1. Neurones in the region of the hypothalamic paraventricular nucleus (PVN) of the rat were studied with intracellular recording in the coronal slice preparation. Three types of hypothalamic neurones were distinguished according to their membrane properties and anatomical positions. Lucifer Yellow or ethidium bromide was injected intracellularly to determine the morphology of some recorded cells. 2. The most distinctive electrophysiological characteristic was the low-threshold depolarizing potentials which were totally absent in type I neurones, present but variable in type II neurones and very conspicuous in type II neurones. Type II neurones generally showed relatively small low-threshold depolarizations (26.5 +/- 2.2 mV) which generated at most one to two action potentials. Type III neurones, on the other hand, generated large low-threshold potentials (40.3 +/- 2.8 mV) which gave rise to bursts of three to six fast action potentials. Deinactivation of the low-threshold conductance in both type II and type III neurones was voltage- and time-dependent. Low-threshold potentials persisted in TTX (1-3-mu-M) but were blocked by solutions containing low Ca2+ (0.2 mM) and Cd2+ (0.5 mM), suggesting they were Ca2+-dependent. 3. Type I neurones had a significantly shorter membrane time constant (14.5 +/- 1.7 ms) than those of type II (21.6 +/- 1.7 ms) and type III neurones (33.8 +/- 4.4 ms). Input resistance and resting membrane potential did not differ significantly among the cell groups. 4. Current-voltage (I-V) relations were significantly different among the three cell types. Type I neurones had linear I-V relations to - 120 mV, while type III neurones all showed marked anomalous rectification. I-V relations among type II neurones were more heterogenous, although most (75%) had linear I-V curves to about - 90 to - 100 mV, inward rectification appearing at more negative potentials. 5. Type I neurones generated fast action potentials of relatively large amplitude (64.2 +/- 1.1 mV, threshold to peak) and long duration (1.1 +/- 0.1 ms, measured at half-amplitude); the longer duration was due to a shoulder on the falling phase of the spike. Type II neurones had large spikes (66.5 +/- 1.6 mV) of shorter duration (0.9 +/- 0.1 ms) with no shoulder. Type III neurones had relatively small spikes (56.1 +/- 2.2 mV) of short duration (0.8 +/- 0.1 ms) with no shoulder. 6. The three cell populations showed different patterns of repetitive firing in response to depolarizing current pulses. Type I neurones ofter generated spike trains with a delayed onset and little spike-frequency adaptation. Type II neurones fired repetitive spikes which showed more marked adaptation and no delayed onset. Type III neurones generated repetitive fast spikes when activated from depolarized membrane potentials, but developed repetitive bursts of spikes when activated from hyperpolarized potentials. Type III neurones sometime showed prolonged after-hyperpolarizations (1-4s) following bursts. 7. Some cells in all three populations displayed repetitive bursting characteristics, although patterns of bursting differed between cell types. Repetitive trains of action potentials separated by periods of silence (i.e. phasic bursting) characterized bursting in type I neurones. Bursting in type II neurones varied, consisting of either single, isolated trains of action potentials in a few cells (7%), or anodal-break membrane oscillations, supporting one to two action potentials, in others (18%). Recurrent low-threshold potentials generated repetitive bursts in 37% of type III neurones. 8. Electrical stimulation near the fornix evoked excitatory and/or inhibitory postsynaptic potentials (EPSPs and IPSPs) in all three cell types. Type I neurones often showed multiple EPSPs. Type II neurones usually generated IPSPs or an EPSP-IPSP sequence. EPSPs and synaptically activated low-threshold potentials with bursts of spikes were seen in type III neurones. 9. Intracellular dye injection revealed different morphologies in the three cell types. Type 1 neurones had relatively large soma diameters (20-30-mu-m) and two to three sparsely branched primary dendrites that were oriented bidirectionally. Type II neurones were smaller (10-25-mu-m) and more highly branched than type I neurones, although they also usually had a bidirectional orientation. Type III neurones were small (11-25-mu-m) and had radially oriented, multipolar dendritic arbors. 10. Based on electrophysiological criteria, three distinct hypothalamic cell types could be identified in the region of the PVN. Type I neurones were located within the PVN and showed electrical properties similar to neurones of the supraoptic nucleus; they were probably PVN magnocellular neurones. Type II neurones were also located inside the PVN and showed heterogeneous electrophysiological properties. distinct from those of type I neurones; they were probably PVN parvocellular neurones. Type III neurones were located dorsal to the PVN and showed distinctive bursting characteristics.
