1. We studied neurons of the nucleus ovoidalis, the principal auditory thalamic relay nucleus of the chicken, with tight-seal whole-cell recording techniques in in vitro slice preparations. Nucleus ovoidalis, marked by anterograde labeling of afferents from the inferior colliculus, consists of a clearly delineated group of densely packed, multipolar cells of approximately uniform diameter. We measured a wide range of non covarying resting potentials (-60 +/- 9 mV, mean +/- SD) and input resistances (277 +/- 168 M omega). All neurons discharged overshooting fast spikes. The observed electrophysiological properties may have a decisive role in the transfer of sensory signals. 2. We grouped neurons on the basis of their firing patterns, in response to intracellular injections of depolarizing current pulses from various membrane potentials. The majority of neurons (86%) displayed weakly adapting, tonic firing. A smaller group of neurons (14%) exhibited qualitative changes in firing modes. They fired repetitively when the stimulus pulse was superimposed on relatively depolarized levels, usually including the resting potential. DC-hyperpolarization led to burst responses consisting of fast action potentials on top of slow potentials. 3. In all neurons, application of 300 nM tetrodotoxin blocked the action potentials and reduced a depolarization-activated inward rectification, observed during 1-s current pulses in a range of membrane potentials depolarized from rest. This rectification is interpreted as a partial result of a persistent Na+ current. 4. During the applications of tetrodotoxin in neurons with burst firing capability, two other slow potentials were visible in isolation. Depolarizing current pulses evoked slow, transient depolarizations at the onset whereas rebound slow potentials occurred on termination of hyperpolarizing current pulses. The slow potentials were blocked by application of 0.5 mM Ni2+ and are likely a result of a low threshold Ca2+ current, such as a T-current. 5. A distinctive property of all ovoidalis neurons was a hyperpolarization-activated inward rectification. Application of Cs+ (3 mM) but not Ba2+ (3 mM), tetraethylammonium (10 mM), or 4-aminopyridine (4 mM) reversibly blocked the current that produced this rectification. The activation time constants for the current varied between approximately 50 and 400 ms and were voltage dependent in some neurons. Thus the hyperpolarization-activated current (IH), responsible for thalamic sleep mechanisms in mammals, also is present in a submammalian thalamus. 6. We suggest that the voltage and time dependencies of the persistent Na+ current and IH participate in generation of the sub- and suprathreshold temporal activity patterns in the neurons.(ABSTRACT TRUNCATED AT 400 WORDS)