Intracellular recordings from 52 supraoptic nucleus neurosecretory neurons in perfused explants of rat hypothalamus revealed abundant spontaneous inhibitory postsynaptic potentials (sIPSPs) and a compound evoked inhibitory postsynaptic potential (eIPSP) following electrical stimulation in the diagonal band of Broca (DBB). These IPSPs were characterized in terms of the magnitude and ionic specificity of the underlying current and in terms of the transmitter responsible for their activation. sIPSPs rose rapidly to peak within 3-5 ms and decayed exponentially with a mean time constant of 20.2 +/- 1.9 ms (mean +/- SE), a value 1.6-fold greater than the mean cell time constant of 13.8 +/- 1.0 ms. The eIPSPs rose rapidly to peak within 3-10 ms and decayed exponentially over 60-100 ms with a mean time constant of 37.0 +/- 2.8 ms, which is 2.6-fold greater than the mean cell time constant. These features imply a brief persistence of the conductance underlying the IPSPs. In recordings with KAcetate-filled micropipettes, sIPSPs were hyperpolarizing at membrane potentials in the range of -50 to -70 mV and reversed polarity when the membrane was hyperpolarized beyond -80 mV. The mean reversal potential (EsIPSP) was -72.4 +/- 1.1 mV. eIPSPs were hyperpolarizing at resting membrane potential and could be reversed by membrane hyperpolarization beyond a mean reversal potential (EIPSP) of -67.4 +/- 1.4 mV. In recordings with KCl-filled micropipettes, sIPSPs were depolarizing at all membrane potentials more negative than -50 mV. Under these conditions, EsIPSP was estimated at -44 mV. sIPSPs were absent when chloride ions were removed from the perfusion medium. eIPSPs were depolarizing at all membrane potentials and often evoked action potentials; mean EeIPSP was 43.2 mV. Reversal potentials of spontaneous and evoked IPSPs were similar. At a given membrane potential, sIPSP amplitudes varied widely between 1 and 20 mV. The conductance increase underlying individual sIPSPs was estimated to vary between 0.17 and 3.0 nS (avg 0.6 nS) against a mean resting input conductance of 3.78 +/- 0.41 nS. Estimates of the conductance underlying eIPSPs varied widely between cells, from 0.8 to 22.0 nS (mean 72 nS). Accordingly, the ratio of evoked to spontaneous IPSP conductance varied from 1.6 to 43.7 (mean 13.1). The reversal potential of evoked IPSPs shifted with the extracellular concentration of Cl- ions ([Cl-]0) with a mean slope of 41 mV/log [Cl-]0.(ABSTRACT TRUNCATED AT 400 WORDS)