Takamasa Koyama

Alterations in male infant behaviors towards its mother by prenatal exposure to bisphenol A in cynomolgus monkeys (Macaca fascicularis) during early suckling period

Bisphenol A (BPA) is an environmental chemical with physiological potencies that cause adverse effects, even at environmentally relevant exposures, on the basis of a number of studies in experimental rodents. Thus, there is an increasing concern about environmental exposure of humans to BPA. In the present study, we used experimentally controlled cynomolgus monkeys (Macaca fascicularis) to assess the influence of prenatal exposure to BPA (10 microg/(kg day)) via subcutaneously implanted pumps and examined social behaviors between infants and their mothers during the suckling period. Mother-infant interactions in cynomolgus monkeys had behavioral sexual dimorphism associated with sex of infant from early suckling period. Prenatal exposure to BPA altered the behaviors of male infants significantly; BPA-exposed male infants behaved as female infants. And it also affected some of female infant behaviors. Consequently, gestational BPA exposure altered some behaviors of their mothers, mainly in male-nursing mothers. These results suggest that BPA exposure affects behavioral sexual differentiation in male monkeys, which promotes the understanding of risk of BPA exposure in human.

Influence of Make-up on Facial Recognition

Make-up may enhance or disguise facial characteristics. The influence of wearing make-up on facial recognition could be of two kinds: (i) when women do not wear make-up and then are seen with make-up, and (ii) when women wear make-up and then are seen without make-up. A study is reported which shows that light make-up makes it easier to recognise a face, and heavy make-up makes it more difficult. Seeing initially a made-up face makes any subsequent facial recognition more difficult than initially seeing that face without make-up.

Altered social interactions in male juvenile cynomolgus monkeys prenatally exposed to bisphenol A.

Bisphenol A (BPA) is a widespread environmental contaminant, and humans are routinely exposed to BPA. We investigated whether prenatal exposure to BPA influences behavioral development in juvenile cynomolgus monkeys (Macaca fascicularis). Pregnant cynomolgus monkeys were implanted with subcutaneous pumps and exposed to 10μg/kg/day BPA or vehicle (control) from gestational day 20 to 132. Both BPA-exposed and control juvenile monkeys (aged 1-2years) were assessed using the peer-encounter test that was conducted to evaluate behaviors in social interaction with a same-sex, same-treatment peer. In the encounter test, prenatal BPA exposure significantly reduced environmental exploration and presenting, a gesture related to sexual reproduction, and increased visual exploration, but only in males; furthermore, it significantly reduced the typical sexual dimorphism of the aforementioned behaviors normally observed between male and female juvenile cynomolgus monkeys. This study demonstrates that prenatal BPA exposure affects behavioral development during adolescence and results in the demasculinization of key sexually dimorphic behaviors in male juvenile monkeys.

The repeated procedure of weaning and peer group formation causes accumulation of stress and changes of plasma cortisol level and natural killer activity in squirrel monkeys (Saimiri sciureus)

The psychological stress was evaluated in repeated and unrepeated procedures of weaning as well as forming peer group in squirrel monkeys. The repeated procedure included the process of increasing the period of separation or formation stepwise during four weeks. The plasma cortisol levels and natural killer (NK) activities were monitored during experiment to evaluate the stress in infant monkeys. The plasma cortisol level rapidly increased two to three times as much as basal level and kept high levels throughout experiment in repeated group. In the infants of unrepeated group, significant increase of cortisol level and decrease of NK activity were observed in day-1, but both of them returned to the basal level at day-7.Both cortisol level and NK activity did not show any change with exception of decrease in NK activity at day-7 in infants who were introduced into peer group without repeated procedure. On the other hand, both cortisol level and NK activity increased during the repeated procedure. These results indicate that both weaning and forming peer group induce the psychological stress in infant squirrel monkeys, resulting in changes of plasma cortisol level and NK activity. Repeating the procedure of separation or introduction applied in this study caused the accumulation of stress. Although plasma cortisol level increased in infants exposed to both weaning and forming peer group, the changing pattern of NK activity differed between them. This finding suggests that social or psychological stress show two different effects on immune function, suppression, and enhancement depending on the level of stress.

Maternal plasma polychlorinated biphenyl levels in cynomolgus monkeys (Macaca fascicularis) affect infant social skills in mother–infant interaction

Polychlorinated biphenyls (PCBs) are endocrine disrupting chemicals that disturb normal development of embryonic brains. In the present study, we evaluated the relationship between maternal plasma PCB concentration and infant behavioral characteristics in mother-infant interactions. We grouped 20 pregnant cynomolgus monkeys (Macaca fascicularis) into higher and lower PCB exposure groups; monkeys in the higher PCB group had PCB concentrations above 15 pg/g, which is representative of natural exposure levels. Maternal PCB concentration correlated negatively with infant behaviors (approach, look, proximity, locomotion) at the age of 6 months (p < .05), when an increase in these behaviors should normally occur. These results suggest that maternal PCB exposure may affect the development of infant social behavior in cynomolgus monkeys. Furthermore, this study provides primate evidence to support observations of associations between behavioral and learning disabilities and prenatal exposure to PCBs in humans.

New type of puzzle-task finger maze learning in Macaca fascicularis

In order to easily estimate the global cognitive ability of nonhuman primates, we developed a 4-step noncorrection-method-type finger maze (4FM) based on the standard puzzle feeder. We tested 7 experimentally naïve long-tailed macaques (Macaca fascicularis) to assess the validity of the apparatus and the testing procedure. The most notable difference between the 4FM and the standard puzzle feeder is the presence of an error box. There is a hole at both ends of each step. One hole of each step is connected to the lower step or feeding box. The other hole of each step is connected to an error box. The monkey had to move the reward into the feeding box without dropping it into the error box and to retrieve the reward from the feeding box. Task difficulties could be controlled by deciding on which step to place the food reward at the beginning of the trial. All the monkeys could complete the tasks without food/water deprivation and pretraining. The results suggest that the 4FM is a suitable device to assess the cognitive ability of the monkeys simply, easily, and objectively.

Effect of Endocrine-Disrupting Chemicals on the Development of Macaque Socialization

More than a decade has passed since publication of the book Our Stolen Future by Colborn and colleagues in 1996. Yet traces of endocrine-disrupting chemicals (EDCs) persist, and there has been no decrease in their concentrations worldwide. We have been investigating the effect of perinatal exposure to EDCs such as dioxin, bisphenol A (BPA), and polychlorinated biphenyls (PCBs) on mother–infant interactions and peer relationships of two species of macaques (mulatta and fascicularis) by analyzing their observed behaviors. We found fewer effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (2,3,7,8-TCDD) than were expected but serious effects of BPA and PCBs. BPA prevents behavioral sex differentiation in infants, and PCBs suppress their social initiative in mother–infant and peer interactions. These studies prove that the observation paradigm for the analysis of mother and infant behaviors is a helpful and practical method to assess the subtle influence of EDCs on the brains of higher primates.