Neural mechanisms of social status during adolescence

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In animals including humans, winning a competitive encounter increases the chances of winning in future contests while losing increases the chance losing again in the future. These effects occur because the experience of winning and losing have different effects on the brain. What these discoveries do not explain, is how individuals can transition from losing to winning. This is especially true during adolescence, when individuals have less competitive experience and are more likely to lose. A specific type of behavioral strategy, social vigilance, may be a key mechanism for facilitating this transition. Social vigilance involves a combination of avoidance and observation of potentially threatening individuals. In this project, the research team will test whether increased testosterone secretion during adolescence facilitates a transition from social vigilance to more assertive aggressive behaviors in males. In adults, short term increases in testosterone after winning play a key role in facilitating winner effects. The researchers predict that the testosterone secretion during adolescence desensitizes neural circuits that promote social vigilance. To address this question this project will determine whether testosterone acts during puberty to alter the activity of neurons within neural circuits that control social vigilance as well as defensive and offensive vocalizations used in aggressive encounters. The University of California at Davis is a Hispanic Serving Institution with a strong track record of supporting an inclusive STEM culture to broaden impact and increase discovery. Support of this research will provide training opportunities for historically disadvantaged groups in STEM and increase community engagement via open house events.This project integrates behavioral, neuroendocrine, and physiological levels of analysis of social behavior. Previous work shows that oxytocin acting in the bed nucleus of the stria terminalis (BNST) increases social vigilance behavior, and that social stress increases the activity of oxytocin neurons. A key hypothesis is that the pubertal surge of testosterone reprograms oxytocin neurons in the BNST to be less sensitive to social stress. Social vigilance is oxytocin dependent, and more prevalent in juvenile males than adults. This research will first test whether increased testosterone during puberty reduces stress-induced vigilance in males and females. The effects of stress on long term potentiation (LTP) of oxytocin neurons will be examined and whether the effects of stress on LTP are modulated by pubertal testosterone exposure. In the rat hippocampus and the zebra finch song control system testosterone acts during puberty to reduce LTP. Finally, the effects of pubertal testosterone on territory formation will be studied by observing aggressive behaviors and the use of well characterized assertive and passive vocalizations during territory formation. Results from these studies will provide important insights into the neural circuits that facilitate social transitions that occurs across vertebrate species. This project will also generate new tools, including a brain atlas of the adolescent California mouse brain which will be hosted on brainmaps.org.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.