Rapid changes in brain estrogen concentration during male sexual behavior are site and stimulus specific

Marie-Pierre De Bournonville,Gregory F Ball,Catherine De Bournonville,Jacques Balthazart,Marianne Fillet,Laura M Vandries,Gwenaël Nys,Charlotte A Cornil

doi:10.1038/s41598-021-99497-1

Marie-Pierre De Bournonville, Gregory F Ball + Show 6 more

Open Access

https://doi.org/10.1038/s41598-021-99497-1

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Abstract

Classically, estrogens regulate male sexual behavior through effects initiated in the nucleus. However, neuroestrogens, i.e., estrogens locally produced in the brain, can act within minutes via membrane-initiated events. In male quail, rapid changes in brain aromatase activity occur after exposure to sexual stimuli. We report here that local extracellular estrogen concentrations measured by in vivo microdialysis increase during sexual interactions in a brain site- and stimulus-specific manner. Indeed, estrogen concentrations rose within 10 min of the initiation of sexual interaction with a female in the medial preoptic nucleus only, while visual access to a female led to an increase in estrogen concentrations only in the bed nucleus of the stria terminalis. These are the fastest fluctuations in local estrogen concentrations ever observed in the vertebrate brain. Their site and stimulus specificity strongly confirm the neuromodulatory function of neuroestrogens on behavior.

Highlights

Estrogens regulate male sexual behavior through effects initiated in the nucleus
We demonstrate that these concentrations rapidly change during sexual interactions in a brain site- and stimulus-specific manner, which is consistent with the idea that these steroids are able to modulate behavior expression in a manner similar to a neuromodulator
We demonstrate here that rapid changes in brain estrogen concentration can be monitored by in vivo microdialysis coupled to an ultra-sensitive RIA with a time resolution of 10 min

Summary

Introduction

Estrogens regulate male sexual behavior through effects initiated in the nucleus. The view of a female or the sexual interaction with her affects within minutes brain AA in nuclei that are part of the social behavior n etwork[25], such as the medial preoptic nucleus (POM) or bed nucleus of the stria terminalis (BST)[26,27] These studies reflect AA measured post-mortem by an ex vivo assay designed to maximize enzymatic activity[28] and do not directly answer the question of whether brain E2 concentrations change in such a dynamic manner. By combining in vivo microdialysis with an ultra-sensitive 125I-based radioimmunoassay, we show here that brain estrogen concentrations can be monitored in the quail brain with a time resolution of 10 min We demonstrate that these concentrations rapidly change during sexual interactions in a brain site- and stimulus-specific manner, which is consistent with the idea that these steroids are able to modulate behavior expression in a manner similar to a neuromodulator. A causal relationship between these rapid changes in estrogens in a given region and behavior has not yet been demonstrated and further research will be necessary to firmly establish the existence of such a link

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