To assess their role in the regulation of gonadotropin secretion in primates, we determined the number of synaptic connections on gondotropin releasing hormone (GnRH)- and non-GnRH neurones of the arcuate nucleus of ovariectomized (OVX) and OVX plus oestradiol benzoate-treated African green monkeys. After 24 h (day 1), 48 h (day 2) and 8 days (day 8), we performed immunostaining for GnRH. Using electron microscopy, synapses on GnRH- and randomly selected non-GnRH neurones were counted and characterized according to the classification of Gray (symmetric/inhibitory or asymmetric/excitatory). Serum concentrations of oestradiol (OVX) needed to 232 pg/ml on day 1, 63 pg/ml on day 2 and 45 pg/ml on day 8. Concentrations of luteinizing hormone (LH) fell after ovariectomy to 9 microg/ml on day 1, surged to 93 microg/ml on day 2 and declined again by day 8. (a) Ten days after ovariectomy, there were no synapses on GnRH neurones, whereas non-GnRH cells received substantial inhibitory innervation and moderate excitatory input. (b) On day 1, GnRH neurones had highest numbers of inhibitory synapses, while inhibitory synapses on non-GnRH neurones decreased, whereas numbers of excitatory synapses remained relatively unchanged compared to OVX monkeys. (c) By day 2, synapses on GnRH neurones decreased, while synapses increased on non-GnRH cells compared to day 1. (d) On day 8, the most pronounced alteration on GnRH cells was an elevated inhibitory input while non-GnRH neurones received the fewest synapses compared to day 2. We conclude that during an oestrogen-induced LH surge, synapses on GnRH- and mixed non-GnRH neurones are differentially regulated. These findings suggest that oestrogen modulation of arcuate nucleus synapses may be important in the regulation of gonadotropin secretion in monkeys.