Effects of stressors in adolescence on learning and memory in rodent models

This article is part of a Special Issue "Puberty and Adolescence".     

How environment and genes shape the adolescent brain

This article is part of a Special Issue “Puberty and Adolescence”.     

Diurnal and Seasonal Cortisol,Testosterone, and DHEA Rhythms in Boys and Girls during Puberty

Diurnal and seasonal rhythms of cortisol, testosterone, and DHEA were examined, as little is known about the relationship between these rhythmicities and pubertal development. Salivary samples were obtained from 60 boys and 60 girls at approximately 07∶45, 08∶00, 08∶30, 12∶00, 16∶50, and 21∶00 h. The participants' ages ranged from 8–14 yrs, and each participant was tested three times at six‐month intervals. The study was conducted at a General Clinical Research Center (GCRC) and at the homes of the participants. All hormones showed diurnal fluctuations. The acrophase (peak time) of cortisol occurred earlier than for testosterone or DHEA and showed a seasonal effect, with the acrophase occurring earlier in spring than in summer. The cortisol acrophase also occurred later in the day for boys than for girls during later puberty. Seasonal effects were found only for cortisol with higher concentrations in the spring and summer. Cortisol concentrations were relatively stable across pubertal maturation, but significantly lower concentrations were observed at pubertal stage 3 compared to the other stages. Morning cortisol levels were also higher in boys at pubertal stage 2. Testosterone concentrations were higher in boys at pubertal stages 3 and 4, and DHEA was lower at pubertal stage 1 than 3 and 4 for both boys and girls. For the total sample, there was a positive correlation between DHEA and testosterone during early puberty (stages 1–3) but not later puberty (stages 4–5). Awakening secretory activity correlated with daytime secretory activity for testosterone and DHEA, but not for cortisol. These data provide novel chronobiological information on cortisol, testosterone, and DHEA as it relates to sexual maturation and encourage further study on both normal and abnormal endocrine rhythms.     

Male sexual behavior does not require elevated testosterone in a lizard (Coleonyx elegans, Eublepharidae)

Male sexual behavior depends on gonadal androgens in species of all major vertebrate lineages, including reptiles. However, male sexual behavior includes distinct appetitive and consummatory phases, typically denoted as courtship and mounting, with potentially different hormonal control. Different proximate controls of courtship versus mounting could enable disconnected evolutionary losses and gains of various aspects of male sexual behavior. Male courtship display, which is activated by testosterone (T) in many species, is an ancestral trait in the lizard family Eublepharidae. However, Coleonyx elegans (Yucatan Banded Gecko) lost the courtship display, while retaining a highly simplified male sexual behavior that involves only mounting for copulation. We performed surgical manipulations (castration with and without T replacement in adult males; implantation of adult females with exogenous T) to investigate hormonal mechanisms involved in this evolutionary novelty. Our results indicate that the expression of simplified sexual behavior in C. elegans does not require elevated circulating levels of T, a finding that is previously unreported in lizards. In females, however, exogenous T induced male-like mounting. Thus, the mounting phase of sexual behavior is not activated by T in the traditional sense of this term but probably requires post-natal, maturational organization (if not periodic reorganization) by androgens. We conclude that the simplification of male sexual behavior and its independence from elevated levels of circulating androgens in C. elegans evolved via 1) evolutionary loss of the androgen-activated courtship display and 2) retention of the mounting phase, which has a longer “functional memory” for the effects of androgenic steroids.     

Pubertal growth of the medial amygdala delayed by short photoperiods in the Siberian hamster, Phodopus sungorus

We investigated whether puberty influences the morphology of the medial nucleus of the amygdala (MeA) by comparing Siberian hamsters (Phodopus sungorus) that had been raised from birth in either long day (LD; 16:8 h light:dark) or short day (SD; 8:16) photoperiods. Hamsters were sacrificed at 42-49 days of age, at which point all LD hamsters were reproductively mature, as evidenced by adult-like testes weights (mean: 657 mg). In contrast, the testes weights of the SD hamsters were low (mean: 31 mg), indicating that the SD photoperiod had delayed puberty. The regional volume and mean soma size of the four MeA subnuclei was estimated bilaterally by stereological procedures. In the posterior dorsal and ventral MeA subnuclei, regional volume was 22-25% larger, and mean soma size 18% larger, in LD males than SD males. Unbiased cell counts in the posterior dorsal MeA showed that LD and SD hamsters have equivalent neuron numbers. In the anterior MeA subnuclei, regional volumes and soma sizes from LD and SD hamsters were equivalent. Additionally, the regional volume of the posteroventral subnucleus was larger in the right hemisphere than the left, but this laterality did not respond to photoperiod manipulation. These results suggest that the extant neurons within the posterior MeA, a steroid-sensitive nucleus implicated in socio-sexual behavior, grow in response to the elevated levels of circulating androgen accompanying puberty, and that photoperiodic regulation of puberty affects morphological maturation of this nucleus.     

