To examine developmental changes in the LH response to estrogen, eight neonatally ovariectomized monkeys received repeated injections (sc) of 50 micrograms/kg estradiol benzoate (EB) at approximately 4-month intervals starting at age 8-12 months and ending at 49-52 months. Serum samples were obtained 24 before and 0, 6, 12, 24, 36, 48, 60, 72, 94, 108, and 120 h after each EB injection. Serum LH and estradiol levels were measured by RIA. The baseline LH level before EB injection during the prepubertal period (greater than 20 months of age) was 14.4 +/- 2.2 ng/ml, and it increased progressively to 115.3 +/- 13.5 ng/ml at 41-44 months, the age shortly before the first ovulation in our intact colony animals, then declined slightly. EB first induced a typical LH response, which consisted of a negative phase (suppression) followed by a positive phase (surge), at the average age of 29.3 +/- 1.9 months (n = 8). This is similar to the age of menarche in our colony animals. The baseline LH level before EB injection at the time of the first typical response (with negative and positive phases) was 36.7 +/- 6.7 ng/ml, a level 2.5 times higher than that of the prepubertal age. The magnitude of LH suppression by EB was significantly correlated with the baseline level of LH; the higher the baseline LH before EB injection, the greater the degree of LH decrease (r = 0.968; P less than 0.001). Similarly, the amplitude of the LH peak from the trough of the negative phase was significantly correlated with the baseline LH; the higher the LH level before EB injection, the higher the LH increase (r = 0.863; P less than 0.001). The latency to the LH peak was shortest when baseline LH was highest; the peak latency (34.4 +/- 1.6 h) of the LH surge at 41-44 months of age was significantly shorter than the latency (46.5 +/- 2.7 h) of the first LH response occurring at 29.3 +/- 1.9 months of age (P less than 0.001). Finally, the pattern of circulating levels of estradiol after EB injection did not differ across the developmental stages examined. These results are interpreted to mean that an increase in LH release, presumably LHRH release, starts at the onset of puberty and continues until the age of first ovulation, and that the levels of LHRH release during the pubertal period may determine the effectiveness of estrogen on the LH surge.(ABSTRACT TRUNCATED AT 400 WORDS)