Puberty in the Sheep

In sheep, internal and external cues are integrated to time the decrease in sensitivity to steroid negative feedback that increases the frequency of gonadotropin-releasing hormone (GnRH) pulses to drive the transition into adulthood. The neural substrate that processes the information used to time the pubertal increase in GnRH secretion is programmed prenatally by the organizational actions of testosterone produced in the male, but not the female (the default sex), in response to an early increase in GnRH and gonadotropin secretion. In both sexes, metabolic cues provide information that sufficient growth has occurred to begin reproduction. However, the young female, being inherently photoperiodic, cannot express her sexual maturity until day length is appropriate. Once she has experienced the long days of summer followed by the short days of autumn, neuroendocrine sensitivity to steroid negative feedback decreases, and high-frequency GnRH pulses are expressed to initiate ovarian cycles. By contrast, prenatal testicular steroids masculinize the photoneuroendocrine system to reduce the reliance on day length as a cue for puberty, and the male lamb does not use photoperiods to time the expression of high-frequency GnRH pulses. Once metabolic signals indicate that energy balance is sufficient in the male, high-frequency GnRH pulses are expressed. Thus, whereas metabolic information provides permissive signals that time sexual maturity in both sexes, the presence or absence of prenatal programming by testosterone determines whether photoperiod also serves as a permissive cue to begin reproductive activity. Viewed in a broad sense, the neuroendocrine response to internal and external signals timing the transition to adulthood has fetal origins in the sheep.