Pubertal testosterone programs context-appropriate agonistic behavior and associated neural activation patterns in male Syrian hamsters

Pubertal testosterone programs the level of aggressive behavior displayed by male Syrian hamsters during resident–intruder interactions. To further explore the pubertal programming of adult male agonistic behaviors, the current study investigated the formation, stability, and maintenance of dominant–subordinate relationships in males that either did (T@P) or did not (NoT@P) experience testicular hormones during adolescent development. NoT@P males were gonadectomized prepubertally and T@P males were gonadectomized in adulthood. Four weeks after gonadectomy, all males received testosterone-replacement. Two weeks later, two males of the same hormonal history were given a 60 min introductory trial in a neutral arena, followed immediately and again 24 h later by three 5-min trials. During the introductory trial, each male was deemed dominant, subordinate, or no-status. Brains were collected 1 h after the last trial and sections were stained for Fos-immunoreactivity. Dominant T@P males flank marked more frequently than subordinate and no-status T@P males; this difference was not found in NoT@P males. NoT@P males showed an increase in the number of offensive postures the day after the first series of tests, whereas T@P males did not. Dominant T@P males had significantly more Fos expression than no-status T@P males in anterior cingulate cortex; this relationship was not observed in NoT@P males. Additionally, dominant T@P males had higher Fos expression than dominant NoT@P males in lateral septum. Thus, pubertal testosterone does not organize the formation or stability of male–male relationships, but does program the behavioral strategies used to maintain these relationships over time and the neural correlates of status.

► Formation of stable male–male relationships is pubertal testosterone-independent. ► Maintenance of male–male relationships is programmed by pubertal testosterone. ► Pubertal testosterone organizes the cingulate cortex to program agonistic behavior. ► Pubertal testosterone organizes the lateral septum to regulate agonistic behavior.