Voltage-gated transient outward currents in neurons with different firing patterns in rat superior colliculus

Abstract

1. We investigated the electrophysiological properties of transient outward currents (TOCs) in neurons with different firing patterns, regular-spiking, fast-spiking and late-spiking neurons, in the intermediate layer (SGI) of the superior colliculus using the whole-cell patch clamp technique in slice preparations obtained from young rats (post-natal days 17-22). 2. Analysis of inactivation kinetics and normalized amplitude revealed that TOCs in regular-and fast-spiking neurons had fast inactivation kinetics (decay time constants (mean ± S.E.M.) of 13·8 ± 1·5 and 11·4 ± 1·2 ms, respectively) and low current densities (36·6 ± 3·3 and 32·1 ± 4·9 pA pF-1, respectively). TOCs in late-spiking neurons, on the other hand, displayed a wide range of both inactivation kinetics (36·7 ± 2·4 ms, with a range from 11·3 to 147·8 ms) and current density (54·0 ± 2·9 pA pF-1, with a range from 9·8 to 131·2 pA pF-1). 3. In regular-, fast- and late-spiking neurons having TOCs with slow time constants (> 50 ms, class II late-spiking neurons), the TOCs were sensitive to 4-aminopyridine (4-AP), with IC50 values of 2·9, 2·4 and 1·2 mM, respectively. In late-spiking neurons having TOCs with fast decay time constants (< 30 ms, class I late-spiking neurons), the TOCs were composed of at least two 4-AP-sensitive components (IC50 values of 0·2 μM and 3·6 mM). 4. Class I late-spiking neurons displayed non-inactivating outward currents which were highly sensitive to 4-AP. They changed their firing patterns to the regular-spiking mode, not only in response to low concentrations of 4-AP (< 50 μM), but also in response to dendrotoxin (200 nM), suggesting that non-inactivating outward currents contribute to the late-spiking property. However, the components of TOCs which were highly sensitive to 4-AP were also sensitive to dendrotoxin. These results suggest that both or either of the two currents contribute to the late-spiking property of class I late-spiking neurons. 5. Although class II late-spiking neurons also displayed non-inactivating outward currents, the late-spiking property was not abolished by low concentrations of 4-AP and dendrotoxin. They changed to a regular firing pattern in response to a high concentration of 4-AP (5 mM), suggesting that TOCs contribute to late-spiking property of class II late-spiking neurons. 6. The results suggest that TOCs with different properties contribute to the different firing patterns of SGI neurons.