Gonadal hormones masculinize and defeminize reproductive behaviors during puberty in the male Syrian hamster
Introduction
The organizational–activational hypothesis (Phoenix et al., 1959) proposes that exposure to steroid hormones early in development masculinizes and defeminizes neural circuits, programming behavioral responses to hormones in adulthood. Since the organizational–activational hypothesis was first proposed, many studies have demonstrated that disruption of perinatal testicular hormone secretion by manipulations such as prenatal stress or neonatal castration reduces the capacity for masculine behavior and increases the capacity for feminine reproductive behavior in adulthood (Eaton, 1970, Gerall et al., 1967, Grady et al., 1965, Ward and Weisz, 1980, Whalen and Edwards, 1967; for review see Ward and Ward, 1985). Thus, the perinatal period is important for the sexual differentiation of behavior by gonadal steroid hormones.
Neonatal castration followed by assessment of behavioral responses to steroid hormones in adulthood has been a commonly used approach for analyzing the contribution of neonatal hormones to the process of behavioral masculinization and defeminization. However, because neonatal castration also prevents exposure of the nervous system to hormone secretions during puberty, this approach confounds the contribution of neonatal hormones to the process of sexual differentiation of behavior with that of pubertal hormones. Furthermore, while many studies have employed prepubertal castration as part of their experimental methods, the purpose of these investigations was not necessarily to assess the role of pubertal hormones in the masculinization and defeminization of reproductive behavior. Thus, while the results of some studies employing prepubertal castration suggest that the absence of testosterone (T) during puberty alters adult reproductive behavior Adkins-Regan et al., 1989, Ford, 1990, Gotz and Dorner, 1976, Larsson, 1967, Sodersten, 1973, the results of other studies do not Dixon, 1993, D'Occhio and Brooks, 1980, Epple et al., 1990, Larsson et al., 1976, Shrenker et al., 1985, and various methodological considerations make it difficult to draw a firm conclusion. For example, in previous studies, the ability of steroid hormones to activate behavior in males castrated prepubertally was not always directly compared to males castrated as adults D'Occhio and Brooks, 1980, Epple et al., 1990, Larsson et al., 1976, steroid hormones were not readministered in adulthood before behavior testing (Dixon, 1993), only one measure of reproductive behavior was reported (Larsson, 1967), and sexual behavior may have been influenced by other social experiences such as aggressive encounters (Shrenker et al., 1985).
One indication that further organization and masculinization of behavior occur during puberty is that hormonal treatments that fully activate masculine reproductive behavior in adult males are less effective in activating behavior in prepubertal males Baum, 1972, Sisk et al., 1992, Sodersten et al., 1977. For example, 1 week of testosterone propionate, dihydrotestosterone, or estradiol benzoate treatment increases mounts, intromissions, and ejaculations in adult but not prepubertal male Syrian hamsters Meek et al., 1997, Romeo et al., 2001, Romeo et al., 2002. Even up to 2 weeks of T treatment fails to activate reproductive behavior in a 28-day-old male hamster (unpublished data). These data suggest that the prepubertal male brain is not fully organized to mediate masculine reproductive responses to steroid hormones.
We, therefore, hypothesize that puberty is a second stage of sexual differentiation during which gonadal hormones fine-tune neural circuits to allow full maturation of sex-typical responses to hormones in adulthood. The current study addresses this possibility by testing whether the presence or absence of gonadal hormones during puberty alters masculine responses to T and feminine responses to estradiol benzoate (EB) and progesterone (P) in adulthood. This hypothesis predicts that males gonadectomized (GDX) before puberty will display lower levels of masculine reproductive behavior than males GDX after puberty when both groups are treated with T in adulthood (Experiment 1). Furthermore, the hypothesis predicts that males GDX before puberty will display higher levels of feminine reproductive behavior than males GDX after puberty when both groups are treated with EB and P in adulthood (Experiment 2). We report here that the absence of gonadal hormones during puberty reduces masculine responsiveness to T in adulthood (Experiment 1), increases feminine responsiveness to EB and P in adulthood (Experiment 2), and that the deficits in masculine behavior are not reversed by prolonged T treatment or sexual experience (Experiment 3).
Section snippets
Animals
Eighteen-day-old male Syrian hamsters (Mesocricetus auratus) were obtained from Harlan Sprague–Dawley laboratories (Madison, WI) and arrived with their mothers. Males were housed with mothers and littermates until weaning at 21 days of age. All animals were housed in clear polycarbonate cages (12 × 4 × 8 in.) with ad libitum access to food (Telkad Rodent Diet No. 8640, Harlan) and water. Animals were exposed to a 14 h light/10 h dark schedule (lights off at 1200 h EST), and the temperature was
Experiment 1A
TduringP males displayed significantly more mounts [t(1,11) = 11.78, P = 0.0056], intromissions [t(1,11) = 22.13, P = 0.0006], and ejaculations [t(1,11) = 5.38, P = 0.04] than noTduringP males (Fig. 2). In addition, TduringP males displayed significantly shorter latencies to ejaculate than noTduringP males [t(1,11) = 5.26, P = 0.04; Fig. 2].
Experiment 1B
No differences in the number of mounts [t(1,13) = 1.24, P = 0.28], intromissions [t(1,13) = 2.37, P = 0.15], or ejaculations [t(1,13) = 0.25, P = 0.62] were
Discussion
The current study demonstrates that the absence of testicular hormones during puberty results in reduced masculine behavioral responses to T (Experiments 1 and 3) and increased feminine behavioral responses to EB and P (Experiment 2) in adulthood. Males that were GDX before puberty displayed fewer mounts, intromissions, and ejaculations than males that were GDX after puberty, as well as longer latencies to ejaculate. Males that were GDX before puberty also displayed shorter lordosis latencies
Acknowledgements
We would like to thank Jane Venier for her exceptional technical assistance. This work was supported by a grant from the National Science Foundation IBN 99-85876.
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2021, Hormones and BehaviorCitation Excerpt :These studies found reduced levels of both copulatory and aggressive behaviors when males were castrated prior to puberty vs. after puberty (Meek et al., 1997; Schulz et al., 2006, 2004; Schulz and Sisk, 2006). For instance, adult male Syrian hamsters castrated prior to puberty failed to show robust copulatory behavior, even after 17 daily doses of testosterone (Schulz et al., 2004). In contrast, when exposed to feminizing gonadal hormones as adults, male Syrian hamsters castrated prior to puberty were quicker to exhibit lordosis than males left intact during puberty and given estrogen (Schulz et al., 2004).