Cognitive performance in rhesus monkeys varies by sex and prenatal androgen exposure.

Men and women differ on performance and strategy on several spatial tasks. Rodents display similar sex differences, and manipulations of early hormone exposure alter the direction of these differences. However, most cognitive testing of nonhuman primates has utilized sample sizes too small to investigate sexually differentiated behaviors. This study presents an investigation of sex differences and the effects of prenatal androgen on spatial memory and strategy use in rhesus monkeys. Monkeys prenatally exposed to vehicle, testosterone, or the androgen receptor blocker flutamide performed a search task in which 5 of 12 goal boxes contained food rewards. Spatial consistency and the presence of local landmarks were varied. Performance when both spatial and marker cues were available did not differ by sex or prenatal treatment. Contrary to predictions, females easily solved the task when local markers were removed, and their performance outscored males. Although eliminating spatial consistency and requiring subjects to use local markers impaired performance by all monkeys, females continued to locate correct goal boxes at higher than chance levels and scored better than males. Blocking prenatal androgen exposure in males improved use of local markers. These findings suggest that the tendency to attend to landmarks and to use them in solving spatial problems is typical of females across many species, including rodents, humans, and rhesus monkeys. In rhesus monkeys and rodents, developmental androgen eliminates this specialization. However, these results are the only known example of better performance of females than males when salient markers are removed.

An outdoor 3-D visual tracking system for the study of spatial navigation and memory in rhesus monkeys.

Previous studies of the navigational abilities of nonhuman primates have largely been limited to what could be described by a human observer with a pen and paper. Consequently, we have developed a system that uses a pair of cameras to automatically obtain the three-dimensional trajectory of rhesus monkeys performing an outdoor spatial navigation and memory task. The system provides trajectories, path length, speed, and other variables that would be impossible for an unaided observer to note. From trajectory data, we computed and validated a path-length measurement. We use this measurement to compare the navigation abilities of several animals. In addition, we provide quantitative data on the accuracy of a method for automatic behavior detection. Currently, the system is being used to examine the sex differences in spatial navigation of rhesus monkeys. We expect that measures derived from the trajectory data will reveal strategies used by animals to solve spatial problems.

Men and women differ in amygdala response to visual sexual stimuli.

Men are generally more interested in and responsive to visual sexually arousing stimuli than are women. Here we used functional magnetic resonance imaging (fMRI) to show that the amygdala and hypothalamus are more strongly activated in men than in women when viewing identical sexual stimuli. This was true even when women reported greater arousal. Sex differences were specific to the sexual nature of the stimuli, were restricted primarily to limbic regions, and were larger in the left amygdala than the right amygdala. Men and women showed similar activation patterns across multiple brain regions, including ventral striatal regions involved in reward. Our findings indicate that the amygdala mediates sex differences in responsiveness to appetitive and biologically salient stimuli; the human amygdala may also mediate the reportedly greater role of visual stimuli in male sexual behavior, paralleling prior animal findings.

Sex differences in interest in infants in juvenile rhesus monkeys: relationship to prenatal androgen.

Yearling rhesus monkey females interact more with infants than do males. However, the continuity of this sex difference throughout the juvenile period is unknown. Human females display similar sexually differentiated interest in infants, and studies of girls with congenital adrenal hyperplasia suggest that this sex difference may be modulated by prenatal androgen exposure. We investigated infant interest in 1- to 3-year-old juvenile rhesus monkeys. Hormonal influences on this behavior were investigated by treating pregnant females with an androgen-receptor blocker (flutamide), testosterone enanthate, or vehicle, early or late in gestation. Subjects were reared in their well-established natal groups, composed of species-typical matrilineal social structures, including members of all ages. Yearling control females interacted with infants more than did yearling control males. At 2 and 3 years of age, the magnitude of the sex difference in interactions with infants increased markedly, producing effect sizes of more than 2.5 standard deviations. These effects are larger than those reported in humans. Androgen treatment did not affect male or female interactions with infants, but late gestation flutamide masculinized aspects of females' interest in infants. Although early flutamide prevented complete masculinization of male genitalia, this treatment was not accompanied by any alterations in the masculine pattern of infant interest. We found no evidence that the robust juvenile sex difference in frequency of infant interactions results from socialization. However, it was largely unaffected by our hormone manipulations. Whether this reflects characteristics of our specific treatments or is evidence of nonhormonal influences on infant interest remains unanswered.