Electrophysiological properties of neurons recorded intracellularly in slices of the pigeon optic tectum

Abstract

The electrical properties of pigeon's optic tectum neurons located in the non-retinorecipient region of layer II have been studied in 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 Ca 2+ with Mg 2+ or Cd 2+ in the saline. These results support the idea that in these two types of neurons the slow hyperpolarizing afterpotential is primarily caused by a Ca 2+-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 Ca 2+ was replaced with Mg 2+ or Cd 2+, Type II neurons exhibited repetitively fired action potentials at high frequency but were incapable of discharging repetitive grouped discharges. These observations indicate that the Ca 2+-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. On the contrary, in Type III cells removal of Ca 2+ from the bath had no effect either on the firing frequency or in the duration of the train of spikes. The present study also demonstrates that pigeon's tectal neurons are capable of generating action potentials corresponding not only to those arising from a sodium conductance but also to those arising from a low threshold calcium conductance.