Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 107; no. 27; pp. 12393 - 12398
• Main Authors: Fuxjager, Matthew J., Forbes-Lorman, Robin M., Coss, Dylan J., Auger, Catherine J., Auger, Anthony P., Marler, Catherine A., McEwen, Bruce S.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 06.07.2010; National Acad Sciences
• Subjects: Aggression - physiology; Androgen receptors; Androgens; Animal aggression; Animal behavior; Animals; Biological Sciences; Brain; Competitive Behavior - physiology; Dominance-Subordination; Female; Gene expression; Genotype & phenotype; Hormones; Human aggression; Immunohistochemistry; Male; Messenger RNA; Mice; Motivation - physiology; Neural Pathways - physiology; Peromyscus; Peromyscus californicus; Receptors, Androgen - genetics; Receptors, Androgen - metabolism; Receptors, Androgen - physiology; Reverse Transcriptase Polymerase Chain Reaction; Rodents; Septal Nuclei - metabolism; Social Behavior; Social Environment; T cell receptors; Territoriality; Testosterone; Ventral tegmental area
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1001394107

Winning aggressive disputes can enhance future fighting ability and the desire to seek out additional contests. In some instances, these effects are long lasting and vary in response to the physical location of a fight. Thus, in principle, winning aggressive encounters may cause long-term and context-dependent changes to brain areas that control the output of antagonistic behavior or the motivation to fight (or both). We examined this issue in the territorial California mouse (Peromyscus californicus) because males of this species are more likely to win fights after accruing victories in their home territory but not after accruing victories in unfamiliar locations. Using immunocytochemistry and real-time quantitative PCR, we found that winning fights either at home or away increases the expression of androgen receptors (AR) in the medial anterior bed nucleus of the stria terminalis, a key brain area that controls social aggression. We also found that AR expression in brain regions that mediate motivation and reward, nucleus accumbens (NAcc) and ventral tegmental area (VTA), increases only in response to fights in the home territory. These effects of winning were likely exclusive to the neural androgenic system because they have no detectible impact on the expression of progestin receptors. Finally, we demonstrated that the observed changes in androgen sensitivity in the NAcc and VTA are positively associated with the ability to win aggressive contests. Thus, winning fights can change brain phenotype in a manner that likely promotes future victory and possibly primes neural circuits that motivate individuals to fight.