Activation of the G protein-coupled estrogen receptor, but not estrogen receptor α or β, rapidly enhances social learning

• Social learning can be modulated by rapid effects of estrogen receptor activation.
• 17β-estradiol rapidly facilitates expression of a socially learned food preference.
• Specific GPER1 activation facilitates social learning, more prolonged than estradiol effects.
• ERα or ERβ activation either rapidly impairs or has no effect on social learning.

SummarySocial learning is a highly adaptive process by which an animal acquires information from a conspecific. While estrogens are known to modulate learning and memory, much of this research focuses on individual learning. Estrogens have been shown to enhance social learning on a long-term time scale, likely via genomic mechanisms. Estrogens have also been shown to affect individual learning on a rapid time scale through cell-signaling cascades, rather than via genomic effects, suggesting they may also rapidly influence social learning. We therefore investigated the effects of 17β-estradiol and involvement of the estrogen receptors (ERs) using the ERα agonist propyl pyrazole triol, the ERβ agonist diarylpropionitrile, and the G protein-coupled ER 1 (GPER1) agonist G1 on the social transmission of food preferences (STFP) task, within a time scale that focused on the rapid effects of estrogens. General ER activation with 17β-estradiol resulted in a modest facilitation of social learning, with mice showing a preference up to 30 min of testing. Specific activation of the GPER1 also rapidly enhanced social learning, with mice showing a socially learned preference up to 2 h of testing. ERα activation instead shortened the expression of a socially learned food preference, while ERβ activation had little to no effects. Thus, rapid estrogenic modulation of social learning in the STFP may be the outcome of competing action at the three main receptors. Hence, estrogens’ rapid effects on social learning likely depend on the specific ERs present in brain regions recruited during social learning.