Elsevier

Hormones and Behavior

Volume 45, Issue 4, April 2004, Pages 242-249
Hormones and Behavior

Gonadal hormones masculinize and defeminize reproductive behaviors during puberty in the male Syrian hamster

https://doi.org/10.1016/j.yhbeh.2003.12.007Get rights and content

Abstract

Three experiments were conducted to test whether testicular hormones secreted during puberty masculinize and defeminize the expression of adult reproductive behavior. Experiment 1 tested the hypothesis that gonadal hormones during puberty masculinize behavioral responses to testosterone (T) in adulthood. Male hamsters were castrated either before puberty (noTduringP) or after puberty (TduringP). All males were implanted with a 2.5-mg T pellet 6 weeks following castration and tested once for masculine reproductive behavior 7 days after the onset of T replacement. TduringP males displayed significantly more mounts, intromissions, and ejaculations than noTduringP males. Experiment 2 tested the hypothesis that gonadal hormones during puberty defeminize behavioral responses to estrogen (EB) and progesterone (P). Eight weeks following castration, noTduringP and TduringP males were primed with EB and P and tested for lordosis behavior with a stud male. Behavioral responses of males were compared to that of ovariectomized (OVX) and hormone primed females. NoTduringP males and OVX females displayed significantly shorter lordosis latencies than TduringP males. Experiment 3 investigated whether prolonged T treatment or sexual experience could reverse the deficits in masculine behavior caused by the absence of T during puberty. Extending the T treatment from 7 to 17 days did not ameliorate the deficits in masculine behavior caused by absence of T during puberty. Similarly, when the level of sexual experience was increased from one to three tests, the deficits in masculine behavior persisted. These studies demonstrate that gonadal hormones during puberty further masculinize and defeminize neural circuits and behavioral responsiveness to steroid hormones in adulthood.

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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