Photoperiod reverses the effects of estrogens on male aggression via genomic and nongenomic pathways

Brian C. Trainor^*,, Shili Lin, M. Sima Finy*^*, Michael R. Rowland^*, and Randy J. Nelson^*

*Departments of Psychology and Neuroscience, Institute for Behavioral Medicine Research, and Department of Statistics, Ohio State University, Columbus, OH 43210

Received for publication February 28, 2007.

Abstract: Despite recent discoveries of the specific contributions of genes to behavior, the molecular mechanisms mediating contributions of the environment are understudied. We demonstrate that the behavioral effects of estrogens on aggression are completely reversed by a discrete environmental signal, day length. Selective activation of either estrogen receptor or decreases aggression in long days and increases aggression in short days. In the bed nucleus of the stria terminalis, one of several nuclei in a neural circuit that controls aggression, estrogen-dependent gene expression is increased in long days but not in short days, suggesting that estrogens decrease aggression by driving estrogen-dependent gene expression. Estradiol injections increased aggression within 15 min in short days but not in long days, suggesting that estrogens increase aggression in short days primarily via nongenomic pathways. These data demonstrate that the environment can dictate how hormones affect a complex behavior by altering the molecular pathways targeted by steroid receptors.

Key Words: estrogen receptor • social behavior • Peromyscus polionotus • seasonality

Author contributions: B.C.T. and R.J.N. designed research; B.C.T., M.S.F., and M.R.R. performed research; B.C.T. and S.L. analyzed data; and B.C.T. and R.J.N. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE5795).

This article contains supporting information online at www.pnas.org/cgi/content/full/0701819104/DC1.

To whom correspondence should be sent at the present address: Department of Psychology, University of California, Davis, 1 Shields Avenue, Davis, CA 95616. E-mail: bctrainor{at}ucdavis.edu

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