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Effects of Androgens and Estradiol on Spine Synapse Formation in the Prefrontal Cortex of Normal and Testicular Feminization Mutant Male Rats

Department of Obstetrics, Gynecology & Reproductive Sciences (T.H., N.J.M., C.L.) and Neurobiology (C.L.), Yale University School of Medicine, New Haven, Connecticut 06510; Laboratory of Molecular Neurobiology (T.H.), Biological Research Center, Hungarian Academy of Sciences, Szeged H-6723, Hungary; Department of Biomedical Sciences (N.J.M.), Ontario Veterinary College, Guelph, Ontario, Canada N1G 2W1; and Neuroscience Program (C.L.J.), Michigan State University, East Lansing, Michigan 48824

Address all correspondence and requests for reprints to: Csaba Leranth, M.D., Ph.D., Department of Obstetrics, Gynecology & Reproductive Sciences, Yale University School of Medicine, 333 Cedar Street, FMB 312, New Haven, Connecticut 06520. E-mail: csaba.leranth{at}yale.edu.

Recent studies suggest that, in female monkeys and rats, estrogens elicit dendritic spine synapse formation in the prefrontal cortex, an area that, similar to the hippocampus, plays a critical role in cognition. However, whether gonadal hormones induce synaptic remodeling in the male prefrontal cortex remains unknown. Here we report that gonadectomy reduced, whereas administration of 5-dihydrotestosterone or estradiol-benzoate to castrated male rats increased, the number of medial prefrontal cortical (mPFC) spine synapses, with estradiol-benzoate being less effective than 5-dihydrotestosterone. To investigate whether the androgen receptor contributes to the mediation of these changes, we compared the response of testicular feminization mutant (Tfm) male rats to that of wild-type animals. The number of mPFC spine synapses in gonadally intact Tfm rats and 5-dihydrotestosterone-treated castrated Tfm males was considerably reduced compared to intact wild-type animals, whereas the synaptogenic effect of estradiol-benzoate was surprisingly enhanced in Tfm rats. These data are consistent with the hypothesis that remodeling of spine synapses in the prefrontal cortex may contribute to the cognitive effect of gonadal steroids. Our findings in Tfm animals indicate that androgen receptors may mediate a large part of the synaptogenic action of androgens in the mPFC of adult males. However, because this effect of 5-dihydrotestosterone is not completely lost in Tfm rats, additional mechanisms may also be involved.

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