The electrical properties of pigeon's optic tectum neurons located in the non-retinorecipient region of layer II have been studied in vitro slice preparations by using intracellular recordings. As judged from the somatodendritic characteristics of cells intracellularly labeled with horseradish peroxidase recordings were obtained from pyramidal neurons, the main morphological type, as well as from ganglion cells. When stimulated with depolarizing current pulses of 300-500 ms duration, three distinct modes of firing were observed. Most neurons (Type I) responded with a continuous firing of fast action potentials whose frequency rate increased regularly when current strength was raised. Another group of cells (Type II) also exhibited sustained firing. However, in Type II cells, grouped discharges formed by 2-6 fast action potentials per group fired in rapid succession were elicited within a certain range of current intensity. Finally, another group of cells (Type III) responded at all intensities tested by a short train of fast action potentials only at the onset of the current step. At current strength close to threshold the spike undershoot of type I neurons was followed by a slow hyperpolarizing afterpotential while the spike undershoot of Type II cells was followed by a hump-like depolarization and a slow hyperpolarizing afterpotential. In Type II cells, we have also observed a pronounced increase of the hyperpolarizing afterpotential after a grouped discharge. Type III cells were characterized by a small amplitude and short duration hyperpolarizing afterpotential, barely visible in most of them. In Type I and II cells the slow hyperpolarizing afterpotential was blocked by replacing Ca2+ with Mg2+ or Cd2+ in the saline. These results support the idea that in these two types of neurons the slow hyperpolarizing afterpotential is primarily caused by a Ca2+-dependent K+ conductance. Furthermore, blocking the slow hyperpolarizing afterpotential provoked a pronounced increase of the firing frequency of Type I cells. In Type II cells blockade of the slow hyperpolarizing afterpotential had a greater effect on firing behavior: i.e. when Ca2+ was replaced with Mg2+ or Cd2+, Type II neurons exhibited repetitively fired action potentials at high frequency but were incapable of discharging repetitive grouped discharges. These observations indicate that the Ca2+-dependent K+ conductance involved in the generation of the slow hyperpolarizing afterpotential is the main modulator of the firing behavior of both types of cells.(ABSTRACT TRUNCATED AT 400 WORDS)