Developmental Changes in Behavior and in Steroid Uptake by the Male and Female Macaque Brain

We describe the sex differences in the development of play initiation, rough-and-tumble play, and mounting behavior in rhesus monkeys. There are also sex differences in the acquisition and maintenance of dominance rank under naturalistic conditions in this female-bonded, matrilineal society. The hormonal control of adult mating behavior, as well as the behavioral patterns expressed, are quite different in males and females, but both sexes have the capacity to show bisexual patterns of behavior in special circumstances. Using high-performance liquid chromatography and autoradiography, we found a well-marked system of neurons that can accumulate steroids in the hypothalamus and amygdala of the fetus by 120 days of gestation. In the male fetus, plasma testosterone is high at this time, so receptors are occupied. In contrast, plasma hormones in the female remain low throughout gestation. The natural masculinization of genetic male fetuses, as well as the masculinization of females whose mothers were administered androgens during pregnancy, are due at least in part to the aromatization of testosterone in the brain and the resulting occupation of estrogen receptors: This was established in fetal males castrated in utero. Many of the deleterious effects of diethylstilbestrol administered to pregnant women can also be accounted for by its uptake by the brain and the genital tract before birth. In adults, we used in vivo competition studies with unlabeled steroids to demonstrate that the major form of radioactivity in the brain after [³H]testosterone administration is its aromatized metabolite [³H]estradiol in the preoptic area, hypothalamus, and amygdala, and in the basal accessory amygdaloid nucleus there is strong evidence for a population of neurons containing tau receptors that accumulate only unchanged [³H]testosterone. Comparison of data from fetuses, neonates, and adults revealed an increase with age in the proportion of cells accumulating [³H]estradiol in the preoptic area and hypothalamus, whereas in the amygdala a similar increase occurred between the neonatal period and adulthood. We were unable to demonstrate any significant sex differences in steroid uptake mechanisms in the brain and pituitary gland at any stage of development, but the hormonal milieu differs vastly in the 2 sexes, and this must affect brain mechanisms differently in the 2 sexes, the most plausible source of sex differences in behavior, although not necessarily a sufficient one.