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The Journal of Neuroscience, June 13, 2007, 27(24):6563-6572; doi:10.1523/JNEUROSCI.1797-07.2007

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Behavioral/Systems/Cognitive
Sexual Behavior Activity Tracks Rapid Changes in Brain Estrogen Concentrations

Mélanie Taziaux, ^* Matthieu Keller, ^* Julie Bakker, and Jacques Balthazart

Center for Cellular and Molecular Neurobiology, University of Liège, B-4000 Liège, Belgium

Correspondence should be addressed to Dr. Jacques Balthazart, Center for Cellular and Molecular Neurobiology, Research Group in Behavioral Neuroendocrinology, University of Liège, 1 Avenue de l'Hôpital (Bat. B36), B-4000 Liège 1, Belgium. Email: jbalthazart{at}ulg.ac.be

Estrogens are classically viewed as hormones that bind to intracellular receptors, which then act as transcription factors to modulate gene expression; however, they also affect many aspects of neuronal functioning by rapid nongenomic actions. Brain estrogen production can be regulated within minutes by changes in aromatase (estrogen synthase) activity as a result of calcium-dependent phosphorylations of the enzyme. To determine the effects of rapid changes in estrogen availability on male copulatory behavior, we mimicked in male mice the rapid upregulation and downregulation of brain estrogen concentration that should occur after inactivation or activation of aromatase activity. A single injection of different aromatase inhibitors [Vorozole, 1,4,6-androstatrien-3,17-dione (ATD), or its metabolite 17-OH-ATD (1,4,6-androstatrien-17ß-ol-3-one)] almost completely suppressed male sexual behavior (mounts and intromissions) expressed 10–20 min later by C57BL/6J mice but did not affect behavior in aromatase knock-out (ArKO) mice, activated by daily injections of estradiol benzoate, thereby confirming the specificity of the behavioral inhibition observed in wild-type mice. The rapid ATD-induced inhibition was reversed by the simultaneous injection of a large dose of estradiol. A single injection of estradiol to ArKO mice also activated male sexual behavior within 15 min. Thus, rapid increases or decreases in brain estrogen concentrations are followed within minutes by corresponding changes in male sexual behavior. Sexual behavior can thus be used to monitor changes in local estrogen concentrations and analyze the mechanisms mediating the rapid decline in estrogen signaling that takes place after inhibition of estrogen synthesis.

Key words: aromatase; aromatase knock-out mice; male sexual behavior; estrogens; rapid effects of steroids; nongenomic effects

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Received Dec. 2, 2006; revised May 10, 2007; accepted May 14, 2007.

Correspondence should be addressed to Dr. Jacques Balthazart, Center for Cellular and Molecular Neurobiology, Research Group in Behavioral Neuroendocrinology, University of Liège, 1 Avenue de l'Hôpital (Bat. B36), B-4000 Liège 1, Belgium. Email: jbalthazart{at}ulg.ac.be

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