The Behavioral Neuroendocrinology of Puberty and Adolescence

We use the male golden hamster as a model system for studying adolescent maturation of social behaviors and their underlying neural circuits. We are especially interested in determining which aspects of maturation are dependent on the pubertal elevation in gonadal hormones and which aspects are hormone-independent, that is, related to age instead of pubertal status.

Some of our early work showed that adult male social behaviors, including sexual behavior, aggression, and scent marking, are compromised if adolescent development proceeds in the absence of testicular hormones. In addition, male hamsters that do not experience testosterone during adolescent development appear to be "socially awkward", showing inappropriate responses during social interactions and failing to learn from social experience. These results showed that testosterone, acting during puberty, organizes neural circuits underlying social behaviors, and we've proposed a two stage model of sexual differentiation, in which perinatal testosterone initially masculinizes the nervous system, and then a second wave of further masculinization occurs when testosterone levels rise again during puberty.

We've also found that the perinatal and pubertal periods are not two separate sensitive periods for brain organization by testosterone, but instead that puberty and adolescence are part of an extended period of postnatal sensitivity to organizational effects of hormones that begins at birth and ends sometime in late adolescence.

We are currently focused on the role of testicular hormones in adolescent maturation of social information processing. Male hamsters are a good model for this line of work, because they show an adolescent change in neural and behavioral responses to female pheromones that are required for successful reproduction. It appears that these female pheromones are rewarding to adults, but not juveniles, because adults will form a conditioned place preference to vaginal secretions that contain the pheromones, whereas juvenile hamsters do not. In addition, the pheromones activate certain elements of the mesocorticolimbic reward circuitry in adults, but not juveniles. We are now investigating the role of testosterone and dopamine in this adolescent change in the perception of this essential social stimulus.


Neurogenesis, Gliogenesis, and Sex Differences in the Adolescent Brain

Many cell groups in the central nervous system are sexually dimorphic, i.e., are structurally different in males and females. Structural sexual dimorphisms include sex differences in neuron and glial cell number, cell size, cell phenotype, and connectivity. These structural dimorphisms are usually related to functional dimorphisms, i.e., physiological or behavioral differences between males and females. It's been thought for many years that sexual dimorphisms are established during early neural development, and arise primarily through the action of a perinatal elevation of testosterone in males, which masculinizes the developing brain. We recently discovered that new neurons and new glia are added to sexually dimorphic brain regions during adolescence, and there are sex differences in this regard. More new cells are added to male-biased cell groups in males, whereas more new cells are added to female-biased cell groups in females. AND, if gonadal hormones are removed prior to the onset of puberty, all of these sex differences disappear! We interpret these findings as evidence that pubertal hormones participate in the maintenance or establishment of sexual dimorphisms while the adolescent brain is undergoing its metamorphosis. We are currently investigating whether pubertal hormones influence cell proliferation and or cell death in order to promote sex differences in the adolescent brain, and what the function of newly added cells is.

Pubertal Hormones and Risk for Disordered Eating

Together with Dr. Kelly Klump at MSU, we have begun to study the role of ovarian hormones on the etiology of binge eating, which is a core component of many eating disorders. We've adapted the Boggiano rat model of binge eating, in which highly palatable food is intermittently presented to female rats that are otherwise provided ad lib access to standard laboratory chow. Rats are categorized as binge eating prone (BEP) or binge eating resistant (BER) if they consistently eat high or low amounts of palatable food, respectively. Approximately 25-30% of female rats fall into each of these two extreme phenotypes, which appear to be stable in adulthood. We have found that the BER/BEP phenotypes are not present in prepubertal rats, but instead, emerge during mid-puberty. If BER/BEP rats are ovariectomized in adulthood, they retain their BER or BEP status, indicating that the extreme phenotypes are not secondary to individual differences in the influence of ovarian hormones on palatable food consumption. We will be investigating sex differences in this model of binge eating, as well as determining the effect of pubertal ovarian hormones on the development of binge eating phenotypes.