Age-related changes in urinary testosterone levels suggest differences in puberty onset and divergent life history strategies in bonobos and chimpanzees

Research on age-related changes in morphology, social behavior, and cognition suggests that the development of bonobos (Pan paniscus) is delayed in comparison to chimpanzees (Pan troglodytes). However, there is also evidence for earlier reproductive maturation in bonobos. Since developmental changes such as reproductive maturation are induced by a number of endocrine processes, changes in hormone levels are indicators of different developmental stages. Age-related changes in testosterone excretion are an indirect marker for the onset of puberty in human and non-human primates. In this study we investigated patterns of urinary testosterone levels in male and female bonobos and chimpanzees to determine the onset of puberty. In contrast to other studies, we found that both species experience age-related changes in urinary testosterone levels. Older individuals of both sexes had significantly higher urinary testosterone levels than younger individuals, indicating that bonobos and chimpanzees experience juvenile pause. The males of both species showed a similar pattern of age-related changes in urinary testosterone levels, with a sharp increase in levels around the age of eight years. This suggests that species-differences in aggression and male mate competition evolved independently of developmental changes in testosterone levels. Females showed a similar pattern of age-related urinary testosterone increase. However, in female bonobos the onset was about three years earlier than in female chimpanzees. The earlier rise of urinary testosterone levels in female bonobos is in line with reports of their younger age of dispersal, and suggests that female bonobos experience puberty at a younger age than female chimpanzees.     

Peripubertal exposure to male odors influences female puberty and adult expression of male-directed odor preference in mice

Testosterone-dependent olfactory signals emitted by male are well known to accelerate female puberty in mice (Vandenbergh effect). However, it remains unclear whether these chemosignals also influence adult expression of male-directed odor preference. Therefore, we exposed female mice to intact or castrated male bedding (vs clean bedding as control) during the peripubertal period (postnatal day (PD) 21–38) and measured male-directed odor preference in adulthood. At PD45 or PD60, females exposed to intact male odors, and thus showing puberty acceleration, preferred to investigate odors from intact males over females or castrated males. Females exposed to castrated male odors did not show puberty acceleration but preferred male (intact or castrated) over female odors. Finally, control females did not show any odor preference when tested at PD45, although a preference for male odors emerged later (PD60). In a second experiment, females that were exposed to intact male odors after pubertal transition (PD36–53) also preferred intact male over castrated male odors. In conclusion, our results indicate that peripubertal exposure to male odors induced early expression of male-directed odor preference regardless of puberty-accelerating effect and that induction of male-directed odor preference is not specific to the peripubertal period.     

Father absence, parental care, and female reproductive development

This study examines female reproductive development from an evolutionary life history perspective. Retrospective data are for 10,847 U.S. women. Results indicate that timing of parental separation is associated with reproductive development and is not confounded with socioeconomic variables or phenotypic correlations with mothers' reproductive behavior. Divorce/separation between birth and 5 years predicted early menarche, first sexual intercourse, first pregnancy, and shorter duration of first marriage. Separation in adolescence was the strongest predictor of number of sex partners. Multiple changes in childhood caretaking environment were associated with early menarche, first sex, first pregnancy, greater number of sex partners, and shorter duration of marriage. Living with either the father or mother after separation had similar effect on reproductive development. Living with a stepfather showed a weak, but significant, association with reproductive development, however, duration of stepfather exposure was not a significant predictor of development. Difference in amount and quality of direct parental care (vs. indirect parental investment) in two- and single-parent households may be the primary factor linking family environment to reproductive development.     

Hormonal responses to gonadotrophin releasing hormone during testicular development in male African green monkeys

Reproductive development in male African green monkeys was characterized by evaluating both luteinizing hormone (LH) and testosterone (T) before and after gonadotrophin releasing hormone (GnRH) stimulation in relation to the physical maturation of the testis. There were LH responses to GnRH at all ages studied, but the failure of some animals to respond at earlier ages suggested developmental changes in the responsiveness of the pituitary. The T secretion developed progressively but did not reach adultlike characteristics until approximately 44 months of age, at which time sperm could be demonstrated in ejaculated semen.     

Exposure of prepubertal beef bulls to cycling females does not enhance sexual development

The objective of this study was to determine whether continuous, long-term, fenceline exposure of prepubertal beef bulls to cycling beef females reduced age at puberty and influenced the percentage of bulls that passed an initial breeding soundness examination (BSE). Bulls (Angus, n = 37; Simmental, n = 22; Hereford, n = 10; Simmental × Angus, n = 8) at an average age of 202 ± 21.5 days were given either continuous fenceline and visual exposure to cycling females (exposed, n = 41) or no exposure (control, n = 36). Estrus was induced in cycling beef females so at least three females were in standing estrus each week during the 182 days of exposure to bulls. Scrotal circumference (SC), body weight, and blood samples were collected every 28 days. When bulls had SC of 26 cm or more, semen samples were obtained monthly via electroejaculation until puberty was achieved (≥50 × 10⁶ sperm/mL with at least 10% progressive motility). Behavioral observations were conducted twice monthly: once when females were in estrus and once during diestrus. Homosexual mounting, flehmen responses, and number of times near penned females were recorded for each observation period. Breeding soundness examinations were conducted when the average age of bulls was 364 ± 21.5 days. Normal sperm morphology of at least 70% and sperm motility of at least 30% were required to pass the BSE. Age, body weight, and SC at puberty did not differ between exposed and control bulls (320 ± 28 and 311 ± 29 days; 466.2 ± 12.2 and 437.7 ± 13.5 kg; and 34.4 ± 2.5 and 34.9 ± 2.5 cm, respectively). Percentage of bulls passing their initial BSE did not differ between treatments (exposed, 87.8%; control, 75.0%). Treatment, month, and female estrous stage interacted (P = 0.05) to affect the number of mount attempts and flehmen responses. Exposed bulls entered the cow area more times (P < 0.001) during estrus than diestrus in Months 1, 2, and 3. We concluded that bulls given continuous, long-term, fenceline exposure to cycling beef females do not have enhanced sexual development.