animal - physiology; Brain - drug effects; Brain - metabolism; Dominance; Estradiol - pharmacology; Estradiol Congeners - pharmacology; Estrogen receptor alpha; Estrogen receptor beta; Estrogens; Estrogens - pharmacology; Estrogens - physiology; Female; GPER; GPR30; Learning - drug effects; Learning - physiology; Male; Mate choice; Memory - drug effects; Memory - physiology; Odorants; Odors; Receptors, Estrogen - metabolism; Receptors, Estrogen - physiology; Rodentia; Rodents; Social Behavior; Social learning; Social recognition; Social transmission of food preference; Time Factors; Odors; Aggression; GPER; Social transmission of food preference; Mate choice; GPR30; Dominance; Estrogen receptor alpha; Social learning; Social recognition; Estrogen receptor beta
• ISSN: 0018-506X; 1095-6867
• DOI: 10.1016/j.yhbeh.2015.05.023

This article is part of a Special Issue (“Estradiol and cognition”).
Estrogens have repeatedly been shown to influence a wide array of social behaviors, which in rodents are predominantly olfactory-mediated. Estrogens are involved in social behavior at multiple levels of processing, from the detection and integration of socially relevant olfactory information to more complex social behaviors, including social preferences, aggression and dominance, and learning and memory for social stimuli (e.g. social recognition and social learning). Three estrogen receptors (ERs), ERα, ERβ, and the G protein-coupled ER 1 (GPER1), differently affect these behaviors. Social recognition, territorial aggression, and sexual preferences and mate choice, all requiring the integration of socially related olfactory information, seem to primarily involve ERα, with ERβ playing a lesser, modulatory role. In contrast, social learning consistently responds differently to estrogen manipulations than other social behaviors. This suggests differential ER involvement in brain regions important for specific social behaviors, such as the ventromedial and medial preoptic nuclei of the hypothalamus in social preferences and aggression, the medial amygdala and hippocampus in social recognition, and the prefrontal cortex and hippocampus in social learning. While the long-term effects of ERα and ERβ on social behavior have been extensively investigated, our knowledge of the rapid, non-genomic, effects of estrogens is more limited and suggests that they may mediate some social behaviors (e.g. social learning) differently from long-term effects. Further research is required to compare ER involvement in regulating social behavior in male and female animals, and to further elucidate the roles of the more recently described G protein-coupled ERs, both the GPER1 and the Gq-mER.
•Mate seeking and territorial aggression are primarily mediated by ERα.•Social recognition is mediated by ERα long-term, and ERα and GPER1 rapidly.•Social learning is modulated by ERβ long term but rapidly via GPER1.•Estrogens affect social learning differently from other types of social behavior.•Differential brain ER distribution may explain estrogens' varying effects on social behaviors.