In male rat, 17b-estradiol (E2) causes fast long-term potentiation (fLTP) of synaptic responses in the medial vestibular nucleus (MVN) and mediates the induction of fLTP by high frequency afferent stimulation (HFS). The HFS-fLTP depends on neural E2 (nE2), locally synthesised from testosterone (T), by aromatase. A question to address is if circulating E2 (cE2) may influence the production of nE2. Since cE2 is low in male, we examined this interaction in rat female, in which cE2 levels fluctuate during the estrous cycle. Therefore, we analysed the field potential (FP) evoked in the MVN by vestibular afferent stimulation, under basal condition, and after HFS, in brainstem slices of female rat during high levels (proestrus, PE) and low levels (diestrus, DE) of cE2. Amplitude of FP was higher in PE (22.4%) than in DE. Moreover, unlike male, HFS caused three different effects: fLTP, slow LTP (sLTP) or long-term depression (LTD). However, the occurrence of these effects depended on the estrous cycle phase: fLTP (DE 29% vs PE 4%), sLTP (DE 7% vs PE 23%), LTD (DE 14% vs PE 30%). As expected, fLTP was due to nE2, since it was prevented by aromatase block (letrozole, 100 nM). Conversely, sLTP and LTD were significantly reduced by 5a-reductase block (finasteride, 1 mM), suggesting a role of androgenic T metabolites. Therefore, different levels of cE2 may modify vestibular synaptic responsiveness and plasticity, by influencing neural conversion from androgenic to estrogenic metabolites.